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This article was downloaded by: [Moskow State Univ Bibliote] On: 14 November 2013, At: 11:07 Publisher: Routledge Informa Ltd Registered in England and Wales Registered Number: 1072954 Registered office: Mortimer House, 37-41 Mortimer Street, London W1T 3JH, UK Journal of Applied Animal Welfare Science Publication details, including instructions for authors and subscription information: http://www.tandfonline.com/loi/haaw20 Impact of Zoo Visitors on the Fecal Cortisol Levels and Behavior of an Endangered Species: Indian Blackbuck (Antelope cervicapra L.) Thangavel Rajagopal a b , Govindaraju Archunan a & Mahadevan Sekar c a Centre for Pheromone Technology, Department of Animal Science , Bharathidasan University , Tiruchirappalli, Tamil Nadu, India b Department of Biotechnology , Ayya Nadar Janaki Ammal College (Autonomous) , Sivakasi, Tamil Nadu, India c Tamil Nadu Forest Department , Arignar Anna Zoological Park , Chennai, Tamil Nadu, India Published online: 28 Dec 2010. To cite this article: Thangavel Rajagopal , Govindaraju Archunan & Mahadevan Sekar (2011) Impact of Zoo Visitors on the Fecal Cortisol Levels and Behavior of an Endangered Species: Indian Blackbuck (Antelope cervicapra L.), Journal of Applied Animal 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 PLEASE SCROLL DOWN FOR ARTICLE Taylor & Francis makes every effort to ensure the accuracy of all the information (the “Content”) contained in the publications on our platform.

Impact of Zoo Visitors on the Fecal Cortisol Levels and Behavior of an Endangered Species: Indian Blackbuck ( Antelope cervicapra L .)

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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

PLEASE SCROLL DOWN FOR ARTICLE

Taylor & Francis makes every effort to ensure the accuracy of all theinformation (the “Content”) contained in the publications on our platform.

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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]

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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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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.

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