Applied Animal Behaviour Science 103 (2007) 255–264

www.elsevier.com/locate/applanim

Group size: Determinants in the wild and implications

for the captive housing of wild mammals in zoos§
Elizabeth E. Price a, Tara S. Stoinski a,b,*
a
Zoo Atlanta, 800 Cherokee Avenue, Atlanta, GA 30315, United States
b
The Dian Fossey Gorilla Fund International, United States

Available online 10 July 2006

Abstract
Group size is one of the most important factors influencing the formation and maintenance of successful
social groups in captivity. For zoos, appropriate social groupings are of the utmost importance to provide
examples of species-typical behaviors, as well as attain captive breeding goals. In the wild, group-living
evolved largely in response to the need for predator avoidance and territory defense. The number of
members in wild groups is a fundamental determinant of individual fitness, affecting net food intake and
reproductive success. Captive animals encounter different environmental pressures than their wild counter-
parts; food availability and predation are no longer concerns, however they still face competition for mates
and are unable to make the social adjustments necessary to decrease social tension. As such, group size has a
large impact on the behavior, welfare and reproductive success of captive animals. Depending on the
species, suboptimal sizes can be associated with increased abnormal behaviors and decreased reproductive
success and infant survival in a range of captive mammals. However, in the absence of environmental
constraints, many species can be housed in a greater diversity of social groups than observed in the wild.
Thus, a key component of captive housing is flexibility.
# 2006 Elsevier B.V. All rights reserved.

Keywords: Group size; Captivity; Reproduction; Behavior

1. Introduction

In this paper, we will examine how group size influences the behavior of captive mammals. As
an introduction, we will start by examining the factors that influence group size in the wild, and

§
This paper is a part of special issue entitled ‘‘Too many, too few: The effects of group size and density in captive
animals’’ Guest Edited by Dr. Inma Estevez.
* Corresponding author. Tel.: +1 404 624 5826; fax: +1 404 624 5841.
E-mail address: tstoinski@zooatlanta.org (T.S. Stoinski).

0168-1591/$ – see front matter # 2006 Elsevier B.V. All rights reserved.
doi:10.1016/j.applanim.2006.05.021
256 E.E. Price, T.S. Stoinski / Applied Animal Behaviour Science 103 (2007) 255–264

how group size in turn affects the behavior and adaptive mechanisms employed by group-living
animals in response to their environment. We will then discuss how captivity exerts a different
range of pressures on animals than those faced in the wild and how appropriate group size, as well
as structure, affect the behavior and reproduction of zoo animals. We will conclude with the
importance of maintaining a flexible approach in terms of group size and structure when housing
wild animals in captivity. Given our backgrounds as primatologists and the wealth of literature on
this taxonomic group, our discussions will focus on primates; however, where appropriate we
will include references to other species, although we acknowledge that our discussion of other
species is by no means a comprehensive one.

2. Group size

2.1. Determinants of group size in the wild

Mammalian sociality shows enormous variation, with animals living as solitary individuals to
members of groups that number in the hundreds. Group living has been shown to confer a number
of benefits to its members, such as increased predator detection and intergroup competitive
ability, but is also associated with costs, specifically increased intragroup competition and
disease transmission (Alcock, 2001; Davies et al., 1991; Loehle, 1995; Müller and Soligo, 2005;
Wilson, 2000). The balance of these costs and benefits, which are influenced by the species’
ecological niche, determines group size. The number of group members in turn affects the social
structure and adaptive mechanisms used by individuals to exploit their environment. Group size
is therefore a fundamental determinant of individual fitness in group-living animals (Alexander,
1974; Alcock, 2001; Fedigan, 1992).
There are a large number of studies on the effects of group size on the social behavior of
nonhuman primates. All primates reside in some form of social group; even the least social
nocturnal prosimian species live in dispersed polygynous groups (Fedigan, 1992; Müller and
Soligo, 2005; Müller and Thalmann, 2000; Pimley et al., 2005). Factors such as habitat type and
activity cycle have been shown to have a large effect on group size, primarily because of
predation. Species living in areas where the risk of predation is greater (i.e. open country and
savannah as opposed to forests) or that are more exposed to predation (i.e. terrestrial species as
opposed to arboreal species) are typically found in larger groups (Crook and Gartlan, 1966; Hill
and Lee, 1998; Richard, 1985). Smaller nocturnal species rely on their inconspicuousness to
avoid detection, whereas larger diurnal species cannot escape notice and therefore depend upon
larger social groups to avoid predation (Clutton-Brock and Harvey, 1977; Müller and Soligo,
2005; Richard, 1985). There are, however, exceptions. For example, orangutans (Pongo
pygmaeus) are unique in that they are diurnal, large bodied primates yet live relatively solitary
lives. As an arboreal species, however, they have no large treetop predators, and do not need the
benefit of a social group for protection. Primarily frugivores, they feed from widely dispersed
food sources, therefore larger groups would necessitate longer foraging times and greater
traveling distances in order to feed all group members.
Intragroup competition for resources, specifically food and mates, is also a major factor
influencing group size. With respect to food resources, as group size increases, competition
between group members often increases, which results in increased foraging efforts and
decreased encounter rates with food (Janson, 2000; Müller and Soligo, 2005; Sterck et al., 1997).
Lemurs (Eulemur spp.), for example, are faced with a nutritionally stressful environment in
which resources are seasonally scarce leading to high rates of competition. Having fewer group
 E.E. Price, T.S. Stoinski / Applied Animal Behaviour Science 103 (2007) 255–264 257

members minimizes the level of intragroup competition, therefore lemurs are found in smaller
group sizes as compared to other primates (Curtis, 2004). In a study of two groups of red colobus
monkeys (Procolobus badius), Gillespie and Chapman (2001) found that the larger group had to
traveled farther and faster and rested less than the smaller group due to rapid food patch
depletion. Some species adapt to this problem by living in a fission–fusion group composition to
increase net food intake. Chimpanzees (Pan troglodytes), orangutans (P. pygmaeus) and spider
monkeys (Ateles paniscus) all have flexible group sizes and will break into smaller groups when
food is scarce, thereby decreasing competition (Richard, 1985; Fedigan, 1992; Chapman et al.,
1995; Sterck et al., 1997).
For folivorous primate species with abundant food resources, the risk of infanticide, not food
availability, may set the upper limit on group size. Steenbeek and van Schaik (2001) found that
some Thomas langurs (Presbytis thomasi) live in small groups despite the relative abundance of
food and low costs of feeding competition. In such cases, smaller groups are preferable because
larger groups tend to have a higher risk of take-over by competing males, which is often
accompanied by infanticide. Watts (2000) found female mountain gorillas to prefer living in
larger, multi-male groups, despite the potential for increased feeding competition, presumably
because of the risk of infanticide.
Group size is a potent determinant of infant survival in cooperatively breeding primates. In
callitrichid species, both male and female offspring remain in the family group and assist
extensively in the rearing of young. Infant survival is directly correlated with the number of
available helpers in several callitrichid species (cotton-top tamarins (Saguinus oedipus): Savage
et al., 1997; common marmosets (Callithrix jacchus): Rothe et al., 1993; Geoffroy’s tamarins
(Saguinus geoffroyi): Kuhar et al., 2003). Larger group sizes ensure more individuals to assist
with infant carrying, thereby reducing energetic costs, and also increase predator detection and
foraging efficiency (Savage et al., 1996).
Alike to the findings in nonhuman primates, studies on other mammals have shown similar
effects of the combination of social and ecological pressures (Carbone et al., 1997; Spong, 2002;
Stokes et al., 2003). Social carnivores are an excellent example. Although the vast majority of
carnivores are solitary, approximately 15% have evolved to live in social groups (Vucetich et al.,
2004). Carbone et al. (1997) suggest that a number of factors contributed to this evolution,
namely territorial defense, communal rearing of young, cooperative hunting and defending prey
from scavengers. In many social carnivores, home range defense is paramount and in contests
over space, larger groups usually dominate smaller ones (Spong, 2002). Larger group sizes also
improve carnivore hunting success. As group size increases, both the number of successes and the
size of the prey killed increase, as well as the control over potential scavengers (Carbone et al.,
1997; Courchamp et al., 2002). The benefit of scavenger protection must then be balanced with
the increased cost of intragroup competition, favoring intermediate group sizes (Courchamp
et al., 2002). This trend has been found in a number of cooperative hunters (wild dogs (Lycaon
pictus): Courchamp and Macdonald, 2001; Courchamp et al., 2002; lions: Spong, 2002; wolves
(Canas lupus): Vucetich et al., 2004).
Finally, the communal rearing of young practiced by many social carnivores also necessitates
larger groups, again checked by intragroup competition. As with cooperatively breeding primates,
offspring survival in wild dogs has been directly correlated with the number of available helpers
(Courchamp and Macdonald, 2001). Likewise, as previously stated, hunting success is related to
the size of the hunting party, and baby-sitters left behind to protect young from predation detract
from this size. The need for group members is so essential in wild African dogs that whole packs
cannot survive below a critical group size (Courchamp and Macdonald, 2001).
258 E.E. Price, T.S. Stoinski / Applied Animal Behaviour Science 103 (2007) 255–264

2.2. The importance of group size in captivity

Optimal group size for captive wild animals is determined by different factors than those faced
in the wild. Environmental pressures such as the availability of resources and predation are
controlled in captivity; animals experience little to no competition for food or predation risk. As a
result, group size is often more flexible in captivity than in the wild. But captivity also poses a
number of challenges with respect to group size, specifically, limited space, genetic
considerations, and decreased opportunities for animals to make social adjustments to alleviate
social tension or find breeding partners. As such, active management with knowledge of the
social structure, reproductive biology, and social needs of each species is essential.
Inappropriately sized groups, both too small and too large, can have a number of negative
consequences on the behavior, welfare, and reproduction of captive animals. The most extreme
example is of normally social animals kept in social isolation. Studies across a number of species
have demonstrated social isolation to be associated with high levels of stereotypic behaviors,
incompetent social and reproductive behaviors, and chronic stress (Carlstead, 1996; Erwin and Deni,
1979; Lewis et al., 2000; Watts and Meder, 1996). Negative effects are also seen if animals are
socially housed but groups are too small. For example, in callitrichids, group size is considered the
most significant predictive factor for infant-rearingsuccess;largergroupshave more helpers and thus
increased infant survival (Bardi et al., 2001; Kuhar, 2003; Leong et al., 2004). Additionally, captive
breeding of drills (Mandrillus leucophaeus) and gorillas has improved through housing animals in
larger, more diverse groups, as opposed to isolated pairs (Maple and Hoff, 1982; Cox, 1997).
Often less mentioned are the negative effects of animals kept at high densities. In primates,
overcrowded groups often show higher levels of aggressive and stress-related behaviors (Elton,
1979; Ha et al., 1999; Plowman et al., 2005). Similar results have been found in ungulates:
increased social density is correlated with increased stereotypic licking in giraffes (Giraffa
camelopardalis), okapi (Okapi johnstoni) and horses (Equus cabullus) (Bashaw et al., 2002;
Redbo et al., 1998). In one of the most dramatic examples, Barnes et al. (2002) found that ‘‘the
group size in which they [duikers] are managed has proved to be critical in the successful
management of these species’’ (p. 111). Groups housed in five or more animals resulted in stress-
related jaw abscesses, and strikingly, when groups were reduced to pairs, trios, or single
individuals, the average life span increased from under 5 years up to 10 years.
Effects of high-density conditions on reproduction can also be substantial. Pig-tailed
macaques (Macaca nemestrina) housed in overcrowded conditions suffered from decreased
gestation length and an increase in aborted fetuses as compared to those housed in smaller groups
(Timmermans et al., 1981; Ha et al., 1999). Felids housed in multiple male/female groups have
reduced reproductive success as compared to those housed in pairs, perhaps because of decreased
semen volume and smaller testes (Swanson et al., 2003) and number of litters produced (Mellen,
1991). The density of males and/or females has been correlated with reduced reproductive rates
and/or life-spans in black rhinoceros (Diceros bicornis), white rhinoceros (Ceratotherium
simum), elephants (Loxodonta africana; Elephas maximus) and wildebeest (Connochaetes spp.;
Laws, 1969; Watson, 1969; Carlstead et al., 1999; Seror et al., 2002). This problem is manifested
in delays in first age of reproduction, longer inter-birth intervals and premature senescence.

2.3. The importance of group structure and the external environment in captivity

Although the focus of this paper is the effect of group size on captive animals, we feel we
would be remiss if we did not mention the influences of group structure and composition as well.
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A group could be of optimal size yet meet few of the social, reproductive or psychological needs
of an individual if the structure and composition are not appropriate. A well-cited example is
reproductive suppression in callitrichids. For many callitrichid species, housing multiple females
together often results in the reproductive suppression of the subordinate female (Epple, 1970;
Baker et al., 2002; Dietz, 2004). The behavioral effects can also be much more subtle than the
complete lack of reproduction. For example, in male gorillas, maternal relatedness and/or early
familiarity are thought to be important for affiliation among adult male gorillas (Robbins, 1996;
Stoinski et al., 2004a). Although unrelated adult males introduced in late adolescence can coexist
in a bachelor group, intragroup relationships under such conditions often provide fewer social
benefits.
It is also important to consider the external environment within the animals’ sensory range
(Newberry, 1995). For territorial species, the presence of nearby groups has been shown to affect
behavior. Small felid species with visual access to large felids, which can prey upon them in the
wild, and without adequate cover had higher levels of cortisol than those provided with shelters
and without visual access (Carlsted et al., 1993; Swanson et al., 2003). Cotton-top tamarins with
visual access to other groups showed higher levels of non-contact aggression and stress-related
behaviors than those without access (De Waal, 1989; Savage et al., 1996; Kuhar et al., 2003).
Kuhar et al. (2003) found that Geoffroy’s tamarins housed with visual, auditory, and olfactory
access to other groups were more likely to practice cannabalism and be abusive towards
offspring than those with reduced access. However, the presence of nearby conspecifics can also
have a positive effect. For example, although mongoose (Eulemur mongoz) and black lemurs
(Eulemur macaco) are found most often in pairs in the wild, when housed in isolated pairs in
captivity, they have very low reproductive rates. Hearn et al. (1996) suggest that this problem can
be alleviated by the social facilitation of reproduction. Specifically, for these species,
the presence of additional nonreproducing males is associated with significantly greater rates
of reproduction—more than 500% increase in mongoose lemurs, and 100% in black lemurs
(Hearn et al., 1996). Similar social facilitation of reproduction has been found in captive
cheetahs (Acinonyx jubatus), birds, red pandas (Ailurus fulgens), and aye-ayes (Daubentonia
madagascariensis) (Caro, 1993).

2.4. Flexibility in captive social size and structure

As previously stated, social group size and structure have physical and psychological effects
on the well-being of captive wild animals, therefore when arranging social groups, zoos often try
to mimic the structures seen in the wild. However, given that captivity lifts some of the earlier
mentioned constraints on group size – specifically, competition for food resources – we often see
increased flexibility in group size and structure in species housed in captivity as compared to the
wild.
For example, constraints of space, as well as exhibitry needs of zoos, have led to the housing of
many naturally solitary animals in social groups. The housing of orangutans provide one of the
more striking examples. In the wild, orangutans are found alone or in small social units, males and
females often interacting only for brief mating consorts. This is largely a result of few benefits of
group living (orangutans have limited predation) and high costs (orangutans depend on widely
dispersed food resources). In captivity, where food resources are guaranteed, orangutans are
successfully housed with conspecifics at most institutions. Such housing conditions provide a
number of benefits for orangutans, including social stimulation and opportunities to observe
maternal care, which could help later parental functioning (Bond and Watts, 1997). Adult males,
260 E.E. Price, T.S. Stoinski / Applied Animal Behaviour Science 103 (2007) 255–264

who perform virtually no role in the rearing of offspring in the wild, have been found to interact with
infants affiliatively, even exhibiting play behavior (Horr, 1977; Zucker et al., 1978; Maple and Hoff,
1982; Munn and Fernandez, 1997; Zucker, 1994). Alternatively, high levels of reproductive success
have also been achieved through the introduction of males and females only for breeding purposes
(Markham, 1990).
Not all species exhibit such flexibility. Many felid species, the majority of which are solitary in
the wild, are often housed in pairs or trios in zoos. Although this arguably provides a source of
social enrichment, it can also be a source of chronic stress (Mellen et al., 1998) and as previously
discussed can negatively affect reproductive success (Swanson et al., 2003). One solution is to
alternate incompatible pairs on exhibit or house solitary cats with visual and/or olfactory access
to conspecifics. The recent presence of a conspecific often stimulates increased investigatory and
scent-marking behaviors (Mellen et al., 1998). This rotation strategy can be an effective tool with
many species, stimulating species typical foraging and reproductive behavior (Hosey, 2005;
Lukas et al., 2003; White et al., 2003).
Additionally, although captive environments may limit competition for food, competition for
mates still exists. For this reason, polygynous species, particularly those that live in single-male,
multi-female groups, pose a particular problem for captive management. Under such social
systems not all males have female social partners, as there are generally an equal number of male
and female infants born into the population. Surplus males have traditionally either been housed
in social isolation or placed in an all-male group. Solitary housing of these animals is undesirable
for many of the reasons listed above. All-male groups, although generally transitory in the wild,
are often a successful long-term solution to providing social housing for surplus males (Lindburg
et al., 1997; Stoinski et al., 2004a,b). However, the optimal group size is often smaller for all-
male than breeding groups (Stoinski et al., 2004b) and group composition is often an important
component of their success (Stoinski et al., 2004a,b).
Problems can also arise for polygynous species that live in multi-male groups. In
chimpanzees, for example, intragroup male aggression in the wild is often intense and
occasionally lethal (Alford et al., 1995; DeWaal, 1998). Similar behavioral patterns are seen in
captivity and can be exacerbated by space constraints and the limited ability for groups to fission
and fuse as they would in the wild (Alford et al., 1995). Although severe social conflict might be a
natural part of chimpanzee interactions in the wild, such behavior must be closely monitored in
captive animals, and many zoos have adopted the conservative approach of housing only single-
male groups. Although such groupings work, this strategy creates a surplus of males and limits
the complexity of male social life. As a result, the Chimpanzee Species Survival Plan is working
to help zoos form and manage multi-male groups.
Flexibility is required not only in terms of actual group size and structure but also in the
methods used to introduce and arrange social groups. Animals are shifted frequently in zoos to
imitate natural migratory and dispersal patterns found in the wild and meet genetic breeding
needs. Potential stressors can be identified and minimized by careful planning. Introducing
individuals with familiar conspecifics can reduce stress, as has been observed in lion-tailed
macaques (Lindburg et al., 1997), whereas male-male introductions are generally smoother if
males are introduced before reaching maturity (Alford et al., 1995; Lindburg et al., 1997; Stoinski
et al., 2004a,b; Pullen, 2005). Methods of introduction can even affect long-term stability of a
group; for example, it has been hypothesized that age-constant groups of male gorillas show
higher long-term success than age-graded groups (Stoinski et al., 2004b).
Problems created by artificial group sizes and/or structures can also be remedied by the quality
of space provided. If the group size is too large, or during situations when social tension might be
 E.E. Price, T.S. Stoinski / Applied Animal Behaviour Science 103 (2007) 255–264 261

higher, adequate escape paths and visual barriers can decrease tension. Increasing the structural
complexity of the environment can also stimulate species appropriate behavior and help diffuse
high concentrations of animals by providing vertical space. Strategically placed visual barriers
can also help reduce the possible perceived threat of the public. All of these practices in turn can
assist reproduction.
All captive environments are ‘‘complex dynamic systems’’ (Newberry and Estevez, 1997, p.
56) which should be viewed as a combination of many different elements. By combining
knowledge of species-specific needs with careful exhibit planning, zoos can house captive
animals in a wider range of social groupings than found in the wild, stimulating species-
appropriate behaviors in a socially enriching environment.

3. Conclusion

The four missions of modern zoos include research, education, conservation, and recreation.
Meeting these goals requires the adequate and appropriate housing of the animals in their care.
Appropriate housing should result in reproduction so that captive populations are available for
research and education. In addition, such housing should stimulate the expression of species-typical
behaviors, which may enhance animal well-being and educate visitors. As the studies highlighted in
this paper have shown, the size and structure of a group in which an animal is housed influences its
social and reproductive behaviors, as well as its physiological and psychological well-being. For
many species, particularly carnivores or territorial species, living in groups that most closely
replicate the wild in terms of size and structure is optimal. Other species may be more flexible,
particularly if a primary constraint on sociality in the wild is access to food resources. Some species
remain unsustainable in captivity, and although it is assumed that this is in part a result of the social
element of captive management, we have yet to isolate the actual mechanisms at work. Social
groupings in captivity should therefore be reevaluated based upon new information gained from
studies of wild populations (Brown, 2000; Freeman et al., 2004). This complex interaction between
a species’ ecological niche, its evolutionary heritage, and the factors influencing its sociality means
that there is no one correct approach for housing wild animals in captivity. Instead, zoo managers
must take into consideration a multitude of factors and continually monitor and research the effects
of various social groupings on the species in their care.

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