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Ape behavior in two alternating environments comparing exhibit and short-term holding areas.

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American Journal of Primatology 72:951–959 (2010)
RESEARCH ARTICLE
Ape Behavior in Two Alternating Environments: Comparing Exhibit
and Short-Term Holding Areas
S.R. ROSS1,2, K.E. WAGNER1, S.J. SCHAPIRO3, AND J. HAU2
1
Lester E. Fisher for the Study and Conservation of Apes, Lincoln Park Zoo, Chicago, Illinois
2
Department of Experimental Medicine, University of Copenhagen, Copenhagen, Denmark
3
Michale E. Keeling Center for Comparative Medicine and Research, Department of Veterinary Sciences, University of Texas
M.D. Anderson Cancer Center, Bastrop, Texas
In many facilities, primates are voluntarily transferred between different enclosures on a daily basis to
facilitate animal husbandry and exhibit maintenance. This procedure is particularly relevant in the
management of great apes living in zoos, where the requirements of functional management must be
balanced with the desire to maintain enriching and naturalistic exhibit enclosures that benefit ape
residents and attract the visiting public. In these settings, examinations of ape behavior and welfare
typically focus exclusively on activity in the primary exhibit area. However, physical, social and sensory
experiences unique to each area may shape different patterns of behavior. In the current study, zooliving chimpanzees and gorillas were moved each day from exhibit areas to off-exhibit holding areas for
a short duration as a part of regular management procedures. Behavioral data indicated species-specific
reactions to the holding area, including increased aggression and self-directed behavior by chimpanzees
and increased activity and prosocial behavior among gorilla subjects. Both species showed more feedingforaging behavior while in the exhibit enclosure. Results suggest that holding areas may not meet all
behavior needs of captive great apes and demonstrate the importance of including all components of the
captive enclosure in comprehensive analyses of great ape behavior and welfare. Am. J. Primatol.
72:951–959, 2010.
r 2010 Wiley-Liss, Inc.
Key words: captivity; chimpanzee; gorilla; enclosure alternation; management; behavior; welfare
INTRODUCTION
In many facilities, captive animals may spend
some proportion of their time in a secondary
enclosure, distinct from the primary environment.
Some agricultural animals are restricted to indoor
pens during winter months [O’Connell & Leonard,
1997; O’Driscoll et al., 2009] and laboratory-housed
animals may be shifted between enclosures to
facilitate regular cage disinfecting schedules [Duke
et al., 2001; Mitchell & Gomber, 1976]. In zoos,
animals including great apes are commonly moved
from their exhibit space to an off-view holding area
on a daily basis. This standard practice of moving
animals to separately enclosed night-quarters during
the evening hours has been used for decades. In an
informal survey of the management practices for
chimpanzees housed at zoos accredited by the
Association of Zoos and Aquariums (AZA), 85% of
the responding institutions (N 5 31) reported that
chimpanzees spend more than 12 hr per 24-hour day
in this off-exhibit space [Ross, unpublished data].
Despite this large proportion of time spent in the
holding area, very few behavioral evaluations of zoohoused apes include data from off-exhibit spaces. As
such, evaluations of activity that cease when the
r 2010 Wiley-Liss, Inc.
animals leave on-exhibit housing may fail to identify
changes in behavior that impact the overall welfare
of captive animals.
In most zoological settings, holding areas for
apes often differ substantially from exhibit spaces in
both design and function. Although modern ape
exhibits are often lush, naturalistic enclosures
featuring a high degree of environmental complexity,
holding areas are designed with primary attention to
functionality. Traditionally, these uniform and lowmaintenance spaces are often constructed of concrete
and steel mesh, with limited or no outdoor access, are
typically smaller in volume and more constraining
than the exhibit enclosure, and are more akin to
conventional indoor laboratory housing [Hediger,
1969; Maple & Finlay, 1986; Maple & Perkins, 1996].
Contract grant sponsor: Leo S. Guthman Foundation.
Correspondence to: S.R. Ross, Lester E. Fisher Center for the
Study and Conservation of Apes, Lincoln Park Zoo, 2001 North
Clark Street, Chicago, IL 60614. E-mail: sross@lpzoo.org
Received 2 February 2010; revised 12 May 2010; revision
accepted 5 June 2010
DOI 10.1002/ajp.20857
Published online 7 July 2010 in Wiley Online Library (wiley
onlinelibrary.com).
952 / Ross et al.
A survey of zoo ape exhibits (circa 2001) indicated
that across 11 AZA-accredited zoos in northern
climates, the average size of the exhibit was over
40 times bigger than the holding space available to
those same ape groups (E 5 4,812.75 m2; H 5 11.43 m2)
[Lukas & Ross, unpublished data]. Additionally, in
holding areas, apes may experience unique forms of
food availability, social access and human interaction, including specialized training and management
activity surrounding medical procedures [Beisner &
Isbell, 2008; Caws & Aureli, 2003]. These attributes
may shape ape behavior in ways distinct from those
that characterize the exhibit area.
The influence of systematic alternation between
enclosures on ape behavior has been addressed
primarily in the context of testing various social
density hypotheses as apes move between enclosures
of very different sizes and compositions. In a study
of long-term, seasonal transfers between large outdoor areas and smaller indoor winter housing,
Nieuwenhuijsen and de Waal [1982] found relatively
little evidence of a negative ‘‘crowding’’ effect and
relatively small increases in aggression, activity, and
locomotion while in the smaller indoor area. However, they suggested that these social strategies may
change in the context of shorter-term alternations.
When Aureli and de Waal [1997] investigated such
short-term (o5 days) alternation between a small
indoor space and a larger indoor–outdoor enclosure,
they found that chimpanzees’ social behavior
(grooming and agonism) decreased in frequency in
the smaller area. Videan and Fritz [2007] found a
similar effect when observing female chimpanzees,
whereas males tended to show increased affiliative
behavior in the smaller indoor space. Similar studies
have been conducted on other great ape species with
even more variable results. Cordoni and Palagi
[2007] studied the alternation of gorillas between
large outdoor enclosures and much smaller indoor
enclosures and found increased self-directed behavior, touching, and reconciliation, but no change in
agonism in the smaller area. Hoff et al. [1997]
similarly found an increase in self-directed behaviors
and low-intensity social interactions among gorilla
subjects in the holding area, additionally accompanied by increased aggression. Forthman et al. [1993],
the only other known study to examine daily
alternation between zoo exhibits and holding areas,
found that Sumatran orangutans showed few behavioral differences, despite substantial differences in
the size and complexity of the spaces.
Together these studies offer mixed results as to
the effect of regularly moving zoo-housed apes
between different types of enclosures and leave open
questions regarding the potential welfare and
management implications of these alternations.
Facility-related differences in enclosure type and
management indicate the need for a comparative
approach within a single setting to reliably document
Am. J. Primatol.
the behavioral influences of different enclosure
components on multiple ape species [Stoinski et al.,
2001]. Most notably, authors of the previous studies
admit to the potential confounding factor of outdoor
access, as animals were only allowed to access the
outdoors in the larger (low density) spaces. In the
current study, daily alternations between two very
different, but indoor, spaces will be investigated. We
compared behavioral differences expressed by zoohoused chimpanzees and gorillas in an indoor,
naturalistic exhibit and a smaller, indoor off-exhibit
holding area, where the animals were held during
daily exhibit maintenance. We predicted that, in
association with the smaller size, lack of environmental complexity, and different human interaction
patterns, subjects in the holding area would show
depressed activity and increased rates of anxietyrelated behavior, including self-directed and stereotypical activity. Characterizing the expression of
behavioral differences between holding and exhibit
spaces will further elucidate ape behavioral reactions
to different captive environments, contribute to our
understanding of daily management strategies for
gregarious great ape species, and ultimately affect
efforts to improve psychological well-being.
METHODS
Subject and Housing
Subjects were seven chimpanzees and seven
gorillas, housed at the Regenstein Center for African
Apes (RCAA) at Lincoln Park Zoo (Chicago, IL)
(Table I). The Lincoln Park Zoo is an accredited
member of the Association of Zoos and Aquariums
and all management and data collection procedures
herein reported complied with all state and federal
animal care and welfare regulations and the standards set forth in the American Society of Primatologists Principles for the Ethical Treatment of
Nonhuman Primates.
Subject characteristics are included in Table I.
The chimpanzee group included three males and
four females ranging in age from 8 to 25 years. The
gorilla group included one adult male, four adult
females and two juveniles ranging in age from 4 to 28
years. All subjects had comparable diets, exposure to
TABLE I. Subject Demographics
Chimpanzees
Name
Hank
Optimus
Kipper
Cashew
Kathy
Nana
Chuckie
Gorillas
Sex
Age
Name
Sex
Age
Male
Male
Male
Female
Female
Female
Female
17
9
8
23
17
14
8
Jojo
Azizi
Makari
Bahati
Tabibu
Rollie
Susie
Male
Male
Female
Female
Female
Female
Female
28
4
21
17
16
11
3
Ape Behavior and Enclosure Alternation / 953
humans, training and enrichment experience, and
opportunity for outdoor access. Subjects in both
groups also had similar levels of experience with and
exposure to a number of noninvasive behavioral and
cognitive research protocols.
The two housing areas of interest were the
publically viewed, naturalistic exhibit space (hereafter the ‘‘exhibit’’) and the off-view, hardscape,
basement-level holding space (hereafter the ‘‘holding
area’’). All apes slept in their exhibit overnight and
every morning (at approximately 8 am), they voluntarily moved from the exhibit to the downstairs
holding areas at the request of animal care staff.
During the period of study, shifting compliance of
the apes averaged 99% for gorilla subjects and 92%
for chimpanzees. Although chimpanzee and gorilla
subjects differ in terms of shifting experience in
previous facilities, all subjects have been managed
with comparable protocols since entering the current
facility in 2004.
The holding areas were composed of a set of six
individual enclosures around a central keeper area,
making a distinct ‘‘suite’’ for each social group
(10.8 m2) (Figs. 1 and 2). Upon reaching the holding
area, each ape participated in a short period of
husbandry training and received its daily morning
ration of fruit and primate chow (the bulk of each
ape’s daily diet, including produce and primate chow,
was provided later in the day, scattered in the exhibit
area). During this time, individual apes were
physically separated from each other (visual and
olfactory access were maintained) for short periods
depending on factors such as age, training experience, and other management and research protocols.
Following exhibit maintenance, all apes were
returned to the public exhibit at approximately
10 am. These naturalistic enclosures consisted of
natural and artificial climbing elements, elevated
nesting platforms and a deep mulch substrate (Fig. 3).
Enclosures measured 109 m2 for gorillas and 124 m2
for chimpanzees. From 10 am until 5 pm, zoo visitors
were present at varying densities and were separated
from the ape exhibits by a glass barrier. Immediately
upon entry to the exhibit from the holding area, apes
had access to scattered foraging resources (including
produce, grains, and chow). Though an adjacent
outdoor yard was available to the apes during warm
weather, this study is limited to times when the apes
were restricted to their indoor spaces only. In both
indoor enclosures, temperature was electronically
regulated to maintain a consistent 201C.
Fig. 2. Chimpanzee subjects in a single enclosure in a holding
area suite, during a period of free access (following training and
research protocols). Photograph was taken from the central
caretaker area.
Hallway observation area
Human management area
Fig. 1. Schematic representation of a typical holding area suite
for an individual chimpanzee or gorilla social group at the
Regenstein Center for African Apes. Shaded areas indicate
animal enclosures; noncolored areas are sections of human
activity (caretakers and data collectors). [Color figures can be
viewed in the online issue, which is available at www.inter
science.wiley.com.]
Fig. 3. A representative indoor on-exhibit enclosure for the focal
gorilla group at the Regenstein Center for African Apes. The
exhibit enclosure provided the primary housing for subjects, was
the site of most feeding activity, and included natural and
artificial climbing structures, a mulch substrate and multiple
areas of exploratory enrichment. Periods of free access to a large
outdoor yard (excluded from the data set) was provided through
exhibit-wide rear glass windows.
Am. J. Primatol.
954 / Ross et al.
Data Collection
Behavioral data were collected on the apes in the
exhibit during public hours (10 am–5 pm) 5 days a week,
across all social, environmental, and management
conditions. Holding area data were typically collected
between 8 and 10 am each weekday. In both settings,
observations were recorded using 10-minute focal
animal follows with a 30-second intersample interval
on a handheld computer [Pocket Observer 2.0, Noldus
Observer, Noldus Information Technology, 2003]
employing a 40-item ethogram. Immediately before
the initiation of each data collection session, observers
recorded the size of the public crowd on a four-point
scale, ranging from the absence of visitors (only familiar
staff were present) (‘‘0’’) to the presence of more than
50 visitors in the immediate exhibit area (‘‘3’’).
Eight observers (staff not directly involved in
ape training or care) collected holding and exhibit
area data on the apes. Each observer met an
interobserver reliability criterion, which required a
mean 85% agreement with the first two authors
during live data collection sessions conducted on at
least four individuals in each social group. Observations of the apes in their exhibit area were taken
from the public visitor floor and mezzanine-level
observation areas. Three of the trained and tested
observers also collected data in the holding area.
Data collection in that context began only after all of
the social groups had entered their individual
holding suites, all training and/or other experimental
testing were complete, and all management staff had
left the immediate area. Subjects in the holding area
were observed unobtrusively from a hallway adjacent
to the front of the enclosures, separate from the area
in which training interactions occurred. During
observation periods, subjects had free access to all
group members and typically all sections of the
holding suite.
Data Analysis
Data were collected over the course of 15
months, between September 2007 and January
2009. To minimize variability associated with environmental factors while in the exhibit enclosure, we
utilized only those data collected while subjects were
restricted to their indoor enclosure. The resulting
data set comprised 208 hr of observations collected in
the exhibit as well as the 73 hr collected in the
holding area.
Raw counts of each behavior on the ethogram
were calculated for each area (exhibit and holding)
and combined into 12 behavioral categories for
analysis (Table II). The in-view behavioral frequencies for each subject were averaged across sessions
and compared between areas first using a Multivariate Analysis of Variance (MANOVA) with a
critical a level of 0.05. We subsequently compared
Am. J. Primatol.
TABLE II. Behavioral Categories Used
Analysis (From a 40-item Ethogram)
in
Data
Behavior
Defining criteria
Abnormal
Subject engages in idiosyncratic or
stereotypical behavior, including
coprophagy and regurgitation
Subject directs an agonistic gesture
(contact or noncontact) toward a
conspecific
Subject directs a sustained (3 sec) gaze to
enclosure or maintenance areas while
adjacent to the enclosure barrier
Subject actively consumes, searches for
and/or collects items for ingestion
Subject rests or is motionless
Subject moves more than 1 body lengths
in any direction
Subject interacts with a feature of the
environment, including natural and
non-natural items
Subject engages in an affiliative
interaction with a conspecifc
Subject rakes the fingers over the skin in
long, brusque strokes
Subject touches, manipulates or examines
the body, skin, or hair
Subject engages in copulation,
masturbation, and/or manipulation of
the genitals
Subject engages in a boisterous and
nonpurposeful bout of nonsocial
activity
Aggression
Attention
Feed/forage
Inactivity
Locomotion
Object
manipulation
Prosocial
Scratching
Self-directed
Sexual
Solitary play
Proximity
Close
Subject is within 1 m of or in direct
contact with the nearest neighbor
rates of each behavior between areas using paired
t-tests with a Bonferroni-adjusted a level of 0.05.
Although previous research suggested that the
behavior of apes at this facility is not significantly
affected by the presence of zoo visitors [Ross et al.,
2008; Milstein & Ross, in preparation], there is
sufficient concern about these potential effects to
include them in our analyses. Before conducting any
statistical tests that compared holding and exhibit
spaces, we determined if there were significant
effects of crowd size on behavior in the exhibit area
using a two factor MANOVA (species crowd size).
Because the holding area is a restricted-access
location, all holding area-based data collection
occurred in the context of a ‘‘0’’-level crowd size
(staff only) and hence was not included in the crowdsize analysis.
RESULTS
Crowd Size Effects
We conducted preliminary analyses to determine
potential effects of human presence on behavior in
Ape Behavior and Enclosure Alternation / 955
TABLE III. Rates of Focal Behaviors Produced by Subjects in the Exhibit and Holding Areas
Mean frequency (%) (SE)
Behavior
t-Value (df 5 6)
P-Value
Exhibit
Holding
(a) Chimpanzee subjects
Abnormal
Aggression
Attention
Feed-forage
Locomotion
Object manipulation
Prosocial
Scratching
Self-directed
Sexual
Solitary play
1.4
2.8
2.3
5.6
0.3
1.0
0.6
2.5
2.8
0.5
1.5
0.2
0.03
0.06
0.001
0.8
0.3
0.6
0.04
0.03
0.6
0.2
3.8
0.1
0.7
18.1
8.2
7.0
17.3
0.4
12.3
1.0
0.0
Proximity
Close
4.1
0.006
46.8 (0.04)
57.6 (0.05)
(b) Gorilla subjects
Abnormal
Aggression
Attention
Feed-forage
Locomotion
Object manipulation
Prosocial
Scratching
Self-directed
Sexual
Solitary play
0.8
2.3
1.9
5.4
2.9
1.1
2.5
1.4
2.3
2.4
2.3
0.5
0.06
0.1
0.002
0.03
0.3
0.04
0.2
0.06
0.05
0.06
3.2
0.1
1.8
30.6
7.2
5.0
4.1
0.2
11.7
0.1
0.6
2.7
0.7
4.4
5.4
11.6
6.7
8.2
0.6
18.0
0.0
1.8
Proximity
Close
2.5
0.049
21.2 (0.06)
the exhibit enclosure. A two-way MANOVA (Wilks’ l),
with the factors of species and crowd size in the
exhibit area did not indicate a main effect of crowd
size on behavior (F(22,52) 5 1.34, P 5 0.19) or a
species crowd size interaction (F(22,52) 5 1.31,
P 5 0.21). As such, we did not include crowd size in
the subsequent analysis and consider resulting
behavioral patterns to emerge from environmental,
sensory and management differences between the
holding and exhibit areas.
Location Effects
A two-way MANOVA indicated significant main
effects of species (F(10,15) 5 9.20, Po0.001) and
location (holding vs. exhibit) (F(10,15) 5 6.8,
P 5 0.001), but no species location interaction
effects (F(10,15) 5 1.23, P 5 0.35). As a result, we
conducted the subsequent paired t-tests independently for each species.
Chimpanzees
Behavior and proximity rates shown by the
chimpanzees in both exhibit and holding areas are
(0.01)
(0.001)
(0.002)
(0.02)
(0.01)
(0.007)
(0.02)
(0.001)
(0.02)
(0.003)
(0.00)
(0.02)
(0.001)
(0.005)
(0.05)
(0.01)
(0.02)
(0.02)
(0.001)
(0.03)
(0.001)
(0.004)
2.8
0.5
2.5
10.5
8.6
8.2
18.8
1.6
17.4
1.1
0.4
(0.01)
(0.002)
(0.007)
(0.01)
(0.01)
(0.02)
(0.03)
(0.004)
(0.02)
(0.003)
(0.002)
(0.02)
(0.003)
(0.02)
(0.007)
(0.02)
(0.02)
(0.04)
(0.003)
(0.03)
(0.001)
(0.009)
27.9 (0.07)
shown in Table IIIa. Compared with their behavior
on exhibit, chimpanzees demonstrated higher rates
of aggression (t(6) 5 2.8, P 5 0.03) in the holding
area, though at relatively low rates in both locations.
Scratching behavior (t(6) 5 2.5, P 5 0.04) and selfdirected behavior (t(6) 5 2.8, P 5 0.03) also
occurred significantly more often in the holding
area. Chimpanzees showed higher rates of feeding
and foraging while on exhibit (t(6) 5 5.6, P 5 0.001).
In the holding area, chimpanzees were more frequently within close proximity to group mates
(t(6) 5 4.1, P 5 0.006). There was no location effect
on the other behavioral categories.
Gorillas
Rates of behaviors in each area are shown in
Table IIIb. Gorillas performed higher rates of
locomotion (t(6) 5 2.9, P 5 0.03) and prosocial behavior (t(6) 5 2.5, P 5 0.04) in the holding area, and
increased feeding and foraging behavior (t(6) 5 5.4,
P 5 0.002) in the exhibit area. Gorilla subjects
also showed increases in aggression (t(6) 5 2.3,
P 5 0.06), self-directed behavior (t(6) 5 2.3, P 5 0.06)
Am. J. Primatol.
956 / Ross et al.
and solitary play (t(6) 5 2.3, P 5 0.06) in the
holding area and increased sexual behavior in the
exhibit enclosure (t(6) 5 2.4, P 5 0.05) at levels that
approached significance. As with chimpanzees, gorillas maintained higher rates of close proximity in
the holding area (t(6) 5 2.5, Po0.05). There were
no location effects on the other behavioral categories.
DISCUSSION
This is one of the few examinations of the effects
of the regular zoological practice of systematically
alternating African great apes between smaller,
functional holding spaces and larger, complex indoor
exhibits on a daily basis. Unlike former studies of
regular alternations between differential spaces, this
investigation does not include data from an outdoor
space, therefore limiting that potentially confounding variable. The results of this study suggest that
these very different environments produce distinct
behavioral patterns for both chimpanzees and
gorillas. Consideration of these differences and the
motivational factors that cause them is important to
promoting optimized environments for captive primates in a variety of settings.
The holding and exhibit areas exposed apes to
unique combinations of many sensory categories.
Along with the overt contrast in size and complexity, the two areas also differed with respect to
cross-species presence and human interaction,
senvironmental factors such as ambient light, and
management variables, including the daily time of
exposure (subjects were housed in the holding area
only for a short period in the morning, and
transferred to the exhibit area during a later, nonoverlapping period of data collection). The extent of
these differences limits the ability to relate changes
in behavior to a particular feature of environment.
Although we expect that size and complexity were
especially significant factors, the current interpretation emerges from a consideration of the holistic
experience of each area rather than an attempt at a
feature-based comparison.
Within this broad comparison, both species
showed evidence of a behavioral sensitivity to the
change in enclosure type, whereas observed species
differences suggest an influence of species traits on the
particular nature of this response [Lukas et al., 2003].
Chimpanzee patterns were generally more robust
than that of gorillas, occurred in a wider range of
behavioral categories and were consistent with a
negatively arousing response to the smaller and less
complex holding area. Gorillas offered a less clearly
interpretable reaction to the holding area. Subjects
demonstrated increased prosocial behavior and locomotor activity in holding—both frequently identified
as indicators of beneficial changes in welfare. These
patterns were accompanied by behavioral changes
suggestive of a negative reaction: there was a five-fold,
Am. J. Primatol.
though nonsignificant, increase in rates of aggression
in holding, and a 54% increase in self-directed
behavior that reached statistical significance when
the adult male gorilla was removed from the data set.
These different reactions may reflect species-typical
forms of reactivity and sociality in interaction with
attributes unique to the holding enclosure. Other
work has suggested that chimpanzees demonstrate a
weak control over response inhibition [Boysen &
Berntson, 1995, 1996, 2001] and are potentially
impulsive in their responses, compared with gorillas
[Wagner & Ross, 2010]. This factor may be important
in interpreting the wider-ranging and more robust
response to the holding area exhibited by chimpanzee
subjects. Conversely, location effects on gorilla social
behaviors may reflect the species-typical social avoidance and dispersal strategies in interaction with
holding area-constraints on social proximity [Lonsdorf
et al., 2009; Ross et al., in preparation; Stoinski et al.,
2002].
In the Regenstein Center for African Apes,
holding spaces were, on average, 9.3% of the size of
exhibit spaces. Consistently, both species showed
evidence of increased ‘‘crowding,’’ as demonstrated
by the increase in close proximity to nearest
neighbor in the holding area. Results of strict
density-effect studies on ape behavior remain variable, with several hypotheses in question. The
tension-reduction model predicts that great apes
should increase affiliative behaviors, but decrease
aggressive behavior as a means of actively reducing
the risk of fighting [Videan & Fritz, 2007]. Alternatively, the conflict-avoidance hypothesis, in which
subjects react to increased densities by decreasing all
social interactions (i.e. both affiliative and aggressive
behavior), has also garnered empirical support in
studies of great apes [Aureli & de Waal, 1997]. In the
current study, chimpanzees showed a significant
increase in aggressive behavior in the holding area;
though, across species, rates of aggressive encounters
in both settings were very low and only rarely
resulted in the need for veterinary intervention
(during the 15-month data collection periods, there
were no wounding events that required immobilization). The increase in agonism shown by chimpanzees is consistent with the density-aggression model
[Calhoun, 1962], in which increased social density
resulted in increased aggression, as demonstrated in
rodents [Gregor et al., 1972; Van Loo et al., 2001] and
some old world monkeys [Alexander & Roth, 1971;
Boyce et al., 1998; Elton & Anderson, 1977].
The increase in prosocial behavior exhibited by
gorillas may have similarly emerged from the change
in social density experienced in the holding area,
potentially in combination with an increase in
perceived risk and/or rates of aggression. The
significant space reduction of the holding area may
have made ineffective gorillas’ typical dispersal
strategy, causing them to rely instead on a partly
Ape Behavior and Enclosure Alternation / 957
effective affiliative coping strategy that may have
counteracted aggressive outcomes.
It is also possible that this change, along with
the observed activity increase, was an expression of
eustress, elicited by the positively arousing aspects of
the holding area (e.g. provisioning of high-value
foods and reinforced human interactions). Future
work that compares behavior around ‘‘holdingtypical’’ interactions that occur in exhibit areas (i.e.
exhibit-based training sessions) may shed light on
these opposing interpretations.
Within the context of the current literature on
enclosure alternation, the chimpanzee increase in
agonism contradicts other reports showing no
change in aggressive behavior [Nieuwenhuijsen &
de Waal, 1982] and either an increase [Videan &
Fritz, 2007] or decrease [Aureli & DeWaal, 1997] in
prosocial behavior. Effects on gorilla social interactions were consistent with the Cordoni and Palagi
[2007] analysis, which indicated a similar rise in
prosocial behavior with a nonsignificant increase in
aggression. Hoff et al. [1994, 1997] also observed
increased prosocial behavior in a holding area, along
with an associated increase in aggression, among
infant and adult gorillas and among adult gorillas
alone. This cross-study observation of increased
affiliation is suggestive of a species-wide trend.
However, the numerous differences in such analyses,
including the confounding provisioning of outdoor
access in previous work, largely limit the ability to
generalize results or connect patterns to characteristics of group composition, duration-of-stay, and
management interactions unique to the holding area.
Further inter-facility examinations with comparable protocols in zoological settings may offer the
needed sample size to better illuminate the particular factors that influence the relationship between
agonism, prosocial behavior, and social density
among captive great apes.
The unique configuration of the holding area
likely also played a role in shaping the overall rate of
all social interactions observed in that setting.
Characteristic visually and physically constrained
paths may have increased the probability of individuals meeting a group mate, increasing the rate of all
social interactions in general. These incidental meetings, along with an expected, associated increase in
mixed-sex and mixed-dominance status encounters,
may have exacerbated competition, influenced perception of vulnerability and heightened arousal
levels to additionally motivate the specific type of
social response produced, in interaction with both
species and facility characteristics [Baker & Aureli,
1996; Erwin & Deni, 1979; Maple, 1979; Maple &
Finlay, 1986; Wilson, 1982].
As might be predicted by this paradigm, anxietyrelated behaviors including scratching and selfdirected behaviors increased for chimpanzees in the
holding area. The change in gorilla self-directed
behavior only approached significance, contradicting
the Cordoni and Palagi [2007] report. It is possible
that the absence of this expected increase in the
current analysis stems from the positive experience
of the holding area, in combination with the
(predictably) short duration of daily exposure. However, as Cordoni and Palagi noted, comparatively few
reports have examined the connection between SDB
and arousal in gorillas. Preliminary analyses conducted by the authors also suggest that cognitive
stress in gorillas, such as that experienced in the
context of a computerized testing paradigm, is
associated with very short-duration self-touches
[Wagner & Ross, unpublished data], rather than
the brusque scratches exhibited by chimpanzee
[Baker & Aureli, 1997; Leavens et al., 2001, 2004;
Wagner & Ross, 2008]. Hence, the lack of change in
levels of gorilla SDB does not conclusively contradict
the pattern of increased arousal indicated by other
reports. In other species, increased locomotion
(‘‘nervous energy’’) has been used as an index of
anxiety [Casper, 2006; Gygax et al., 2008]. The
observed increase in this category by gorillas in the
holding area may reflect subjects’ redirection of
arousal along alternative behavioral channels, with
rates potentially further increased as a method of
active social dispersal in the more constrained
holding area. However, this potential association is
inconsistent with other reports for gorillas, which
found, for example, increased inactivity in an indoor
holding area [Hoff et al., 1997]; such differences may
again indicate the interaction with facility-specific
characteristics.
The ability to generalize these results to other
facilities is dependent on structural and space
differences in both holding and exhibit areas, as well
as the degree to which the observed behavior changes
are related to duration of stay in each area. The apes
in this study were typically provided access to their
most complex and enriching environment (the
exhibit) for the greatest proportion of their day. As
a result, the time spent in holding was substantially
less than 85% of AZA-accredited facilities that house
resident apes in comparable holding areas for more
than 12 hr per day [Ross, unpublished data]. There is
evidence that animals with longer-duration daily
experience in a holding area, a ‘‘night quarters,’’
demonstrate a preference for these areas [Stoinski
et al., 2001] and that long-term alternations between
spaces differ from shorter-term alternations [Videan
& Fritz, 2007]. In these cases, apes may demonstrate
fewer behavioral changes between enclosures due to
subject use of the area moreso as an extension of the
home ‘‘territory’’ [Forthman et al., 1993; Ogden
et al., 1990; Stoinski et al., 2001].
Nonetheless, responses to the holding area
indicate that, even over short periods, apes are
sensitive to the unique characteristics that define
enclosure areas in a captive facility. In general, the
Am. J. Primatol.
958 / Ross et al.
holding area was the setting of a greater frequency
of arousal-related and agonistic interactions for
chimpanzees. Holding area-effects on behavior were
more variable for gorillas, but suggested some
association with increased social density and potentially also reflected increased arousal. It is notable
that for both species, gross changes in behavior were
generally limited and not exclusively negative:
abnormal behaviors showed no change across settings and gorillas showed increases in typically
‘‘positive’’ behaviors, including prosocial behavior.
If these patterns persist across studies, then entire
facilities (including both exhibit and holding enclosures) may be further improved by integrating
favored elements of each setting into the other
[Stoinski et al., 2002]. Interfaces for holding-typical
caretaker interactions in the exhibit enclosure may
minimize necessary time spent in a holding area and
facilitate the transition between areas. An increase
in the number of enrichment and feeding opportunities and the opportunity for outside access in the
holding area may further converge exhibit and
holding behavior patterns, while preserving the
functionality of the area for management purposes.
As a result of these findings, we advocate
consideration of species-typical functional, physical,
and social preferences in designing enclosure components, particularly including those intended for
management activities [Boese, 1990]. Ape sensitivities to location also demonstrate the need for
comprehensive evaluations of behavior in each
enclosure area occupied by captive apes, regardless
of frequency of use. The current welfare evaluation
paradigm must be extended with this recognition
that captive ape needs must be addressed in every
component of the captive environment.
ACKNOWLEDGMENTS
The authors respectfully thank Maureen Leahy
and the RCAA carestaff for their cooperation in
facilitating this study, Michelle Marquart for help
with peripheral analyses, and the Fisher Center
intern staff for their careful data collection. Thanks
also to the Leo S. Guthman Foundation for their
financial support of the Lester E. Fisher Center for
the Study and Conservation of Apes.
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