Effects of Ambient Environmental Factors on the Stereotypic Behaviors of Giant Pandas (Ailuropoda melanoleuca)
Effects of Ambient Environmental Factors on the Stereotypic Behaviors of Giant Pandas (Ailuropoda melanoleuca)
He Liu 0 1
Hejun Duan 1
Cheng Wang 1
0 Beijing Key Laboratory of Captive Wildlife Technology, Giant Panda Research Centre , Beijing Zoo, Beijing , China , 2 Beijing Municipal Key Laboratory of Food Poisoning Diagnosis Traceability Technology, Beijing Centre of Disease Control and Prevention , Beijing , China , 3 Key Laboratory of Digital Earth Science, Institute of Remote Sensing and Digital Earth, Chinese Academy of Sciences , Beijing , China
1 Editor: Zhigang Jiang, Institute of Zoology , CHINA
Stereotypies are commonly observed in zoo animals, and it is necessary to better understand whether ambient environmental factors contribute to stereotypy and how to affect animal welfare in zoo settings. This study investigated the relationships between stereotypic behaviors and environmental factors including ambient temperatures, humidity, light intensity, sound intensity and number of visitors. Seven giant pandas were observed in three indoor enclosures and three outdoor enclosures. Environmental factors were measured for both indoor and outdoor enclosures and the effect they had on stereotypical behaviors was investigated. Our research found that light intensity significantly correlated with all stereotypies behaviors. Higher environmental temperature reduced the duration of pacing but increased the frequency of pacing, the duration and frequency of door-directed, meanwhile the duration of head-toss. However, we found no noticeable effect of humidity on stereotypic behaviors except for the frequency of head-toss. We also found that sound intensity was not correlated with stereotypies. Finally, the growth of visitors was negatively associated with the duration of door-directed. These results demonstrated that various environmental factors can have significant effects on stereotypic behaviors causing the expression of various stereotypies. Thus, stereotypies in zoo animals may not simply represent suboptimal welfare, but rather might be adopted as a means of coping with an aversive environment.
Data Availability Statement: All relevant data are
within the paper and its Supporting Information
Funding: This study was financially supported by
the Memphis Zoo Collaborative Project
(MPES0611), Science & Technology Project of Beijing
City Park Management Center (No.2017), the
International Science & Technology Cooperation
Program of China (2013DFG21640) and Beijing
Health Research and Development of Special
Project (No.2011-1013-01). The funders had no
role in study design, data collection and analysis,
Zoo environments, though they often strive to mimic natural environments, are necessarily
different from an animal's in-situ habitat. Stereotypic behavior is rarely observed in wild
animals, which means that zoo-housed animals may reflect an abnormal interaction between
animal and environment [
]. Stereotypies are often associated with a variety of possible stressors,
including inadequate control over environment and lack of opportunity to express natural
]. Thus, stereotypies have often been used as behavioral measures of animal
welfare or psychological well-being [
4, 5, 6, 7
]. Although the causes of stereotypic behavior are
often unknown, stereotypies have been shown to be environmentally induced, developing in
decision to publish, or preparation of the
situations when an animal's life is in some way less than optimal [
1, 8, 9
]. In such instances, it is
thought that stereotypy is a homeostatic adaptation by zoo-housed animals to cope with their
10, 11, 12
]. It is also suggested that stereotypic behavior may be one method by
which captive animals pass their time, or use it as a substitute for normal free-ranging behavior
]. Furthermore, some authors have demonstrated that stereotypies have evolved as a kind
of self-generated enrichment [
Stereotypic behavior has been well documented in zoo-housed animals [
16, 17, 18, 19, 20,
21, 22, 23, 24, 25
]. Several environmental factors, including space limitation [
], effects of
feeding schedule [
], restraint of environmental control , and lack of stimulation [
have been identified in relation to the development of stereotypies [
carnivores generally exhibit stereotypic pacing . For example, leopard cats (Felis bengalensis)
housed near natural predators or provided with inadequate hiding spaces, increased their
stereotypic pacing [
]. Similarly, stereotypical pacing in leopards (Panthera pardus) also increased
when kept ªoff exhibitº in small, barren holding quarters devoid of natural light [
Other studies have found that there were great interspecies differences in terms of the types
of stereotypies which zoo-housed animal might develop. Farmed blue foxes (Alopex lagopus)
increased locomotory stereotypic behaviors, when they were provided with larger cages [
Alternatively, walruses (Odobenus rosmarus) and giraffes (Giraffa camelopardalis) often display
an oral stereotypic behavior [16, 35±37]. Even closely related animals often differ in their
behavioral responses to zoo environments [
]. Polar bears (Ursus maritimus) express stereotypic head
swing, stereotypic walking and repetitive swimming bouts in a zoo setting [
]. Asiatic black
bears (Ursus thibetanus) and Malayan sun bears (Helarctos malayanus) have been observed to
exhibit locomotor, oral and head swaying stereotypies [36±38]. Mammals are not the only
species to express stereotypies and different species develop different stereotypic behaviors .
Cockatoos are very prone to self-plucking, whereas certain other parrot species are far less
].While previous research has explored the relationship between a single ambient
environmental factor and stereotypical behaviors [
], there is a general lack of information on
how zoo-housed animals cope with variations to a suite of different environmental factors. Rees
] described how zoo-housed Asian elephants (Elephas maximus) exhibited a strong negative
correlation between maximum daily temperature and the frequency of stereotypic behavior.
] reported that the time spent pacing in fennec foxes (Vulpes zerda) was linked to
the number of zoo visitors. Owen et al. [
] and Powell et al. [
] analyzed the effect of
construction noise on giant pandas and found that noise was associated with changes in behavior.
Very few studies report the influence of multiple environmental factors, such as ambient
temperature, humidity, sound intensity, light intensity and visitors on the stereotypic behaviors
within a zoo environment. It is also unclear if specific environmental factors induce certain
stereotypies or if they cause a general increase.
As an endangered species, giant pandas represent a symbol of animal conservation,
becoming quite common in worldwide zoos, with 396 individuals distributed within 72 zoos in 15
countries including the United states, Canada, Mexico, United Kingdom, Austria, Belgium,
France, Spain, Australia, Japan, Malaysia, Singapore and Thailand in 2014 [
44, 45, 46
]. For the
well-being of species kept in zoos outside of their natural habitat, including but not limited to
the giant panda, it is crucial to learn the relationship between ambient environmental factors
of zoos and stereotypic behaviors. However, there is a lack of specific studies on ambient
environmental conditions and their relationship to stereotypies.
The objectives of the current study on giant panda are as follows: a) to compare the
duration and frequency of stereotypic behaviors exhibited by giant pandas in both outdoor and
indoor enclosures; b) to determine whether stereotypic behaviors are influenced by ambient
environmental factors; c) to analyze the relationship between stereotypy and animal welfare.
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Born in Wolong
Born in Wolong
Born in Beijing
Born in Wolong
Born in Wolong
Born in Beijing
Born in Beijing
Material and Methods
No special permission for use of animals in observational behavioral studies is required in
China. This study was approved by the faculty of the Beijing zoo and National Bureau of
Forestry. The individual in this manuscript has given written informed consent (as outlined in
PLOS consent form) to publish case details of this study.
Study Animals and Husbandry
The seven zoo-housed giant pandas in the study were born in captivity and held individually
by the Beijing zoo (Table 1). The giant pandas alternate between inside enclosures and outside
exhibition areas every two days. Pandas were moved outside between 08:00 and 08:30 and
were returned to indoor enclosures between 16:00 and 17:00. Behavioral observation sessions
did not include the time period of 11:00±14:00 because zoo-housed giant pandas usually rest
during this time frame and are largely inactive[
47, 48, 49
]. Details of the three large outside
exhibitions and three small indoor enclosures are presented in Table 2.
Bamboo and water were supplied to the giant pandas at various times of day at every
enclosure as their main diet. Supplementary diets containing small amounts of apple, carrot, egg,
beef and specialized biscuit, were fed to the pandas twice daily between 08:30±09:30 and 15:30±
16:30 at every enclosure. In order to minimize interference from keepers during the observation
period, the feeding time was delayed in the afternoon until the end of the observation.
Behavioral Data Collection
An ethogram with four categories of stereotypic behavior is listed in Table 3[
]. At the
beginning of the formal observation, there was a pilot observation allowing observers to become
familiar with giant pandas behavior. After a brief training session, interobserver agreement
was determined based on observers scoring the same 10 mins video of giant panda behavior.
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Back and forth, or perimeter traveling in a repetitive, sustained, stereotyped
pattern. Must travel the same route at least 3 times.
Animal abruptly lifting head upward and/or to the side in a swinging
movement, often occurs during turning. These actions are repeated at least
Standing in one place and continuously moving the head from side to side
horizontally at least 3 times.
Animal waits at the door with restlessness. Standing on hind legs and
putting fore legs on door to knock or push the door, or scratching itself to
indicate an anticipatory of food or keepers. These actions are repeated at
least 3 times in succession.
Interobserver reliability was greater than or equal to 95% [
50, 51, 52
]. Focal sampling and
continuous recording methods were taken during observation [
]. Observations were conducted
over two periods (9:00±11:00 and 14:00±16:00) daily from 1st February to10th May. One giant
panda was observed for each period.
Giant pandas were randomly observed on an individual basis in different enclosures.
Observation lasted 4 hours with five different environmental factors being measured each day.
The observers were located on the outside perimeter of enclosures to ensure visual access to
pandas during the entirety of the recording period [
All behavioral data were recorded as duration and frequency of occurrence. The duration
of behavior was the percentage of time spent on performing the behavior within one hour[
]. The frequency of behavior was the number of times that behavior occurred per hour[
]. The different observations in the indoor versus outdoor were considered as statistically
independent and multiple observations from the same individual in one hour were considered
as statistically independent of one another hour [
Environmental Data Collection
Ambient temperature and humidity were measured using a TES 1360A digital humidity/
temperature meter (TES Electrical Electronic Corp, Taiwan). Light intensity was collected by a
TES 1335 digital light meter (TES Electrical Electronic Corp. Taiwan). Temperature, humidity
and light intensity were examined at 09:00, 10:00, 11:00, 14:00, 15:00 and 16:00. The
temperature, humidity and light intensity were calculated by averaging each measurement per hour.
Ambient sound was measured using a TES-1351 sound level meter (TES Electrical Electronic
Corp. Taiwan) inside and outside of the enclosures. A low range measurement of 35±90 dB
(decibel units) and A-weighting were used to obtain a slow response and comparatively stable
sound level of giant panda house. The sound intensity was recorded in decibels at ten-minute
intervals and averaged all measurement per hour. The number of visitors were recorded by
counting the total number of people around the subject's enclosures in each hour.
The conventional statistics are applied for the effects of environmental measurements on each
individual test. Total seven giant pandas were observed and then each giant panda was
examined independently, the descriptive statistics are reported.
PASW Statistics software for Windows (version 17.0, SPSS Inc.: Chicago, IL, USA) was
applied in the statistical analysis. All data were determined for assumption of normality by
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one-sample Kolmogorov-Smirnov test and homogeneity of variance by Levene's test. The
duration and frequency of each behavior were calculated for one hour observation period. All
data including environmental factors and behaviors were tested to be non-normally
distributed, thus non-parametric data was transformed by arcsine, square root or logarithm.
However, for most data were still non-parametric after transformation, non-parametric analysis
was then used to analyze all data. Generalized Linear Models (GLMs) were conducted to
examine the relationship between behavior and environmental factors. Mann-Whitney U test was
used to compare the environmental factors between indoor enclosure and outdoor enclosure.
Nonparametric Kruskal-Wallis tests were used to determine the individual difference within
samples. There were no significant differences in the stereotypic behaviors based on gender
and age (P>0.05). Wilcoxon signed ranks test was performed to compare the difference of
behaviors and environmental variables between indoor enclosures and outdoor enclosures.
The Mean±SE was reported for the untransformed data. All values (P<0.05) are presented in
Differences between Outdoor Enclosures and Indoor Enclosures
More than 522 hours of data were collected from seven giant pandas in five months, with each
panda being observed for seventy hours on average. The sum of duration of all four stereotypies
(Pacing, Head-toss, Head-weaving, and Door-directed) between outdoor and indoor enclosures
exhibited similar trends in different periods (Fig 1). The duration and frequency of stereotypic
behaviors in outdoor enclosures were significantly higher than those in indoor enclosures (Z =
-5.381, P<0.001; Z = -6.651, P<0.001; respectively). Particularly, giant pandas showed
significantly higher duration (Z = -5.737, P<0.001; Z = -7.477, P<0.001; respectively, Fig 2) and
Fig 1. The duration of stereotypies in different periods between outdoor enclosures and indoor
enclosures. Standard errors are represented in the figure by the error bars attached to each sign. Diamonds
represent outdoor enclosures, circles represent indoor enclosures.
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Fig 2. The duration of stereotypies between outdoor enclosures and indoor enclosures. The dark column
represents the mean duration of stereotypies in outdoor enclosures. The wall column respresents the mean
duration of stereotypies in indoor enclosures. Standard errors are represented in the figure by the error bars
attached to each column. There was a significant difference in the duration for head-toss and pacing between
outdoor enclosures and indoor enclosures(P<0.05).
frequency (Z = -5.697, P<0.001; Z = -7.550, P<0.001; respectively, Fig 3) for head-toss and
pacing in outdoor enclosures. By contrast, there were no significant differences in the duration for
door-directed and head-weaving (Z = -0.498, P = 0.619; Z = -0.869, P = 0.385; respectively; Fig
2), but the frequency of door-directed in outdoor environment was higher than those for indoor
enclosures (Z = -3.557, P<0.001, Fig 3).
There was a significant difference in environmental factors between indoor enclosures and
outdoor enclosures (Table 4). Light intensity of outdoor enclosures was significantly higher
than that of indoor enclosures (Z = -19.652, P<0.001, Table 4). However, the humidity, sound
intensity and number of visitors for external enclosures were significantly lower than those for
internal enclosures (Z = -3.392, P = 0.001; Z = -11.973, P<0.001; Z = -2.440, P = 0.015;
respectively, Table 4). Temperature of the indoor enclosures was higher than that of the outdoor
enclosures from February to mid-March, but lower from mid-March to May. However, there
was no significant temperature difference between both enclosures (Z = -1.771, P = 0.077).
The relationship of Environmental Factors and Stereotypies
In this study, environmental temperature ranged between -2.38ÊC and 29.20ÊC (Table 4).
Ambient temperature negatively related with duration of pacing, but positively correlated with
the duration of head-toss, the duration of door-directed, the frequency of door-directed and
the frequency of pacing (P<0.05, Table 5). By contrast, ambient temperature did not
significantly affect the other stereotypic behaviors such as the duration of head-weaving, the
frequency of head-weaving and head-toss. Environmental humidity varied between 10.58% RH
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Fig 3. The frequency of different stereotypy in outdoor enclosures and indoor enclosures. The dark column
represents the proportion of stereotypies in outdoor enclosures. The wall column respresents the proportion of
stereotypies in indoor enclosures. Standard errors are represented in the figure by the error bars attached to each
column. There was a significant difference in the frequency of Door-direct, Head-toss and Pacing between outdoor
enclosures and indoor enclosures(P<0.05).
and 85.50% RH with a mean of 35.10% RH (Table 4). Pacing, door-directed, head-weaving
and the duration of head-toss did not significantly correlate with RH. (P>0.05, Table 5).
In outdoor exhibition, light intensity maximum was at midday when the sun was directly
overhead at 70,016.67 Lux. The average Lux value was 25,363.00 (SD = 13,866.08; n = 279).
Light intensity diminished to 11.20 Lux (SD = 50.37, n = 243) in indoor enclosures, averaging
at 68.63. Head-toss, pacing and door-directed behaviors presented a strong correlation with
light intensity (P<0.05, Table 5).
The mean sound intensity was 59.16±5.47 dB (n = 511). The maximum noise was 79.20dB
and the minimum was 46.87 dB (see Table 4). The level of sound did not significantly affect
Note: ªNº represents the sample size.
* indicate signi®cant differences between indoor and outdoor enclosures P<0.05.
Note: Bold indicate that the stereotypies were signi®cantly negatively correlated with environmental factors (P<0.05). The duration of pacing negatively
correlated with temperature and light intensity. The duration of head-toss positively correlated with temperature and light intensity, while the frequency of
head-toss positively correlated with humidity and light intensity. The frequency of pacing positively correlated with temperature and light intensity; the
frequency of head-weaving negatively correlated with light intensity. Door-directed positively correlated with temperature, while negatively correlated with
light intensity. The duration of door-directed negatively correlated with the number of visitors
the stereotypic behaviors and there were no significant correlations between number of visitors
and the stereotypic behaviors (P>0.05, Table 5).
Effect of Environmental Factors
Of the five environmental factors recorded in this study, humidity had the lowest effect on the
stereotypic behavior. Nevertheless, temperature and light intensity were significantly related to
stereotypic behaviors. When comparing stereotypic behaviors of giant pandas, a significant
difference emerges between outdoor and indoor enclosures. Giant pandas surprisingly spent
more time on pacing and head-tossing and showed a significant increase in frequency of
doordirected behavior when located in the outdoor enclosures. Similar results were observed in
Indian leopards (Panthera pardus) which displayed higher levels of stereotypic pacing in
offshow exhibit areas than on-show exhibit enclosures [
]. Similarly, Tian et al.[
] found that
stereotypic behaviors of juvenile giant pandas did not differ significantly between semi-natural
enclosures and traditional enclosures. Our results indicate that environmental differences
between outdoor versus indoor enclosures play an important role in behavioral management
and husbandry of zoo-housed giant pandas.
Different Environmental Factors Induced Different Stereotypies
Giant pandas may take an avoidance strategy to cope with anthropogenic environmental
change, due to the absence of an ability to escape the potential inadequate environmental
stimuli in the zoo. Ambient temperature and light intensity had a significant influence on pacing
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behavior. Rees [
] reported that low environmental temperature caused an increase of
stereotypic behavior in zoo-housed Asian elephants. In contrast, our current study showed that
higher ambient temperature caused a reduction of the duration and a rise of frequency on
pacing in giant pandas. Giant pandas have thick fur and usually prefer cooler temperatures [
but they also regulate their body temperatures to avoid thermal stress by changing their
location based on microclimate [
], so elevated environmental temperatures may have increased
their desire to return to their indoor enclosure for food or shelter. With an increase of light
intensity, giant pandas showed the reduced door-directed behavior and the percentage of
pacing, conversely an increase of head-toss behavior and the frequency on pacing. The giant
panda adapted to the sound level and the number of visitors in zoos which did not influence
their stereotypy. Similarly, the giant pandas in San Diego zoo and Washington National zoo
were reported to be relatively unaffected by ambient noise[
Light intensity promoted the duration and frequency of head-toss and the frequency of
pacing, but declined the duration and frequency of door-directed and the duration of pacing in
this study. Free-ranging giant pandas usually live in a dense bamboo forest where there is an
absence of sunlight [
]. Owen et al.[
] reported that giant pandas often avoid bright lights.
Thus, light conditions could be a key factor for stereotypic behaviors of giant pandas in zoo
environments. When visitors became crowded, giant pandas only showed the decreased
duration of door-directed. The other stereotypic behavior including pacing, head-toss and
headweaving behavior did not significantly change with increasing visitors. Similarly Mallapur and
] revealed that the levels of stereotypic pacing for Indian leopards were not
influenced by the presence of visitors, but they exhibited higher level of stereotypic pacing in small
and barren enclosure devoid of natural light. These results demonstrate that environmental
factors have different effects on stereotypic behaviors.
In zoo-housed animals, the cause of stereotypic behavior is multifaceted, so the function
and purpose of stereotypic behaviors are controversial. When species-typical primary behavior
patterns (foraging for food, searching for a mate, escaping or distancing oneself from
conspecifics) can't be performed in a zoo environment, a stereotypic behavior may occur as a result of
this frustrated motivation [
]. Our results present evidence that giant pandas exhibited
different stereotypies in response to variable environmental factors; the expression of some
stereotypic behavior patterns was increased, while that of others was diminished. Understanding the
role of environmental factors in development of stereotypic behavior is important to improve
the husbandry of zoo-housed animals. The current study indicates there is much more to learn
about environmental factors and stereotypy. A more complete understanding should aid in
public awareness, zoo environment design and wildlife management.
Stereotypy Cannot Simply Evaluate Welfare
In zoo-housed animals, stereotypic behaviors are often found to be idiosyncratic [
Stereotypies shifted in diversity and in different levels at which they were exhibited compared with
their free-ranging counterparts [
]. Different stereotypic behaviors were adapted by
different animals for coping with the artificial environment [
6, 13, 18
]. Other environmental
factors such as enclosure design, group composition, and rearing history have been described to
have a profound influence on stereotypic behaviors [
Animals can normally regulate their behavior to conform to their surroundings [
is extremely difficult to replicate a giant panda's natural environment in a zoo. Compared to
the wild, a zoo environment is exceedingly confined, provides few places to hide, few species
of bamboo for feeding, is often much louder than the wild, and is surrounded by human
beings. However, the wild is not an idyllic place free from all problems. Giant pandas have
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evolved over millions of years, adapting to live in certain types of natural environments.
Placing giant pandas in very different surroundings can elicit stereotypic behaviors. Thus,
stereotyping may be a means of coping with an aversive environment. Stereotypic behavior is often
defined as an abnormal behavior that involves diminished welfare [
5, 6, 18
]. Mason and
] have statistically analyzed that most of environments inducing stereotypies were
connected with poor wellbeing. This suggests that stereotypical behaviors are often associated
with diminished welfare [
In the current study, giant pandas performed stereotypic behaviors in different
environmental conditions, suggesting that their well being is less than optimal. The San Diego zoo's
giant pandas also displayed abnormal behavior in response to varying levels of noise from
]. Powell et al. [
] found that giant pandas exhibited more stereotypic behavior when
demolition was occurring. However, they did not detect that the pandas experienced a
significant decline in welfare. In fact, ªIndividual animals that perform stereotypies in suboptimal
environments may well have better welfare than those that do not perform stereotypies in the
same environmentº [
]. Stereotypic behaviors should be a warning signal of variances in zoo
environment, not the sole animal welfare index [
]. Thus, the relationship between stereotypy
and welfare should be systematically investigated. One cannot simply rely on stereotypic
behavior to evaluate welfare of animals.
In conclusion, zoo-housed pandas are maintained in captive environments that have a
particular range of environmental variables that may not be found in wild setting. We found that
some of these environmental factors influenced stereotypic behaviors. There is no simple
connection between stereotypy and welfare. Further research should focus on the relationship
between the evaluation of welfare and stereotypy.
S1 Fig. Indoor exhibition of giant panda at Beijing zoo.
S2 Fig. Diagram of giant panda house at Beijing zoo.
S1 Table. Duration and Frequency of Stereotypic Behaviors for Individual Giant Panda.
Many thanks to Prof. Qiao Huili, Dr. Zhang Meijia (China Agriculture University) and Dr.
Bao Weidong (Beijing Forestry University) for collecting data. Our deep gratitude to Nathan J.
P. Wintle of PDXWildlife, Dr. Carin Harrington, Mr. Christopher Baxter and Ms. May Fong
Ho for correcting English. We thank two anonymous reviewers for valuable suggestions that
have improved this manuscript. We would also like to thank keepers and lovely giant pandas.
This study was financially supported by the Memphis Zoo Collaborative Project (MP-ES0611),
Science & Technology Project of Beijing City Park Management Center (No.2017), the
International Science & Technology Cooperation Program of China (2013DFG21640) and Beijing
Health Research and Development of Special Project (No.2011-1013-01).
Data curation: HL HD.
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Formal analysis: HL HD.
Funding acquisition: HL HD CW.
Methodology: HL HD.
Project administration: HL.
Software: HL HD.
Validation: HD CW.
Visualization: HD CW.
Writing ± original draft: HL.
Writing ± review & editing: HL HD.
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