Restricting animals to different areas of
their enclosure, for both brief and extended
durations, is a key element of animal management
practices. With such restrictions, available
space decreases and the choices the animals can
make are more limited, particularly in relation
to social dynamics. When unfamiliar individuals
are introduced to each other, group dynamics can
be unpredictable and understanding space usage
is important to facilitate successful
introductions.
We studied the behavioral, welfare-related
responses of two groups of zoo-housed
chimpanzees (n = 22) as they were introduced to
each other and experienced a variety of
enclosure restrictions and group composition
changes. Our analysis of available space while
controlling for chimpanzee density, found that
arousal-related scratching and yawning decreased
as the number of enclosure areas (separate
rooms) available increased, whereas only yawning
decreased as the amount of available space (m2)
increased.
Allogrooming, rubbing, and
regurgitation/reingestion rates remained
constant as both the number of enclosure areas
and amount of space changed. Enclosure space is
important to zoo-housed chimpanzees, but during
introductions, a decrease in arousal-related
scratching indicates that the number of
accessible areas is more important than the
total amount of space available, suggesting that
it is important to provide modular enclosures
that provide choice and flexible usage, to
minimize the welfare impact of short- and
long-term husbandry needs.
INTRODUCTION
An important element in the captive
management of animals is safely moving groups
between enclosure areas to allow care staff to
provide for the animals' needs [Hosey et ah,
2009]. Husbandry requirements may
temporarily limit animals to off-exhibit areas
for cleaning or maintenance purposes [e.g.,
Ross et ah, 2010] and sections of enclosures
might be closed off on a long-term basis for
major events such as animal introductions
[e.g., Schel et ah, 2013]. Additionally,
zoos in temperate climates have to deal with the
challenges of temperature fluctuations and
inclement weather, prompting animal care staff
to occasionally limit animal access to indoor
areas (e.g., when moats freeze over [de
Waal, 1982]). Even when access is permitted
during inclement weather, animals may choose to
stay indoors [Ross et ah, 2011]. As a
result, the space (m ) and number of available
enclosure areas (separate rooms) often
change.
This may lead to shifts in behavioral and
social opportunities, making it important to
understand the impact of short- and long-term
spatial restrictions on animal welfare.
Individuals often indicate strong location
preferences; however, suggest¬ing that
having a choice of locations may be more
important for optimal welfare than overall space
availability [Ross et ah, 2011].
Crowding and space availability impact
social relationships with an increased
likelihood of social conflict under higher
density conditions [Judge, 2000].
Primates are known to employ different
strategies to mediate the stressors of
high-density situations: The conflict-avoidance
model describes when social interactions
decrease during short-term conflict management
[Judge and de Waal, 1993]. The
tension-reduction model occurs when affiliative
behaviors are increased and aggressive behaviors
are decreased during long-term conflict
management [de Waal, 1989]. With many
captive habitats consisting of two or three
separate areas (e.g., one outdoor enclosure and
one indoor enclosure, often with an indoor,
off-exhibit area), restricted access decreases
the degree of choice animals have regarding
location and interactions [Ross et ah,
2011]. This can lead to an increase in
negative behaviors, such as stereotypies and
aggression (e.g., giant pandas [Owen et ah,
2005]; great apes [Ross et ah,
2010]).
Although social contact is essential for
gregarious species, if social interaction only
fills 10% of a chimpanzee's day in the wild
[Pruetz and McGrew, 2002], is it
desirable to encourage captive situations in
which interactions are unavoidable
[Schapiro, 2003]? Over the past few
decades, we have increased our awareness of the
importance of enclosure design, group density,
and the ability to form subgroups on the
behavior of chimpanzees (Design&emdash;usage
[Traylor-Holzer and Fritz, 1985];
Design&emdash;differences within facilities
[Ross and Lukas, 2006; Ross et ah,
2010]; differences between facilities
[Jensvold et al., 2001; Ross et ah,
2009]; Density [Nieuwenhuijsen and de
Waal, 1982; Aureli and de Waal, 1997; Videan and
Fritz, 2007]; Fission-fusion [Bloomsmith
and Barker, 2001; Amici et ah, 2008; Clark,
2011]), providing helpful background
information for facility design and renovation.
The impact of enclosure size is of particular
concern as it is often limited due to practical
as well as financial constraints.
Previous research has identified few
behavioral changes in relation to differences in
enclosure size, suggesting that we should focus
our resources on other enclosure elements (e.g.,
opportunities for enrichment, foraging, and
socialization) rather than enclosure size alone
[Line et ah, 1991]. For example,
although aggression was higher in an indoor
enclosure than a larger outdoor enclosure, the
increase was not proportionate to the difference
in spatial density in these two areas
[Nieuwenhuijsen and de Waal, 1982].
Chimpanzees may use strategies to avoid conflict
by reducing social interaction when space is
restricted on a short-term basis [Judge and
de Waal, 1993; Aureli and de Waal, 1997; Videan
and Fritz, 2007]. They may use other coping
strategies to reduce aggression at higher
spatial densities for longer durations (e.g.,
increase affiliative behavior and decrease
aggressive behaviors [de Waal, 1989];
increase of self-directed (e.g., scratching) or
abnormal behaviors
Although the internal states of animals are
difficult to assess, we can look to specific
behavioral indicators as a means to evaluate
their well-being, particularly self-directed
behaviors (SDBs: scratch, rub, and yawn) and the
abnormal behavior, regurgitation/reingestion
(R/R). Known as dis¬placement behaviors,
SDBs are considered to be a redirection of
behavior when the animal is uncertain about how
to behave [Maestripieri et ah, 1992].
Scratching, in particular, has been well studied
and increased rates are linked to social changes
that have the potential to produce negative
outcomes, such as proximity of other groups
[Aureli and de Waal, 1997; Baker and Aureli,
1997]. Regurgitation/ reingestion, on the
other hand, is considered to be an abnormal
undesirable behavior and was exhibited by the
individuals in one of the two groups included in
this study. Although R/R has been well studied
[e.g., Baker and Easley, 1996; Lukas, 1999;
Hill, 2007; Struck et ah, 2007], there are
several suggestions regarding its etiology
(e.g., to cure boredom, to taste an enjoyable
food again, as a coping mechanism, etc.), making
it difficult to eradicate. The functional
significance of allogrooming is widely known as
more than simple hygiene [Dunbar, 1991]
and has been linked to the development of
relationships and group formation, as it has
shown to reduce negative outcomes [Baker and
Aureli, 2000]. Given that these behaviors
may serve as coping mechanisms, variations in
frequency and duration may indicate a change in
welfare conditions.
When managing animal introductions or other
social issues (e.g., separating individuals to
create a bachelor group), sustained restrictions
on social groupings and available enclosure
space are inevitable [e.g., McDonald, 1994;
Brent et ah, 1997; Fritz and Howell, 2001; Seres
et ah, 2001]. Despite the best efforts of
care staff to minimize the impact of social
upheavals and provide active and enriched lives
for those going through the introduction
process, these changes have a substantial impact
on their physical and social opportunities. This
study examines the impact of changes in
available space and enclosure areas (number of
separate rooms) for chimpanzees as two groups
merged. Group mergers can prove acutely
challenging for individuals and require careful
monitoring, as many group size and enclosure
availability changes take place during the
process. We examined chimpanzee self-directed
behaviors, and regurgitation/reingestion in
varying combinations of enclosure number, size,
and group density situations, to assess how
these factors might impact upon welfare.
DISCUSSION
When considering available space in
captivity, density studies are often at the
forefront; however, the results of this study do
not directly translate to previous group density
research in terms of group size. While group
composition frequently changed as a result of
the introduction process, group composition in
previous research remained constant [e.g.,
Nieuwenhuijsen and de Waal, 1982; Aureli and de
Waal, 1997; Videan and Fritz, 2007].
Thinking of density in terms of low versus high
amounts of space in addition to the number of
individuals provides a broader understanding of
how enclosure size and design relate to
behavior.
Although the available space in terms of the
number of areas and the m available varied
during the introduction process, an analysis of
group density across the number of available
areas indicates that density alone does not
explain our findings. Group density decreased
from one to two areas, but remained comparable
when comparing two to three areas, while
behavioral changes (scratching and yawning) were
only seen in the latter comparison, suggesting
that those changes were a product of the number
of accessible areas rather than absolute space
available or density. Although high density
situations can increase social tension
[Aureli and de Waal, 1997] and the
likelihood of social conflict [Judge,
2000], having an increased choice of
different locations ameliorates the impact of
social density and suggests that location
preferences for social groupings may be a result
of their visual proximity to other
individuals.
We would expect allogrooming, an affiliative
behav¬ior, to fluctuate in accordance with
a known coping strategy to manage social density
changes [e.g., de Waal, 1989]. Given the
relative stability of density across the number
of areas, however, the consistency of
allogrooming shown in this study is fitting. As
a result, we looked to known indicators of
anxiety or uncertainty (SDBs) and an abnormal
behavior (R/R) to identify the perception of
available space in terms of the number of areas
versus size of the accessible
While scratching and yawning decreased as
the number of accessible enclosure areas
increased (from two to three areas), scratching
did not decrease as available space increased.
This contradicts previous density research where
both yawning and scratching increased when less
space (high density) was available [Aureli
and de Waal, 1997]. Since scratching did not
decrease as available space (m ) increased and
the observed behaviors did not increase or
decrease over the introduction phases in a way
that clearly reflected desensitization or
sensitization to the introduction process, it
suggests that having the choice of where to be
or who to be with (particularly when three
options are provided) is more important than the
amount of space available or total density.
Choice and control are important aspects of
animals' lives [Sambrook and Buchanan-Smith,
1997; Badihi, 2006; Meehan and Mench, 2007;
Buchanan-Smith, 2010]. Previous research
suggests that great apes avoid open spaces
[Traylor-Holzer and Fritz, 1985; Ogden et
ah, 1993; Stoinski et ah, 2002; Ross et ah,
2011] and exhibit preferences for enclosure
elements that provide: oppor¬tunities to
escape from conspecifics (doorways, even if they
were closed), security (corners), or interaction
with keepers (mesh walls [Ross and Lukas,
2006]). When individuals were allowed to
choose to be together or in different areas, we
saw a reduction in SDBs. Access to three areas,
regardless of overall space, provided the
greatest decrease in these behaviors suggesting
that the ability to exhibit choice and
preferences when it comes to their physical
location plays an important role in the welfare
of captive chimpanzees [e.g., Ross et ah,
2011].
Zoos are often restricted when it comes to
the amount of space available for animal
enclosures, but by working with what is
available (or when designing new exhibits) and
incorporating separate areas or perhaps visual
barriers into enclosures, the concept of choice
can be provided, potentially without the cost of
a larger enclosure. While the impact of visual
barriers was not specifically isolated in this
study, they provide similar opportunities as
separate areas (e.g., hide, reduce eye contact,
etc.) and could be a low-cost option for
alleviating the social pressure of space
restrictions [e.g., Chamove et al., 1984;
Reinhardt and Reinhardt, 1991; Westergaard et
al., 1999; Stoinski et al., 2004; Coe et al.,
2009]. This is not to suggest that the
overall amount of space is irrelevant. While
usable space should always be a consideration
for the physical and psychological well-being of
the species being housed [e.g., Ross
andLukas, 2006; USDA and APHIS, 1991a,b],
the number of separate areas within the
enclosure during the introduction process also
seems to be important for the psychological
health of the animal.
With regards to R/R, no changes were seen in
relation to the number of areas or available
space. It is important to note that for the
Beekse Bergen group (the only individuals in
this study who exhibited R/R) nearly every
aspect of their daily lives had recently changed
and they were continually getting used to an
unfamiliar environment, with both unfamiliar
staff and chimpanzees. Although other behaviors
were influenced by enclosure access, this might
suggest that for this group of chimpanzees,
space restrictions or coping mechanisms
[Lukas, 1999] were not the underlying
reasons behind their performance of R/R.
The variety of enclosure areas within
Budongo Trail exhibit offered the residents many
choices. The Beekse Bergen group could often be
found in the smaller, off-exhibit area; their
previous experiences in a laboratory environment
likely determined their spatial decisions in the
new enclosure [e.g., Novak et al., 1992;
Duncan et al., 2013]. The freedom to choose
to be in this preferred area might have assisted
in their adjustment to life in the new enclosure
and in the larger, integrated group. However, it
can be difficult to disentangle additional
influences such as the strengthening of existing
close bonds within the original Beekse Bergen
group [Schel et al., 2013] and
preferences for different location
characteristics (e.g., off-exhibit versus
on-exhibit, small and enclosed versus large and
open, concrete floors versus biofloors,
etc.).
One challenging aspect of the choice concept
is striking a balance between what is best for
the animal, for example, tending to the animals'
need for physical exercise and to benefit from
being outdoors in nice weather (e.g., vitamin D
from the sun) with their need to "feel safe"
indoors in smaller areas. Although data
measuring the impact of different life histories
in relation to choice are lacking, there has
been a recent focus on the long-term outcomes
for chimpanzees with atypical life histories
(e.g., former entertainment or pet chimpanzees
[Ross and Vreeman, 2013]; former
biomedical laboratory chimpanzees
[Kalcher-Sommersguter et al., 2013]).
The question of providing optimal levels of
choice without compromising welfare is likely to
be an on-going discussion and challenge for zoos
and sanctuaries, particularly in relation to
animals with atypical life histories. However,
despite strong preferences for specific
locations, there is no evidence suggesting that
smaller enclosures could improve welfare
[Ross et al., 2011].
CONCLUSIONS
1. Enclosure space is important to
chimpanzees [Ross and Lukas, 2006; Ross et
al., 2009], but the number of different
areas is more important than the total amount of
space during chimpanzee introductions.
2. When designing orrefitting enclosures,
multiple areas should be provided to allow
chimpanzees to exercise choice [Markowitz,
1982] over where they are and to whom they
are near, particularly during animal management
scenarios that involve space restrictions.
3. Increased flexibility, in terms of the
potential configurations of access to multiple
areas, is important for reducing the negative
welfare impact of both short- and long-term
animal management decisions.
4. While increased flexibility in enclosure
choice might be an expected result for
fission-fusion species like chimpanzees, given
that captivity and the introduction process
reduces social choices so greatly for most
species, it is likely to be important for many
other animals in captive environments.
