Correlates of
self-directed and stereotypic behaviours in
captive red-capped mangabeys (Cercocebus
torquatus torquatus)
Lisa Reamer,Zena Tooze, Claire Coulson,
Stuart Semple
Centre for Research in
Evolutionary Anthropology, Roehampton
University, Holybourne
The quantification of behaviours linked to
anxiety or stress provides a powerful means to
address applied questions related to the
well-being of captive animals. This study
explored correlates of two such behaviours
&endash; self-directed (SDB) and stereotypic
behaviour (STB) &endash; among captive
red-capped mangabeys, Cercocebus torquatus
torquatus. Study animals were held at two sites
run by CERCOPAN, a primate sanctuary in Nigeria.
At the first site (Calabar), animals were housed
in traditional cage enclosures, while at the
second (Rhoko), they lived in a semi-free
ranging environment. Analyses revealed that
while animals at the two sites did not differ in
time spent in SDB (self-scratching,
self-grooming, yawning and body shaking),
animals at Calabar showed a higher prevalence
of, and spent more time in STB (pacing and head
rolling). There were no significant differences
in time spent in SDB or STB between the sexes,
or between captive-born and wild-born animals. A
positive correlation was found between age and
time spent in SDB, but not between age and time
spent in STB. Finally, positive relationships
were found between time spent in SDB and both
time spent grooming and time spent being
groomed; no relationships were found between
grooming behaviour and STB. As stress and
anxiety can have detrimental effects on
psychological well-being, physical health and
reproduction, these findings have important
implications for the captive welfare and
conservation of red-capped mangabeys, and also
potentially of other endangered vertebrate
species.
1. Introduction The study of anxiety
and stress among animals in captivity has
important implications for welfare and
management (Moberg and Mench, 2000). The
non-human primates represent particularly
important animals for studies of this kind
(Honess and Marin, 2006a). This is due primarily
to ethical concerns about the well-being and
potential for suffering of such animals
(Wolfensohn and Honess, 2005). In addition, and
closely related to this issue, is the potential
impact of poor welfare on the health and
reproduction of animals in captive breeding
programmes for endangered species (Cockrem,
2005; Swaisgood, 2007). Understanding the
factors linked to anxiety and stress levels in
captivity, and investigating how animals might
mediate these levels in such environments
represent, therefore, important goals.
Quantification of self-directed and stereotypic
behaviours provides a powerful, noninvasive tool
to address these issues.
Behavioural and pharmacological evidence
from a range of primate species indicates that
self-directed behaviours (SDB &endash;
self-scratching, self-grooming, yawning
and body shaking) provide an index of anxiety
(Maestripieri et al., 1992a). While some SDBs,
most notably selfgrooming or scratching, may
normally have hygienic functions (Maestripieri
et al., 1992a; Ventura et al., 2005), SDB rates
have been observed to increase markedly in
situations likely to elicit anxiety, such as
when in close proximity to a dominant animal
(olive baboons, Papio anubis: Castles et al.,
1999), or after aggression (chimpanzees, Pan
troglodytes: Fraser et al., 2008). Manipulations
designed to reduce anxiety have also been seen
to lower SDB levels; for example, in captive
red-capped mangabeys, Cercocebus torquatus
torquatus, environmental enrichment in the form
of seeds and litter was found to be associated
with a decline in rates of SDB's (Blois-Heulin
and Jubin, 2004). Maestripieri et al. (1992b)
found that administration of an anxiogenic drug
increased the rate of selfscratching among
infant rhesus macaques, while administration of
an anxiolytic reduced the rate of body shaking.
Two other measures of SDB &endash; self-grooming
and yawning &endash; were unaffected by
either treatment. Schino et al. (1996) found
that combined rates of three SDBs
(self-scratching, self-grooming and body
shaking) in captive long-tailed macaques, M.
fascicularis, increased after administration of
anxiogenic drugs, and decreased when anxiolytic
drugs were given.
Stress has been implicated as a key risk
factor in the development and maintenance of a
range of primate stereotypic behaviours (STB)
(Honess and Marin, 2006a; Novak et al., 2005a).
Both early social deprivation and later social
isolation/separation are closely linked to the
occurrence of STB in rhesus macaques (review by
Novak et al., 2005b). In the same species, it
has been found that exposure to stimuli
associated with stressful experiences such as
capture (Cross and Harlow, 1965) or electric
shock (Gluck et al., 1985) can trigger or
increase the frequency of stereotypies.
Furthermore, pharmacological evidence supports
the role of anxiety in maintaining stereotypic
behaviour patterns. Hugo et al. (2003) found a
reduction over time in STB among a group of
vervet monkeys, Cercopithecus aethiops, given
fluoxetine (Prozac1), with no such reduction
seen in a control group. Similarly, Prosen and
Bell (2001) reported that selective serotonin
reuptake inhibitor treatment significantly
reduced STB in a male bonobo, Pan paniscus,
displaying marked behavioural problems linked to
abnormal rearing conditions.
A number of environmental parameters may
affect the anxiety or stress experienced by
captive primates. Key factors in this regard are
the nature and size of the captive environment.
Semi-free ranging environments are more
naturalistic than caged enclosures and typically
have a lower density of individuals; both
factors may be expected to be associated with
improved welfare. Where animals are kept in
traditional cage enclosures, larger and more
enriched cages have been linked to reduced
levels of aggression (Honess and Marin, 2006b),
a major factor impacting on psychological
well-being.
As well as this extrinsic factor, a range of
intrinsic parameters may also be related to the
anxiety and stress experienced by individuals in
captivity, perhaps the most important of which
are sex, age and rearing history. Lutz et al.
(2003), for example, found that stereotypic
(including self-injurious) behaviours were more
common among male than female captive rhesus
monkeys; Mallapur et al. (2005), by contrast,
found that female captive lion-tailed macaques,
M. silenus, showed higher rates of self-grooming
than did males. Fittinghoff et al. (1974)
proposed that stereotypic behaviour may change
with age in male rhesus macaques, with the
repertoire of such behaviours decreasing as
individuals get older. Finally, Mallapur et al.
(2005) provided evidence that rearing history
can also affect the expression of abnormal
behaviours in captive lion-tailed macaques; no
STBs were seen in any wild-born animals, whereas
captive-born animals did exhibit such repetitive
behaviour.
Animals experiencing anxiety or stress in
the captive environment may attempt to mediate
these states behaviourally. In particular, it
has been suggested that grooming may have an
important tension-reduction function (Terry,
1970). In support of this hypothesis, Schino et
al. (1988) found evidence in long-tailed
macaques that the receipt of allogrooming from
females reduced males' self-directed behaviour.
In addition, an association between the receipt
of grooming and lowered heart rates has been
documented in rhesus macaques (Aureli et al.,
1999) and pig-tailed macaques, M. nemestrina
(Boccia et al., 1989). More recently, Shutt et
al. (2007) provided evidence that the giving of
grooming may also provide stress-reducing
benefits: in this study of female Barbary
macaques, M. sylvanus, the amount of grooming
given was negatively associated with long term
stress levels, as assessed from faecal
concentrations of glucocorticoid
metabolites.
The current study investigated factors
linked to SDB and STB among captive red-capped
mangabeys (C. torquatus torquatus). Time spent
in SDB/STB was first compared between animals in
different sized cages and between different
enclosure types (cage enclosure or semi-free
ranging). The relationships between SDB/STB and
sex, age, and rearing history (captive-born or
wild-born) were then examined. Finally, the
relationship between SDB/STB and grooming
behaviour was investigated.
