Upload
s-montaudouin
View
222
Download
7
Embed Size (px)
Citation preview
Comparison between 28 zoological parks:
stereotypic and social behaviours of
captive brown bears (Ursus arctos)
S. Montaudouina,b,*, G. Le Papea
aFaculte des Sciences et Techniques, DESCO, Parc de Grandmont, 37200 Tours, FrancebUMR 5173 MNHN-CNRS ‘Conservation des especes, restauration et suivi des populations’,
57 rue Cuvier, 75231 Paris, France
Accepted 31 October 2004
Available online 7 January 2005
Abstract
In the present study we compared 33 enclosures in 28 parks, with a total of 66 bears. We chose
direct observation of behaviour rather than surveys. Each enclosure was observed during one day;
stereotypies and social relationships were qualitatively noted in types and amount. The connections
of behaviour with bears characteristics and types of management were established. Young bears
exhibited fewer stereotypies than adult ones, especially if these adults were kept indoor at night.
Contrary to stereotyped pacing and circling, head-tossing was more frequent in young subjects.
Occurrences of stereotypical behaviour were more numerous during the afternoon, especially if
animals received a single main feed in the evening. Whereas circling was observed only in bears kept
with related fellows, pacing was more frequent when they were kept with unrelated. Neither social
isolation nor sex did influence stereotypies. Keeping more than two bears together was a source of
social conflict. These results suggest some recommendations for housing and management of captive
brown bears.
# 2004 Elsevier B.V. All rights reserved.
Keywords: Care management; Exhibit design; Housing; Husbandry procedures; Social interactions; Stereotyped
behaviour; Zoo animals
www.elsevier.com/locate/applanim
Applied Animal Behaviour Science 92 (2005) 129–141
* Corresponding author. Tel.: +33 2 47 36 6998; fax: +33 2 47 36 7285.
E-mail address: [email protected] (S. Montaudouin).
0168-1591/$ – see front matter # 2004 Elsevier B.V. All rights reserved.
doi:10.1016/j.applanim.2004.10.015
1. Introduction
The wish to achieve the best layout of enclosures in zoological parks is not recent and
applies to all species (Hediger, 1955). However, this can be motivated by very different
expectations (Robinson, 1998). The purpose may be to increase activity of the animals or to
make them more visible to the public (Little and Sommer, 2002; Bashaw et al., 2003), to
prevent the animals from performing stereotypies, to promote natural behaviours or to
increase reproductive success. The way to achieve these goals is generally called
‘enrichment’ and often consists in new feeding methods (Carlstead et al., 1991; Forthman
et al., 1992; Wiedenmayer, 1998; Fischbacher and Schmid, 1999; Mc Phee, 2002;
Morimura, 2003) or in new facilities (Renner et al., 2000; Renner and Plebani Lussier,
2002). The model is generally the natural habitat. Other procedures described by
Seidensticker and Doherty (1996) as ‘occupational therapy’ includes regularly moving
animals to new enclosures (Lukas et al., 2003) or introducing predatory species (Little and
Sommer, 2002) and more recently trained animals to suppress boredom (Laule and
Desmond, 1998). Moreover, grouping subjects of the same species is generally considered
as decreasing boredom, even if the species is essentially solitary in nature. Because brown
bears, in particular males, generally are solitary animals, we compared enclosures with
quite different grouping situations, from isolated subjects to groups of six. Although zoos
get better and better, most of these ‘enrichments’ have actually poor efficiency
(Wiedenmayer, 1998) or only a brief one (Forthman et al., 1992); sometimes they do not
improve well-being at all (Mason, 1993; Swaisgood et al., 2001; Little and Sommer, 2002)
or they may even cause stressful situations (Mc Phee, 2002).
Stereotypies are repetitive behaviours, invariant in form, and have no apparent
functional consequences (Mason, 1991b). Zoo exhibits for bears are usually small and
often poorly furnished. Bears kept in such barren environments, particularly from an early
age, tend to perform stereotypies (Forthman et al., 1992). For this reason the decrease of the
amount of stereotypies is often considered a good indication of an improvement in well-
being. However, the barren environments are not the unique explanation for stereotypies.
Rearing and husbandry procedures as well as genetic factors have been implicated in the
etiology of stereotyped behaviour (e.g., Mason, 1993; Liu et al., 2003). Hosey (2000)
noticed that visitors may affect the behaviour of primates contrary to that of other species.
Individual factors such as behavioural temperament are also known to play a role in the
development of stereotypy, because closely related animals, reared and housed under
identical conditions, can vary in stereotypy frequency (Mason, 1991a). However, it still
remains unclear that exactly what stereotypy performance tells us about the animal’s
subjective experience (Mason, 1991a,b). According to Vickery and Mason (2003), animals
with higher levels of stereotypy are behaviourally more persistent (for definition see Garner
and Mason, 2002). A good way to understand a captive animal is perhaps as emphasized by
Seidensticker and Doherty (1996) to know ‘just what mammals do in their exhibit spaces’.
As pointed out by Robinson (1998), inter-zoo comparisons between the different habitats
of the same species are potentially fruitful field of research. Most comparative studies using
large samples of parks to study the relationships between stereotypies and environmental
characteristics use surveys (Van Keulen-Kromhout, 1978; Carlstead et al., 1991; Bashaw
et al., 2001). In the present study, we chose to visit the parks, of course for a short period
S. Montaudouin, G. Le Pape / Applied Animal Behaviour Science 92 (2005) 129–141130
each, in order to collect the amount of stereotypy and quality of social relationships.
Moreover, keepers often do not know exactly the amount of stereotyped behaviours,
because animals generally change their activity when the keeper comes. Because, 26 out of
about 30 parks exhibiting brown bears in France were visited in the present study, we can
give a relatively exhaustive assessment of the situation.
In order to identify variables related to stereotypical behaviour or related to social
conflicts, in the present study we recorded numerous characteristics of each park such as
the individual animal history (sex and age, origin and years in present exhibit), the features
of the zoo environment (enclosure size, ground and vegetation), the rearing conditions
(food delivery schedule, indoor or not at night), the number of visitors, the presence of
nearby species. Because time of day, probably associated with management procedures
such as feeding, may be an important determining factor for the occurrence and/or
frequency of stereotypies, it was also recorded.
2. Methods
2.1. Data collection
A total of 26 French parks, one Belgian and one German park were visited at the rate of
one day each, from April to June 2003 except for five parks (Vincennes, Pesheray, Clos aux
Ours, Gramat, Han-sur-Lesse) which were visited in 2002 at the same season and for at
least three days each. Five parks were considered twice because either they had two
different enclosures or bears were alternatively outside in the morning and in the afternoon.
The total number of enclosures was 33.
In each case we consulted bear keepers and curators in order to learn about their animals
history and the rearing conditions they applied. Animals were observed from the opening
of the park (9 or 10 a.m.) till closing time (6 or 7 p.m.). All observations were performed by
the same person, positioned at the visitors site. Percentage of time spent in stereotyped
behaviour was evaluated and social interactions were qualitatively assessed. The amount of
stereotyped behaviour, as well as the kind of social relationships, is generally quite
consistent from one day to the next. Only one observation day in each park was considered
sufficient for a good estimate. Nevertheless a precise measure of behaviour during only one
day did not seem necessary and categorical data were prefered to quantitative data.
2.2. Subjects
Thirty-two male and 34 female bears were observed. Ages were encoded as young
(under 11 years old, 21 subjects) and adults (11 years old or more, 45 subjects). Six
enclosures exhibited exclusively female(s), 11 enclosures exhibited exclusively male(s),
and 16 exhibited both sexes. Three females had cubs (4 months old or 1 year old). Only one,
with two 1-year-old cubs, was not allowed out with the male.
Fourteen bears were born in the present enclosure, 35 in another one, 16 came from
tamers or circuses (bought from a zoo or caught in the wild), and one had an unknown
origin.
S. Montaudouin, G. Le Pape / Applied Animal Behaviour Science 92 (2005) 129–141 131
Five enclosures exhibited exclusively young animal(s), 7 enclosures exhibited
exclusively old animal(s): (25 years old or more), 12 enclosures exhibited medium age
animal(s), and 9 enclosures exhibited animals of varying age.
Number of years exhibited were almost equally distributed on both sides of 10 years (12
below and 16 above, four combined). Forty-nine out of the 66 bears were either born in the
enclosure or arrived before 4 years of age.
2.3. Housing
The enclosures were classified in five categories:
- cages: bears are confined in an enclosure less than 100 m2 with bars (2 enclosures);
- concrete pits: bears are totally surrounded by walls (8 enclosures);
- concrete plateaux: bears are surrounded by walls and separated from visitors by a frontal
moat (8 enclosures);
- natural ground surrounded by walls not allowing bears to see the surroundings
(6 enclosures);
- natural ground surrounded by fences or walls allowing bears to see the area around the
enclosure (9 enclosures).
A total of 21 enclosures allowed bears (n = 43) to see the surroundings.
More detailed environmental characteristics were classified as follows:
- outdoor surface area: more than 1000 m2 (8 enclosures), 400–1000 m2 (10 enclosures),
300 m2 or less (15 enclosures);
- ground: only concrete (12 enclosures), grass and concrete (9 enclosures), no concrete (12
enclosures);
- vegetation: lush grass (9 enclosures), a little grass (7 enclosures), no grass (17 enclosures),
accessible trees (10 enclosures), no trees or inaccessible trees (23 enclosures);
- pool size: small (size of one bear; 10 enclosures), medium (one or more bear can move
but not swim in it; 20 enclosures), large (bears can swim; 3 enclosures);
- visitors position: above (23 enclosures) or level with (10 enclosures);
- number of visitors during observation (personal estimate): no visitor (4 enclosures), low
crowd (10 enclosures), medium or large crowd (19 enclosures).
Lastly, the following items were encoded in ‘yes’ or ‘no’: presence of a pit (10
enclosures), carnivores in a neighbouring enclosure (17 enclosures), presence of a waterfall
(8 enclosures), of a den (8 enclosures), rocks (22 enclosures), treetrunks (27 enclosures);
visitors passing by train (6 enclosures).
2.4. Management
Most bears were housed in a separate indoor area when zoos were closed, and were
released each morning. However, in 12 enclosures bears were not locked inside at night and
had free access to indoor during the day.
S. Montaudouin, G. Le Pape / Applied Animal Behaviour Science 92 (2005) 129–141132
In 13 enclosures, bears were fed in the evening, in 9 enclosures they were fed with fruit
and vegetables in the morning in addition to the evening meal, in 10 enclosures they were
fed in the morning or in the afternoon. In 15 enclosures bears received popcorn from the
public and in 17 enclosures they received food thrown during shows by the staff.
2.5. Stereotypies
Four types of stereotypies were observed:
- pacing, present in 20 enclosures: the bear is continuously walking from left to right in a
straight line, placing its feet in exactly the same position on each way;
- circling or walking in figure-of-eight, present in 10 enclosures: the bear walks around
and around the enclosure, always following the same path;
- head-tossing, present in 7 enclosures: the bear suddenly throws its head back and turns it.
Head-tossing might be combined with pacing or circling;
- swaying, present in only 3 enclosures: the bear stands in front of door or fence and
continuously rocks the head from left to right, cyclically punctuated by leaping.
The amount of stereotypy was encoded in:
- no stereotypy: 20 bears;
- low: less than 21% of time; 22 bears;
- medium: 21% to 45% of time; 17 bears;
- high: more than 45% of time; 7 bears.
2.6. Social relationships
Social relationships were studied in the 25 enclosures exhibiting either two (17
enclosures) or three or more animals (8 enclosures). Each group of bears was labeled as
playful, medium or agonistic, these categories being as follows:
- playful (9 enclosures with paired animals and 1 enclosure with mother and two cubs):
when bears spent at least half the day playing with warm embraces, there was neither
attack nor avoidance movements;
- medium (9 enclosures): when there was neither play nor charge. While there was no
charge, threats and submission postures were sometimes observed. In enclosures with
three or more animals, relationships were called ‘medium’ if play in one pair and
avoidance movements in another one were observed, (n = 3 enclosures).
- agonistic (6 enclosures): when an animal kept a long distance between itself and another
one or when charges occurred an animal moves, generally growling, towards another one
and puts it to flight. There was no play.
2.7. Data analysis
Because several bears exhibiting stereotyped behaviours could live in the same
enclosure, and, on the other hand, stereotyped and non-stereotyped subjects could be
S. Montaudouin, G. Le Pape / Applied Animal Behaviour Science 92 (2005) 129–141 133
encountered in the same enclosure, stereotypy was considered as an individual
characteristic and subjects independent for statistical tests. As a consequence a database
with the 66 subjects as rows was used to study the relationships between stereotypy
and individual characteristics, housing and management. On the contrary, social
interactions were considered as characteristics of enclosures. Therefore, a database with
rows for the 25 enclosures with two or more bears was used to study social relationships. In
this database the amount of stereotypy was coded as the highest one observed in the
enclosure.
Different statistical tests were performed depending on cross tables. If the variable to
explain was binary (e.g., stereotypy versus no stereotypy), a logistic regression was
performed and followed by the Chi-square associated to the maximum likelihood (ML x2)
and his p-value. If both variables were non-ordered multinominal variables, the Chi-square
(x2) test was used with exact approximation. If only one variable was ordinal (e.g., amount
of stereotypy), the non-parametric Kruskal–Wallis (KW) test was used. If both variables
were ordered the non-parametric Jonckheere–Terpstra (JT) test for ordered alternatives
was used (Siegel and Castellan, 1988).
Because numerous tests were possible on this set of data a p = 0.025 level was chosen
for type one risk. This Bonferoni-like correction was not very important in order to
highlight effects with a noteworthy range. As a consequence these results need to be
strengthened using further observations on another population.
3. Results
3.1. Stereotypical behaviour
Except for Tables 1 and 7, only bears showing stereotypies were used for calculations.
All tables hold frequencies i.e., the number of bears of each category.
3.1.1. Individual characteristics of animals
Stereotyped behaviour was more frequent in adult than in young bears (ML x2 = 4.19,
one-tailed p = 0.020; Table 1). The amount of stereotypy increased with the years spent in
the enclosure (JT = 2.22, one-tailed p = 0.013; Table 2).
Head-tossing was significantly more frequent in young animals than in adult ones (ML
x2 = 9.94, two-tailed p = 0.002; Table 3).
Pacing was more frequent when bears were housed with unrelated bears (ML x2 = 8.48,
two-tailed p = 0.004; Table 4).
S. Montaudouin, G. Le Pape / Applied Animal Behaviour Science 92 (2005) 129–141134
Table 1
Age of animals and presence of stereotypy in all subjects
No stereotypy Stereotypy ML x2-test
Adult 10 35 ML x2 = 4.19,
one-tailed p = 0.020
Young 10 11
Number of bears of each category.
On the contrary, circling was never observed in bears housed with only unrelated bears
and was more frequent in bears housed with only related bears (ML x2 = 15.28, two-tailed
p < 0.001; Table 4).
3.1.2. Enclosures characteristics
The frequence of stereotyped circling behaviour was significantly lower when the
surrounding was visible by bears (ML x2 = 5.61, two-tailed p = 0.018; Table 5).
S. Montaudouin, G. Le Pape / Applied Animal Behaviour Science 92 (2005) 129–141 135
Table 2
Years spent in the enclosure and amount of stereotypy in the 45 stereotyped bears for which the time spent in the
enclosure was known
Low level
of stereotypy
Medium level
of stereotypy
High level
of stereotypy
Jonckeere–Terpstra test
More than 10 years 8 9 6 JT = 2.22, one-tailed
p = 0.013
Below 11 years 14 7 1
Number of bears of each category.
Table 3
Head-tossing stereotypy and age in the 46 streotyped bears
No head-tossing Head-tossing ML x2 test
Adult 33 2 ML x2 = 9.94,
two-tailed p = 0.002
Young 5 6
Table 4
Pacing/circling stereotypy in bears housed with either only related or only unrelated fellows
Type of stereotypy Housing fellows ML x2-test
Only related Only unrelated
Pacing = yes 6 12 ML x2 = 8.48,
two-tailed p = 0.004
Pacing = no 14 2
Circling = yes 11 0 ML x2 = 15.28,
two-tailed p < 0.001
Circling = no 9 14
Table 5
Circling behaviour and surrounding view in the 46 stereotyped bears
Surrounding view No surrounding view ML x2-test
Circling = yes 6 10 ML x2 = 5.61,
p = 0.018
Circling = no 22 8
The amount of stereotypy was significantly lower in enclosures with a medium or large
pool (JT = 69, p < 0.001; Table 6).
Most of the time the number of visitors was medium or high. There was no significant
relationship between number of visitors and number of stereotyped bears.
Surface area, types of ground, grass or trees did not show significant relationships
neither with the presence nor with the amount of stereotypies.
3.1.3. Enclosures management
As noted above adult bears showed stereotypical behaviour more frequently than young
ones. This was particularly the case in bears locked inside by night (ML x2 = 5.62, one-
tailed p = 0.009; Table 7).
Stereotyped behaviour occurred more often in the afternoon (x2 = 13.73, p = 0.001;
Table 8, bottom). 54% of bears showed stereotypy only in the afternoon, 9% only in
the morning and 37% throughout the day. This was related to feeding time, bears fed in
the evening showing more stereotypy in the afternoon (x2 = 18.79, p = 0.004; Table 8,
top).
S. Montaudouin, G. Le Pape / Applied Animal Behaviour Science 92 (2005) 129–141136
Table 7
Age of animals and presence of stereotypy in the 41 bears locked by night
No stereotypy Stereotypy ML x2-test
Adult and old 3 23 ML x2 = 5.62,
one-tailed p = 0.009
Young 7 8
Table 8
Main feeding time and periods of stereotypy in 45 bears for which feeding time was known
Feeding time Periods of stereotypy x2 exact test
Only morning Only afternoon All day
Morning 0 1 3 x2 = 18.8, p = 0.004
Afternoon 3 1 2
Morning and evening 0 7 6
Evening 1 15 6
Total 4 24 17 x2 = 13.73, p = 0.001
Table 6
Pool size and amount of stereotypy in the 46 stereotyped bears
Pool size Low level
of stereotypy
Medium level
of stereotypy
High level
of stereotypy
Jonckeere–Terpstra test
Small 0 9 4 JT = 69, p < 0.001
Large or medium 22 8 3
3.1.4. Stereotypies and social relationships
No significant relationships were found between stereotypy and social behaviour.
3.2. Social relationships
Only the 25 enclosures with at least two bears were studied in this chapter.
A relationship was observed between social behaviour and the number of bears in the
enclosure. Playful interactions were more common in paired bears, and agonistic
behaviours were more common in enclosures with more than two bears (KW = 5.16,
p = 0.023; Table 9).
Playful interactions were not related to the gender of the pairs. They were observed in
nine paired bears: one male/male enclosure, two female/female enclosures, and six mixed
enclosures. Social interactions did not seem to be influenced by differences in enclosure
management.
4. Discussion
4.1. Age, sex and origin
Origin and sex were not related to the occurrence of stereotypy. Stereotyped behaviour
was more frequent in animals over 10 years old (78% of stereotyped bears versus 52% in
young subjects). Because the amount of stereotypy was higher in subjects living for more
than 10 years in the enclosure (six animals with a high level after more than 10 years in the
enclosure versus only one in subject below 11 years), the effect of ageing is difficult to
understand. The case of old animals recently introduced in an enclosure was lacking in our
sample.
Contrary to pacing or circling, head-tossing was very typical of young bears (only 6% in
adults versus 55% in young subjects). This movement was occasionally observed during
strained moments in cubs reared with both parents. Some stereotyped movements observed
in young captive animals may also be due to a deprived early mother-rearing experience
and are not necessarily a direct response to the present environment. For example, a too
early mother–cub separation can cause such disorders, as it was observed in orphaned
Rhesus monkeys (Berman, 1981, in Stevenson, 1983). Liu et al. (2003) observed that hand-
reared sloth bears performed stereotyped and self-directed behaviours more frequently
than did mother-reared sloth bears. Four bears in this study came from a trainer, five from a
S. Montaudouin, G. Le Pape / Applied Animal Behaviour Science 92 (2005) 129–141 137
Table 9
Social behaviour and number of bears in the 25 enclosures with non-isolated animals. Cells are frequencies i.e., the
number of enclosures of each category
Playful
relationship
Medium
relationship
Agonistic
relationship
Kruskal–Wallis test
Paired bears 9 6 2 KW = 5.16, two-tailed p = 0.023
Three or more bears 1 3 4
circus, and seven from a tamer. All these bears were separated at a very early age from their
mother (in the wild or in a zoo), before one year. We observed an isolated orphaned cub
sucking his forepaws (not in the present data). Pajetnov and Pajetnov (1998) suggested that
cubs which adopted this behaviour became easily irritated, were hyper-reactive, and stayed
motionless for long periods. Berman (1981 in Stevenson, 1983), observed the same
characteristics in orphaned Rhesus monkeys.
4.2. Housing and management
In the present data only adult subjects were housed alone. Social isolation was not
associated with a significantly higher occurrence of stereotypy (87.5% in isolated versus
67.2% in grouped subjects), contrary to what is observed in social animals like stabled
horses (Cooper et al., 2000). Even if brown bears are able to live in pairs or to make up
groups in some situations (Fagen and Fagen, 1996), the social isolation is not so different
from the natural habits of this animal.
Although wild brown bears use large areas, stereotyped movements and bad social
relationships were observed both in small and large enclosures.
The frequency of stereotypy was higher if over 10 years old animals were locked
indoors during the night (88.5% of stereotyped subjects). Moreover, stereotypies were
particularly frequent in the afternoon, especially if bears received their main feeding in the
evening. Expectation of the indoor cage and/or of the meal is probably the cause of this
result, especially when pacing or circling are exhibited in front of the cage’s door. An
expectation of the cage per se cannot be dispelled, especially if cages are not open during
the day. Waitt and Buchanan-Smith (2001) found that when macaques were waiting to be
fed, rates of self-directed behaviour, inactivity, vocalization and abnormal behaviours
increased significantly. Cooper et al. (2000) founded that weaving in horses was most
common before feeding in the morning and before leading animals to pasture in the
afternoon. Wechsler (1991) observed yawning and tongue-flicking regularly during
stereotyped walking of polar bears, this being interpreted by the author as feeding
anticipation. It can be hypothesised that stereotypies in the late afternoon are generally
related to feeding. However, hunger is not necessarily the cause. Some keepers tried to
decrease these stereotyped movements by doubling the daily food ration, but in vain. In the
wild, brown bears spent a long time gleaning small fruits or leaves and are not adapted to a
single substantial meal. They are probably interested in food and foraging for the pleasure
it brings.
When some stereotypies can be viewed as food or indoor cage expectation, some
seemed to be related to physical or social environment. In our results, the amount of
stereotypy was lower in enclosures equipped with a large or medium pool (not any case
with low level of stereotypy when the pool was small versus 22 when the pool was large or
medium), and circling was less frequent in enclosures with view of the surroundings (21%
of bears exhibiting circling versus 56% when a surrounding view was lacking).
Contrary to circling, pacing was predominant in bears housed with unrelated fellows
(86% of bears pacing and no one circling when housed with unrelated). Moreover,
aggression was lower and play was higher when the group was made up of only two
subjects (53% of playful relationships in pairs versus 13% in larger groups; 12% of
S. Montaudouin, G. Le Pape / Applied Animal Behaviour Science 92 (2005) 129–141138
agonistics relations in pairs versus 50% in larger groups). Pajetnov and Pajetnov (1998)
observed that despite intrafamilial bonds, large litters of four or more cubs were ‘unstable’,
i.e. were aggressive to each other. Competition for social contact, including sexual
attraction, seemed to be very common in groups of three or more. In 2 enclosures,
aggression was related to the presence of a cub. In one case the mother was mating and kept
the cub away. In the other case she chased the male when he was too close to the cub. It
must be emphasized that observations were all performed in spring. Because of heat and
the accompanying sexual behaviour, spring is probably the period with the most potential
sources of conflict.
5. Conclusion
The results of the present study suggest changes in housing and management strategies
that may reduce stereotypical behaviour and improve the social relationships of brown
bears. A surrounding view is desirable. A large or medium pool is a recommended facility.
Locking animals inside at night increases the frequency of stereotypy, especially in adult
subjects.
The social relationships will be more playfull and less agonistic if not more than two
bears are housed together, even in the case of a male with females.
This study suggests not to separate the cub from the mother too early. Moreover,
zookeepers must watch out for appearance of head-tossing movements. Large daily meals
only in the evening are not suitable. Scattering small pieces of food around the enclosure
will probably promote curiosity and food-exploration.
As suggested by Mellen and MacPhee (2001), enrichment must be defined for each
animal’s individual history and the constraints of each specific exhibit, and may change
over time. A real understanding of the motivations underlying behaviour is necessary. It
would be probably helpful to have a better knowledge of the repertoire of free-ranging
bears and to know if similar movements are performed in the wild, not to justify but rather
to understand.
Acknowledgements
Without the enthusiastic welcome in many parks, this study could not have been
representative of French zoo-housed brown bears. These Park Zoos were Parc zoologique
of Bois de Saint Pierre (F-Poitiers), Boissiere du Dore, CERZA (F-Hermival les Vaux),
Mulhouse, Maubeuge, Belval, Bois de Coulange (F-Amneville), Sainte-Croix (F-Rhodes),
La Fleche, Menagerie du Jardin des Plantes (F-Paris), Abrets, Les Angles, Casteil, La
Barben, Mont Faron, Lunaret (F-Montpellier), Jardin Botanique Tours, Pessac (F-
Bordeaux), Bassin d’Arcachon (F-La teste de Buch), La Colline aux Marmottes (F-Argeles
Gazost) La Maison de l’Ours (F-St Lary), Le Pal (F-St Pourcain-sur-Besbre), Pescheray (F-
Le Breil-sur-Merize), Le Clos aux Ours (F-Borce), Gramat, Vincennes, Grottes de Han-
sur-Lesse (Belgium), NP Bayerischer Wald (Germany).
We are grateful to Dr. S. Rogerson for improving the English.
S. Montaudouin, G. Le Pape / Applied Animal Behaviour Science 92 (2005) 129–141 139
References
Bashaw, M.J., Tarou, L.R., Maki, T.S., Maple, T.L., 2001. A survey assessment of variables related to stereotypy in
captive giraffe and okapi. Appl. Anim. Behav. Sci. 73, 235–247.
Bashaw, M.J., Bloomsmith, M.A., Marr, M.J., Maple, T.L., 2003. To hunt or not to hunt? A feeding enrichment
experiment with captive large felids. Zoo Biol. 22, 189–198.
Carlstead, K., Seidensticker, J., Baldwin, R., 1991. Environmental enrichment for zoo bears. Zoo Biol. 10, 3–16.
Cooper, J.J., McDonald, L., Mills, D.S., 2000. The effect of increasing visual horizons on stereotypic weaving:
implications for the social housing of stabled horses. Appl. Anim. Behav. Sci. 69, 67–83.
Fagen, R., Fagen, J.M., 1996. Individual distinctiveness in brown bears, Ursus arctos. Ethology 102, 212–226.
Fischbacher, M., Schmid, H., 1999. Feeding enrichment and stereotypic behavior in spectacled bears. Zoo Biol.
18, 363–371.
Forthman, D.L., Elder, S.D., Bakeman, R., Kurkowski, T.W., Noble, C.C., Winslow, S.W., 1992. Effects of feeding
enrichment on behavior of three species of captive bears. Zoo Biol. 11, 187–195.
Garner, J.P., Mason, G.J., 2002. Evidence for a relationship between cage stereotypies and behavioural
disinhibition in laboratory rodents. Behav. Brain Res. 136, 83–92.
Hediger, H., 1955. Studies of the Psychology and Behaviour of Captive Animals in Zoos and Circuses.
Butterworths Scientific Publications, London, UK, pp. 166.
Hosey, G.R., 2000. Zoo animals and their human audiences: what is the visitor effect? Anim. Welfare 9,
343–357.
Laule, G., Desmond, T., 1998. Positive reinforcement training as an enrichment strategy. In: Shepherdson, D.J.,
Mellen, J.D., Hutchins, M. (Eds.), Second Nature: Environmental Enrichment for Captive Animals. Smith-
sonian Institution Press, Washington, DC, pp. 302–313.
Little, K.A., Sommer, V., 2002. Change of enclosure in Langur monkeys: implications for the evaluation of
environmental enrichment. Zoo Biol. 21, 549–559.
Liu, D., Wang, Z., Tian, H., Yu, C., Zhang, G., Wei, R., Zhang, H., 2003. Behavior of giant pandas (Ailuropoda
melanoleuca) in captive conditions: gender differences and enclosure effects. Zoo Biol. 22, 77–82.
Lukas, K.E., Hoff, M.P., Maple, T.L., 2003. Gorilla behavior in response to systematic alternation between zoo
enclosures. Appl. Anim. Behav. Sci. 81, 367–386.
Mason, G.J., 1991a. Stereotypies and suffering. Behav. Proc. 25, 103–115.
Mason, G.J., 1991b. Stereotypies: a critical review. Anim. Behav. 41, 1015–1037.
Mason, G.J., 1993. Forms of stereotypic behaviour. In: Lawrence, A.B., Rushen, J. (Eds.), Stereotypic Animal
Behaviour: Fundamentals and Applications to Welfare. CAB International, Wallingford, pp. 7–40.
Mc Phee, M.E., 2002. Intact carcasses as enrichment for large felids: effects on on- and off-exhibit behaviors. Zoo
Biol. 21, 37–47.
Mellen, J., MacPhee, M.S., 2001. Philosophy of environmental enrichment: past, present, and future. Zoo Biol. 20,
211–226.
Morimura, N., 2003. A note on enrichment for spontaneous tool use by chimpanzees (Pan troglodytes). Appl.
Anim. Behav. Sci. 82, 241–247.
Pajetnov, V., Pajetnov, S., 1998. Food competition and grouping behavior of orphaned brown bear cubs in Russia.
Ursus 10, 571–574.
Renner, M.J., Plebani Lussier, J., 2002. Environmental enrichment for the captive spectacled bear (Tremarctos
ornatus).. Pharmacol. Biochem. Behav. 73, 279–283.
Renner, M.J., Feiner, A.J., Orr, M.G., Delaney, B.A., 2000. Environmental enrichment for new world
primates: introducing food-irrelevant objects and direct and secondary effects. J. Appl. Anim. Welfare
Sci. 3 (1), 23–32.
Robinson, M.H., 1998. Enriching the lives of zoo animals, and their welfare: where research can be fundamental.
Anim. Welfare 7, 151–175.
Seidensticker, J., Doherty, J.G., 1996. Integrating animal behavior and exhibit design. In: Kleiman, D.G., Allen,
M.E., Thompson, K.V., Lumpkin, S. (Eds.), Wild Mammals in Captivity: Principles and Techniques.
University of Chicago Press, Chicago, pp. 180–190.
Siegel, S., Castellan, N.J., 1988. Non Parametric Statistics for the Behavioral Sciences. McGraw-Hill, New York,
USA, p. 399.
S. Montaudouin, G. Le Pape / Applied Animal Behaviour Science 92 (2005) 129–141140
Stevenson, M.F., 1983. The captive environment: its effect on exploratory and related behavioural responses in
wild animals. In: Archer, J., Birke, L. (Eds.), Exploration in Animals and Humans. Van Nostrand Reinhold,
University Press, Cambridge, pp. 176–197.
Swaisgood, R.R., White, A.M., Zhou, X., Zhang, H., Zhang, G., Wei, R., Hare, V.J., Tepper, E.M., Lindburg, D.G.,
2001. A quantitative assessment of the efficacy of an environmental enrichment programme for giant pandas.
Anim. Behav. 61, 447–457.
Van Keulen-Kromhout, G., 1978. Zoo enclosures for bears: their influence on captive behaviour and reproduction.
Int. Zoo Yearb. 18, 177–186.
Vickery, S.S., Mason, G.J., 2003. Behavioral persistence in captive bears: implications for reintroduction. Ursus
14 (1), 27–34.
Waitt, C., Buchanan-Smith, H.M., 2001. What time is feeding ? How delays and anticipation of feeding schedules
affect stump-tailed macaque behavior. Appl. Anim. Behav. Sci. 75, 75–85.
Wechsler, B., 1991. Stereotypies in polar bears. Zoo Biol. 10, 177–188.
Wiedenmayer, C., 1998. Food hiding and enrichment in captive Asian elephants. Appl. Anim. Behav. Sci. 56,
77–82.
S. Montaudouin, G. Le Pape / Applied Animal Behaviour Science 92 (2005) 129–141 141