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Visitor Influence on the Behavior of Captive Greater Rheas
(Rhea americana, Rheidae Aves) . . . . . . . . . . . . . . . . . . . . . . . . . . . . 000
Cristiano Schetini de Azevedo, Márcia Fontes Figueiredo Lima,
Vitor Caetano Alves da Silva, Robert John Young, and
Marcos Rodrigues
HAAW #624895, VOL 15, ISS 1 (November 10, 2011)
Visitor Influence on the Behavior
of Captive Greater Rheas
(Rhea americana, Rheidae Aves)
Cristiano Schetini de Azevedo, Márcia Fontes Figueiredo
Lima, Vitor Caetano Alves da Silva, Robert John Young, and
Marcos Rodrigues
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HAAW #624895, VOL 15, ISS 1 (November 10, 2011)
JOURNAL OF APPLIED ANIMAL WELFARE SCIENCE, 15:1–13, 2012
Copyright © Taylor & Francis Group, LLC
ISSN: 1088-8705 print/1532-7604 online
DOI: 10.1080/10888705.2012.624895
Visitor Influence on the Behavior
of Captive Greater Rheas
(Rhea americana, Rheidae Aves)
Cristiano Schetini de Azevedo,1 Márcia Fontes Figueiredo Q1
Lima,2 Vitor Caetano Alves da Silva,2 Robert John Young,3 5
and Marcos Rodrigues1
1Laboratório de Ornitologia, Instituto de Ciências Biológicas,
Universidade Federal de Minas Gerais, Brazil
2Centro Universitário de Belo Horizonte, Minas Gerais, Brazil Q2
3Conservation, Ecology and Animal Behavior Group, Pontifíca 10
Universidade Católica de Minas Gerais, Brazil
Visitors can affect and reduce the welfare of nonhuman animals. The Belo Hor-
izonte Zoo, Brazil, had a group of greater rheas intended for reintroduction to
the wild. Because this group received public visitation, evaluating its effect on the
birds’ behavior and welfare was important. The study conducted 60 hr of behavioral 15
observations: 30 with, and 30 without, visitors in front of the birds’ enclosure. The
study, conducted April–December 2009, collected data using scan sampling with
instantaneous recording of behavior every minute. The study collected data on
public behavior, visitor density, and time spent observing the birds. More than
4,000 persons visited the birds’ enclosure: 9.86 s average time spent. Public 20
behaviors most expressed were walking-watching-talking and stopped-watching-
talking; visitors or not, greater rheas’ most expressed behaviors (inversed between
treatments) were foraging and walking alert; defecating/urinating and other behav-
iors differed statistically between treatments. Walking alert was most expressed
in the presence of visitors; defecating/urinating and other behaviors were most 25
expressed in their absence. Greater rheas seemed to habituate to visitors. Birds’
behaviors differed little in visitors’ presence or absence.
Correspondence should be sent to Cristiano Schetini de Azevedo, Laboratório de Ornitologia,
Instituto de Ciências Biológicas, Universidade Federal de Minas Gerais Av.: Antônio Carlos, 6627,
Pampulha, Belo Horizonte, Minas Gerais, Brazil. Email: cristianoroxette@yahoo.com
1
2 Q3SCHETINI DE AZEVEDO ET AL.
Visitor influence (such as inducing behavioral changes) on the behavior of
nonhuman animals in captivity has been widely documented (Davey, 2007;
Farrand, 2007; Hosey, 2000; Sekar, Rajagopal, & Archunan, 2008). This visitor-
effect influence often results in stress for captive animals and can be measured 30
behaviorally (Birke, 2002; Chamove et al., 1998; Sekar et al., 2008) and physi- Q4
ologically (Davis, Schaffner, & Smith, 2005; Montanha, Silva, & Boere, 2009;
Rajagopal, Archunan, & Sekar, 2011).
Stress is defined as the biological responses of an organism to cope with
threats to the organism’s homeostasis (Moberg & Mench, 2000). Some studies 35
have shown a link between the increase of people in front of exhibits and a
greater expression of aggressive behavior (Hosey, 2000; Sekar et al., 2008).
Thus, captive animals intended to be part of conservation programs (rein-
troduction) need to receive special attention in relation to their exposure to
visitation. It is predicted that animals who are not exhibited to visitors will 40
experience less stress than animals exposed to visitors (Burrel & Altman, 2006; Q5
Davey, 2006; Glatston, Geilvoet-Soeteman, Hora-Pecek, & Van Hoof, 1984);
thus, these animals should be preferred for conservation projects such as rein-
troduction (McDougall, Réale, Sol, & Reader, 2006). However, many zoos do
not have off-exhibit enclosures. 45
On the other hand, for captive management, animals habituated to visitors and
caretakers would suffer less stress than would nonhabituated animals (Jezierski
et al., 1999). Some authors even suggested that the daily contact with visitors Q6
could function as environmental enrichment, providing sources of novelty in
the environment, thus increasing the welfare of the captive animals (Hosey, 50
2000; Margulis, Royos, & Anderson, 2003). This is, at least theoretically, the
worst situation for animals intended to be reintroduced to the wild. They could
be attracted to the human presence, increasing human-animal conflicts and
increasing their chance of being captured or killed (Hayward et al., 2007).
Consequently, zoo visitation needs to be evaluated carefully, depending on the 55
species in question and on the goals of the zoo; thus, conservation versus animal
welfare is a conflict faced by zoo managers.
Greater rheas (Rhea americana, Rheidae Aves) are the largest South American
bird (Del Hoyo, Elliot, & Sargatal, 1992; Sick, 1997); they are flightless, om-
nivorous birds who occur from Brazil to southern Argentina, habiting grasslands 60
and cerrados (savannah-like vegetation) also in Paraguay, Uruguay, and Bolivia
(Davies, 2002). Greater rheas’ populations are diminishing throughout their
distribution due to habitat loss, hunting, crop burnings, and egg losses caused
by the use of heavy agricultural machinery (Dani, 1993; Sick, 1997). In Minas
Gerais State, southeastern Brazil, greater rheas are classified as vulnerable on 65
the IUCN’s red list of species threatened with extinction (Machado, Fonseca, Q7
Machado, Aguiar, & Lins, 1998). Considering this scenario, conservation mea-
sures need to be implementedto avoid the greater rheas’ local extinction.
Q8BEHAVIOR OF CAPTIVE GREATER RHEAS 3
Zoos and other institutions that hold these birds constitute the main sources of
individuals for potential reintroduction projects; thus, evaluation of the public’s 70
effect on the behavior of captive greater rheas is important for the planning of
conservation programs. The evaluation of the public’s effect on the behavior of
captive greater rheas is important for the planning of conservation programs.
This is the case of the Belo Horizonte Zoo (BH Zoo) in southeastern Brazil
that intends to reintroduce greater rheas in the near future. If negative effects 75
of visitors’ presence on the birds’ behavior or welfare are detected, then new
management strategies could be implemented to conserve greater rheas’ natural
behavior and to avoid health problems.
The aim of this study was to detect the visitor effect on captive greater
rheas by comparing their behavioral expression on days with and without public 80
visitation. It was expected that (a) greater rheas would exhibit more abnormal
behaviors, such as pacing, on the days with visitation; (b) larger numbers of
visitors would elicit more abnormal behavior; and (c) the intensity of visitation
(visitor behavior) would influence greater rheas’ behavior. The greater rheas’
behaviors (alert, running, walking alert, defecating/urinating, pacing, eating fe- 85
ces, and drinking water) were considered indicative of stress (Azevedo & Young,
2006; Codenotti, Beninca, & Alvarez, 1995). The behaviors (eating feces, pacing,
and drinking water excessively) were considered abnormal due to their lack of
presence in conspecifics in the wild or to their high rate of expression during
this study’s pilot study. 90
In the pilot study, rheas drank water for more than 12% of their daily
activity budget. Greater rheas normally drink water for less than 4% of their
activity budget (Azevedo, Ferraz, Tinoco, Young, & Rodrigues, 2010; Codenotti
et al., 1995). All other behaviors were considered relaxed behaviors as shown in
the rheas’ ethogram (Table 1). Alert and walking alert are behaviors normally Tab195
expressed during vigilance for predators or during male-male fights for mating
(Martella, Renison, & Navarro, 1995); running is expressed during events of
predation or during fights between males (Azevedo & Young, 2006; Codenotti
et al., 1995). Defecating/urinating is a normal behavior; however, its expression
increases during stressful or fear-inducing events (Sanger, Yoshida, Yahyah, & 100
Kitazumi, 2000).
MATERIAL AND METHODS
Five greater rheas were studied (2 males and 3 females) who were held in
the Bird Square of the Belo Horizonte Zoo (BH Zoo), Minas Gerais, Brazil
(S 19ı51044.800; W 44ı00040.100). The greater rheas’ exhibit was open to public 105
visitation every week, Tuesday–Sunday, 9:00 a.m.–5:00 p.m. Birds were housed
in a wire-fenced enclosure 28 m in length and 16 m wide. The front of the
4 Q3SCHETINI DE AZEVEDO ET AL.
TABLE 1
Q9Ethogram of the Greater Rheas (Rhea americana, Rheidae, Aves) at BH Zoo
Behavior Description
Alert Rhea stretches neck, elevating head, and moves head from side to side,
watching vicinity.
Walking Rhea walks through enclosure.
Foraging Rhea searches for food on the ground or on the vegetation.
Inactive Rhea stands or sits inactive.
Eating Rhea eats the food provided by keeper.
Drinking water Rhea drinks water from the water hole.
Running Rhea runs straight or in zigzags through enclosure.
Fighting Two males stretch their necks, striking each other with thrusts and bill
snapping.
Preening Rhea preens feathers with beak.
Threatening Rhea opens bill and gapes, drawing head back slightly and turning it so
as to face the other rhea continually.
Eating feces Rhea eats own or other rheas’ feces.
Pacing Rhea walks continually in an eight-shaped route for no apparent reason.
Vocalization Rhea produces a deep-toned two-note call.
Mating The female lies flat on the ground as the male grasps the feathers on the
back of her neck with his bill; he rests on his legs while copulating.
Incubating eggs The male incubates the eggs in the nest.
Courting The male slowly approaches the female, lowers his neck in a low loop,
and walks beside her, sometimes bobbing his head slightly.
Walking alert Rhea walks with an alert posture.
Play-escape Rhea jumps in the air and then run in zigzags as soon as he or she
touches the ground, for no apparent reason.
Pecking Rhea pecks objects in the ground or the enclosure’s fence.
Dust bathing Rhea extends neck and picks up some soil or dust with bill, throwing the
dust onto own wings and body.
Defecating/urinating Rhea defecates or urinates.
Other behaviors Behaviors not previously recorded.
Not visible Birds not visible to the observer.
enclosure was the visitors’ viewing area (28 m length); a female cassowary
(Casuarius casuarius) and two ostriches (Struthio camelus) were housed in
neighboring enclosures. Rheas were fed twice a day with a mixture of ratite 110
ration (Socil®; 1.2 kg in total) and vegetables (carrot and cabbage; 1.3 kg in
total). Water was provided ad libitum in a water hole. The enclosure was cleaned
three times a week (Tuesdays, Thursdays, and Saturdays) but never during the
data-collection period. Birds’ ages ranged from 4 to 8 years (5.6 ˙ 0.8 years)
and the birds had been exposed to the public between ages 3 and 7 years. Birds 115
younger than 1 year were not exposed (4.6 ˙ 0.7 years).
Q8BEHAVIOR OF CAPTIVE GREATER RHEAS 5
The study was divided into two treatments: (a) the presence of visitors in
front of the greater rheas’ enclosure and (b) the absence of visitors in front of
the greater rheas’ enclosure. Data collection in the absence of the public was
conducted only on Mondays, when the zoo was closed to visitation. In addition, 120
no keeper was allowed to enter or pass in front of the rheas’ enclosure during
data collection. Data collection in the presence of the public was conducted on
Tuesdays and weekends, days when the BH Zoo receives most of its visitors;
the flow of the public in front of the greater rheas’ enclosure was continuous.
Thirty hours of behavioral data were collected in each treatment. All data were 125
collected using scan sampling with instantaneous recording of behaviors every
minute (Altmann, 1974). All behavioral data-collection sessions were conducted
between 1500h and 1600h daily, April–December 2009. This period was chosen
because pilot observations had shown rheas to be most active at this time of
day. 130
An ethogram for greater rheas (Table 1) was constructed. The ethogram was
based on scientific literature (Brandt & Neto, 1999; Codenotti et al., 1995) and
on 12 hr of ad libitum pilot observations (Martin & Bateson, 2007). Stress-related
activities were inferred only on behavioral changes and were not measured
physiologically. 135
Data on behavior of the public were also collected in the same time period by
a second observer. The study used scan-sampling data collection for more than
two visitors, and behaviors of all visitors in the groups were recorded. Focal
sampling was used (when only one visitor was present), with instantaneous
recording of behaviors every minute (Altmann, 1974). An ethogram of the 140
visitors’ behavior (Table 2) was based on 10 hr of ad libitum pilot observations Tab2
(Martin & Bateson, 2007). Data concerning visitor number (number of visitors
per hour in front of the greater rheas’ enclosure) and time spent in front of
the greater rheas’ enclosure (period each visitor or group of visitors stayed in
front of the greater rheas’ enclosure) were also collected by a third observer. 145
Tests of interobserver reliability were conducted during the 1 month of pilot
observations.
Data on greater rheas’ behavior was quantified (total number of each behavior
recordings per day) and tested with an Anderson-Darling test to determine if
they met therequirements for parametric statistics, which they did not; therefore, 150
nonparametric statistical tests were used throughout. The Mann-Whitney U test
was used to compare the mean number of behavioral recordings in both presence
and absence of the visitors in front of the greater rheas’ enclosure.
Data on the visitors’ behavior was quantified; focal and scan samplings were
summed and the total number of each behavior recordings per day analyzed. 155
Results of the visitor-behavior analysis are presented as percentages.
Spearman’s rank correlations between (a) behaviors expressed by the greater
rheas and by the visitors and between (b) behaviors expressed by the greater
6 Q3SCHETINI DE AZEVEDO ET AL.
TABLE 2
Q10Ethogram of the Visitors’ Behavior at the Greater Rhea Exhibit at BH Zoo
Behavior Description
Reading label Visitor reads the label of the rhea’s exhibit.
Walking-watching-quietly Visitor walks quietly through the visitor’s viewing area when
watching the rheas.
Walking-watching-talking Visitor walks talking through the visitor’s viewing area when
watching the rheas.
Walking-watching-shouting Visitor walks shouting through the visitor’s viewing area
when watching the rheas.
Walking-not-watching-quietly Visitor walks quietly through the visitor’s viewing area but
not watching the rheas.
Walking-not-watching-talking Visitor walks talking through the visitor’s viewing area but
not watching the rheas.
Walking-not-watching-shouting Visitor walks shouting through the visitor’s viewing area but
not watching the rheas.
Running Visitor runs through the visitor’s viewing area of the greater
rheas’ exhibit.
Stopped-watching-quietly Visitor stops in the visitor’s viewing area and quietly
watches the rheas.
Stopped-watching-talking Visitor stops in the visitor’s viewing area and talks while
watching the rheas.
Stopped-watching-shouting Visitor stops in the visitor’s viewing area and shouts while
watching the rheas.
Stopped-not-watching-quietly Visitor stops quietly in the visitor’s viewing area but not
watching the rheas.
Stopped-not-watching-talking Visitor stops in the visitor’s viewing area and talks but not
watching the rheas.
Stopped-not-watching-shouting Visitor stops in the visitor’s viewing area and shouts but not
watching the rheas.
Interacting with the rheas Visitor interacts with the rheas, throwing food to the birds or
calling the birds to approach him or her.
Other behaviors Any other behavior expressed that is not in this ethogram.
Not visible Birds not visible to the observer.
rheas and the number of visitors were undertaken. For all statistical analyses,
the confidence level was 95% (˛ D 0.05; Zar, 1999). 160
RESULTS
The number of the public who visited the greater rheas’ enclosure during the
study period was 4,182, with a mean of 139.4% (˙ 15.3) per hour. The minimum
number of visitors in front of the greater rheas’ enclosure at the same time
Q8BEHAVIOR OF CAPTIVE GREATER RHEAS 7
was 1; the largest group of visitors had 103 individuals. The mean time spent 165
by the visitors in front of the greater rheas’ enclosure was 9.86 (˙ 1.49) s, the
minimum time spent by the visitors in front of the greater rheas’ enclosure was
9 s, and the maximum time was 319 s. The percentages of behaviors expressed
by the visitors are shown in Figure 1. The most performed visitor behav- Fig1
iors were as follows: stopped-watching-talking (40.08%) and walking-watching- 170
talking (30.25%). The least exhibited behaviors were walking-watching-shouting
(0.17%) and interacting-with-the-birds (0.33%); walking-not-watching-shouting
behavior was not performed by the visitors during the study.
The most expressed behaviors by the greater rheas in the presence of the
public were foraging (19.12%) followed by walking (18.62%); the least exhibited 175
behaviors by the greater rheas in the presence of the public were play-escape
(0.03%) and running (0.04%). The most expressed behaviors by the greater
rheas without the presence of the visitors were walking (21.71%) and foraging
(19.49%); the least exhibited behaviors by the greater rheas without the presence
of the visitors were play-escape and intimidating, both with only three records 180
(0.03% each).
Only walking alert, defecating/urinating, and other behaviors differed statisti-
cally between the treatments (Table 1). Walking alert was expressed more often
in the presence of visitors, whereas defecating/urinating and other behaviors
were more often expressed in the absence of the visitors (Table 3). Tab3185
A negative significant correlation was found between the following behaviors:
alert and walking-watching-talking (rs D �0.64, N D 30, pshould be avoided. After release, rheas might approach 205
humans; such approaches could cause problems for the birds (Kloppers, St. Clair,
& Hurd, 2005; Lamarque et al., 2008).
Only the following behaviors differed between treatments: walking alert, defe-
cating/urinating, and other behaviors. Walking alert was more often expressed
when the visitors were present in front of the greater rheas’ enclosure. This 210
could be vigilance (antipredator) response; that is, with the presence of people,
greater rheas became more stressed. Greater rheas increased their vigilance when
presented with predators (stuffed jaguar and a dog) in an antipredator training
study conducted by Azevedo and Young (2006). Stress due to visitors’ presence
has been observed for primates in many studies (Chamove, Hosey, & Schaetzel, 215
1988; Wells, 2005; Wood, 1998). Studies include the following: Indian leopards
(Panthera pardus; Mallapur & Cheilant, 2002), black rhinos (Diceros bicornis; Q12
Carlstead & Brown, 2005), birds (Bennet & Zuelke, 1999), and Indian gaurs
(Bos gaurus; Sekar et al., 2008).
Three factors influence vigilance in greater rheas in the wild: size of the 220
group, sex of the bird, and time of year. Solitary birds exhibit more vigilance
behavior than do groups of 2 or more birds (Martella et al., 1995; Reboreda
& Fernandez, 1997); males exhibit more vigilance behaviors than do females
(Reboreda & Fernandez, 1997); and, during breeding season, rheas become more
vigilant (Azevedo et al., 2010). These variables did not seem to have influenced 225
the results found in this study. All data in this study were recorded during
greater rheas’ breeding season. Of 5 birds studied (Reboreda & Fernandez,
1997), none showed differences in vigilance behaviors between groups of 2
to 26; further, the sex ratio of the group was nearly 1:1. Defecating/urinating
was most exhibited when the public was absent from the visitor area; when 230
frequently expressed, this behavior may be associated with fear (Candland &
Campbell, 1962; Munksgaard, de Passile, Rushen, Thodberg, & Jensen, 1997;
Vargas, Marques, & Schenberg, 2000). Such association was not the case in this
study; the behavior occupied only 0.2% (0.53 ˙ 0.13) of the greater rheas’
activity budget. Thus, the recording of this behavior was disproportionately 235
higher in the absence of visitors, probably due to chance.
Other behaviors such as head scratching, stretching, and building nests were
also more often expressed when the public was absent from the visitor area.
These behaviors could indicate a relaxed behavioral state; because without the
10 Q3SCHETINI DE AZEVEDO ET AL.
presence of the public, greater rheas expressed significantly more of these relaxed 240
behaviors, their low occurrence in the presence of visitors could be interpreted
as a low source of stress to the birds. It is important to emphasize that other
behaviors were expressed at very low levels (less than 1% of the activity-time
budget; 0.2% in the presence and 0.7% in the absence of visitors). None of the
abnormal behaviors differed statistically between treatments. 245
Most of the behaviors expressed by the visitors were not considered threats to
the welfare of the greater rheas. All the correlations found between visitor and
rhea behavior supported this statement. Shouting and rhea-visitor interactions
were rare, and the time spent by the visitors in front of the greater rheas’
enclosure was minimal (9.8 s on average). Public flux was high; this could act as 250
a source of novelty for the birds, even functioning as environmental enrichment
(Morris, 1964; Pazol & Bloomsmith, 1993). The negative correlations found
between the alert, pacing, and not visible behaviors support this hypothesis. In
this study, audience activities and noisiness, the most common variables inferred
as sources of animal stress (Birke, 2002; Hosey & Druck, 1987; Mitchell, 255
Herring, & Obradovich, 1992), did not appear to show great negative effects
on greater rheas’ welfare.
The behaviors expressed by the rheas were also influenced by a number of
other variables not measured in this study; thus, it is important to remember
that generalizations of these results should be made with care. For example, 260
contact with zookeepers and the regular maintenance of the enclosure (cleaning
days) had been reduced due to the prohibition of such activities during the
periods of data collection. In addition, other factors could have influenced the
results (Mitchell & Hosey, 2005): frequency of camera flashes, objects (such
as umbrellas) carried by the public, smoking, sex and age of the visitors, and 265
period of data collection. Behavioral data collection at different times of the day
could have shown differences, related to the effect of the public, in the activity
budget of the rheas. For example, had rheas rested in the morning when no
visitors were present but did not rest when visitors were present, this would be
a better indicator of visitor-induced stress. 270
CONCLUSION
The results found in this study showed that the greater rheas of BH Zoo
appeared habituated to the presence of the public. There were, however, animal
welfare implications. The greater rheas’ habituation to the public indicates
visitors probably were not a significant source of stimuli causing animal welfare 275
problems (stress). To avoid changes in this scenario, it is important that the
zoo’s staff provide educational support to the public visiting the greater rhea’s
enclosure, namely, to avoid shouting or performing behaviors that might be
Q8BEHAVIOR OF CAPTIVE GREATER RHEAS 11
stress-inducing for the birds. The greater rheas in this study did not show signs
of stress problems; however, density and intensity of visitors have been shown 280
to affect the behavior of captive animals (Hosey & Druck, 1987; Sellinger &
Ha, 2005). Q13
For animals intended for reintroduction to the wild, the results found in
this study are worrying. Habituated animals have a greater probability of dying
after release than nonhabituated animals (Kasereka, Muhigwa, Shalukoma, & 285
Kahekwa, 2006). On the other hand, the maintenance of nonhabituated animals in
the zoo could generate welfare problems due to acute or chronic stress resulting
from daily contact with humans (Moberg & Mench, 2000).
ACKNOWLEDGMENTS
MR thanks the Fundação O Boticário de Proteção à Natureza for supporting 290
the Laboratório de Ornitologia of Universidade Federal de Minas Gerais. RJY Q14
and MR are supported by FAPEMIG (Pesquisador Mineiro) and CNPq (Bolsa
de Produtividade). We thank Angela Faggioli and Carlyle Mendes Coelho for
permission to use the BH Zoo’s facilities and birds and for their invaluable Q15
suggestions on this article. 295
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