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

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.     

Influence of zoo visitor presence on the behavior of captive Indian gaur (Bos gaurus gaurus) in a zoological park

Visitors to zoos can be a source of potential disturbance and stress to some captive, nonhuman animals in the wild. To determine the influence of visitor presence on captive bison (Bos gaurus gaurus), the study analyzed the behavior of 4 individuals at the Arignar Anna Zoological Park, India. The study often observed the behavior of the animals on visitor-present days and on days when visitors were absent. In the presence of zoo visitors, the bison showed a higher level of intragroup aggression and moving behavior. In contrast, the bison rested more when no visitors were present. The results revealed that the presence of zoo visitors significantly influenced the behavior of captive bison and thereby may have affected their welfare.     

Influence of Zoo Visitor Presence on the Behavior of Captive Indian Gaur (Bos gaurus gaurus) in a Zoological Park

Visitors to zoos can be a source of potential disturbance and stress to some captive, nonhuman animals in the wild. To determine the influence of visitor presence on captive bison (Bos gaurus gaurus), the study analyzed the behavior of 4 individuals at the Arignar Anna Zoological Park, India. The study often observed the behavior of the animals on visitor-present days and on days when visitors were absent. In the presence of zoo visitors, the bison showed a higher level of intragroup aggression and moving behavior. In contrast, the bison rested more when no visitors were present. The results revealed that the presence of zoo visitors significantly influenced the behavior of captive bison and thereby may have affected their welfare.     

An hourly variation in zoo visitor interest: measurement and significance for animal welfare research

A methodological difficulty facing welfare research on nonhuman animals in the zoo is the large number of uncontrolled variables due to variation within and between study sites. Zoo visitors act as uncontrolled variables, with number, density, size, and behavior constantly changing. This is worrisome because previous research linked visitor variables to animal behavioral changes indicative of stress. There are implications for research design: Studies not accounting for visitors' effect on animal welfare risk confounding (visitor) variables distorting their findings. Zoos need methods to measure and minimize effects of visitor behavior and to ensure that there are no hidden variables in research models. This article identifies a previously unreported variable—hourly variation (decrease) in visitor interest—that may impinge on animal welfare and validates a methodology for measuring it. That visitor interest wanes across the course of the day has important implications for animal welfare management; visitor effects on animal welfare are likely to occur, or intensify, during the morning or in earlier visits when visitor interest is greatest. This article discusses this issue and possible solutions to reduce visitor effects on animal well-being.     

An Hourly Variation in Zoo Visitor Interest: Measurement and Significance for Animal Welfare Research

A methodological difficulty facing welfare research on nonhuman animals in the zoo is the large number of uncontrolled variables due to variation within and between study sites. Zoo visitors act as uncontrolled variables, with number, density, size, and behavior constantly changing. This is worrisome because previous research linked visitor variables to animal behavioral changes indicative of stress. There are implications for research design: Studies not accounting for visitors' effect on animal welfare risk confounding (visitor) variables distorting their findings. Zoos need methods to measure and minimize effects of visitor behavior and to ensure that there are no hidden variables in research models. This article identifies a previously unreported variable—hourly variation (decrease) in visitor interest—that may impinge on animal welfare and validates a methodology for measuring it. That visitor interest wanes across the course of the day has important implications for animal welfare management; visitor effects on animal welfare are likely to occur, or intensify, during the morning or in earlier visits when visitor interest is greatest. This article discusses this issue and possible solutions to reduce visitor effects on animal well-being.     

A Case for a Naturalistic Perspective: Response to Lawrence and Bekoff

ABSTRACT

We evaluated three forms of primate free-ranging displays at Singapore Zoo, each with varying restrictions on ranging area and freedom for the primates, as well as visitor proximity. The cotton-top tamarin (Saguinus oedipus), the white-faced saki (Pithecia pithecia), and the orangutan (Pongo pygmaeus) displays illustrated differences in primate visibility to visitors, visitor–primate proximity, frequency of visitor–primate interactions, visitor crowd size, and responses. Amongst the three free-ranging displays, the cotton-top tamarins offered the highest visibility, closest proximity between visitors and primates, highest interaction levels, and attracted the largest crowds. However, undesirable interactions occurred most between the cotton-top tamarins and visitors. We found consistently positive visitor perceptions (total n = 464) of all three primate displays in terms of visitor enjoyment (> 95%); naturalistic zoo experience (> 95%); learning experience (> 90%); and the promotion of good welfare (> 90%). Increasingly naturalistic displays of animals in zoos through the free-ranging of animals can have considerable benefits for both zoo visitors as well as animals, and is a display concept that deserves implementation on a wider scale. Design and implementation of such displays should, however, achieve a balance to maximise display value and animal welfare while curtailing the effects of undesirable human–primate interactions through the restriction of visitor–primate proximity.     

Visitor effects on a zoo population of California sea lions (Zalophus californianus) and harbor seals (Phoca vitulina)

The effects of visitor presence on zoo and aquarium animals have become increasingly well studied, using measures such as behavioral responses and exhibit usage. Many taxa remain underrepresented in this literature; this is the case for marine mammals, despite widespread public concern for their welfare in managed care settings. The current study therefore used behavioral activity budgets and exhibit usage to assess the responses of California sea lions (Zalophus californianus) and harbor seals (Phoca vitulina) to visitors at the Seal Cove exhibit at Six Flags Discovery Kingdom, Vallejo CA. Data was collected via focal follow video recordings over the summer season of 2016, and analyzed using MANCOVAs, discriminant analyses, and modified Spread of Participation Indices. The sea lions showed no significant changes in behavior when visitors were present, but did show greater preference for the water bordering visitor viewing areas during these times. Two sea lions gave birth during the study period, and showed greater preference for land areas both adjacent to and out of sight of visitors when nursing compared to while pregnant. In contrast, the harbor seals showed significant behavioral changes in the presence of visitors, including increased vigilance and feeding. This was associated with increased preferential use of water areas adjacent to the visitor viewing area. Visitors were able to purchase fish to throw to the animals, which likely contributed to the differences observed. Overall, this study found little evidence for negative visitor impacts on two pinniped species in a zoo setting.     

Visitor reaction to pacing behavior: influence on the perception of animal care and interest in supporting zoological institutions

Many publications within the field of zoo animal welfare have stated the importance of decreasing stereotypic behavior (e.g., pacing) to help ensure a positive visitor experience. The idea behind these statements is that visitors want to see animals engaged in natural behavior. Additionally, it is thought that watching an animal exhibit species-appropriate behavior could help increase a visitor's connection to wildlife and ultimately their interest in conservation. However, until recently, no information was available to validate such statements. The purpose of this research was to examine people's reaction to viewing an animal engaged in pacing behavior. Participants were randomly selected to fill out a survey after watching a short video of either a tiger pacing or resting (control). Results indicate that having viewed a tiger pacing significantly decreases people's perception of the level of care animals receive at that facility. In addition, people's interest in supporting zoos decreased as a result of viewing this behavior. Results are discussed from an animal welfare, business, and conservation perspective.     

Activity budget and spatial distribution of Bennett's wallabies (Macropus rufogriseus) in open versus closed exhibit designs

Although many studies investigating the impacts of zoo exhibit designs on captive animals exist, none have been performed on how they influence the behavior and welfare of captive Bennett's wallabies (Macropus rufogriseus). Here, we assess the impact of exhibit design on the activity budget and spatial distribution of Bennett's wallabies. We compared animal behavior in two open exhibits (i.e. physical interaction between animals and visitors permitted) to two closed exhibits (i.e. physical interaction between animals and visitors prohibited). Behavioral data were collected using focal sampling, and spatial distribution was recorded on exhibit maps at regular time intervals. We found a significant increase in feeding and interactive behaviors in closed exhibits in comparison to open exhibits. However, other behaviors such as resting, locomotion, and vigilance did not vary with design. Functional use of space was similar between both designs; however, the effect of habituation may be relevant to consider in future studies. Although some support for visitor effects were present, our study provided no evidence for strong impacts of exhibit design on Bennett's wallaby welfare. Our study emphasizes the need for additional research into the impacts of how zoo environments affect Bennett's wallaby behavior and welfare.     

Siamangs (Hylobates syndactylus) and White-Cheeked Gibbons (Hylobates leucogenys) Show Few Behavioral Differences Related to Zoo Attendance

The effect of visitors on behavior and welfare of nonhuman animals in the zoo has been an active research topic during the last few decades. Although research has variously shown negative or positive impacts of zoo visitors on animals in captivity, previous primate research at Disney's Animal Kingdom® suggests the importance of visual barriers in allowing animals to cope with large crowds. Examining this further, this study monitored the behavior of white-cheeked gibbons (Hylobates leucogenys) and siamangs (Hylobates syndactylus) in large, open exhibits. Behavioral data showed rates of social behavior and percentage of time engaged in solitary behavior did not differ between low and high visitor-attendance days. Both gibbons and siamangs spent more time in areas away from the public on high attendance days. Supporting previous findings, results imply visual barriers and ability to retreat from crowds may have provided these animals with choice and minimized potential negative visitor impact. Future research should focus on the relationship between attendance and actual crowds at exhibits; it should utilize multi-institutional methodologies to control for variance and look for individual and demographic differences between individuals.     

Effect of felid activity on zoo visitor interest

The extent to which the presence of zoo visitors influences animal behavior, and the ways in which animal activity influences visitor interest and perception, are of great interest to zoological parks. Visitors have been variously characterized as being enriching for zoo animals, as being stressors, and generally as influencing behavior in measurable ways. Most studies have focused on primates, and have assumed a “visitor effect” paradigm (i.e., visitors influence animal behavior). Here we present findings from a study of a nonprimate group (felids), and examine the “visitor attraction” model, which assumes that visitors are attracted to active animals. We assessed visitor interest and number at seven cat exhibits at the Brookfield Zoo during the spring and summer of 2002. Data were collected during 1‐min scans of each exhibit at 10‐min intervals. The results indicate that visitor presence per se did not influence cat activity, and that visitor interest was generally greater when cats were active. Various species differences may be explained by visitor familiarity with the species, variations in exhibit design, and species‐specific activity budgets. We conclude that the visitor attraction model may be more appropriate for taxa, such as large cats, that tend naturally to be largely inactive and to respond little (if at all) to visitor disturbances or efforts to engage. The relationship must be viewed as bidirectional: visitors influence animal behavior, and animal behavior influences visitor interest. However, the strength and primary direction of this relationship is likely taxon‐specific. We suggest that a visitor attraction model may be more appropriate not only for felids, but for other taxa with similar behavioral patterns and responses as well. Zoo Biol 22:587–599, 2003. © 2003 Wiley‐Liss, Inc.     

Fecal corticoid metabolite measurement in the cheetah (Acinonyx jubatus)

This longitudinal study addresses the relationship of cortisol excretion to ovarian activity in captive female cheetahs. A radioimmunoassay was developed and validated to measure corticoid metabolite concentrations in feces. A restraint experiment was used to demonstrate that fecal cortisol is detectable following stressful episodes. In studies of 7 females, fecal cortisol output indicated that they could be placed into 3 different categories. Females of the high-in-cortisol category (∼200 ng/g feces, n = 2) were independently rated by caretakers as the most nervous individuals in the collection (n = 24). These females appeared to be compromised in their ovarian cycling, as indicated by fecal estrogen measurements. In contrast, reproducing females fell into the low and intermediate cortisol excretion categories. A non-cycling high-cortisol female had an episodic cycle following a period of relatively low (intermediate) cortisol levels, followed by resumption of acyclicity and high cortisol excretion. Stress and reproductive failure may, therefore, be associated in the female cheetah. The close proximity of conspecifics as a potential source of stress and, consequently, suppressed ovarian activity in some females is suggested by these results. Zoo Biol 16:133–147. 1997 © 1997 Wiley-Liss, Inc.     

Relationships between exhibit naturalism,animal visibility and visitor interest in a Chinese Zoo

Efforts to meet the welfare needs of captive animals (such as the provision of environmental enrichment and naturalistic furnishings) often compromise visitors’ needs (naturalistic exhibits often decrease the visibility of animals on display even though visitors pay to view them). The literature offers different predictions about how zoo visitors respond to decreased animal visibility in naturalistic exhibits but they require further evaluation. Further, visitor research is currently confined to Europe and America and studies outside these areas are limited. This paper investigates the relationships between exhibit naturalism, animal visibility and visitor interest in a Chinese Zoo. Visitor interest was observed at both naturalistic and barren exhibit designs. The study showed that the influence of animal presence on visitor behaviours was similar at both exhibit designs. Further, visitor interest was not compromised at the naturalistic exhibit when animals were not visible. The results demonstrate that the needs of animals and visitors can be balanced at naturalistic exhibits and support the transformation of exhibits to those representing naturalistic environments.     

Relationship between behavior, adrenal activity, and environment in zoo-housed western lowland gorillas (Gorilla gorilla gorilla)

Monitoring adrenal activity through noninvasive fecal hormone sampling is rapidly gaining popularity as a tool to assess zoo animal welfare. However, few studies have sought to investigate the interrelationships between behavior, adrenal activity, and environment, and ask whether both behavioral and adrenal monitoring strategies are required to assess welfare sufficiently. We present the findings of a 9-month study of a small group (one male, two females) of Western lowland gorillas, Gorilla gorilla gorilla. First, we examined the effect of environmental variables on gorilla behavior. Second, we examined the effect of environmental variables on the concentration of fecal glucocorticoid metabolites (FGC) and the relationship between behavior and FGC. Environmental variables had similar effects on all three gorillas. Negative vigilance of visitors (NVV; staring, posturing, and charging at visitors) significantly increased in all subjects as environmental noise levels increased, and food-related behavior significantly decreased in all subjects as crowd size increased. Exhibit modifications had a number of positive effects on behavior. Notably, when privacy screens were used, NVV significantly decreased in two subjects. We found no significant effects of environmental variables on FGC. However, we did find significant relationships between behavior and FGC in one female. Specifically, her NVV was significantly higher one day before, and on the same day as, raised FGC. Also, hair plucking significantly increased in the two days following raised FGC. Overall, this study demonstrates how concurrent noninvasive fecal and behavioral monitoring can be used for gorilla welfare assessment.     

游客密度对动物园中黇鹿行为的影响

2006年9月20日-10月10日,以江苏省扬州市茱萸湾公园半散放鲇鹿为研究对象,采用目标动物取样法和全事件记录法,研究了不同游客密度条件下黇鹿日行为时间分配.并探讨了游客密度对鲇鹿日活动的影响.结果表明:在游客高峰期与低峰期,雄性取食、观望行为,雌性观望以及幼鹿取食、观望和修饰行为之间均存在显著差异(P＜0.05).在游客低峰期,雄性与雌性取食、反刍、卧息行为,雄性与幼鹿观望、其它行为,雌性与幼鹿取食、卧息、观望均存在极显著差异(P＜0.01);在游客高峰期,雄性与雌性取食、卧息,雌性与幼鹿取食、卧息、观望及移动行为均差异极显著(P＜0.01),雄性和幼鹿观望行为差异显著(P＜0.05).不同游客密度条件下游客活动对鲇鹿的取食、观望具有显著影响,当游客密度达到6人·min-1以上时,雄性观望行为显著增加,当达到16人·min-1以上时,雄性取食行为差异极显著(P＜0.01),此时雌性和幼鹿观望行为差异亦达到极显著水平(P＜0·01).因此,在旅游管理中,应将游客密度限制在16人·min-1以下,以减少对鲇鹿日活动影响.     

The Effect of Fission–Fusion Zoo Housing on Hormonal and Behavioral Indicators of Stress in Bornean Orangutans (Pongo pygmaeus)

The welfare of captive animals could be improved if zoos were to place more emphasis on their species-specific needs. In the wild, orangutans live in a fission–fusion social system and have a semisolitary lifestyle. However, most zoos keep orangutans in permanent groups, which may be stressful for them. Apenheul Primate Park in Apeldoorn, Netherlands, houses 14 Bornean orangutans in a simulated fission–fusion social system. To assess how this housing system affects indicators of stress, we measured fecal glucocorticoid metabolites (fGCM) and determined proportions of self-directed behavior (scratching and autogrooming). We compared fGCM concentrations of the Apenheul animals to those of zoo orangutans kept in permanent groups. In addition, we tested the effect of group size, visitor number, sex, age, and change of group composition on fGCM concentrations and proportions of self-directed behavior in the Apenheul orangutans. In contrast to Bornean orangutans housed in permanent groups, we did not find a group size effect on fGCM or on self-directed behavior in Apenheul’s fission–fusion housing system. In addition, fGCM concentrations in Apenheul orangutans increased significantly with visitor numbers. Visitor number also affected proportions of self-directed behavior, and mean proportions of scratching were positively correlated with mean values of fGCM concentrations. Although these results suggest that the fission–fusion housing system in Apenheul reduces the group size effect leading to social stress in Bornean orangutans, they also show that visitors are an important factor that needs to be mitigated if the well-being of captive primates and other zoo animals is to be improved.     

Zoo‐housed mammals do not avoid giving birth on weekends

There is evidence that zoo visitor presence can influence the behaviour and, in some cases, adrenal response of zoo animals, and can sometimes compromise animal welfare. In some laboratory studies, significantly more primate births have been reported on weekends, when fewer people are working there, compared with weekdays when staffing levels are at their highest. Here, we investigate whether there is evidence of a “weekend effect” on births in zoo animals as a result of visitor numbers. Unlike laboratories, zoos are typically busier with visitors on weekends than on weekdays, although staffing levels remain fairly consistent across days of the week. If zoo animal parturition is sensitive to human presence, then fewer births would be expected on weekends compared with weekdays. We tested this using birth data and visitor numbers on the entrance gate from zoo records across 16 species representing artiodactyls, perissodactyls, carnivores and primates at four British zoos, to see whether there is an association between mean daily birth rates and average visitor numbers. We predict that, if there is a visitor effect, daily births should be lower on weekends than weekdays and should correlate with mean daily visitor numbers. Results showed that births for all 16 species were randomly distributed through the week, and there was no significant decline in births on weekends. We conclude that the “weekend effect”, if such a thing exists, does not appear to be a feature of zoo births, suggesting that elevated weekend visitor numbers are not sufficiently stressful to trigger delayed parturition.     

Seasonal changes in ovarian steroid hormone concentrations in the large hairy armadillo (Chaetophractus villosus) and the crying armadillo (Chaetophractus vellerosus)

Knowledge of armadillo reproductive physiology is essential for developing ex situ and in situ assisted reproductive techniques for propagating and/or controlling populations of these animals. The present study included assessment of fecal sex steroids by radioimmunoassay, determining reproductive status via monitoring ovarian activity (in the wild) and therefore reproductive status, in wild females of the large hairy armadillo (Chaetophractus villosus) and the crying armadillo (Chaetophractus vellerosus) in the southern hemisphere. Plasma and fresh fecal progesterone concentrations were not significantly correlated in either species. However, in both species, there was a significant positive correlation between plasma progesterone and dry fecal progesterone concentrations (r = 0.82, P < 0.05 and r = 0.60, P < 0.05, respectively). Dry fecal progesterone and estradiol concentrations were measured in one captive C. villosus (average baseline progesterone and estradiol concentrations 28.72 ± 11.75 ng/g dry feces and 3.04 ± 0.80 ng/g dry feces, respectively) and one captive C. vellerosus (average baseline progesterone and estradiol concentrations 14.05 ± 3.03 ng/g dry feces and 3.46 ± 1.20 ng/g dry feces, respectively) to detect hormonal peaks over 1 y; these occurred from late fall to early summer. Feces from wild C. villosus and C. vellerosus were also collected over 1 y to determine progesterone peaks, which occurred in winter and spring in both species (with no peaks during the summer or fall). Accordingly, C. villosus and C. vellerosus had a seasonal reproductive pattern. The significant correlations between dry fecal and plasma progesterone concentrations validated this method for monitoring reproductive status in these species.     

Preliminary analysis of reproductive,behavioral and physiological characteristics of military working dogs

The use of dogs in military work environments has always aroused great interest in the general population and determining the stress levels they go through is extremely important to maintain their welfare. The aim of this research was to evaluate if the work shifts in military working dogs leads to stress conditions and if this working influences on the reproductive performance and life quality. The study was conducted at the Military Police Kennel located at Campinas, Sao Paulo, Brazil. Eight male dogs of four different breeds (German Shepherd, Belgian Malinois Shepherd, Doberman, and Rottweiler) were evaluated during two different shifts: Working Shifts: animals working 12 hours a day with 2 hour-interval; and Control Shifts: animals that were on their day off (36 hours). Saliva samples were collected for cortisol analysis at the control and working shifts. The study was carried out over 60 days and analyzed behavior, physiology, and reproduction quality. Saliva samples, behavior observation of stereotyping, resting and moving activities and semen analysis were collected by digital stimulation (for combined second and third fractions). The salivary cortisol levels during the control and working shifts were between 0.361–0.438 and 0.312–0.592 µg/dL, respectively; the highest values were found at the end of working shifts. The animals were resting during most of the observation period, but few showed stereotypic behaviors. The testicular consistency was firm and semen parameters were within the normal values in German Shepherd, Belgian Malinois Shepherd, and Doberman dogs. However, Rottweiler dogs had a higher rate of sperm abnormalities, higher salivary cortisol levels, and more stereotypic behaviors. Nevertheless this work highlights the importance of further research relating reproduction and cortisol levels in military dogs.     

Lion,Ungulate, and Visitor Reactions to Playbacks of Lion Roars at Zoo Atlanta

Felids in captivity are often inactive and elusive in zoos, leading to a frustrating visitor experience. Eight roars were recorded from an adult male lion and played back over speakers as auditory enrichment to benefit the lions while simultaneously enhancing the zoo visitor experience. In addition, ungulates in an adjacent exhibit were observed to ensure that the novel location and increased frequency of roars did not lead to a stress or fear response. The male lion in this study roared more in the playback phase than in the baseline phases while not increasing any behaviors that would indicate compromised welfare. In addition, zoo visitors remained at the lion exhibit longer during playback. The nearby ungulates never exhibited any reactions stronger than orienting to playbacks, identical to their reactions to live roars. Therefore, naturalistic playbacks of lion roars are a potential form of auditory enrichment that leads to more instances of live lion roars and enhances the visitor experience without increasing the stress levels of nearby ungulates or the lion themselves, who might interpret the roar as that of an intruder.