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This article was downloaded by: [Moskow State Univ Bibliote]On: 14 November 2013, At: 11:07Publisher: RoutledgeInforma Ltd Registered in England and Wales Registered Number: 1072954Registered office: Mortimer House, 37-41 Mortimer Street, London W1T 3JH,UK
Journal of Applied AnimalWelfare SciencePublication details, including instructions forauthors and subscription information:http://www.tandfonline.com/loi/haaw20
Impact of Zoo Visitors on theFecal Cortisol Levels andBehavior of an EndangeredSpecies: Indian Blackbuck(Antelope cervicapra L.)Thangavel Rajagopal a b , Govindaraju Archunan a &Mahadevan Sekar ca Centre for Pheromone Technology, Departmentof Animal Science , Bharathidasan University ,Tiruchirappalli, Tamil Nadu, Indiab Department of Biotechnology , Ayya Nadar JanakiAmmal College (Autonomous) , Sivakasi, Tamil Nadu,Indiac Tamil Nadu Forest Department , Arignar AnnaZoological Park , Chennai, Tamil Nadu, IndiaPublished online: 28 Dec 2010.
To cite this article: Thangavel Rajagopal , Govindaraju Archunan & MahadevanSekar (2011) Impact of Zoo Visitors on the Fecal Cortisol Levels and Behavior of anEndangered Species: Indian Blackbuck (Antelope cervicapra L.), Journal of AppliedAnimal Welfare Science, 14:1, 18-32, DOI: 10.1080/10888705.2011.527598
To link to this article: http://dx.doi.org/10.1080/10888705.2011.527598
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JOURNAL OF APPLIED ANIMAL WELFARE SCIENCE, 14:18–32, 2011
Copyright © Taylor & Francis Group, LLC
ISSN: 1088-8705 print/1532-7604 online
DOI: 10.1080/10888705.2011.527598
Impact of Zoo Visitors on the FecalCortisol Levels and Behavior of an
Endangered Species: Indian Blackbuck(Antelope cervicapra L.)
Thangavel Rajagopal,1;2 Govindaraju Archunan,1 andMahadevan Sekar3
1Centre for Pheromone Technology, Department of Animal Science,
Bharathidasan University, Tiruchirappalli, Tamil Nadu, India2Department of Biotechnology, Ayya Nadar Janaki Ammal College
(Autonomous), Sivakasi, Tamil Nadu, India3Tamil Nadu Forest Department, Arignar Anna Zoological Park,
Chennai, Tamil Nadu, India
This study investigated behavioral activities (resting, moving, aggressive, social,
and reproductive behavior) and fecal cortisol levels in 8 individually identified adult
male blackbucks during periods of varying levels of zoo visitors (zero, low, high,
and extremely high zoo visitor density). This study also elucidated whether zoo
visitor density could disturb nonhuman animal welfare. This study analyzed fecal
cortisol from the samples of blackbuck by radioimmunoassay and found significant
differences (p < .05) for time the animals devoted to moving, resting, aggressive,
reproductive, and social behavior on days with high and extremely high levels of
zoo visitors. The ANOVA with Duncan’s Multiple Range Test test showed that
the fecal cortisol concentration was higher (p < .05) during the extremely high
(137.30 ˙ 5.88 ng/g dry feces) and high (113.51 ˙ 3.70 ng/g dry feces) levels
of zoo visitor density. The results of the study suggest that zoo visitor density
affected behavior and adrenocortical secretion in Indian Blackbuck, and this may
indicate an animal welfare problem.
Correspondence should be sent to Govindaraju Archunan, Centre for Pheromone Technology,
Department of Animal Science, Bharathidasan University, Tiruchirappalli 620 024, Tamil Nadu,
India. Email: [email protected]
18
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IMPACT OF ZOO VISITORS ON FECAL CORTISOL 19
Thousands of nonhuman animals are held in captive conditions for conservation
efforts worldwide through breeding programs, where they are routinely exposed
to the sight and sound of human audiences. During the past 20 years, great
attention has been given to behavioral investigations in zoos. Most of this
research is applied research, which is designed to tell us about how the captive
environment and the human audience could influence animal behavior (Hosey,
1997, 2000).
Various studies have suggested that the presence of visitors is detrimental to
wild animals in the zoo and results in behavioral changes such as increased intra-
group aggression or stereotypies and decreased exploration (Birke, 2002; Davis,
Schaffner, & Smith, 2005; Hosey, 2005; Sekar, Rajagopal, & Archunan, 2008;
Skyner, Amory, & Hosey, 2004). In contrast, some researchers have reported no
effect of zoo visitors on animals (Synder, 1975); other researchers have reported
that zoo visitors may be enriching for some zoo animals (S. Cook & Hosey,
1995). Venugopal and Sha (1993) reported that the teasing of animals by zoo
visitors may precipitate behavioral problems. A decrease in social integration
within groups in captivity and an increase in behavioral abnormalities during the
presence of visitors has been reported (Mitchell, Obradovich, Herring, Dowd,
& Tromburg, 1991). However, Carlstead and Brown (2005) have suggested that
chronic exposure of captive animals to zoo visitors has reduced stress in some
species.
Glucocorticoids are stress hormones that are the end product of hypothalamic-
pituitary-adrenal activity and are also effective indices of stress in many verte-
brates, such as fish (Bonga, 1997; Turner, Rogers, & Nemeth, 2003), reptiles
(Knapp & Moore, 1997), birds (Silverin, 1997), and mammals (Alexander &
Irvine, 1998; Kirkpatrick, Baker, Turner, Kenney, & Ganjam, 1979; Sapol-
sky, 1985; Turner, Tolson, & Hamad, 2002). Due to the potential effects on
physiological status, the measurement of glucocorticoids could serve as a valu-
able tool in studies of evolutionary ecology, conservation biology, and animal
welfare. In addition, the measurement of glucocorticoids has been used to
investigate adrenocortical activity during exposure to stressful stimuli, such as
novel environment, transportation, social tension and aggression, human distur-
bances, and exposure to predators (Terio, Citino, & Brown, 1999; Wielebnowski,
Fletchall, Carlstead, Busso, & Brown, 2002). It is reported that an increase
of cortisol may influence behavior (more aggression, moving, and grooming
activities) and physiological functions (depression, hypertension, suppression
of immune system, gastrointestinal ulceration, electrolyte imbalances, calcium
loss and bone mass reduction, and inhibition of growth; Birke, 2002; Breazil,
1987; Palme & Mostl, 1997; Steward, 2003). The use of blood samples for
various measurements is restricted in wild captive species because animals must
typically be captured, thus potentially compromising an accurate assessment of
stress (R. C. Cook, Cook, Garrott, Irwin, & Monfort, 2002; Le Maho et al.,
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20 RAJAGOPAL, ARCHUNAN, SEKAR
1992). However, in many free-ranging cervid species, these endocrine studies
are not practical and may even be dangerous due to excessive stress caused
by capture and restraint (Schwarzenberger, Mostl, Palme, & Bamberg, 1996).
Consequently, noninvasive monitoring of fecal steroid metabolite assays are
now being used in a variety of disciplines, including animal science, behavioral
ecology, conservation biology, ornithology, and primatology (Dehnhard et al.,
2003; Ganswindt, Palme, Heistermann, Borragan, & Hodges, 2003; Good, Khan,
& Lynch, 2003; Goymann, Mostl, & Gwinner, 2002).
In light of these advantages, immunoassay has been widely used to measure
fecal glucocorticoids and has been extensively adopted for use in studying mam-
mals, including bighorn sheep (Miller, Hobbs, & Sousa, 1991), domestic sheep
(Palme & Mostl, 1997), chimpanzees (Whitten, Stavisky, Aureli, & Russell,
1997), cheetahs (Jurke, Czekala, Lindburg, & Millard, 1998), African wild dogs
(Monfort, Mashburn, Brewer, & Creel, 1998), common marmosets (Sousa &
Ziegler, 1998), spotted hyenas (Goymann, Mostl, Van’t Hof, East, & Hofer,
1999), red deer (Ingram, Crockford, & Matthews, 1999), spider monkeys (Davis
et al., 2005), black rhinoceroses (Carlstead & Brown, 2005; Turner et al., 2002),
and Pere David’s deer (Li, Jiang, Tang, & Zeng, 2007). Mostl and Palme (2002)
reported that increases in levels of cortisol may relate to changes in the behavior
and physiology of captive zoo animals. Carlstead (1996) suggested that, for
some wild animal species, the captive environment may be stressful because
of its limited space, deficient environmental elements, and additional human
disturbance. Earlier studies have indicated that prolonged high cortisol levels
could lead to loss of body weight, reproductive failure, immunosuppression,
and a shorter life span (Carlstead & Brown, 2005; Clubb & Mason, 2003).
Monitoring of adrenocortical steroids and their relationships with behavioral
responses as measures of stress in captivity has been emphasized in ex-situ
conservation and animal welfare research (Cockrem, 2005; Goymann et al.,
1999; Mostl & Palme, 2002).
This study investigated behavior and fecal cortisol concentrations in captive
Indian Blackbuck under different conditions of zoo visitor density: zero level
(zoo visitor absence or zoo holiday), low level, high level, and extremely high
level (festival times). This study may help researchers and zoo managers to
understand the influence of zoo visitor density on the fecal cortisol concentration
and the behavioral repertoire of this species.
MATERIALS AND METHODS
Study Area
This study was conducted in the conservation and breeding center of Arignar
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IMPACT OF ZOO VISITORS ON FECAL CORTISOL 21
Anna Zoological Park (AAZP; 13ı160S and 79ı540E at an altitude of MSLC
10 m to 100 m), Vandalur, Chennai, Tamil Nadu, South India. Chennai has
the distinction of having the first zoo in India, which was started in 1855. In
1976, the zoo moved to the Vandalur Reserve Forest, an area near Chennai of
about 510 ha. The habitat of AAZP is considered a tropical evergreen scrub,
a degraded forest mostly consisting of thorny bushes. Special features of this
park include a lion and deer safari, bird aviaries, a reptile house, and a nocturnal
house. Average annual rainfall is about 250 mm. Annual average temperature is
26ıC. The annual average of people who visit the zoological park is 600,000–
700,000.
Study Animals
The Indian Antelope (Antelope cervicapra L.), commonly called blackbuck, is
a member of the antelopini group of the subfamily antelopinea. Blackbuck
is a highly endangered species that is more prevalent in India and Indian
subcontinents (Nepal and Pakistan). The occurrence of this species in arid
grasslands, marshy coastal plains, and open woodlands is a unique feature.
Blackbucks are primarily grazers who associate in herds with characteristically
loose and unstable associations that can range from fewer than 10 individuals
to several hundred. The study subjects were 8 adult males with a mean age of
5.5 ˙ 0.37 years. All animals were captive born and were living in an outdoor
enclosure at the AAZP. Water was offered ad libitum, and food was served twice
a day. This is a preliminary study of stress-related behavior and cortisol in adult
male blackbuck only. Other animals (females and young) were also living in the
same enclosure. In the future, we plan to study the stress-related parameters for
female and young blackbuck.
Blackbuck Enclosure
All blackbucks were housed in an outdoor enclosure of about 3.5 acres (1.4 hec-
tares) within a dry moat. The zoo was open to zoo visitors from 9 a.m. to 5 p.m.
every day except Tuesday (zoo holiday). The blackbuck enclosure consists of
three zones:
1. Edge zone: the visitor area in which the distance between visitors and the
blackbuck is about 7 m;
2. Rear zone: the access area for zoo employees for the purpose of cleaning
and feeding (twice daily); and
3. Enrichment zone: a central area with trees, food, and water troughs and
sheds.
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22 RAJAGOPAL, ARCHUNAN, SEKAR
Zoo Visitor Density
Visitor density was defined as the number of people admitted to the AAZP on
a given day. Systematic data was not available on the number of visitors to the
blackbuck enclosure. The study was carried out in four different conditions:
1. Zero visitor density, when visitors were absent (zoo holiday);
2. Low visitor density (weekdays, when the mean daily number of visitors
to the zoo was 1262.46 ˙ 149.81; range: 528 to 1774);
3. High visitor density (weekends, when mean daily number of visitors to
the zoo was 3381.66 ˙ 204.38; range: 2632 to 4677); and
4. Extremely high visitor density (festival times, when mean daily number
of visitors to zoo was 10379.93 ˙ 2054.24; range: 4851 to 36886).
Behavioral Observation
During behavioral observation, each individual blackbuck was recognized by
variation in coat color, length of horn, and some morphological identification
(scar, broken horn, damaged ear pinna). Blackbucks were observed for 360 hr
over a period of approximately 12 months. Each animal was observed on 15
separate days for 6 hr per day to record behaviors at each visitor density; 90 hr of
data were collected in each study condition. Blackbuck behavior was recorded
every 5 min during 40-min intervals 6 hr per day for 15 days in each study
condition. Observations occurred at the same time of day (10 a.m. to 1 p.m.
and 2 p.m. to 5 p.m.) for all animals to prevent any inconsistent exposure
to extraneous events in the environment, such as feeding and cleaning. Each
blackbuck behavior (moving, resting, reproductive, social, and aggressive) was
recorded every 5 min over the 6 hr per day for each condition using scan-
sampling techniques (Altmann, 1974). At every sample point, the behavioral
state of each individual was recorded systematically according to an ethogram.
The following behavioral variables were monitored in each condition of zoo
visitor density:
1. Moving behaviors: walking and running;
2. Resting behaviors: sitting, standing, and lying down;
3. Social behaviors: grooming, horn bushing, playing, and scent marking;
4. Reproductive behaviors: approach, flehmen, mounting, and sniffing; and
5. Aggressive behaviors: fighting and chasing other individuals.
Collection of Fecal Materials
Three fecal samples were collected from each individual during each condition
of zoo visitor density. The fecal samples were collected the day after visitors at
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IMPACT OF ZOO VISITORS ON FECAL CORTISOL 23
a certain density, during the early morning hours of 6 to 8 a.m. A total of 96
fecal samples were collected during the study period. Samples were sealed in
plastic bags and immediately stored at �20ıC until further analysis.
Extraction of Steroids for Radioimmunoassay
Fecal samples were lyophilized for 24 hr (Model LGA05, MLW, Leipzig, Ger-
many). Dried feces were then pulverized in a blender and all solid inert materials,
such as seeds and rough dietary fiber, were removed. Steroids were extracted
according to the modified method described by Palme, Robia, Messmann, and
Mostl (1998), in which a proportion of the resulting powder (0.5 g) was weighed
and extracted with 5 ml 80% methanol. After vortexing for 30 s at high speed,
the sample was shaken for 12 hr on a mechanical shaker and then centrifuged
at 700 � g for 15 min at 4ıC; the resulting supernatant was collected into a
clean tube. An aliquot of the supernatant (100 �l) was diluted 1:16 with assay
buffer (20 mMol. trishydroxyaminomethan, 0.3 Mol. NaCl, 0.1% bovine serum
albumin, and 0.1% Tween 80; pH 7.5) for radioimmunoassay (RIA) analysis.
Levels of cortisol were measured in all fecal samples using a modified RIA
as described by Palme et al. (1998) and Huber, Palme, and Arnold (2003). Intra-
and interassay coefficients of variation for cortisol were calculated at less than
5.0% (n D 24) and 14.4% (n D 24), respectively.
Statistical Methods
The data for each behavior and fecal cortisol concentration were measured using
the one-factor analysis of variance (ANOVA; SPSS 11.0) to compare within
subjects each behavior and cortisol level across the four categories of zoo visitor
density (p < .05 considered significantly different for all statistical tests).
RESULTS
Visitor density had a significant effect (p < .001) on each of the five behaviors
recorded (moving, resting, reproductive, social, and aggressive; Tables 1–5).
Animals spent significantly (p < .05) more time resting during the periods of
zero and low levels of visitor density than during high and extreme densities
(Tables 2 and 3). There was no significant effect of zero and low level of
visitor density on the frequency of reproductive and social behaviors. High and
extremely high levels of visitor density influenced moving, resting, reproductive,
social, and aggressive behaviors (p < .05; Tables 4 and 5).
The mean levels of cortisol were recorded at the zero (35.44 ˙ 4.84 ng/g), low
(55.07 ˙ 5.57 ng/g), high (113.51 ˙ 3.70 ng/g), and extremely high (137.30 ˙
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24 RAJAGOPAL, ARCHUNAN, SEKAR
TABLE 1
ANOVA With Post Hoc Comparison (One-Way) of Five Behaviors
in Four Conditions of Zoo Visitor Density
Zoo Visitor Density
Sum of
Squares df
Mean
Square F Sig.
Zero level density Between groups 6737.733 4 1684.433 96.469 <.001*
Within groups 1222.267 70 17.461
Total 7960.000 74
Low level density Between groups 3810.587 4 952.647 85.935 <.001*
Within groups 776.000 70 11.086
Total 4586.587 74
High level density Between groups 3563.333 4 890.833 63.458 <.001*
Within groups 982.667 70 14.038
Total 4546.000 74
Extremely high level density Between groups 5399.733 4 1349.933 161.733 <.001*
Within groups 584.267 70 8.347
Total 5984.000 74
Note. The means were compared using Duncan’s Multiple Range Test. The means gain score
of zero, low, high, and extremely high visitor density conditions for five behaviors is statistically
significant.
*High statistical significance (p < .001).
TABLE 2
Comparison of Means (Zero Level Density)
From Table 1 Using Duncan’s Multiple Range Test
Post Hoc Tests
Subset for Alpha D .05
Types of Behavior 1 2 3
Reproductive behavior 9.2000
Moving behavior 12.0000
Aggressive behavior 18.3333
Social behavior 20.0667
Resting behavior 36.4000
Significance 0.071 0.260 1.000
Note. Means for groups in homogeneous subsets are displayed.
Means within a subset are not different from each other.
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IMPACT OF ZOO VISITORS ON FECAL CORTISOL 25
TABLE 3
Comparison of Means (Low Level Density)
From Table 1 Using Duncan’s Multiple Range Test Post Hoc Tests
Subset for Alpha D .05
Types of Behavior 1 2 3 4
Reproductive behavior 12.3333
Social behavior 12.6667
Aggressive behavior 16.6000
Moving behavior 23.4667
Resting behavior 31.0000
Significance 0.785 1.000 1.000 1.000
Note. Means for groups in homogeneous subsets are displayed. Means within a
subset are not different from each other.
TABLE 4
Comparison of Means (High Level Density)
From Table 1 Using Duncan’s Multiple Range Test Post Hoc Tests
Subset for Alpha D .05
Types of Behavior 1 2 3 4 5
Reproductive behavior 9.1333
Social behavior 15.2000
Resting behavior 19.4000
Aggressive behavior 22.6667
Moving behavior 29.6000
Significance 1.000 1.000 1.000 1.000 1.000
Note. Means for groups in homogeneous subsets are displayed. Means within a subset are not
different from each other.
5.88 ng/g) levels of zoo visitor density. The one-way ANOVA with post hoc
comparison (Duncan’s Multiple Range Test) test clearly showed that the average
fecal cortisol concentration was significantly (p < .05) higher during high and
extremely high levels of zoo visitor density than during the zero and low levels
(Tables 6 and 7).
DISCUSSION
For many years, human audiences and tourists have been permitted into sanctu-
ary, wildlife, and zoological parks, facilitating awareness about the importance
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TABLE 5
Comparison of Means (Extremely High Level Density)
From Table 1 Using Duncan’s Multiple Range Test Post Hoc Tests
Subset for Alpha D .05
Types of Behavior 1 2 3 4 5
Reproductive behavior 8.6000
Social behavior 11.0000
Resting behavior 20.8000
Aggressive behavior 23.9333
Moving behavior 31.6667
Significance 1.000 1.000 1.000 1.000 1.000
Note. Means for groups in homogeneous subsets are displayed. Means within a subset are not
different from each other.
TABLE 6
ANOVA With Post Hoc Comparison (One-Way) of Fecal Cortisol
Concentration in Four Conditions of Zoo Visitor Density
Comparison of Fecal
Cortisol Concentration Sum of Squares df Mean Square F Sig.
Between groups 55235.067 3 18411.689 99.633 <.001*
Within groups 5174.261 28 184.795
Total 60409.328 31
Note. The means were compared using Duncan’s Multiple Range Test. The means gain score
of zero, low, high, and enormous visitor density interns of fecal cortisol concentration of eight
identified male blackbucks is statistically significant.
*High statistical significance (p < .001).
TABLE 7
Comparison of Means From Table 6 Using Duncan’s Multiple Range
Test Post Hoc Tests
Subset for Alpha D .05
Zoo Visitor Density 1 2 3 4
Zero visitor density 35.4475
Low visitor density 54.9875
High visitor density 113.5113
Enormous visitor density 137.3038
Significance 1.000 1.000 1.000 1.000
Note. Means for groups in homogeneous subsets are displayed. Means within a subset are not
different from each other.
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IMPACT OF ZOO VISITORS ON FECAL CORTISOL 27
of wild animal conservation and management (Cox, 1993). Since the 1970s,
research on the effects of zoo visitors on the welfare of wild zoo animals has
intensified. Numerous studies have shown that characteristics such as visitor
presence, density, activity, and position can affect zoo animal behavior and,
to some extent, physiology. Hosey (2008) has reviewed the interactions be-
tween human audiences and captive wild zoo animals. These studies showed
variable results, where some zoo animals were tolerant of large numbers of
visitors, and others were negatively impacted. The exposure to visitors resulted
in higher levels of stereotyped locomotion, masturbation, and leg/hair pulling
in captive mandrills. Furthermore, adult orangutans covered their heads with
paper sacks, and infants held on to adults more often (Birke, 2002). There
were also increased levels of urinary cortisol in spider monkeys (Davis et al.,
2005) when they were exposed to high visitor densities. During a study of
green monkeys at a Mexican zoo, Fa (1989) found that there were no effects
on locomotion and aggressive behaviors. However, in this case the public was
feeding these animals and this may have changed the animals’ perceptions of
the visitors.
The findings of the present study indicate that the zoo visitors significantly
influenced behavior and fecal cortisol concentrations in captive Indian Black-
buck. The study is in agreement with some earlier investigations, which have
described that the presence of visitors markedly increases disturbance in a
number of captive species, such as cotton-topped tamarins (Glatston, Geilvoet-
Soeteman, Pecek, & Hooff, 1984), golden bellied mangabeys (Mitchell, Her-
ring, & Obradovich, 1992), sloth bears (Forthman & Bakman, 1992), gorillas
(Nakamichi, 1998), dama gazelles (Cassinello & Pieters, 2000), tigers (Terio
& Munson, 2000), North American clouded leopards (Wielebnowski, Fletchall,
et al., 2002), cheetahs (Wielebnowski, Ziegler, Wildt, Lukas, & Brown, 2002),
white and black rhinoceroses (Turner et al., 2002), Indian leopards (Mallapur &
Chellam, 2002; Mallapur, Qureshi, & Chellam, 2002), jaguars (Sellinger & Ha,
2005), lion-tailed macaques (Mallapur, Sinha, & Waran, 2005), spider monkeys
(Davis et al., 2005), Asian elephants (Laws et al., 2007), and Indian bison (Sekar
et al., 2008).
The blackbuck engaged in more intergroup aggression and moved more
during days of high and extremely high visitor density than during zero and
low levels. Aggressive behavior, which is considered the result of competition
for resources and social dominance, is largely related to social stress, and cap-
tivity usually amplifies the social stress in animals (Carlstead, 1996). Wormell,
Brayshaw, Price, and Herron (1996) and Birke (2002) have suggested that
aggressive behavior might be increased or decreased under audience conditions.
A detailed study by Mitchell et al. (1992) on golden bellied mangabeys showed
that a number of animals increased visitor-directed and within-group aggression
when audiences were present, but affiliative behaviors, such as grooming, were
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28 RAJAGOPAL, ARCHUNAN, SEKAR
largely unchanged. Conflict behavior or aggression may result in an increase in
cortisol secretion (Creel, 2001; Mostl & Palme, 2002).
Based on the present study, it seems that elevated concentration of fecal
cortisol levels in blackbuck are associated with higher levels of zoo visitor
density. Similarly, elevated fecal cortisol was found in black rhinoceroses in zoos
where the animals had been kept in enclosures with a great degree of public
exposure (Carlstead & Brown, 2005). Li et al. (2007) reported that the size of
the animal enclosure, animal density, and human audience could significantly
influence the behavior and adrenocorticol secretion in Pere David’s deer. It is
also reported that variations of fecal cortisol concentration occur due to animal
density and the facilities available in husbandry such as enclosure size, height,
degree of exposure to the public and/or predators, and type of keeper interaction
(Wielebnowski, Fletchall, et al., 2002). In contrast, significantly lower levels of
fecal corticoids have been observed for white rhinoceroses when the keepers
were rated highly in terms of friendliness (Carlstead & Brown, 2005).
This study examined the effect of zoo visitor density within the zoo setting
on blackbuck behavior and levels of fecal cortisol. Further study is needed to
examine more closely the effects of visitor behavior on fecal cortisol levels and
behavior of other zoo animals. In Indian zoos, disturbances by zoo visitors that
are continuously high may be due to the lack of well-established conservation
and animal welfare awareness programs. Human practices such as shouting,
teasing, and feeding—and even causing physical harm—to animals are common
experiences in most Indian zoos (Venugopal & Sha, 1993). Such disturbances
have been shown to adversely influence the behavior of wild animals in captivity
(Birke, 2002; Kratochvil & Schwammer, 1997). The problem may be solved by
recommending that zoos simply post a notice outside of enclosures asking that
the public cooperate and not tease or interact with the animals because that will
subsequently affect animal welfare.
The findings of this study suggest that blackbucks are excited to the point of
stress induction by higher zoo visitor density. It is reported that adrenocortisol
hormones are indicators of stress in many wild zoo animals (Mostl & Palme,
2002). The results of our study further confirm the value of noninvasive fe-
cal hormone monitoring as a powerful tool for evaluating adrenal activity in
blackbuck. Based on the present and previous results, it can be recommended to
maintain a sufficient distance between zoo audience sites and animal enclosures
to improve animal welfare.
ACKNOWLEDGMENTS
We are thankful to the Chief Wildlife Warden and Mr. P. L. Ananthaswamy, Chief
Conservator of Forests, & Director of the Arignar Anna Zoological Park, Van-
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IMPACT OF ZOO VISITORS ON FECAL CORTISOL 29
dalur, Chennai, for granting permission to carry out this study and for providing
the facilities and encouragement. We are thankful to Professor John W. Turner,
University of Toledo College of Medicine, United States, for critical reading and
valuable suggestions. The University Grant Commission-Rajiv Gandhi National
fellowship (TR); University Grant Commission-Special Assistance Programme;
and Department of Science and Technology-Fund for Improvement of Science
and Technology, New Delhi, are acknowledged for their financial assistance.
REFERENCES
Alexander, S. L., & Irvine, C. H. G. (1998). The effect of social stress on adrenal axis activity
in horses: The importance of monitoring corticosteroid-binding globulin capacity. Journal of
Endocrinology, 157, 425–432.
Altmann, J. (1974). Observational study of behaviour: Sampling methods. Behaviour, 22, 377–383.
Birke, L. (2002). Effects of browse, human visitors and noise on the behaviour of captive orangutans.
Animal Welfare, 11, 189–202.
Bonga, S. E. W. (1997). The stress response in fish. Physiological Reviews, 77, 591–625.
Breazil, J. E. (1987). Physiological basis and consequences of distress in animals. Journal of
American Veterinary Medicine Association, 191, 1212–1215.
Carlstead, K. (1996). Effects of captivity on the behavior of wild mammals. In D. G. Kleiman,
M. E. Allen, K. V. Thompson, & S. Lumpkin (Eds.), Wild mammals in captivity (pp. 317–333).
Chicago, IL: The University of Chicago Press.
Carlstead, K., & Brown, J. L. (2005). Relationships between patterns of fecal corticoid excretion and
behavior, reproduction, and environmental factors in captive black (Diceros bicornis) and white
(Ceratotherium simum) rhinoceros. Zoo Biology, 24, 215–232.
Cassinello, J., & Pieters, I. (2000). Multi-male captive group of endangered dama gazelle: Social
rank, aggression and enclosure effects. Zoo Biology, 19, 121–129.
Clubb, R., & Mason, G. (2003). Captivity effects on wide-ranging carnivores. Nature, 425, 473.
Cockrem, J. F. (2005). Conservation and behavioral neuroendocrinology. Hormone and Behaviour,
48, 492–501.
Cook, R. C., Cook, J. G., Garrott, R. A., Irwin, L. L., & Monfort, S. L. (2002). Effects of diet and
body condition on fecal progestagen excretion in elk. Journal of Wildlife Disease, 38, 558–565.
Cook, S., & Hosey, G. R. (1995). Interaction sequences between chimpanzees and human visitors
at the zoo. Zoo Biology, 14, 431–44.
Cox, G. W. (1993). Conservation ecology: Biosphere and biosurvival. Dubuque, IA: Wm. C. Brown.
Creel, S. (2001). Social dominance and stress hormone. Trends in Ecology and Evolution, 16, 491–
497.
Davis, N., Schaffner, C. M., & Smith, D. E. (2005). Evidence that zoo visitors influence HPA activity
in spider monkeys (Ateles geoffroyii rufiventris). Applied Animal Behaviour Science, 90, 131–141.
Dehnhard, M., Schreer, A., Krone, O., Jewgenow, K., Krause, M., & Grossmann, R. (2003).
Measurement of plasma corticosterone and fecal glucocorticoid metabolites in the chicken (Gallus
domesticus), the great cormorant (Phalacrocorax carbo), and the goshawk (Accipiter gentiles).
General and Comparative Endocrinology, 131, 345–352.
Fa, J. E. (1989). Influence of people on the behavior of display primates. In E. F. Segal (Ed.),
Housing, care and psychological well-being of captive and laboratory primates (pp. 270–290).
Park Ridge, NJ: Noyes.
Forthman, D. L., & Bakman, R. (1992). Environmental and social influences on enclosure used and
activity patterns of captive sloth bears (Ursus ursinus). Zoo Biology, 11, 405–415.
Dow
nloa
ded
by [
Mos
kow
Sta
te U
niv
Bib
liote
] at
11:
07 1
4 N
ovem
ber
2013
30 RAJAGOPAL, ARCHUNAN, SEKAR
Ganswindt, A., Palme, R., Heistermann, M., Borragan, S., & Hodges, J. K. (2003). Non-invasive
assessment of adrenocortical function in the male African elephant (Loxodonta africana) and its
relation to musth. General and Comparative Endocrinology, 134, 156–166.
Glatson, A. K., Geilvoet-Soeteman, E. G., Pecek, E. H., & Hooff, J. A. R. A. M. V. (1984).
The influence of the zoo environment on social behaviour of groups of cotton-topped tamarins,
Saguinus oedipus oedipus. Zoo Biology, 3, 241–253.
Good, T., Khan, M. Z., & Lynch, J. W. (2003). Biochemical and physiological validation of a
corticosteroid radioimmunoassay for plasma and fecal samples in oldfield mice (Peromyscus
polionotus). Physiology and Behaviour, 80, 405–411.
Goymann, W., Mostl, E., & Gwinner, E. (2002). Corticosterone metabolites can be measured non-
invasively in excreta of European stonechats (Saxicola torquata rubicola). Auk, 119, 1167–1173.
Goymann, W., Mostl, E., Van’t Hof, T., East, M. L., & Hofer, H. (1999). Non-invasive fecal
monitoring of glucocorticoids in spotted hyenas, Crocuta crocuta. General and Comparative
Endocrinology, 114, 340–348.
Hosey, G. R. (1997). Behavioural research in zoos: Academic perspectives. Applied Animal Be-
haviour Science, 51, 199–207.
Hosey, G. R. (2000). Zoo animals and their human audiences: What is the visitor effect? Animal
Welfare, 9, 343–357.
Hosey, G. R. (2005). How does the zoo environment affect the behaviour of captive primates?
Applied Animal Behaviour Science, 90, 107–129.
Hosey, G. R. (2008). A preliminary model of human–animal relationships in the zoo. Applied Animal
Behaviour Science, 109, 105–127.
Huber, S., Palme, R., & Arnold, W. (2003). Effects of season, sex, and sample collection on
concentrations of fecal cortisol metabolites in red deer (Ceruus elephus). General and Comparative
Endocrinology, 130, 48–54.
Ingram, J. R., Crockford, J. N., & Matthews, L. R. (1999). Ultradian, circadian and seasonal rhythms
in cortisol secretion and adrenal responsiveness to ACTH and yarding in unrestrained red deer
(Cervus elaphus) stags. Journal of Endocrinology, 162, 289–300.
Jurke, M. H., Czekala, N. M., Lindburg, D. G., & Millard, S. E. (1998). Fecal corticoid metabolite
measurement in the cheetah (Acinonyx jubatus). Zoo Biology, 16, 133–147.
Kirkpatrick, J. F., Baker, C. B., Turner, J. W. Jr., Kenney, R. M., & Ganjam, V. K. (1979). Plasma
corticosteroids as an index of stress in captive wild horses (Eguus caballus). Journal of Wildlife
Management, 93, 801–804.
Knapp, R., & Moore, M. C. (1997). Male morphs in tree lizards have different testosterone responses
to elevated levels of cortico-sterone. General and Comparative Endocrinology, 107, 273–279.
Kratochvil, H., & Schwammer, H. (1997). Reducing acoustic disturbance by aquarium visitors. Zoo
Biology, 16, 349–353.
Laws, N., Ganswindt, A., Heistermann, M., Harris, M., Harris, S., & Sherwin, C. (2007). A case
study: Fecal corticosteroid and behavior as indicators of welfare during relocation of an Asian
elephant. Journal of Applied Animal Welfare Science, 10, 349–358.
Le Maho, Y., Karmann, H., Briot, D., Handrich, Y., Robin, J. P., Mioskowski, E., : : : Farni, J. (1992).
Stress in birds due to routine handling and how to avoid it. American Journal of Physiology
Regulatory, Integrative and Comparative Physiology, 263, 775–781.
Li, C., Jiang, Z., Tang, S., & Zeng, Y. (2007). Influence of enclosure size and animal density on
fecal cortisol concentration and aggression in Pere David’s deer stags. General and Comparative
Endocrinology, 151, 202–209.
Mallapur, A., & Chellam, R. (2002). environmental influences on stereotypy and the activity budget
of Indian leopards (Panthera pardus) in four zoos in Southern India. Zoo Biology, 21, 585–595.
Mallapur, A., Qureshi, Q., & Chellam, R. (2002). Influences of enclosure design on the utilization
of space by leopards (Panthera pardus) in four zoos in southern India. Journal of Applied Animal
Welfare Science, 5, 111–124.
Dow
nloa
ded
by [
Mos
kow
Sta
te U
niv
Bib
liote
] at
11:
07 1
4 N
ovem
ber
2013
IMPACT OF ZOO VISITORS ON FECAL CORTISOL 31
Mallapur, A., Sinha, A., & Waran, N. (2005). Influence of visitor presence on the behaviour of
captive lion-tailed macaques (Macaca silenus) housed in Indian zoos. Applied Animal Behaviour
Science, 94, 341–352.
Miller, M. W., Hobbs, N. T., & Sousa, M. C. (1991). Detecting stress responses in Rocky Mountain
bighorn sheep (Ovis Canadensis canadensis): Reliability of cortisol concentrations in urine and
feces. Canadian Journal of Zoology, 69, 15–24.
Mitchell, G., Herring, F., & Obradovich, S. (1992). Like threaten like in mangabeys and people?
Anthrozoös, 5, 106–112.
Mitchell, G., Obradovich, S. D., Herring, F. H., Dowd. B., & Tromburg, C. (1991). Threats to
observers, keepers, visitors, and others by zoo mangabeys (Cercocebus galeritus chrysogaster).
Primates, 32, 515–522.
Monfort, S. L., Mashburn, K. L., Brewer, B. A., & Creel, S. R. (1998). Evaluating adrenal activity
in African wild dogs (Lycaon pictus). Journal of Zoo Wildlife Medicine, 29, 129–133.
Mostl, E., & Palme, R. (2002). Hormones as indicators of stress. Domestic Animal Endocrinology,
23, 67–74.
Nakamichi, M. (1998). Stick throwing by gorillas (Gorilla gorilla gorilla) at the San Diego Wild
Animal Park. Folia Primatology, 69, 291–295.
Palme, R., & Mostl, E. (1997). Measurement of cortisol metabolites in faeces of sheep as a parameter
of cortisol concentration in blood. International Journal of Mammalian Biology, 62, 92–197.
Palme, R., Robia, C., Messmann, S., & Mostl, E. (1998). Measuring faecal cortisol metabolites: A
non-invasive tool to evaluate adreno-cortical activity in mammals. Advanced Study in Ethology,
33, 27.
Sapolsky, R. M. (1985). Stress-induced suppression of testicular function in the wild baboon: Role
of glucocorticoids. Endocrinology, 116, 2273–2278.
Schwarzenberger, F., Mostl, E., Palme, R., & Bamberg, S. E. (1996). Faecal steroid analysis for non-
invasive monitoring of reproductive status in farm, wild and zoo animals. Animal Reproductive
Science, 42, 515–526.
Sekar, M., Rajagopal, T., & Archunan, G. (2008). Influence of zoo visitor presence on the behavior
of captive Indian gaur (Bos gaurus gaurus) in a zoological park. Journal of Applied Animal
Welfare Science, 11, 352–357.
Sellinger, R. L., & Ha, J. C. (2005). The effect of visitor density and intensity on the behaviour of
two captive jaguars (Panthera onca). Journal of Applied Animal Welfare Science, 8, 233–244.
Silverin, B. (1997). The stress-response and autumn dispersal behavior in willow tits. Animal
Behaviour, 53, 451–459.
Skyner, L. J., Amory, J. R., & Hosey, G. R. (2004). The effects of visitors on the self-injurious
behaviour of a male pileated gibbon (Hylobates pileatus). Der Zoologische Garten, 74, 38–41.
Sousa, M. B. C., & Ziegler, T. E. (1998). Diurnal variation on the excretion patters of fecal steroids in
common marmosets (Callithrix jacchus) females. American Journal of Primatology, 46, 105–117.
Steward, P. M. (2003). The adrenal cortex. In P. R. Larsen, H. M. Kronenberg, S., Melmed, & K. S.
Polonsky (Eds.), Williams textbook of endocrinology, (10th ed., pp. 491–551). Philadelphia, PA:
Saunders.
Synder, R. L. (1975). Behavioral stress in captive animals. In G. Rabb (Ed.), Research in zoos and
aquariums (pp. 41–76). Washington, DC: National Academy of Sciences.
Terio, K. S., Citino, S. B., & Brown, J. L. (1999). Fecal cortisol metabolite analysis for non-
invasive monitoring of adrenocortical function in the cheetah (Acinonyx jubatus). Journal of Zoo
and Wildlife Medicine, 30, 484–491.
Terio, K. S., & Munson, L. (2000). Gastritis in cheetahs and relatedness to adrenal function. In
B. Pukazhenthi, D. Wildt, & J. Mellen (Eds.), Felid taxonomy advisory group action plan, 2000
report: 36 (pp. 143–157). Wheeling, WV: American Zoo and Aquarium Association.
Turner, J. W., Rogers, C., & Nemeth, R. (2003). Measurement of faecal glucocorticoids in parrot-
fishes to assess stress. General and Comparative Endocrinology, 133, 341–352.
Dow
nloa
ded
by [
Mos
kow
Sta
te U
niv
Bib
liote
] at
11:
07 1
4 N
ovem
ber
2013
32 RAJAGOPAL, ARCHUNAN, SEKAR
Turner, J. W., Tolson, P., & Hamad, N. (2002). Remote assessment of stress in white rhinoceros
(Ceratotherium simum) and black rhinoceros (Diceros bicornis) by measurement of adrenal
steroids in feces. Journal of Zoo Wildlife Medicine, 33, 214–221.
Venugopal, B., & Sha, A. A. (1993). Visitor behaviour at lion-tailed macaque in the Mysor zoos.
Zoos Print Journal, 8, 45–48.
Whitten, P. L., Stavisky, R., Aureli, F., & Russell, E. (1997). Response of fecal cortisol to stress in
captive chimpanzees (Pan troglodytes). American Journal of Primatology, 44, 57–69.
Wielebnowski, N. C., Fletchall, N., Carlstead, K., Busso, J. M., & Brown, J. L. (2002). Noninvasive
assessment of adrenal activity associated with husbandry and behavioural factors in the North
American clouded leopard population. Zoo Biology, 21, 77–98.
Wielebnowski, N. C., Ziegler, K., Wildt, D. E., Lukas, J., & Brown, J. L. (2002). Impact of social
management on reproductive, adrenal and behavioural activity in the cheetah (Acinonyx jubatus).
Animal Conservation, 5, 291–301.
Wormell, D., Brayshaw, M., Price, E., & Herron, S. (1996). Pied tamarins, Saguinus bicolor bicolor
at the Jersey Wildlife Preservation Trust: Management, behavior and reproduction. Dodo, Journal
of the Wildlife Preservation Trusts, 32, 76–97.
Dow
nloa
ded
by [
Mos
kow
Sta
te U
niv
Bib
liote
] at
11:
07 1
4 N
ovem
ber
2013