Visitor Influence on the Behavior of Captive

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

Cristiano Schetini de Azevedo , Márcia Fontes b

b

Figueiredo Lima , Vitor Caetano Alves da Silva , c

Robert John Young & 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, 113-125 To link to this article: http://dx.doi.org/10.1080/10888705.2012.624895

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JOURNAL OF APPLIED ANIMAL WELFARE SCIENCE, 15:113–125, 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 Lima,2 Vitor Caetano Alves da Silva,2 Robert John Young,3 and Marcos Rodrigues1 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. Email: [email protected]

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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).


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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 19ı510 44.800; W 44ı 000 40.100 ). The greater rheas’ exhibit was open to public

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TABLE 1 Ethogram of the Greater Rheas (Rhea americana, Rheidae Aves) at Belo Horizonte Zoo Behavior


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

Description 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 (5.6 ˙ 0.8 years) and the birds had been exposed to the public between ages 3 and 7 years. Birds younger than 1 year were not exposed (4.6 ˙ 0.7 years).



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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 2009. 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

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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



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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 (rs 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.

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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

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 a Behaviors

16.37 64.67 66.13 45.73 16.43 31.23 0.13 0.27 9.73 0.17 13.10 42.83 0.70 0.20 32.30 3.53 1.03 0.10 0.23 2.00 0.53 0.63 1.80

˙ ˙ ˙ ˙ ˙ ˙ ˙ ˙ ˙ ˙ ˙ ˙ ˙ ˙ ˙ ˙ ˙ ˙ ˙ ˙ ˙ ˙ ˙

2.28 4.50 6.14 5.32 2.77 7.85 0.07 0.20 2.01 0.08 3.14 8.62 0.30 0.20 7.77 1.18 0.37 0.06 0.11 0.71 0.13 0.19 0.59

Without Public

MannWhitney

p Value

˙ ˙ ˙ ˙ ˙ ˙ ˙ ˙ ˙ ˙ ˙ ˙ ˙ ˙ ˙ ˙ ˙ ˙ ˙ ˙ ˙ ˙ ˙

838.5 1000.5 930.0 948.5 1027.5 833.5 938.0 885.5 921.5 898.5 926.0 831.0 923.5 915.5 890.0 899.0 796.0 915.0 900.0 942.0 1058.0 1093.0 853.0

.26 .21 .83 .63 .10 .23 .59 .32 .93 .67 .88 .22 .88 1.00 .69 .78 .02a 1.00 .73 .66 .02a