transfer and acclimatization effects on the behavior of two species of african great ape (pan...

Transfer and Acclimatization Effectson the Behavior of Two Species of African GreatApe (Pan troglodytes and Gorilla gorilla gorilla)Moved to a Novel and Naturalistic ZooEnvironment

Stephen R. Ross & Katherine E. Wagner &

Steven J. Schapiro & Jann Hau & Kristin E. Lukas

Received: 9 December 2009 /Accepted: 23 April 2010 /Published online: 30 September 2010# Springer Science+Business Media, LLC 2010

Abstract Studying the effects of moving animals to new enclosures is of value toboth captive managers and to scientists interested in the complex interplay betweenenvironment and behavior. Great apes represent some of the greatest challenges inthis regard. Given the cognitive sophistication of these species and the substantialinvestments in new primate facilities, these investigations are particularly important.Using post-occupancy evaluation (POE) methodology, we compared behaviorexhibited by chimpanzees (Pan troglodytes) and gorillas (Gorilla gorilla gorilla)in indoor hardscape-type exhibits to behavior of the same individuals in newnaturalistic enclosures with outdoor access. In the new facility, chimpanzees showeddecreases in the frequency of abnormal behaviors and visual monitoring of humans(attention behaviors) whereas gorillas exhibited reduced agonism as well asdecreased attention behaviors. Both gorillas and chimpanzees demonstrated higherrates of inactivity after transfer to the new facility. All subjects in additiondemonstrated transitory changes in behavior after the move to the new facility(higher rates of scratching in yr 1 than in subsequent years), indicating a period ofacclimatization. Seasonal effects on feeding behavior and activity levels (both

Int J Primatol (2011) 32:99–117DOI 10.1007/s10764-010-9441-3

S. R. Ross (*) :K. E. WagnerLester E. Fisher Center for the Study and Conservation of Apes, Lincoln Park Zoo,Chicago, IL 60614, USAe-mail: [email protected]

S. J. SchapiroDepartment of Veterinary Sciences, University of Texas M. D. Anderson Cancer Center,Bastrop, TX 78602, USA

J. HauDepartment of Experimental Medicine, University of Copenhagen, Copenhagen, Denmark

K. E. LukasCleveland Metroparks Zoo, Cleveland, OH 44109, USA

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species were more active in the winter) were evident as well. The results indicatethat behavioral adjustment to a new facility is an extended process for both speciesand that seasonal effects should be considered in longitudinal analyses ofacclimatization. Behavioral patterns supported the benefits of naturalistic, functionalexhibit spaces and the utility of post-occupancy evaluations in assessing captiveanimal welfare.

Keywords Captive welfare . Great apes . Post-occupancy evaluation . Zoologicalexhibits

Introduction

The environment for animals in captivity is a complex interrelationship of landscape,enclosure structure, climate, environmental resources, and the physical andbehavioral traits of the living organisms it supports. Those invested in designingand managing captive environments to meet best the behavioral and psychologicalneeds of animals are constantly challenged to integrate new findings, test new ideas,and learn from the successes and failures of past efforts. As the architect John Zeisel(1977) asserted, “buildings themselves must be seen as hypotheses to be tested ratherthan solutions to be lived with” (p. 3).

Post-occupancy evaluation (POE) is the systematic assessment of constructedenvironments and has been used in human architectural settings for several decades(Zimring and Reizenstein 1980). More than 20 yr ago, Maple and Finlay (1987)outlined how these methods could appropriately be adapted for use in zoologicalsettings to evaluate existing enclosures, and thus ultimately improve the design offuture generations of animal environments. They listed 3 primary benefits toempirical evaluations of captive environments: 1) enhancement of captive breeding;2) identification of design errors; and 3) appraisal of “user satisfaction” (in this case,a measure of animal behavior). The most comprehensive POE will assess the effectof the environment on the full range of potential users. In the case of a zoo exhibit,the group includes the animals themselves, zoo visitors, care and maintenance staff,researchers, and veterinarians. However, given that the nonhuman residents occupythese spaces 24 h/d, the most extensive evaluation should be made with their needsin mind.

In zoological parks, and to a certain extent also in laboratory animal facilities, apredominant trend in enclosure design is the promotion of naturalistic environments.Ideally, such spaces should not only reproduce the aesthetic characteristics of a wildsetting, but more importantly should mimic the functional attributes of thoseenvironments as well (Chamove and Rohrhuber 1989). As such, naturalisticenclosures are purported not only to enhance public education and increase visitorrespect for wildlife (Finlay et al. 1988; Rhoads and Goldsworthy 1979; Wolf andTymitz 1980), but also to support the increased expression of species-typicalbehavior from resident animals (Coe and Maple 1987; Maple and Stine 1982; Ogdenet al. 1990; Redshaw and Mallinson 1991). Several studies have demonstratedsubstantial changes in activity and exploration for a range of primate speciestransferred from traditional enclosures to more complex and naturalistic environ-

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ments (chimpanzees (Pan troglodytes): Clarke et al. (1982); gorillas (Gorilla gorillagorilla): Bowen (1980); Goerke et al. (1987); langurs (Presbytis entellus): Little andSommer (2002); rhesus macaques (Macaca mulatta): O’Neill et al. (1991); mandrills(Mandrillus sphinx): Chang et al. (1999); tamarins (Saguinus oedipus): Price (1992);marmosets (Callithrix jacchus): Chamove and Rohrhuber (1989). The effects onsocial behavior are more variable: Some moves have elicited positive changes,including increases in allogrooming and decreases in agonism (Little and Sommer2002; Maple and Stine 1982; O’Neill et al. 1991); others report negative changes,such as decreased prosocial behavior (Chang et al. 1999; Goerke et al. 1987); andsome indicate no changes at all (Clarke et al. 1982).

Stress-related behaviors are among the most frequently accessed behavioralindices in evaluations of captive environments. Abnormal behavior, psychopathol-ogies, and stereotypies are thought to emerge and displace species-typical behaviorswhen an environment fails to meet the biological and behavioral needs of the animalsufficiently (Visser et al. 2008). There are conflicting results in the literature on theeffects of functionally naturalistic environments on stereotypical behavior, but moststudies indicate that complex enclosures reduce frequencies of these behaviors(Bowen 1980; Clarke et al. 1982; Goerke et al. 1987). In some cases, abnormalbehaviors that occurred in the nonnaturalistic environment disappeared completelyin the naturalistic environment (Chang et al. 1999; Maple and Finlay 1986).

Behavioral changes subsequent to a translocation from one environment toanother may also stem from the relatively short-term process of adaptation andacclimatization to the new environments. Ogden et al. (1990) reported thatacclimatization of zoo-living gorillas to a new, naturalistic environment extendedover a period of 6 mo, as measured by exploratory behavior. Price (1992) similarlytraced a progressive increase (over a 16-wk period) in the amount of time thatcaptive cotton-top tamarins left familiar indoor quarters to explore a new woodedhousing area. This work suggests a process of gradually increasing exploration of anovel habitat after translocation.

However, as a result of changes in and interactions between the social andphysical environment, new and more complex enclosures may influence apes inways that prevent a clear delineation of the acclimatization period. Behavioralanalyses of the effects of translocation may result in unpredicted changes in typicalindicator behaviors, especially in young individuals that may display additionaleffects related to social and physical development. For example, Goerke et al. (1987)reported that the rate of solitary play exhibited by a juvenile gorilla after moving to anatural exhibit failed to reach pretranslocation levels, even 2 yr after introduction. Itis not clear how this effect was influenced by the subject’s maturation or the newexhibit itself. The dynamic interaction between individual behavior and enclosurecharacteristics both emphasizes the importance of distinguishing between short- andlong-term effects of novel environments and highlights the value of including thefull activity repertoire in post-translocation analyses of behavior.

Aiding the examination of behavioral effects of relocation, the breadth ofempirical evaluations across multiple enclosures and enclosure-types is growing.However, the opportunities for substantive, long-term comparisons across thesecategories are still relatively rare. The dearth of such analyses is especially relevantin the case of large primates, for which multimillion dollar facilities have become the

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norm. The 3 published cross-enclosure comparisons on African great apes (Bowen1980; Clarke et al. 1982; Goerke et al. 1987) are now all >20 yr old. Considering theprogress in exhibit design during that time, an evaluation of translocation to amodern, naturalistic enclosure is due. Further, there is a relative scarcity oflongitudinal data that allow for a detailed analysis of acclimatization and seasonaleffects that may also impact the results of post-occupancy evaluations. Finally, withonly 1 exception (Bowen 1980), these cross-facility comparisons of ape enclosureswere performed in relatively warm climates. The degree to which theseenvironmental and acclimatization effects are affected by a more variable temperatelocation, where outdoor access may be seasonally unavailable, is virtually unknown.

As an important component of a large POE project, the aim of this study was tocompare intrasubject behavior produced in the context of a traditional, hardscapeenvironment to that expressed in a new, more naturalistic enclosure, to assess theeffects of modern environment design on a zoological population of gorillas andchimpanzees. Convergent with the literature, we predicted that transfer to the larger,more complex exhibit would influence a range of positive changes in behavior,including increased activity and prosocial behavior, and reduced abnormal and self-directed behaviors.

Importantly, the traditional environment from which individuals were moved wasa considerably enriched environment and effective in supporting species-typicalactivities, making this analysis different from those involving impoverished andsubstandard housing. This intermediate upgrade—compared to one spanning thehistorical continuum of exhibit types—provides an opportunity to examine anarrower range of causal factors and may also be most relevant to current zoologicalmangers who oversee comparable second-generation exhibits that include bothnaturalistic and traditional components. In addition, by examining behavioralpatterns across 3 complete years in the new facility, we seek to detail interactionsbetween acclimatization and seasonal effects. Together, these results will informunderstanding of the complex interactions between captive environments and greatape behavioral and psychological welfare.

Methods

The Lester Fisher Great Ape House (GAH) at Lincoln Park Zoo (LPZ) was built in1976 and was replaced by the Regenstein Center for African Apes (RCAA) in 2004.To aid in the design of RCAA, a comprehensive evaluation of GAH was conductedthat included detailed ape space use studies (Ross and Lukas 2006; Ross et al.2009), visitor behavior studies (Ross and Lukas 2005; Ross et al. in review), andvisitor surveys (Lukas and Ross 2005). We present here an analysis of ape behaviorin each setting.

Facility

GAH comprised 6 similarly shaped rooms in a circular, interconnected configura-tion. Four of these rooms were used primarily for 2 gorilla groups and the 2remaining rooms were used for the chimpanzees. Individual enclosures ranged in


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size from 35 to 55 m2, with climbable mesh ceilings, 7–10 m in height. The floorswere concrete and heavily bedded with straw, and a variety of steel climbingstructures, supplemented with ropes and platforms, were available (Fig. 1). On theouter perimeter, a tall glass partition separated the apes from the visiting public. Theopposite side of each enclosure was separated from the caretaker management areaby a mesh divider. A small outdoor enclosure was infrequently used by gorillas, butwas not provided to the chimpanzees. Data from the outdoor space are not includedin these analyses.

The design of the RCAA (Fig. 2) was influenced by the initial data on structuralpreferences collected at GAH (Ross and Lukas 2006). RCAA was divided into 4exhibits, one of which is not publicly viewed, each composed of an indoor enclosureand an outdoor yard. The indoor enclosures ranged in size from 75 to 124 m2 and theoutdoor yards varied from 112 to 1127 m2. Concrete and natural deadfall trees,artificial steel bamboo shoots, synthetic vines, and a substrate of deep-litter pinemulch bedding (0.6–0.9 m) comprised a naturalistic and functional space in theindoor components. A meshed ceiling 10 m above the ground, stable nestingplatforms of varied heights, and several mesh panels dividing the apes’ space frommanagement areas provided additional climbing opportunities. Like GAH, a largeglass partition to the visitor area extended around a portion of the exhibit. In contrastto the GAH facility, access for both species to the outdoor yards of the RCAA wasprovided whenever possible (weather permitting) by remotely controlled slidingglass doors, allowing social groups simultaneous and voluntary use of both indoorand outdoor enclosure areas, when weather and temperature permitted. We excludedperiods of outdoor access from the current analysis.

An additional difference stemmed from the behavioral and cognitive researchpresence in each facility. Though we collected observational behavioral data viasimilar methods in both facilities, the RCAAwas patterned with an in-house researchcenter (Lester E. Fisher Center for the Study and Conservation of Apes) thatconsiderably expanded apes’ participation in experimental protocols. We conductedseveral tool-use and learning studies, including computer-guided cognitive inves-tigations, though they represent a very small proportion of the daily activity budget

Fig. 1 Indoor enclosure at theLester Fisher Great Ape House(1975–2002), which featuredsteel and concrete climbingstructures. The concretefloor was often bedded withhay (not pictured).


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of the apes and many studies, such as touch-screen investigations, are conducted inoff-exhibit spaces.

Although GAH and RCAA differed along a number of critical dimensions, it isimportant to highlight the elements shared by both facilities. In fact, though GAHincluded fewer naturalistic elements than RCAA, it nonetheless met many of thecriteria outlined for even modern ape enclosures. Both enclosures provided subjectswith considerable space and innovative furnishings. In both settings, individuals hadaccess to their exhibit spaces ca. 22 h/d and were moved to smaller holding areas(upstairs for GAH and downstairs for RCAA) only during daily exhibit maintenance(0080–1000 h). Beyond short-duration exposure to research-related activities,subjects in both facilities were provisioned with largely comparable forms ofenvironmental enrichment, including natural browse, objects for manipulation, andmaterial for nesting. Feeding protocols were closely matched across facilities aswell, incorporating 3 daily feeding periods in which diet items were scatteredliberally in all areas of the exhibit. These practices also included provisioning ofnovel foods and novel forms of food presentation, complicating the foraging processby concealing food inside other objects, and providing regular access to baitedfeeding enrichment devices. Though research participation in the RCAA includedsome food-provisioning, we consider these opportunities as additional environmentalenrichment, rather than a change in feeding protocol per se.

There were 2 main components to the present investigation: 1) determination offacility effects (GAH vs. RCAA) on behavior and 2) examination of time-dependentchanges in behavior after the translocation to RCAA. Time-dependent analysesincluded examination of both seasonal and acclimatization, i.e., greater behavioralchange in the first year after translocation vs. subsequent years, effects.

Data Collection

We collected focal observations on each gorilla and chimpanzee via instantaneoussampling with a 30-s intersample interval in 10-min sessions. Table I shows thenumber of sessions per individual. At each interval, we collected data on 1) thebehavior of the focal ape and 2) the proximity of its nearest groupmate. For theproximity measure, we recorded nearest-neighbor distance on a 4-level scale basedon a distance criterion; the current analysis focused exclusively on the Physical

Fig. 2 Indoor enclosure atthe Regenstein Center forAfrican Apes (2004–present),which features naturalistic andfunctional climbing structures.The floor is composed ofa deep-mulch substrate.


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Contact and Proximate levels, which we combined into 1 category because theDistant category was expected to be confounded by volumetric changes betweenenclosures. The ethogram consisted of 40 behaviors that we subcategorized to 9primary measures for analysis. We assigned each of the 9 measures a predicteddirection of change that was targeted by the facility design staff during theconceptualization of the building, with the objective of increasing social and activebehaviors while decreasing anxiety-related and species-atypical behaviors (Table II).A total of 12 observers (including S. R. Ross and K. E. Wagner) collected data inGAH between May 2001 and August 2002 and in RCAA between July 2004 andJune 2007, with all observations proportionately distributed between 1000 and1700 h. All observers completed extensive training and passed interobserver tests ata proficiency of ≥85% agreement before commencing data collection.

Table I Focal subjects

Name Sex Age Sample size (no. of 10-min observation sessions)

GAH RCAA Year 1 RCAA Year 2 RCAA Year 3

Chimpanzees

Keo Male 46 83 199 282 283

Donna Female 40 83 180 263 312

Vicky Female 40 83 181 273 297

June Female 38 83 182 268 301

Kibale Female 23 83 178 279 299

Hank Male 14 — 228 290 249

Optimus Male 6

— 228 299 230

Kipper Male 5 — 237 295 224

Kathy Female 14 — 228 285 255

Cashew Female 20 — 234 317 230

Nana Female 11 — 234 312 218

Chuckie Female 5

— 228 312 224

Gorillas

Kwan Male 16 67 251 295 235

Bulera Female 16 67 252 291 223

Kowali Female 23 67 249 294 224

Madini Female 7 64 355 314 123

Jojo Male 23 83 228 299 250

Bahati Female 13 83 228 298 245

Makari Female 16 83 228 308 219

Rollie Female 7 64 205 343 220

Tabibu Female 13 83 231 294 263

We used apes present in both GAH and RCAA for facility comparisons. We used apes present only inRCAA for acclimatization analyses. Listed age is that as of 2004, when the new facility opened.


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Apes

The apes and the analyses to which their behavioral data were subject are listed inTable I. To study the effects of facility, we used only individuals for which we had≥60 sessions (10 h) in each building. This included 5 chimpanzees (in 1 group) and9 gorillas (in two groups) with a mean observation sample of 142.3 h per subjectover the course of the 4 yr of study (ranging from 11 to 14 h per subject in GAH; 42to 44 h per subject per year in RCAA). To study acclimatization effects, we usedonly individuals for which we had ≥180 sessions (30 h) of data in each of the first3 yr after translocation to RCAA. This included 12 chimpanzees (in 2 groups) and 9gorillas (in 2 groups), with a mean observation time of 127.8 h per subject over thecourse of the 3 yr of study (ranging from 42 to 44 h per subject per year).

The 2 chimpanzee groups differed in several respects. Keo’s group (facility andacclimatization sample) was older (mean age=38.9 yr), and 3 of the 5 individualswere wild born. With the exception of 20 mo housed at another AZA-accredited zooduring the new enclosure construction (2003–2004), all members of the group hadlived at LPZ for their entire adult lives. Hank’s group (acclimatization sample) wasyounger (mean age=11.7 yr), all captive born, and until their translocation toRCAA, had lived primarily outdoors at another AZA-accredited zoo in Florida fortheir entire lives. Both groups were stable in terms of group composition before,

Table II Behavioral ethogram and the targeted direction of change as a result of the new facility

Behavior Description Targeted direction

Abnormal Subject engages in repetitive or unnaturalbehaviors such as coprophagy, regurgitation,stereotyped body movements, etc.

Decrease

Scratch Subject rakes fingers across skin with largesweeping movements.

Decrease

Self-directed behavior Subject attends to its own body usually in theform of self-grooming. Includes shorter-durationbehaviors such as self-touching but does notinclude scratching (see above).

Decrease

Feed/forage Subject eats food or is actively searching for food. Increase

Attention Subject is stationary, proximate to a barrier throughwhich it can view human activities. Includes visitorspace and keeper space.

Decrease

Prosocial Subject engages in positive, friendly social behaviorwith a conspecific. Includes social grooming and playing.

Increase

Agonism Subject engages in aggressive behavior with aconspecific including fighting, biting, displaying.Also includes submissive behaviors such as bared-teeth grin, screaming and hunched posture.

Decrease

Inactive Subject is stationary and not engaged in other behaviors. Decrease

Other Subject is engaged in behaviors not listed above n/a

Proximity Description

Proximate Subject is touching or within 1 m of a conspecific. Increase

Note that measures of proximity are recorded independent of behavioral measures.


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during, and after the transition to RCAA and experienced no significant changes inhealth or well-being during and before data collection

The 2 gorilla groups were more similar. Both Kwan’s and Jojo’s groups hadsimilar mean ages (14.4 vs. 15.3 yr) and all were captive born. Both groups hadlived at GAH until 2002, were transferred together to other AZA-accredited zoosduring construction, and then moved back together to RCAA in 2004. Eachgroup also experienced similar changes in membership on arriving to RCAA: ineach case a female group member died in the first year at RCAA (not includedin the sample) and an infant was born within 2 yr of arrival. Jojo’s groupexperienced an additional birth during the construction of RCAA, and the grouparrived to the new facility with the 6-mo-old infant (no infants were included inthe sample).

Analyses

We first summarized each individual’s data for each of the 9 behavioralcategories in the 2 facilities. We removed data recorded as out-of-view fromthe denominator to control for variance in visibility between facilities. As such,the unit of analysis was the mean percentage of in-view scans during which agiven behavior occurred. To determine the quantitative effect of facility on apebehavior, we used intrasubject paired t-tests. Because we predicted that behaviorsdemonstrated at the new facility would change in a predicted direction, all testswere 1-tailed. We set the α level at 0.05.

To determine temporal acclimatization and seasonal effects, we determinedindividual behavior means for each quarter year across the 3-yr period of datacollection in the RCAA. We divided the year into 4 seasonal periods of 3consecutive months each: summer (June–August), autumn (September–November),winter (December–February), and spring (March–May). We ran a mixed-modelANOVA with 3 factors: group (2 groups per species), season (4 seasons), and yearafter arrival at RCAA (3 yr) to determine the effects of those factors along withassociated interaction effects and followed up with Tukey HSD tests (α=0.05) todetect specific pairwise differences (Sokal and Rohlf 1994).

Results

Facility Effects

A multivariate ANOVA confirmed significant effects of the main factors of facility(RCAA vs. GAH) (F=7.77, df=1,228, p<0.001) and species (chimpanzee vs.gorilla) (F=4.71, df=1,228, p=0.002) on the behavior of the apes. Because of this,we conducted all subsequent analyses separately for chimpanzees and gorillas(Tables III and IV).

Chimpanzees We conducted interfacility tests on the 5 chimpanzees that lived inboth enclosures. The mean frequencies of each behavioral class in each facility areshown in Table III. Housing in the new RCAA facility was associated with a


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decrease in both abnormal behavior and frequency of visual monitoring of publicand caretaker areas (hereafter attention behaviors). None of the other behaviors orthe measure of social proximity differed significantly between facilities.

Gorillas We conducted interfacility tests were conducted on the 9 gorillas that livedin both enclosures. The mean frequencies of each behavioral class in each facility areshown in Table IV. As expected, in the RCAA enclosure, gorillas exhibited asignificant reduction in agonism and attention-related behaviors. However, they alsoexhibited an unexpected significant increase in inactivity. None of the otherbehaviors or social proximity measures differed significantly between facilities.

Table III Comparison of chimpanzee (n=5) behavior in 2 facilities

Behavior GAH RCAA Percent change t (df=4) p

Abnormal 1.80 0.49 –72.7 2.38 0.038

Scratch 0.79 0.74 –3.8 0.63 0.281

Self-directed 4.69 3.44 –26.7 1.38 0.120

Feed/forage 28.66 33.02 +15.2 0.75 0.254

Attention 15.78 2.92 –81.5 3.22 0.016

Prosocial 7.19 11.07 +5.4 0.91 0.217

Agonism 0.92 0.12 –86.9 1.33 0.127

Inactive 26.71 32.58 +22.0 1.04 0.179

Other 13.46 15.62 +16.0 0.91 0.793

Proximate 17.12 22.18 +29.6 1.49 0.105

Measures are percent of in-view time displaying behavior. Measures of proximity are recordedindependent of behavioral measures.

Table IV Comparison of gorilla (n=9) behavior in 2 facilities

Behavior GAH RCAA Percent change t (df=8) p

Abnormal 2.74 2.79 +1.8% 0.178 0.431

Scratch 0.45 0.64 +42.2% 1.764 0.054

Self-directed 4.68 6.17 +31.8% 1.409 0.095

Feed/forage 36.50 30.82 –15.6% 1.555 0.076

Attention 6.90 2.31 –66.5% 3.752, 0.002

Prosocial 4.16 3.08 –26.0% 0.860 0.205

Agonism 0.31 0.08 –74.2% 3.496 0.003

Inactive 30.38 44.84 +47.6% 3.442 0.003

Other 13.88 7.28 –47.6% 0.852 0.211

Proximate 16.62 19.51 +17.4% 0.785 0.225

Measures are percent of in-view time displaying behavior. Measures of proximity are recordedindependent of behavioral measures.


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Acclimatization Effects

Behavioral categories that showed significant changes in mean frequency for eachspecies across year and season are shown in Fig. 3.

Chimpanzees Rates of attention-related behaviors changed over the course of thestudy (F=9.19, df=2,120, p<0.001) and were higher in yr 1 than yr 2 (p<0.001).

Rates of combined feeding and foraging behaviors were also affected by year(F=4.88, df=2,120, p=0.005) along with season (F=10.84, df=3,120, p<0.001).Further, there was a year×season effect in which season was influential in yr 3(F=11.63, df=3,44, p<0.001) but not earlier. In yr 3, rates of feeding and foragingbehavior were higher in winter and spring than in summer or autumn (all p<0.01).

Chimpanzees also demonstrated a seasonal effect on activity (F=14.43,df=3,120, p<0.001). Subjects were less inactive in the winter vs. the spring,summer, and fall (all p<0.001).

Rates of scratching observed by the chimpanzees were affected by year(F=26.64, p<0.001). This frequency was significantly higher in yr 1 than in bothyr 2 and 3 (p<0.001). There was a group effect on scratching (F=34.86, df=1,120,p<0.001), in which the older chimpanzee group showed higher rates of scratching,

Per

cent

age

of in

-vie

w s

cans

Fig. 3 Acclimatization and seasonal effects on chimpanzee and gorilla behavior (as measured by percentof in-view scans) after transfer to a new facility.


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and a yr×group effect (F=8.63, df=2,120, p<0.001) in which rates of scratching forthe older group differed in yr 1 vs. yr 2 and 3 (p<0.001), but remained relativelyunchanged for the younger group.

Several other group effects also emerged in analysis. The younger chimpanzeegroup showed lower rates of inactivity (F=33.09, df=1,120, p<0.001) and attention-related behaviors (F=168.96, df=1,120, p<0.001) and higher rates of self-directedbehavior (F=63.06, df=1,120, p=0.004), and were more likely to be positioned inproximity to a groupmate (F=63.06, df=1,120, p=0.004) vs. the older group ofchimpanzees.

Gorillas We performed acclimatization analyses on 9 gorillas in 2 groups. As withchimpanzees, there was a significant effect of year on rates of scratching (F=40.36,df=2,84, p<0.001) in which we observed scratching more frequently in yr 1 than inyr 2 and 3 (p<0.001).

Seasonal effects on gorilla behavior were similar to those observed among thechimpanzees. Gorillas were more inactive (F=6.86, df=3,84, p<0.001) during thesummer vs. the winter (F=19.90, df=1, 42, p<0.001). Likewise, season affectedfeeding-foraging behavior rates (F=4.31, df=3, 84, p=0.007) such that frequencieswere higher in the winter than in the summer (p=0.002).

The 2 gorilla groups differed in several respects. Group 1 showed higher rates ofabnormal behavior (F=9.06, df=1,84, p=0.003) and feeding (F=13.28, df=1,84,p=0.001) and lower rates of inactivity (F=43.06, df=1,84, p<0.001). However, weobserved no significant interaction effects.

There was no effect of year, season, or group on rates of social proximity for thegorillas.

Discussion

Our results demonstrate positive—though conservative—behavioral changes among 2species of great apes in association with relocation from a traditional, hardscape settinginto a modern, naturalistic environment. Chimpanzees, in particular, showed a broadrange of potentially beneficial changes. Though not all differences were statisticallysignificant, that the range of these changes tended to be in a positive direction andconsistent with predictions suggests an overall beneficial effect of RCAA.

In relation to the relatively modest changes that were observed, it is important tonote that the older facility did not represent a suboptimal environment in all respects.Even on its closing in 2002, GAH remained an innovative captive ape habitat,showcasing relatively expansive vertical space, and complex and functionalinteriors. The comparison between these facilities is thus different from previouslypublished accounts of transfers from barren cages to naturalistic enclosures, and isbetter characterized as a move from a functional, indoor, hardscape setting to amodern, indoor-outdoor, naturalistic setting. As such, considerable differences inbehavioral rates may be an unrealistic benchmark for evaluating the success of thenew facility. This is especially evident in evaluating the behavior of the gorillas,which changed less in the new facility vs. that of the chimpanzees.


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As predicted, both gorillas and chimpanzees showed significantly lower levels ofhuman-directed visual attention in RCAA than in GAH. The design of GAHfacilitated this form of behavior, as individuals were separated from service andkitchen space by a large mesh wall at which they often spent long periods watchingkeeper activity, and consequently turning their backs to the visitors on the other sideof the exhibit. RCAA was designed to reduce this form of distraction, by visuallyseparating service areas from animal holding areas. Nor did individuals in the newbuilding merely redirect this proportion of monitoring time to human visitors. Theseresults parallel the analysis of exhibit use for these facilities, in which both speciesshifted from a preference for areas adjacent to mesh to an underutilization of thosespaces (Ross et al. 2009) and a nondifferential use of areas adjacent to visitorviewing windows (Milstein and Ross unpublished data).

Several previous reports describing ape transfers to new exhibits reportedsubstantive increases in activity and exploration (Clarke et al. 1982; Goerke et al.1987). Chimpanzees and gorillas in the present study showed no such behavioraltrend, reducing their activity levels by 22% and 48%, respectively. Although adecrease in inactivity was the targeted, and predicted, direction of change, it is notclear whether this type of change unequivocally indicates a negative shift inbehavior. Traditionally, inactivity has been characterized as a problem for captiveanimals (Stevenson 1983) and is appropriately targeted as a potential factorinfluencing the high rate of cardiac disease in captive great apes (Doane et al.2006). However, other fields of inquiry have characterized elevated activity andincreased posture changes as restlessness. Such traits have been linked to infanticidalbehavior in domestic pigs (Sus scrofa domesticus: Ahlstrom et al. 2002), elevatedheart rate in dairy cows (Bos taurus: Gygax et al. 2008), and psychological disordersin humans (Homo sapiens: Casper 2006). Though we expected an increase inexploratory behavior, we are hesitant to characterize this facility effect as a negativechange in terms of welfare. For chimpanzees, the decrease in abnormal behaviorsmay account for this increase. In general, increased inactivity may be indicative ofanimals that are relaxed or content rather than bored or unmotivated. Given that toomuch or too little activity may be considered problematic, research developingoptimum target activity levels for different sex and age classes for apes would be ofsubstantial benefit. For instance, an extensive study of free-ranging chimpanzeesshowed that they spent ca. 36% of their time resting (Doran 1997), which is morethan what we report here in either facility. Reduction of unusually high activity(continuous stereotyped pacing, restlessness) and inactivity (apathetic torpor,boredom) levels may be critical indications of positive changes in animals’ welfareand, specifically, ability to cope with the challenges of their environment.

For gorillas, interpretation of the general response to the enclosure change isfurther clouded by the nonsignificant rises in negative, arousal-linked behaviors,including abnormal activities—predominantly regurgitation and reingestion—andscratching, and the significant increase in self-directed behaviors, contrary topredicted patterns. Given the relatively low levels of these behaviors in bothfacilities, it is unclear whether the nonsignificant changes that were observed evincea change in welfare or merely a statistical variation in interaction with otheracclimatization effects. The literature on regurgitation behaviors has identified nosingle cause or function (Lukas 1999) and hence offers no clear indication as to


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whether the changed elements of the new facility may have supported an increase orno change in frequency. Self-directed behavior and more robustly scratchingbehavior are associated with increased arousal across primate species (Leavens etal. 2004); however, as with inactivity, these behaviors may not be exclusively linkedto negative arousal (Maestripieri et al. 1992). We suggest that the observed increasein self-directed behavior and the possible, though currently nonsignificant rise inscratching behavior may also be associated with the exploratory behaviors supportedin the new facility and social interest, rather than emerging solely from stress oranxiety.

A clearer indication of a positive effect of relocation was indicated by theexpected decrease in abnormal behaviors by the chimpanzees and the decrease inagonism by gorillas. Notably, although not statistically significant, chimpanzeeagonism also decreased by 87%. Other researchers have reported decreases inagonistic and abnormal behavior following a transfer to a naturalistic environment(Bowen 1980; Clarke et al. 1982; Goerke et al. 1987); however in all of thesestudies, pretransfer rates were considerably higher than baseline (GAH) rates in thepresent study, in which rates of both behaviors made up <3% of in-view observedtime.

Although these data represent one of the most complete assessments ofacclimatization and transfer for captive great apes, it remains difficult to isolate asingle particular causal factor from the complex of physical and sensory character-istics forming the pre- and post-translocation landscape. However, the similarity ofthe exhibits with respect to the substantial vertical height, spatial complexity, andexpansive visual access to zoo visitors via glass partitions suggest that these factorsalone did not exert a substantial effect. Alternatively, exhibit changes including thesubstantial volumetric expansion, increased naturalism, and readily accessibleoutdoor access were intended to increase exhibit complexity and expand spaceuse. We expect that these elements stimulated increased exploratory behaviors,reduced the available time for the production of abnormal behaviors, and facilitatedspecies-typical behavior. In the sections that follow, we examine each of thesefactors individually.

Space Increase

Regulatory space requirements for primates exist but have not been empiricallyvalidated (Weng et al. 1998), and they typically focus on parameters at the level ofsingle individuals. However, individuals’ space needs may change in the context ofsocial groups of different sizes, wherein interactions are supported or constrained byspatial topography and proximity (Coe 2001). RCAA provided ca. 300% more areavs. GAH. However, given that the behavioral profiles demonstrated in the oldfacility were not indicative of high levels of stress or anxiety, it is difficult todetermine whether this large increase in space directly influenced the behavioraleffects observed. More likely, the successful design attributes of GAH curtailed thedegree to which the move to RCAA could produce wide-ranging signs of improvedbehavior and welfare. We may predict the most robust effects of increasing useablespace to occur when individuals are maintained in an enclosure at the minimal sizethreshold. Once this threshold is crossed—as was the case in GAH—we would then


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expect diminishing behavioral and welfare benefits with further increases, i.e., theexpansion provided by RCAA (Appleby 1997). Further, there is little reason toexpect a negative behavioral change when providing as much space as possible formost species, especially those that display large home ranges in the wild. Increasingspace provides increased opportunity for choice: Subjects may use a restricted areawithin their larger space allowance if they choose, and explore a wider area whenappropriate (Appleby 1997).

Outdoor Access

Another obvious difference between the facilities was the provision of outdoorspace. The specific benefits of allowing captive primates access to outdoor areas arestill in question, and there remains relatively little empirical evidence of behavioralbenefits that can be directly attributed to this practice. Reports demonstrating apositive preference for, and influence of, outdoor access (marmosets: Pines et al.2007; chimpanzees: Baker and Ross 1998) contrast with those that have shown lesssubstantial effects (Bellingham 1998; Chamove and Rohrhuber 1989). Although thecurrent analysis does not quantify the use of the outdoor space nor include periods ofoutdoor access in the sample, the positive changes seen in RCAA may be attributedat least in part to the provision of expansive outdoor yards. Chimpanzees that werenot provided outdoor access in GAH showed a significant decrease in rates ofabnormal behavior when moved to RCAA and its frequent outdoor access. Gorillas,which had occasional outdoor access in the old facility, showed no change inabnormal behaviors. Rates of anxiety-related scratching also dropped significantlyduring exhibit acclimatization for the chimpanzee group with no previous outdooraccess (Keo’s group), but did not for the group formerly managed with constantoutdoor access (Hank’s group). Directed investigation of the use of the outdoorspace and analysis of its effect on the behavior of these apes is forthcoming (Ross etal. in press).

Naturalistic Substrate

The final substantial difference between the 2 facilities was in the primary substrateused to cover the ground in the indoor enclosures. Though regularly supplementedwith hay, the substrate at GAH was similar to most great ape facilities: easily cleanedand physically unforgiving. With both aesthetic and functional motives, the indoorenclosures at RCAA were designed to be maintained with a deep-litter substrateusing pine bark mulch. Multiple reports have demonstrated that substrateenhancement, i.e., replacing hardscape flooring with destructible material such ashay or woodchips, supports positive behavioral changes in a range of primatespecies, including chimpanzees (Baker 1997; Brent 1992; Chamove et al. 1982). InRCAA, we have also observed that the manipulable substrate supports other species-typical behaviors: providing a physical foundation for nesting, rough and tumbleplay, widely distributed use of exhibit space, and extended foraging behaviors.Though the amount of time that the apes chose to spend on the exhibit floor did notdiffer between facilities (Ross et al. 2009), previous reports suggest that this type ofsubstrate may influence behavior (Chamove et al. 1982, 1984; Ludes and Anderson


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1996). In this case, the naturalistic mulch may be linked to the reduction of human-directed attention behaviors and the increase in resting time. Further cross-facilityanalyses will offer a platform on which to evaluate the effects of substrate change ina zoological setting.

Exhibit Acclimatization Effects

Both species showed significant decreases in scratching behavior after a peak in thefirst year in the new exhibit. In addition, chimpanzees showed a significant decreasein attention directed toward visitor and staff areas after the first year in the newfacility. These changes suggest a process of acclimatization to the new exhibit,which was relatively extended compared to other evaluations (Ogden et al. 1990:6 mo; Bowen 1980: 2 mo; Goerke et al. 1987: 3 wk; Clarke et al. 1982: 1 wk). Inthis case, the long familiarization period may have been exacerbated bycorresponding changes in management protocols from the previous facility; theeffects of physical transport (Wolfensohn 1997); exhibit complexity (Paquette andPrescott 1988); and social variables including age, experience (Stevenson 1983), andhierarchical structure. Nonetheless, managers of great apes should note thatbehavioral patterns observed even at 1 yr after translocation may not be indicativeof those observed thereafter.

Seasonality affects wild ape behavior in ways most overtly associated with thedifferential availability of food resources (Doran 1997). Seasonal factors may alsounderlie some behavioral variation observed in captive environments: During thecoldest winter months, the apes were locked inside and exhibit space was reduced anaverage of 80%. As a result, it remains unclear whether the observed season-associated behavioral changes (increased feeding and activity by both species) werea result of natural variation (temperature, sunlight, day length, etc.) or weresomehow associated with a reduction in space. Increased social density may accountfor an increase in ape activity, as was evident in studying these apes during daily,short-term alternations between off-exhibit holding areas and much larger exhibitspaces (Ross et al. 2010) and other studies of social density effects (Nieuwenhuijsenand de Waal, 1982). Nonetheless, these relationships remain poorly understood, evenin more controlled experimental settings (Novak et al. 1994). Future analyses willfocus on the direct effects of outdoor access and temperature variability, but thepresent results suggest that winter housing does not seem to have a negativeinfluence on major behavioral patterns of activity and sustenance, and that carefullydesigned enclosures can effectively house great ape species in variable climatesthroughout the year.

In combination with earlier analysis of great ape space use in these exhibits(Ross et al. 2009), this post-occupancy evaluation supports the assertion thatbehavioral benefit can result from modern, naturalistic enclosures designed withdue consideration of analyses of empirical data on the species in question. ThePOE paradigm provides a systematic template with which to assess the success orfailure of enclosure designs for captive animals. The new RCAA facility providedincreased volumes of useable space, outdoor access, and a naturalistic substrate, aswell as increased opportunities for choice and control. Chimpanzees in particularappear to have benefited from these changes, but the relative lack of effect on


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gorilla behavior is worthy of further investigation. The behavioral changesrecorded in this POE, both within and across species, may assist in futureassessments of design functionality in accommodations for nonhuman primates inzoological and laboratory settings.

Acknowledgments We thank the animal care staff at both the Lester Fisher Great Ape House and theRegenstein Center for African Apes for their cooperation with the research, and the research intern stafffor collecting much of the behavioral data. We acknowledge the helpful comments of 2 anonymousreviewers and also thank the Leo S. Guthman Foundation for their financial support of the Lester E. FisherCenter for the Study and Conservation of Apes.

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transfer and acclimatization effects on the behavior of two species of african great ape (pan...

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