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Applied Animal Behaviour Science 115 (2008) 211–220

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Visitor effects on anxiety in two captive groups of

western lowland gorillas
Gemma Carder *, Stuart Semple
Centre for Research in Evolutionary Anthropology, School of Human and Life Sciences,
Roehampton University, London SW15 4JD, UK
Accepted 4 June 2008
Available online 11 July 2008

Abstract
There is growing interest in examining the effects that visitors have on the welfare of zoo primates. Most
recently, the importance of evaluating the combined impacts of visitors and management practices on
anxiety levels of these animals has been highlighted. Studies that take such an approach have the potential
not only to highlight how visitors affect the welfare of zoo primates, but also how these impacts may be
mediated by management interventions, such as enrichment. The aim of this study was to explore the
potential impact of visitor numbers on behavioural indices of anxiety among western lowland gorillas in two
UK zoos, Port Lympne and Chessington, and to determine whether feeding enrichment mediates any such
visitor effects. During fifteen minute focal watches, visitor numbers were assessed and all occurrence data
collected on two behavioural indices of anxiety: self-scratching and visual monitoring of visitors. Data
collected at each site were divided according to whether they were taken during periods of feeding
enrichment, or during periods when no such enrichment was being given. Analyses revealed no evidence for
a visitor effect at Chessington, with durations of self-scratching and visual monitoring unrelated to visitor
number, either during periods of enrichment or outside of such times. At Port Lympne, durations of both
self-scratching and visual monitoring were positively associated with visitor number when no feeding
enrichment was taking place; no such relationships were seen, however, during periods of feeding
enrichment. Potential reasons for the difference between sites in the occurrence of visitor effects, and
for the absence of visitor effects during feeding enrichment at Port Lympne are discussed. The results of this
study highlight the importance of assessing visitor effects on the same species at multiple sites, and also
suggest that such effects may be reduced by positive management approaches.
# 2008 Elsevier B.V. All rights reserved.

Keywords: Gorillas; Zoos; Visitors; Enrichment; Welfare

* Corresponding author. Tel.: +44 7889891551.

E-mail address: Gemma765@aol.com (G. Carder).

0168-1591/$ – see front matter # 2008 Elsevier B.V. All rights reserved.
doi:10.1016/j.applanim.2008.06.001
212 G. Carder, S. Semple / Applied Animal Behaviour Science 115 (2008) 211–220

1. Introduction

In recent years there has been a significant increase in the number of zoo-based studies that
have explored the relationship between visitors and zoo animals, in particular non-human
primates. While some studies have found evidence that zoo primates find visitors enriching
(Cook and Hosey, 1995), the majority have found evidence indicative of an aversive effect of
visitors (reviewed by Hosey, 2000, 2008). Most often, this evidence takes the form of changes in
behaviour of the animals linked to visitor presence or number. These behavioural changes
include a decrease in affiliative social behaviours (Wood, 1998; Todd et al., 2007), an increase in
antagonistic behaviours (Wells, 2005; Kuhar, 2008) or both (Mallapur et al., 2005; Glaston et al.,
1984). Alternatively, or in addition, impacts of visitors on behavioural indices of anxiety have
been considered (e.g. Wells, 2005; Cooke and Schillaci, 2007). The latter type of study, focussing
directly on behavioural measures linked to negative emotional state, provide an invaluable tool to
assess the impacts of visitors on the psychological well-being of zoo animals.
Two such indices of anxiety are self-scratching and visual monitoring. Experimental and
observational studies on a range of old world primate species indicate that self-scratching is
linked to underlying levels of anxiety. For example, long tailed macaques (Macaca fascicularis)
given anxiogenic drugs show increased rates of self-scratching, while administration of
anxiolytic drugs reduces the rates of this behaviour (Schino et al., 1996). Scratching has also been
observed to increase in situations likely to elicit anxiety, such as when in close proximity to a
dominant animal (Papio anubis: Castles et al., 1999), after aggression (Macaca fuscata: Schino
et al., 2007) or during separation from offspring (Macaca mulatta: Maestripieri, 1993).
Behavioural evidence also indicates that visual monitoring may provide a further tool to assess
anxiety. Maestripieri (1993), for example, found that rhesus macaque mothers spent less time in
visual monitoring as their infants grew older and thus less vulnerable to aggression. Watts (1998)
found that female mountain gorillas (Gorilla beringei) spent more time monitoring potentially
aggressive conspecifics, such as adult males or other females with which they had agonistic
relationships. Visual monitoring may reflect anticipation of potentially dangerous situations
(Maestripieri, 1993) and such monitoring of visitors in a zoo environment may thus be linked to a
perceived threat from them (Cooke and Schillaci, 2007).
Despite the growing interest in assessing impacts of the zoo environment on the welfare of
primates, there remains an urgent need to assess the interaction between these impacts and factors
such as enclosure design and management practices (Hosey, 2005). As management
interventions such as enrichment may improve welfare, they have the potential to ameliorate
the negative impacts of visitor presence, number or behaviour. To our knowledge only one study
has assessed the potential interaction between enrichment and visitor effects. In this study of
captive chimpanzees (Pan troglodytes), high crowd numbers were found to reduce the frequency
of a number of key behaviours in the presence of both new and one day old enrichment (Wood,
1998). Thus, visitor effects were found in the presence of enrichment but the potential role of
enrichment in reducing these effects was not assessed, as their magnitude was not compared
between times when enrichment was present and those when it was not.
In addition to investigating visitor effects with respect to other aspects of the zoo environment,
it is also crucial to investigate variation in visitor effects within single species, whether such
variation occurs between individuals at the same site, or between sites (Hosey, 2005). This is
particularly true in the case of species for which contrasting results have been found in different
groups; the western lowland gorilla is one such species. A study by Wells (2005) at Belfast
Zoological Gardens found that during periods of high visitor numbers, significantly more
 G. Carder, S. Semple / Applied Animal Behaviour Science 115 (2008) 211–220 213

intergroup aggression occurred, as well as increased frequency of abnormal behaviours and self-
grooming. Kuhar (2008) looked at visitor effects on two groups of captive western lowland
gorillas (a family and bachelor group) both housed at Disney’s Animal Kingdom. While no
behavioural evidence of a visitor effect was found in the family group, in the bachelor group there
was an increase in aggression during high visitor numbers. Differences of this nature within and
between sites are interesting as they provide an opportunity to investigate factors associated with
the occurrence and/or magnitude of visitor impacts (Hosey, 2005).
The objective of this study was to investigate visitor effects in captive western lowland gorilla
groups at two UK zoos, Port Lympne and Chessington. Specifically, the associations between
visitor number and two behavioural indices of anxiety – self-scratching (Schino et al., 1991) and
visual monitoring (Maestripieri, 1993) – were examined. In addition, the potential impact on
such visitor effects of a widely used type of enrichment intervention, feeding enrichment, was
investigated. This study meets two important needs: adding to the very limited number of studies
of visitor effects on western lowland gorillas, and providing novel information on the potential
ameliorating impact of enrichment on such effects.

2. Methodology

2.1. Subjects

The subjects were 20 western lowland gorillas (Gorilla gorilla gorilla) living within two social groups,
one at Port Lympne Zoo in Kent and the other at Chessington Zoo in Surrey. The age, sex and rearing history
of individuals in the two study groups are shown in Table 1. The adult composition had changed very little in
the Port Lympne group in recent years. However, in the Chessington group approximately 18 months ago the
silverback male and an older low ranking female were removed from the group, leaving the group without a
silverback. Apart from that the adult composition had not changed in recent years.

2.2. Housing

Both groups lived in enriched enclosures, with ropes, climbing structures and movable objects, with deep
straw lining the floor in which food items could be hidden. Both enclosures had an indoor out of view area,

Table 1
Individual information for study animals
Port Lympne Chessington
Name Sex Age (years) Rearing history Name Sex Age (years) Rearing history
Djala M 25 Wild caught (Rescued) Kaga F 28 Captive/mother reared
Mumba F 20 Captive/mother reared Asili F 16 Captive/mother reared
Kishi F 19 Captive/mother reared Mjuku F 8 Captive/mother reared
Tamki F 18 Captive/hand reared Kumili F 3 Captive/mother reared
Emmie F 16 Captive/hand reared Shani F 17 Captive/mother reared
Kibi F 15 Captive/mother reared Buu F 11 Captive/mother reared
Fou Fou F 15 Captive/mother reared Shanga F 6 Captive/mother reared
Ja Ja M 8 Captive/mother reared Kumi M 3 Captive/mother reared
Dishi M 7 Captive/mother reared
Yene F 6 Captive/mother reared
Kouni M 6 Captive/mother reared
M Passa M 4 Captive/mother reared
214 G. Carder, S. Semple / Applied Animal Behaviour Science 115 (2008) 211–220

where the gorillas could retreat from visitors. In addition the Port Lympne enclosure had a large grass area
(1/2 acre) with a climbing structure in the centre. Both enclosures had glass at the front of the outdoor area
through which the public looked. However in addition at Port Lympne visitors could view the animals from
one side of the enclosure, which was made of metal caging. The outdoor grass area at Port Lympne had no
glass or caging, just electric fencing, to separate the visitors from the gorillas.

2.3. Feeding enrichment

Due to the nature of presentation of all food at both zoos, which was designed to promote foraging
and provide mental and physical stimulation over extended periods of time, all feeding was considered
for the purposes of this study as feeding enrichment. The keepers at both zoos scattered the morning
feed through the straw; this morning feed consisted of a variety of fruit and vegetables and usually took
place between 10:00 and 10:30 am. In addition, both zoos conducted two further scatter feeds per day,
in which small food items such as nuts and grapes were dropped from the roof of the enclosure, into the
straw at Chessington and onto the grass area at Port Lympne. The scatter feeds were at 12:00 and 15:00
at Port Lympne and 11:30 and 13:45 at Chessington. The gorillas at Chessington were supplied with
large pieces of browse and bark on a daily basis, the Port Lympne gorillas received smaller pieces of
browse on Mondays, Wednesdays and Fridays. In addition, on these days the Port Lympne gorillas were
supplied with ‘honey pots’ during breakfast feeding. There were two large pots in the enclosure on these
days the pots would be filled with honey, jam or marmite. The gorillas would then use the sticks from
the browse as tools to extract the sticky substances; these pots were filled in the morning as they were
being given their morning feed.

2.4. Procedure and data collection

Observational data were collected from 18/03/07 to 16/4/07 at Port Lympne Zoo and from 25/04/07
to 01/06/07 at Chessington Zoo, with all observations made from the public viewing area. In total 151 h
of data were collected during fifteen minute focal samples. This represented 79 h of data collected at
Port Lympne zoo (315 focal watches on 12 individuals), and 72 h of data at Chessington zoo (287 focal
watches on 8 individuals). The order of the focal watches on each day was randomised. Information on
the visitors present (i.e. those in viewing range of the enclosure) was recorded every 5 min during the
focal watch; these data included total number of people, the number of adult males, adult females and
children. Overall noise level was also recorded every 5 min, and scored using the following scale:
0 = low level noise, no noise/a small percentage of the viewing group making low level noise;
1 = moderate noise, most of the viewing group talking, no raised voices; 2 = loud noise, most or
all of the viewing group talking in addition there is raised voices such as shouting, screaming or
children crying. Preliminary analyses found highly significant positive correlations between all five
independent variables (rs = 0.770–0.980; P < 0.001 in all cases) and therefore only the total number of
people viewing the gorillas was used in further analyses, with an average number of people viewing the
gorillas calculated for each focal watch.
In addition to instantaneous sampling of visitor numbers, the duration of both self-scratching
(defined as ‘a [usually repeated] movement of the hand or foot during which the fingertips are drawn
across the individual’s fur’; Schino et al., 1988) and visual monitoring of visitors (defined as when the
focal animal was judged to show visual orientation towards one or more visitors) were recorded. There
is substantial pharmacological and behavioural validation of the use of self-scratching as an index of
anxiety (Maestripieri et al., 1992). While such broad based evidence is not available for the use of
visual monitoring as a measure of anxiety, increased monitoring has been observed in behavioural
contexts likely to elicit anxiety, for example, the approach of potentially antagonistic individuals in wild
mountain gorillas (Watts, 1998). Durations rather than frequencies of occurrence of both of these
behaviours were used, as duration of the behaviour may reveal information about the intensity of the
anxiety eliciting event.
 G. Carder, S. Semple / Applied Animal Behaviour Science 115 (2008) 211–220 215

2.5. Data analyses

Durations of self-scratching and visual monitoring in each focal watch were corrected for the time that
the focal animal was out of view. Focal watches were then classified according to whether they were
collected during periods of feeding enrichment, or outside of this time. Data from a pilot study were used to
determine the cut-off point between these periods; these pilot data indicated that most gorillas had returned
to non-feeding activities 75 min after the start of the breakfast feeding and 30 min after the start of the later
scatter feeds.
To test for visitor effects, data collected for each measure of anxiety during periods of feeding
enrichment and no feeding enrichment were analysed separately for each study site, giving a total of
eight separate analyses (2 sites  2 conditions  2 measures of anxiety). In each of these, data were
analysed for each individual gorilla separately, and the results for all animals in each group then combined as
follows. A Spearman’s correlation was carried out for each individual in order to assess the relationship
between duration of self-scratching/visual monitoring and the average numbers of visitors viewing the
gorillas. The correlation coefficients for all animals at each site were then pooled and the mean of these
values compared in a one sample t-test to an expected value of zero (predicted under the null hypothesis of
no relationship between visitor number and anxiety). This analysis allows investigation of the correlation
between anxiety and visitor number while avoiding problems of pseudoreplication inherent when data are
pooled across individuals within study groups.
Further analyses were carried out to explore the results found with respect to visitor effects, and the
potential impact of feeding enrichment on these effects. The first of these analyses assessed, at each site
separately, the impact of feeding enrichment on duration of measures of anxiety. Here, data from focal
watches were used to calculate for each animal a mean duration of self-scratching/visual monitoring during
(i) periods of feeding enrichment and (ii) periods of no feeding enrichment. Wilcoxon matched signed pairs
rank tests were then carried out to compare these values between enrichment conditions at each site. A
second analysis compared the average duration of self-scratching/visual monitoring between the two sites,
with periods of feeding enrichment and no feeding enrichment considered separately. Here, the mean values
for individuals in each of the two enrichment conditions, calculated as described above, were used in a
Mann–Whitney U-test. A third analysis compared visitor number between the two study sites in each of the
two enrichment conditions. Here, a mean visitor number was calculated for each focal watch and a Mann–
Whitney U-test was used to compare the average number of visitors viewing the gorillas at each zoo. In the
final analysis, visitor number was compared within sites between periods of feeding enrichment and non-
feeding enrichment, using a Wilcoxon matched signed pairs rank tests.
SPSS version 14.0 was used for all analyses, and all test were two-tailed.

3. Results

All animals at both sites were seen to engage in self-scratching and visual monitoring. The
mean duration of self-scratching calculated across study animals was 43.9 (range 3.2–153.0)
seconds per hour at Port Lympne and 21.2 (range 0.4–78.1) seconds per hour at Chessington. The
mean duration of visual monitoring was 60.1 (range 6.1–253.6) seconds per hour at Port Lympne
and 8.6 (range 0.7–21.2) seconds per hour at Chessington.

3.1. Visitor effects during periods of feeding enrichment and no feeding enrichment
at each zoo

At Port Lympne Zoo, during periods of no feeding enrichment there was a positive association
between the average number of people viewing the gorillas and the duration of self-scratching
(one sample t-test; t11 = 3.803, P = 0.003) and visual monitoring (t11 = 3.901, P = 0.002). For
both behaviours, 10 out of the 12 animals showed a positive association between the duration of
216 G. Carder, S. Semple / Applied Animal Behaviour Science 115 (2008) 211–220

Table 2
Results of Spearman correlations between total people viewing the gorillas and stress related behaviours performed by the
gorillas at Port Lympne during periods of no feeding enrichment
Name Self-scratching Visual monitoring
rs P rs P
Djala < 0.229 0.394 0.696 0.003
Kishi , 0.694 0.026 0.127 0.726
Mumba , 0.132 0.626 0.175 0.516
Tamki , 0.259 0.031 0.347 0.205
Emmie , 0.057 0.812 0.507 0.005
Kibi , 0.137 0.075 0.208 0.591
Fou Fou , 0.08 0.76 0.288 0.378
Ja Ja < 0.289 0.297 0.971 <0.01
Dishi < 0.386 0.193 0.387 0.191
Yene , 0.382 0.246 0.299 <0.01
Kouni < 0.125 0.632 0.318 0.213
M Passa < 0.241 0.406 0.049 0.868

the behaviour and visitor numbers (Table 2). By contrast, during periods of feeding enrichment at
this zoo there were no significant associations between visitor numbers and duration of either
self-scratching (t11 = 0.431, P = 0.675) or visual monitoring (t11 = 0.885, P = 0.395). At
Chessington Zoo, there were no significant relationships found between the average number of
people viewing the gorillas and duration of self-scratching or visual monitoring during feeding
enrichment (self-scratching: t7 = 0.779, P = 0.462; visual monitoring: t7 = 1.446, P = 0.191) or
during periods when no feeding enrichment was taking place (self-scratching: t7 = 1.431,
P = 0.196; visual monitoring: t7 = 0.691, P = 0.512).

3.2. Comparison of gorilla behaviour between periods of feeding enrichment and no feeding
enrichment at each zoo

At both zoos, there was a significantly lower duration of self-scratching during periods of
feeding enrichment compared to when such enrichment was absent (Wilcoxon matched pairs
test; Port Lympne: Z = 2.197, P = 0.028; Chessington: Z = 2.100, P = 0.036; see Fig. 1). No

Fig. 1. Time spent self-scratching at each zoo during periods without (black bars) and with (grey bars) feeding
enrichment. Values indicate mean  1S.E.
 G. Carder, S. Semple / Applied Animal Behaviour Science 115 (2008) 211–220 217

Fig. 2. Time spent visual monitoring at each zoo during periods without (black bars) and with (grey bars) feeding
enrichment. Values indicate mean  1S.E.

such difference was seen at either zoo in duration of visual monitoring (Port Lympne:
Z = 1.569, P = 0.117; Chessington: Z = 0.420, P = 0.674; see Fig. 2).

3.3. Comparison of gorilla behaviour between zoos during periods of feeding enrichment
and no feeding enrichment

There was no significant difference between sites in duration of self-scratching either during
feeding enrichment (Mann–Whitney test: U = 44.50, P = 0.785) or outside of these periods
(Mann–Whitney test: U = 34.00, P = 0.280; see Fig. 1). Both during periods of feeding
enrichment and outside of this time, the Port Lympne group spent significantly longer looking at
visitors than did the Chessington group (Mann–Whitney test; during feeding enrichment:
U = 20.30, P = 0.034; no feeding enrichment: U = 7.00, P = 0.002; see Fig. 2).

3.4. Comparison of the average number of people viewing the gorillas between zoos and
between periods of feeding enrichment and no feeding enrichment at each zoo

There were significantly more visitors at Port Lympne than at Chessington during periods
without feeding enrichment (Port Lympne mean = 11.90, Chessington mean = 7.63; Mann–
Whitney test, U = 12,166, P = 0.012), but no significant difference between sites during periods
of feeding enrichment (Port Lympne mean = 9.78, Chessington mean = 6.26; U = 8189.5,
P = 0.588). At Port Lympne, there were significantly fewer visitors during periods of feeding
enrichment than outside of this time (feeding enrichment, mean = 9.78, no enrichment,
mean = 11.90; U = 10,036, P = 0.005). There was no significant difference in visitor numbers
between periods with and without feeding enrichment at Chessington (feeding enrichment
mean = 6.26, no enrichment mean = 7.63; U = 8740, P = 0.065).

4. Discussion

The results of this study provide evidence for an effect of visitor numbers on gorilla anxiety
levels at Port Lympne, but not Chessington, and suggest that this effect was alleviated by the
provision of feeding enrichment. In evaluating visitor impacts, this study focussed on two
particular components of the gorilla social repertoire, namely self-scratching and visual
218 G. Carder, S. Semple / Applied Animal Behaviour Science 115 (2008) 211–220

monitoring of visitors. Behavioural and pharmacological studies indicate these behaviours

provide a reliable measure of anxiety in non-human primates (Maestripieri, 1993; Watts, 1998;
Schino et al., 1991; Maestripieri et al., 1992). Quantification of such behaviours affords
advantages over measuring changes in, for example, resting, feeding, locomotion, social
behaviour or aggression (e.g. Todd et al., 2007; Cooke and Schillaci, 2007; reviews by Davey,
2007; Hosey, 2008). Ross et al. (2007) highlight the difficulties associated with linking such
changes to actual welfare impacts. As behaviours such as self-scratching and visual monitoring
provide a means to track short-term changes in affective state, we feel that incorporation of such
measures into behavioural studies of visitor impacts should be encouraged. Most
comprehensively, such measures could also be combined with quantification of physiological
measures of stress such as faecal or urinary cortisol metabolites (e.g. Davis et al., 2005).
The occurrence of visitor effects at Port Lympne but not Chessington highlights the
importance of examining intra-specific variation in visitor effects on captive primates. Kuhar
(2008) documented a similar difference with respect to the occurrence of visitor effects between
gorilla groups, in this case between two groups at the same study site. Differences between
groups of the same species in their response to visitors provide an invaluable tool to address in
more detail the potential mechanisms underlying such impacts on captive primate populations
(Hosey, 2005; Kuhar, 2008). The difference between sites in the current study may be due to their
differing group composition (e.g. the absence of a silverback at Chessington), although it is not
obvious how this may affect visitor related impacts. Alternatively, this inter-site difference may
be due to the significantly higher visitor numbers at Port Lympne than Chessington during
periods without feeding enrichment. There was no difference in visitor number between the two
zoos during periods of feeding enrichment, and no evidence for a visitor effect at either site. It is
important to acknowledge, however, that seasonal effects may also contribute to the difference
between sites in the occurrence of visitor effects; all data at Port Lympne were collected before all
data for Chessington. Ross et al. (2007) highlight the potential for data collected during two
separate time periods to differ in more variables than simply visitor number. Unfortunately, in the
current study logistical reasons prevented sampling taking place at both sites simultaneously or
alternately through the study period.
The lack of a positive association between visitor numbers and either self-scratching or visual
monitoring at Port Lympne during feeding enrichment provides tentative evidence that this
husbandry technique may reduce the impact of visitors on captive gorillas. These findings
potentially have important animal welfare implications, indicating that engagement of animals in
a stimulating activity ameliorates the effects of visitors on their anxiety levels. One potential
criticism of this interpretation is that the behaviours increased by enrichment (such as looking for
or processing food) may be incompatible with behaviours such as scratching and looking at
visitors. However, while a significant reduction was seen in rates of self-scratching, this
behaviour still occurred and even though rates were lower when feeding enrichment was
provided, there is no a priori reason why this reduction in overall rate should necessarily lead to
the loss of the association with visitor number. Moreover, visual monitoring was not reduced
during periods of feeding enrichment at Port Lympne, but the association between visual
monitoring and visitor numbers was not found during this time.
The finding that visitor numbers at Port Lympne were significantly lower during feeding
enrichment than when enrichment was not being provided suggests that a further alternative
explanation for the lack of visitor effect during periods of feeding enrichment at this site should
be considered. This is that the gorillas’ anxiety levels at this site were only linked to visitor
number when the latter exceeded a certain threshold. The data in this study do not allow us to
 G. Carder, S. Semple / Applied Animal Behaviour Science 115 (2008) 211–220 219

distinguish definitively between this explanation and one invoking a positive effect of enrichment
on anxiety levels; however, both potential explanations have important welfare implications and
merit further investigation.

5. Conclusion

This study adds to the growing literature on the impact of zoo visitors on captive primates; by
focussing on easily quantifiable indices of anxiety, the approach used here provides a very direct
measure of likely welfare costs to animals. The findings of this study further highlight the value of
investigating visitor effects at multiple sites for the same species, and also of exploring the potential
ameliorating effect of positive management techniques on the manifestation of such impacts.

Acknowledgments

We sincerely thank the management of Chessington and Port Lympne for kindly granting
permission to carry out this study. We are also very grateful to the keepers at both sites for their
generous co-operation and assistance during the study. Peter Shaw provided invaluable statistical
advice and James Higham and Lauren Brent gave constructive comments on this paper.

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