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Article history: Visitors are known to affect zoo animals, and such effects may be stressful, neu-
Accepted 9 May 2011 tral, or enriching. The majority of research has focused on visitor number or visitor
Available online 8 June 2011
presence–absence, yet few studies have examined effects of other variables such as sound
volume, visitor activity, and whether visitors interact with animals. In this study, the effects
Keywords: of visitor number, activity and proximity to animals were investigated on a group of captive
Visitors
orangutans in two treetop, ‘free-ranging’ exhibits at Singapore Zoo. Multinomial logis-
Captive
tic regressions were used to elucidate the relationships between visitor and orangutan
Welfare
Orangutan behaviours. Results from these analyses revealed a significant overall effect of the three
Behaviour visitor variables on orangutan behaviour. Interestingly, visitor number had little effect on
the orangutans, except at one of the exhibits where the likelihood of food soliciting and
looking at visitors increased when the number of people numbered more than 40. Visitor
activity was generally not associated with any obvious signs of stress in the orangutans;
visitors with food could even be a form of enrichment. However, visitors at close proxim-
ity decreased play behaviour and increased the chances of animals looking at the visitors.
Enclosure design and habituation could have alleviated visitor effects for these two groups
of orangutans. This study shows how investigation of a wider range of visitor variables may
allow for more meaningful conclusions about the visitor effect, and that other factors such
as enclosure design and habituation to visitors may also influence captive animal welfare.
© 2011 Elsevier B.V. All rights reserved.
0168-1591/$ – see front matter © 2011 Elsevier B.V. All rights reserved.
doi:10.1016/j.applanim.2011.05.007
Y. Choo et al. / Applied Animal Behaviour Science 133 (2011) 78–86 79
Table 1
Individual details of study animals. All individuals were born in the Singapore Zoo except Anita who was donated to the zoo at 1 year of age.
Group A
Ah Meng Jnr Female 1 Pongo pygmaeus
Bento Male 3 Pongo pygmaeus
Budi Male 7 P. pygmaeus/P. abelii cross
Gunta Male 7 Pongo pygmaeus
Chomel Female 13 Pongo abelii
Anita (with infant Ah Meng Jnr) Female 24 Pongo pygmaeus
Group B
Saloma Female 0.5 Pongo pygmaeus
Merlin Male 5 Pongo pygmaeus
Vira Male 9 Pongo pygmaeus
Labu Male 11 Pongo pygmaeus
Binte (with infant Saloma) Female 25 Pongo pygmaeus
interactivity, proximity and gender (Davey, 2007). This brachiation and other species-specific behaviour. During
emphasis on particular variables may lead to an incom- the 2009/2010 study period, there were two such exhibits
plete understanding of how visitors affect zoo animals. (Fig. 1). The “Island exhibit” consisted of a straight row of
Also, it is common that only one or two visitor variables trees located next to a main track, where vehicles, trams
are considered within the same study. This is most likely and visitors passed by regularly. Visitors on the main track
due to the practical limitations of collecting several types were able to look up into the trees to view the orangutans.
of data at once. Furthermore, ‘visitor activity’ is not always The other free-ranging exhibit, the “Boardwalk exhibit”,
well defined (Davey, 2007). A finer level of resolution, was similar to the Island exhibit but visitors could choose
such as whether the visitor is walking, looking, or hold- to view the orangutans from the main track, or from an
ing food, may allow for more meaningful conclusions to be elevated boardwalk. This boardwalk allowed visitors to
drawn. In addition, visitor effects have traditionally been come into much closer proximity with the animals (as
considered as separate from other factors such as exhibit close as 3 m).
design and visitor circulation (Davey, 2005; Fernandez Two groups of orangutans were rotated daily between
et al., 2009). Finally, and of particular relevance to the the two free-ranging exhibits. Although orangutans in the
present study, even though most visitor effects investi- wild are semi-solitary (Galdikas, 1985), all subjects in this
gations have focused on primates, there exist only two study had been housed together in various combinations
published reports on orangutans (Birke, 2002; Bloomfield since they were young (Jackson Raj, head orangutan
et al., 2010). keeper, personal communication). The groups were made
In an attempt to address some of these issues, we up of individuals of varying ages, and each group had
investigated the effects of three visitor variables – visitor one mother–infant pair (Table 1). As the infants were still
number, visitor proximity to animals, and visitor activity, dependent on their mothers, they were excluded from the
on orangutans housed at Singapore Zoo. Visitor activity observations. The composition of the groups remained the
was broken down into sub-categories to allow for a more same throughout the study period. This display arrange-
in-depth analysis. Because the two groups of orangutans ment presented a unique opportunity: usually, studies that
under study had a unique husbandry routine, in which compare animal behaviour across different enclosures use
they were rotated daily between two different enclosures, data from different animals; however, in Singapore Zoo,
we were also able to more accurately assess the effects because the same animals were regularly rotated between
of exhibit design. We hypothesised that larger groups of two exhibits, we had the rare chance to study the same
visitors, visitors who were more active (e.g. taking pho- subjects in different enclosures, simulating a manipulative
tographs), and visitors who were closer in proximity would experiment.
be stressful to the orangutans. This may lead to low- In order to capture visitor crowds of varying sizes, we
ered incidences of feeding, playing and social behaviours, collected data on both weekdays and weekends from Octo-
and increased incidences of stereotypic behaviour such as ber 2009 to February 2010, between 09:30 h and 17:00 h.
regurgitation. We also hypothesised that visitors with food Instantaneous scan sampling, with the aid of binoculars,
would result in more begging behaviour. was used for both the orangutans and visitors. Follow-
ing Engel’s (1996) protocol, we calculated that scans taken
2. Materials and methods at 10 min intervals were sufficiently far apart enough to
avoid autocorrelation. A total of 192 h of observations
2.1. Enclosure design, subjects and data collection (48 h for each group-exhibit combination) were made, and
all data were collected by the same observer. As regu-
Singapore Zoo introduced ‘free-ranging’ enclosures lar feeding sessions were held twice daily, at 11:30 h and
for its orangutans in 2006 (Jackson Raj, head orangutan 15:30 h for the Island exhibit and 14:15 h and 16:30 h for
keeper, personal communication). These exhibits each the Boardwalk exhibit, we paused data collection 15 min
comprises a row of tall trees connected by artificial vines, before each session started and only resumed 15 min after
hammocks and platforms, and are designed to encourage the feeding ended. Browse (fresh leaves) was provided
80 Y. Choo et al. / Applied Animal Behaviour Science 133 (2011) 78–86
Fig. 1. Island exhibit (top) and Boardwalk exhibit (bottom). Each exhibit consisted of trees joined by vines, nets, platforms and logs. Low-current electrical
wires were present midway up the tree trunks to prevent the animals from descending to the ground. Some vines and foliage have been omitted for
purposes of clarity. Island exhibit: (a) large net across trees, (b) ground-to-foliage view of exhibit trees, (c) low vine across main track where orangutans
often interacted with visitors. Boardwalk exhibit: (d) low vine across main track where visitor–orangutan interaction often occurred, (e) elevated visitor
boardwalk, (f) orangutan platform next to visitor boardwalk, (g) low log next to the visitor track where animals would interact with visitors.
Y. Choo et al. / Applied Animal Behaviour Science 133 (2011) 78–86 81
Table 2 Table 3
Definitions for orangutan and visitor variables (also see Table 3). Definitions and levels of variables for multinomial logistic regression.
Table 5
Results from multinomial logistic regression testing effects of visitor number, activity and proximity on orangutan behaviour in the two exhibits. Only odds
ratios with significant P-values (P < 0.05) are shown.
Table 6
Effects of visitor variables on the likelihood of each orangutan behaviour for both exhibits.
Orangutan Vis no Vis no Vis no Vis no Vis Vis Vis Vis with Vis <10 m
behaviour 11–20 21–30 31–40 >40 standing looking photo’s Food
Vis = visitor; Photo’s = taking photographs; NS = visitor variable had no significant effect on the likelihood of occurrence of orangutan behaviour;
More = likelihood of orangutan behaviour increased when visitor variable was present (OR > 1), Less = likelihood of the orangutan behaviour decreased
(OR < 1).
behaviours. Visitors with food had a significant effect only As with the Boardwalk exhibit, the OR for begging was
on the likelihood of begging (OR = 254.754) and looking at very large when visitors had food (OR = 256.210). Out of
visitors (OR = 12.344). No other orangutan behaviours were 10 instances, begging occurred four times when the vis-
affected by visitors with food (Tables 5 and 6). itors were holding food, three times when visitors were
Visitors who were nearer (<10 m away) significantly taking photographs of the orangutans, and one instance
increased the chances that the orangutans would regur- each when visitors were walking, standing or looking at
gitate (OR = 2.610), beg (OR = 3.014) or look at the visitors the orangutans.
(OR = 2.924). However, visitors who were <10 m away
significantly decreased the chances that the orangutans 4. Discussion
would feed (OR = 0.481) or play/socialize (OR = 0.669)
(Tables 5 and 6). This study incorporated several variables of visitor num-
The OR for begging was very large when visitors ber, activity and proximity in an attempt to improve our
had food (OR = 254.754), suggesting that this behaviour understanding of how visitors affect captive orangutans.
occurred mostly when food was present. Out of the 29 Previous research has suggested that active visitors elicit
instances, begging occurred 14 times when the visitors more audience-directed behaviours from primates (Hosey
were holding food, nine times when visitors were looking and Druck, 1987; Mitchell et al., 1992a), but there has
at the orangutans, and one, two and three times respec- been little research on the effects of specific visitor activ-
tively when visitors were walking, standing and taking ities. Here, we broke down visitor activity into distinct
photographs of the orangutans. categories. We also utilised the fact that the two groups
of orangutans were rotated daily between two exhibits.
3.2. Effect of visitors on orangutan behaviour in the This regular rotation formed a natural experiment and
Island exhibit allowed us to compare visitor effects across the different
enclosures while controlling for between-group variation
Visitor activity and proximity had significant effects on in behaviour. Overall, our results showed that large crowds,
orangutan behaviour in the Island exhibit, but not visitor visitors with food, visitors who were looking or taking
number (Table 4). photographs, and visitors who were close by, all affected
Visitors who were standing decreased the chances orangutan behaviour. On the whole, however, the effects of
of orangutans feeding (OR = 0.599), but had no other visitors on orangutans in Singapore Zoo’s enclosures were
effects on orangutan behaviour. Visitors who were look- generally less than hypothesised. The free-ranging exhibit
ing at the orangutans did not significantly affect any of design, habituation to humans, or both, may explain this.
their behaviours; however, visitors who were photograph- Compared to other studies of visitor effects on
ing the orangutans significantly decreased the chances orangutans (Birke, 2002; Jones, 2003), our research reveals
of play/social behaviour (OR = 0.218), and increased the little effect of visitor number on orangutan behaviour. The
chances of begging behaviour (OR = 31.094). Visitors likelihood of begging and looking at visitors increased only
with food significantly increased the likelihood that the when there were crowds of more than 40 individuals. No
orangutans would be looking at the visitors (OR = 14.869) other behaviours were affected by visitor number, sug-
or begging (OR = 256.210) (Tables 5 and 6). gesting that human presence induces little or no stress
Visitors who were <10 m away increased the chances in the orangutans at Singapore Zoo. This is in contrast to
that the animals would feed (OR = 1.544) or beg Birke’s (2002) study, in which orangutans covered them-
(OR = 7.307). Such visitors also decreased the chances selves with paper sacks more and foraged less when
that the orangutans would regurgitate (OR = 0.327) more (>8) visitors were present. Visitor-induced stress
(Tables 5 and 6). such as reduced social play and mobile feeding activities
84 Y. Choo et al. / Applied Animal Behaviour Science 133 (2011) 78–86
has also been reported in orangutans when there were As hypothesised, food was a very strong stimulus of
more than 100 visitors (Jones, 2003). However, as the vis- orangutan behaviour, with the likelihood of begging and
itor numbers in our study rarely rose above 80, whether looking at visitors increasing significantly in both exhibits
higher visitor numbers could induce stress on orangutans when food was present. The increase in likelihood (OR) for
at Singapore Zoo is unknown. Nevertheless, because the these behaviours was similar across both exhibits, which
exhibits were positioned along tracks with heavy human suggests that food was a strong and constant stimulus
traffic, it is possible that orangutans in Singapore Zoo have even across different enclosure designs. Although beg-
been habituated to larger visitor crowds as well. Also, ging occurred less than 30 times in each exhibit, food
being at a higher position (usually in trees) above visi- was present during approximately half of such instances.
tors may have provided a sense of security or dominance This result contributes to the consensus from other studies
(Coe, 1985). The fact that a large visitor crowd increased where apes were also motivated to interact with visi-
the chances of visitor-oriented behaviour only in the tors for food (Birke, 2002; Cook and Hosey, 1995; Jones,
Boardwalk exhibit, where an elevated boardwalk allowed 2003; Wood, 1998). The lives of zoo animals may often
visitors to get closer to the animals, indicates that exhibit be routine; therefore, novel occurrences of visitors with
design may influence how visitor numbers affect orangutan food may serve as a source of variability and enrich-
behaviour. ment (van Rooijen, 1991; Wiepkema and Koolhaas, 1993).
Changes in orangutan behaviour were more strongly All orangutans would immediately and fixatedly look at
associated with active visitors (those looking or tak- visitors who were holding food; they would also occasion-
ing photographs) than passive (standing) visitors. Similar ally solicit food by hanging from a branch directly above
results have been reported in other studies (e.g. Chamove and extending their hand towards the visitor. Interest-
et al., 1988; Hosey and Druck, 1987; Mitchell et al., ingly, only some of the orangutans begged consistently
1992a), in which significantly more behaviours were and a clear difference in individual begging styles was
directed towards active than passive audiences. However, also observed. It has been shown previously that person-
in these papers, visitor activity was defined quite gener- ality may influence an orangutan’s response to stimuli
ally: either as ‘active’ (whereby at least one visitor tried (Uher et al., 2008) and Fraser (2009) highlighted this phe-
to interact with the animals) or ‘passive’ (no attempt nomenon for further study.
at interaction); whereas in our study, we divided visitor We also examined the effects of visitor proximity on
activity into five categories. We found that the associ- orangutans. The results showed interesting trends between
ation between active visitors and orangutan behaviour exhibits, and a possibly stressful visitor effect at closer
was more pronounced at the Boardwalk exhibit than the proximities. The likelihood of both begging and looking
Island exhibit, which again suggests that proximity of at visitors were increased in the Boardwalk exhibit when
visitors to animals can affect the visitor–animal interac- visitors were less than 10 m away, but only begging was
tion. The greater probability that the orangutans would affected at this distance at the Island exhibit. This dif-
be feeding, playing/socializing, or moving when visitors ference between enclosures may have been due to the
looked or took photographs could be explained by the ‘vis- elevated boardwalk in the Boardwalk exhibit (Fig. 1), which
itor attraction’ hypothesis, where active animals attract allowed much closer proximity (3–7 m), as well as inter-
more attention from visitors (Hosey, 2000). Conversely, actions at eye level between orangutans and visitors. This
we suggest that the ‘visitor effect’ hypothesis may explain was in contrast to the Island exhibit, where the orangutans
why visitors in the Boardwalk exhibit who looked at the were always in trees above the crowds (Fig. 1), and hence,
orangutans, and visitors who photographed orangutans at least 7 m above the visitors. Consequently, any effects
in the Island exhibit, were linked to a higher chance of of visitor proximity may have been reduced in the Island
begging. exhibit. When visitors were nearer (<10 m away), regur-
Overall, the increase in likelihood of feeding, play and gitation increased in the Boardwalk exhibit but decreased
social behaviours when visitors were looking or taking pho- in the Island exhibit. We noted that regurgitation almost
tographs in the Boardwalk exhibit suggest that the visitors always took place at platforms; while the platform in the
were not a source of stress. At the Island exhibit, visitors Boardwalk exhibit was less than 10 m away from all visi-
standing were linked to lowered incidences of feeding in tor viewing areas, the platform in the Island exhibit was
orangutans while those taking photographs were linked further than 10 m from all visitor viewing areas. Hence,
to lowered incidences of playing/socializing in the ani- the results for regurgitation may have been influenced by
mals. The latter result was the opposite of what we found the location of the platforms where regurgitation usually
at the Boardwalk exhibit but we suggest that, because occurred. The differences in feeding in relation to visi-
play/social behaviour in the Boardwalk exhibit occurred tor proximity can also be explained by where the browse
mostly in highly visible locations near the raised visitor (fresh leaves) was usually consumed in both exhibits. In
walkway, these behaviours were more likely to attract vis- the Boardwalk Exhibit, browse was usually provided by
itor attention and hence more photography. On the other the keepers at the low branch overhanging location ‘g’
hand, playing/socializing at the Island exhibit occurred at (Fig. 1), and the orangutans often liked to move the browse
less obvious places (i.e. cargo nets in the upper branches of to a cargo net (that was defined as more than 10 m from
the trees). The association between visitors standing and the visitors) before consuming it. However in the Island
lowered incidence of feeding was unexpected and cannot Exhibit, browse was provided at the low branches of the
be easily explained by either the visitor attraction or visitor tree to the left of location ‘a’ (Fig. 1), and the orangutans
effect hypothesis. usually consumed the browse at those branches, which
Y. Choo et al. / Applied Animal Behaviour Science 133 (2011) 78–86 85
was defined to be less than 10 m away from visitor view- staff – Alagappasamy s/o Chellaiyah, Charlene Yeong, Jack-
ing areas. Hence results for feeding and regurgitation son Raj, John Sha, Kumaran Sesshe, Mohamed Arshad Bin
may be influenced by the locations where these activities Mohamed Ayob, Mohammad Marzuki Bin Azis, Moham-
mostly occurred, as well as the definitions of proximity mad Noor Bin Mohd Idris, Nantha Gabriel and Prakash
in the study. The association between visitor proximity Naidu for their generous cooperation and assistance during
and decreased play/socializing in the orangutans was also the study. Many thanks also to Chan Yiok Huak, Chua Kia
limited to the Boardwalk exhibit. To date, there has only Chong, Giam Xingli, James Ha, Lainie Qie, and Lin Yangchen
been one other study on visitor proximity, Bloomfield et al. for their invaluable statistical advice.
(2010), who did not find evidence that orangutans avoid
close visitor contact. In our study however, visitors at <10 m
proximity decreased the chances of play/socializing, sug-
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