Visitor Influence on the Behavior of Captive Greater Rheas (Rhea americana, Rheidae Aves)

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1 This article was downloaded by: [Cristiano Azevedo] On: 29 March 2012, At: 12:32 Publisher: Routledge Informa Ltd Registered in England and Wales Registered Number: Registered office: Mortimer House, Mortimer Street, London W1T 3JH, UK Journal of Applied Animal Welfare Science Publication details, including instructions for authors and subscription information: Visitor Influence on the Behavior of Captive Greater Rheas (Rhea americana, Rheidae Aves) Cristiano Schetini de Azevedo a, Márcia Fontes Figueiredo Lima b, Vitor Caetano Alves da Silva b, Robert John Young c & Marcos Rodrigues a a Ornithology Laboratory, Instituto de Ciências Biológicas, Universidade Federal de Minas Gerais, Brazil b Department of Biological Sciences, Centro Universitário de Belo, Horizonte, Minas Gerais, Brazil c Conservation, Ecology and Animal Behavior Group, Pontifíca Universidade Católica de Minas Gerais, Brazil Available online: 29 Mar 2012 To cite this article: Cristiano Schetini de Azevedo, Márcia Fontes Figueiredo Lima, Vitor Caetano Alves da Silva, Robert John Young & Marcos Rodrigues (2012): Visitor Influence on the Behavior of Captive Greater Rheas (Rhea americana, Rheidae Aves), Journal of Applied Animal Welfare Science, 15:2, To link to this article: PLEASE SCROLL DOWN FOR ARTICLE

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3 JOURNAL OF APPLIED ANIMAL WELFARE SCIENCE, 15: , 2012 Copyright Taylor & Francis Group, LLC ISSN: print/ online DOI: / Visitor Influence on the Behavior of Captive Greater Rheas (Rhea americana, Rheidae Aves) Cristiano Schetini de Azevedo, 1 Márcia Fontes Figueiredo Lima, 2 Vitor Caetano Alves da Silva, 2 Robert John Young, 3 and Marcos Rodrigues 1 1 Ornithology Laboratory, Instituto de Ciências Biológicas, Universidade Federal de Minas Gerais, Brazil 2 Department of Biological Sciences, Centro Universitário de Belo Horizonte, Minas Gerais, Brazil 3 Conservation, Ecology and Animal Behavior Group, Pontifíca Universidade Católica de Minas Gerais, Brazil Visitors can affect and reduce the welfare of nonhuman animals. The Belo Horizonte 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 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 behaviors most expressed were walking-watching-talking and stopped-watchingtalking; visitors or not, greater rheas most expressed behaviors (inversed between treatments) were foraging and walking alert; defecating/urinating and other behaviors differed statistically between treatments. Walking alert was most expressed in the presence of visitors; defecating/urinating and other behaviors were most 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. cristianoroxette@yahoo.com 113

4 114 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 visitoreffect influence often results in stress for captive animals and can be measured behaviorally (Birke, 2002; Chamove, Hosey, & Schaetzel, 1988; Sekar et al., 2008) and physiologically (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 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 (reintroduction) need to receive special attention in relation to their exposure to visitation. It is predicted that animals who are not exhibited to visitors will experience less stress than animals exposed to visitors (Burrell & Altman, 2006; Davey, 2006; Glatston, Geilvoet-Soeteman, Hora-Pecek, & Van Hoof, 1984); thus, these animals should be preferred for conservation projects such as reintroduction (McDougall, Réale, Sol, & Reader, 2006). However, many zoos do not have off-exhibit enclosures. On the other hand, for captive management, animals habituated to visitors and caretakers would suffer less stress than would nonhabituated animals (Jezierski, Jaworski, & Górecka, 1999). Some authors even suggested that the daily contact with visitors could function as environmental enrichment, providing sources of novelty in the environment, thus increasing the welfare of the captive animals (Hosey, 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 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, omnivorous birds who occur from Brazil to southern Argentina, habiting grasslands 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 the International Union for Conservation of Nature s (2011) red list of species threatened with extinction (Machado, Fonseca, Machado, Aguiar, & Lins, 1998).

5 VISITOR INFLUENCE ON GREATER RHEAS BEHAVIOR 115 Considering this scenario, conservation measures need to be implemented to avoid the greater rheas local extinction. Zoos and other institutions that hold these birds constitute the main sources of individuals for potential reintroduction projects; thus, evaluation of the public s 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 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 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 feces, 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. 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 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, & 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 19 ı ; W 44 ı ). The greater rheas exhibit was open to public

6 116 AZEVEDO ET AL. TABLE 1 Ethogram of the Greater Rheas (Rhea americana, Rheidae Aves) at Belo Horizonte Zoo Behavior Description Alert Walking Foraging Inactive Eating Drinking water Running Fighting Preening Threatening Eating feces Pacing Vocalization Mating Incubating eggs Courting Walking alert Play-escape Pecking Dust bathing Defecating/urinating Other behaviors Not visible Rhea stretches neck, elevating head, and moves head from side to side, watching vicinity. Rhea walks through enclosure. Rhea searches for food on the ground or on the vegetation. Rhea stands or sits inactive. Rhea eats the food provided by keeper. Rhea drinks water from the water hole. Rhea runs straight or in zigzags through enclosure. Two males stretch their necks, striking each other with thrusts and bill snapping. Rhea preens feathers with beak. Rhea opens bill and gapes, drawing head back slightly and turning it so as to face the other rhea continually. Rhea eats own or other rheas feces. Rhea walks continually in an eight-shaped route for no apparent reason. Rhea produces a deep-toned two-note call. 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. The male incubates the eggs in the nest. The male slowly approaches the female, lowers his neck in a low loop, and walks beside her, sometimes bobbing his head slightly. Rhea walks with an alert posture. Rhea jumps in the air and then run in zigzags as soon as he or she touches the ground, for no apparent reason. Rhea pecks objects in the ground or the enclosure s fence. Rhea extends neck and picks up some soil or dust with bill, throwing the dust onto own wings and body. Rhea defecates or urinates. Behaviors not previously recorded. Birds not visible to the observer. 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 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 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 ( years) and the birds had been exposed to the public between ages 3 and 7 years. Birds younger than 1 year were not exposed ( years).

7 VISITOR INFLUENCE ON GREATER RHEAS BEHAVIOR 117 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, 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 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 This period was chosen because pilot observations had shown rheas to be most active at this time of day. 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. 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 visitors behavior (Table 2) was based on 10 hr of ad libitum pilot observations (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. 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 the requirements for parametric statistics, which they did not; therefore, 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. 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

8 118 AZEVEDO ET AL. TABLE 2 Ethogram of the Visitors Behavior at the Greater Rhea Exhibit at Belo Horizonte Zoo Behavior Reading label Walking-watching-quietly Walking-watching-talking Walking-watching-shouting Walking-not-watching-quietly Walking-not-watching-talking Walking-not-watching-shouting Running Stopped-watching-quietly Stopped-watching-talking Stopped-watching-shouting Stopped-not-watching-quietly Stopped-not-watching-talking Stopped-not-watching-shouting Interacting with the rheas Other behaviors Not visible Description Visitor reads the label of the rhea s exhibit. Visitor walks quietly through the visitor s viewing area when watching the rheas. Visitor walks talking through the visitor s viewing area when watching the rheas. Visitor walks shouting through the visitor s viewing area when watching the rheas. Visitor walks quietly through the visitor s viewing area but not watching the rheas. Visitor walks talking through the visitor s viewing area but not watching the rheas. Visitor walks shouting through the visitor s viewing area but not watching the rheas. Visitor runs through the visitor s viewing area of the greater rheas exhibit. Visitor stops in the visitor s viewing area and quietly watches the rheas. Visitor stops in the visitor s viewing area and talks while watching the rheas. Visitor stops in the visitor s viewing area and shouts while watching the rheas. Visitor stops quietly in the visitor s viewing area but not watching the rheas. Visitor stops in the visitor s viewing area and talks but not watching the rheas. Visitor stops in the visitor s viewing area and shouts but not watching the rheas. Visitor interacts with the rheas, throwing food to the birds or calling the birds to approach him or her. Any other behavior expressed that is not in this ethogram. 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). 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

9 VISITOR INFLUENCE ON GREATER RHEAS BEHAVIOR 119 was 1; the largest group of visitors had 103 individuals. The mean time spent 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 behaviors were as follows: stopped-watching-talking (40.08%) and walking-watchingtalking (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 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 (0.03% each). Only walking alert, defecating/urinating, and other behaviors differed statistically 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). A negative significant correlation was found between the following behaviors: alert and walking-watching-talking (r s D 0.64, N D 30, p <.01); alert and FIGURE 1 Percentage of visitor behaviors in front of the greater rheas enclosure at Belo Horizonte Zoo. RL D reading label; WWQ D walking-watching-quietly; WWT D walking-watching-talking; WWS D walking-watching-shouting; WNWQ D walkingnot-watching-quietly; WNWT D walking-not-watching-talking; WNWS D walking-notwatching-shouting; RUN D running; SWQ D stopped-watching-quietly; SWT D stoppedwatching-talking; SWS D stopped-watching-shouting; INT D interacting with the rheas; OTH D other behaviors; NV D not visible.

10 120 AZEVEDO ET AL. TABLE 3 Behaviors (Daily Mean Number of Observations) Expressed by the Greater Rheas of BH Zoo in the Presence and Absence of Visitors in Front of Their Enclosure (Mean Standard Error, DF D 1, N D 30 in All Cases) and Mann-Whitney U Test Results Behavior With Public Without Public Mann- Whitney p Value Alert Walking Foraging Inactive Eating Drinking water Running Fighting Preening Threatening Eating feces Pacing Vocalization Mating Incubating eggs Courting Walking alert a Play escape Pecking Dust bathing Defecating/Urinating a Other behaviors <.01 a Not visible a Behaviors that differed statistically between treatments. running (public; r s D 0.37, N D 30, p <.05); alert and stopped-watchingtalking (r s D 0.47, N D 30, p <.01); preening; stopped-watching-talking (r s D 0.49, N D 30, p <.01); pacing; and other behaviors (public; r s D 0.58, N D 30, p <.01). A positive correlation was also found between foraging and stopped-watching-quietly behaviors (r s D 0.54, N D 30, p <.01). The first behaviors in the correlation referred to greater rheas behaviors; second behaviors in the correlation referred to the public s behaviors). A negative, significant correlation was found between the number of visitors in front of the exhibit and the following greater rheas behaviors: alert, pacing, and not visible (r s D 0.59, N D 30, p <.01, r s D 0.38, N D 30, p <.05, r s D 0.42, N D 30, p <.05).

11 VISITOR INFLUENCE ON GREATER RHEAS BEHAVIOR 121 DISCUSSION Greater rheas seemed habituated to visitor presence; the majority of their behaviors did not differ in either the presence or absence of visitors in front of their enclosure. Habituation is good for greater rheas captive management because it probably, reduces stress (Owen, Swaisgood, Czekala, Steinman, & Lindburg, 2004; Waitt, Buchanan-Smith, & Morris, 2002). For conservation programs, however, habituation should be avoided. After release, rheas might approach 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, defecating/urinating, and other behaviors. Walking alert was more often expressed when the visitors were present in front of the greater rheas enclosure. This 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 et al., 1988; Wells, 2005; Wood, 1998). Studies include the following: Indian leopards (Panthera pardus; Mallapur & Chellam, 2002), black rhinos (Diceros bicornis; 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 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 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 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% ( ) of the greater rheas activity budget. Thus, the recording of this behavior was disproportionately 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

12 122 AZEVEDO ET AL. presence of the public, greater rheas expressed significantly more of these relaxed 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. 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 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, 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, 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 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. 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 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

13 VISITOR INFLUENCE ON GREATER RHEAS BEHAVIOR 123 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 to affect the behavior of captive animals (Hosey & Druck, 1987; Sellinger & Ha, 2005). 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, & 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 the Laboratório de Ornitologia of Universidade Federal de Minas Gerais. Robert John Young and Marcos Rodrigues are supported by Fundação de Amparo à Pesquisa de Minas Gerais (Pesquisador Mineiro) and Conselho Nacional de Pesquisa (Bolsa de Produtividade). We thank Angela Faggioli and Carlyle Mendes Coelho for permission to use the Belo Horizonte Zoo s facilities and birds and for their invaluable suggestions on this article. REFERENCES Altmann, J. (1974). Observational study of behavior: Sampling methods. Behavior, 49, Azevedo, C. S., Ferraz, J. B., Tinoco, H. P., Young, R. J., & Rodrigues, M. (2010). Time-activity budget of greater rheas (Rhea americana, Aves) on a human-disturbed area: The role of habitat, time of the day, season and group size. Acta Ethologica, 13, Azevedo, C. S., & Young, R. J. (2006). Behavioral responses of captive-born greater rheas (Rhea americana) Linnaeus (Rheiformes, Rheidae) submitted to antipredator training. Revista Brasileira de Zoologia, 23, Bennet, K. A., & Zuelke, E. F. (1999). The effects of recreation on birds: A literature review. Wilmington, DE: Department of Natural Resources and Environmental Control. Birke, L. (2002). Effects of browse, human visitors and noise on the behavior of captive orangutans. Animal Welfare, 11, Brandt, L. F. S., & Neto, A. S. (1999). Introdução e Monitoramento de Rhea americana na EPDA Galheiro (Perdizes, MG) [Introduction and monitoring of Rhea americana at EPDA Galheiro (Perdizes, MG)]. Belo Horizonte, Brazil: CEMIG. Burrell, A. M., & Altman, J. D. (2006). The effect of captive environment on activity of captive cotton-top tamarins (Saguinus oedipus). Journal of Applied Animal Welfare Science, 9, Candland, D. K., & Campbell, B. A. (1962). Development of fear in the rat as measured by behavior in the open field. Journal of Comparative and Physiological Psychology, 55, 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,

14 124 AZEVEDO ET AL. Chamove, A. S., Hosey, G. R., & Schaetzel, P. (1988). Visitors excite primates in zoos. Zoo Biology, 7, Codenotti, T. L., Beninca, D., & Alvarez, F. (1995). Etograma y relacion de la conducta con el habitat y con la edad en el ñandú [Ethogram and the relation of the behavior of greater rheas with habitat and age]. Doñana, Acta Vertebrata, 22(12), Dani, S. (1993). A Ema Rhea americana: Biologia, manejo e conservação [The greater Rhea americana: Biology, management, and conservation]. Belo Horizonte, Brazil: Fundação Acangaú. Davey, G. (2006). Visitor behavior in zoos: A review. Anthrozoos, 19, Davey, G. (2007). Visitors effects on the welfare of animals in the zoo: A review. Journal of Applied Animal Welfare Science, 10, Davies, S. J. J. F. (2002). Ratites and tinamous. Oxford, UK: Oxford University Press. Davis, N., Schaffner, C. M., & Smith, T. E. (2005). Evidence that zoo visitors influence HPA activity in spider monkeys (Ateles geoffroyii rufiventris). Applied Animal Behavior Science, 90, Del Hoyo, J., Elliot, A., & Sargatal, J. A. (1992). Handbook of the birds of the world (Vol. 1). Barcelona, Spain: Lynx Editions. Farrand, A. (2007). The effect of zoo visitors on the behavior and welfare of zoo mammals (Doctoral thesis, University of Stirling, Edinburgh, Scotland). Glatston, A. R., Geilvoet-Soeteman, E., Hora-Pecek, E., & Van Hoof, J. A. R. A. M. (1984). The influence of the zoo environment on social behavior of groups of cotton-topped tamarins, Saguinus aedipus aedipus. Zoo Biology, 3, Hayward, M. W., Adendorff, J., O Brien, J., Sholto-Douglas, A., Bissett, C., Moolman, L. C., : : : Kerley, G. I. H. (2007). Practical considerations for the reintroduction of large, terrestrial, mammalian predators based on reintroductions to South Africa s Eastern Cape Province. The Open Conservation Biology Journal, 1, Hosey, G. R. (2000). Zoo animals and their human audiences: What is the visitor effect? Animal Welfare, 9, Hosey, G. R., & Druck, P. L. (1987). The influence of zoo visitors on the behavior of captive primates. Applied Animal Behavior Science, 18, International Union for Conservation of Nature. (2011). IUCN Red List of Threatened Species (Version ). Retrieved from Jezierski, T., Jaworski, Z., & Górecka, A. (1999). Effects of handling on behaviour and heart rate in konik horses: Comparison of stable and forest reared young stock. Applied Animal Behaviour Science, 62, Kasereka, B., Muhigwa, J. B., Shalukoma, C., & Kahekwa, J. M. (2006). Vulnerability of habituated Grauer s gorilla to poaching in the Kahuzi-Biega National Park, DRC. African Study Monographs, 27, Kloppers, E. L., St. Clair, C. C., & Hurd, T. E. (2005). Predator-resembling aversive conditioning for managing habituated wildlife. Ecology and Society, 10, 31. Lamarque, F., Anderson, J., Chardonnet, P., Fergusson, R., Lagrange, M., Osei-Owusu, Y., : : : Tabi Tako-Eta, P. (2008). Human-wildlife conflict in Africa: An overview of causes, consequences and management strategies. Rome, Italy: International Foundation for the Conservation of Wildlife, Food and Agriculture Organization of the United Nations. Machado, A. B. M., Fonseca, G. A. B., Machado, R. B., Aguiar, L. M. S., & Lins, L. V. (1998). Livro vermelho das espécies ameaçadas de extinção da fauna de Minas Gerais [The red list of animal threatened species of Minas Gerais]. Belo Horizonte, Brazil: Fundação Biodiversitas. 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, Margulis, S. W., Royos, C., & Anderson, M. (2003). Effect of felid activity on zoo visitor interest. Zoo Biology, 22, Martella, M. B., Renison, D., & Navarro, J. T. (1995). Vigilance in the greater rhea: Effects of vegetation height and group size. Journal of Field Ornithology, 66,

15 VISITOR INFLUENCE ON GREATER RHEAS BEHAVIOR 125 Martin, P., & Bateson, P. (2007). Measuring behavior: An introductory guide (3rd ed.). Cambridge, UK: Cambridge University Press. McDougall, P. T., Réale, D., Sol, D., & Reader, S. M. (2006). Wildlife conservation and animal temperament: Causes and consequences of evolutionary change for captive, reintroduced, and wild populations. Animal Conservation, 9, Mitchell, G., Herring, F., & Obradovich, S. (1992). Like threaten like in mangabeys and people? Anthrozoos, 5, Mitchell, H., & Hosey, G Zoo research guidelines: Studies on the effects of human visitors on zoo animal behavior. London, UK: British and Irish Association of Zoos and Aquariums. Moberg, G. P., & Mench, J. A. (2000). The biology of animal stress: Basic principles and implications for animal welfare. Wallingford, UK: CABI. Montanha, J. C., Silva, S. L., & Boere, V. (2009). Comparison of salivary cortisol concentrations in jaguar kept in captivity with differences in exposure to the public. Ciência Rural, 39, Morris, D. (1964). The response of animals to a restricted environment. Symposium of the Zoological Society of London, 13, Munksgaard, L., de Passile, A. M., Rushen, J., Thodberg, K., & Jensen, M. B. (1997). Discrimination of people by dairy cows based on handling. Journal of Dairy Science, 80, Owen, M. A., Swaisgood, R. R., Czekala, N. M., Steinman, K., & Lindburg, D. G. (2004). Monitoring stress in captive giant pandas (Ailuropoda melanoleuca): Behavioral and hormonal responses to ambient noise. Zoo Biology, 23, Pazol, K. A., & Bloomsmith, M. A. (1993). The development of stereotyped body rocking in chimpanzees (Pan troglodytes) reared in a variety of nursery settings. Animal Welfare, 2, Rajagopal, T., Archunan, G., & Sekar, M. (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, Reboreda, J. C., & Fernandez, G. J. (1997). Sexual, seasonal and group size differences in the allocation of time between vigilance and feeding in the greater rhea (Rhea americana). Ethology, 103, Sanger, G. J., Yoshida, M., Yahyah, M., & Kitazumi, K Increased defecation during stress or after 5-hydroxytryptophan: Selective inhibition by the 5-HT 4 receptor antagonist, 5B British Journal of Pharmacology, 130, Sekar, M., Rajagopal, T., & Archunan, G. (2008). Influence of zoo visitor presence on the behavior of captive Imdian gaur (Bos gaurus gaurus) in a zoological park. Journal of Applied Animal Welfare Science, 11, Sellinger, R. L., & Ha, J. C. (2005). The effects of visitor density and intensity on the behavior of two captive jaguars (Panthera onca). Journal of Applied Animal Welfare Science, 8, Sick, H. (1997). Ornitologia Brasileira [Brazilian ornithology]. Rio de Janeiro, Brazil: Editora Nova Fronteira. Vargas, L. C., Marques, T. A., & Schenberg, L. C. (2000). Micturition and defensive behaviors are controlled by distinct neural networks within the dorsal periaqueductal gray and deep gray layers of the superior colliculus of the rat. Neuroscience Letters, 280, Waitt, C., Buchanan-Smith, H., & Morris, K. (2002). The effects of caretaker-primate relationships on primates on the laboratory. Journal of Applied Animal Welfare Science, 5, Wells, D. L. (2005). A note on the influence of visitors on the behavior and welfare of zoo-housed gorillas. Applied Animal Behavior Science, 93, Wood, W. (1998). Interactions among environmental enrichment, viewing crowds, and zoo chimpanzees (Pan troglodytes). Zoo Biology, 17, Young, R. J. (2003). Environmental enrichment for captive animals. Oxford, UK: Blackwell. Zar, J. H. (1999). Biostatistical analysis. Newark, NJ: Prentice Hall.