Factors affecting the behavior of captive white rhinoceros (Ceratotherium simum) and the accuracy of ad-hoc keeper data.

Although white rhinoceros (Ceratotherium simum) are common in captivity, few behavioral studies have been conducted and there is seemingly no research for immersive exhibits where potential for visitor effects is high. Moreover, little information exists on possible effects of weather and temperature on rhino outside their native range. Here we analyze 14,501 observations of rhino in a drive-through enclosure. Data were collected by researchers (n = 12,160 datapoints) and keepers (n = 2341 datapoints) over a 4-month period. We aimed to: (1) quantify behavior using detailed researcher-collected data and contemporaneous but ad hoc keeper-collected data; (2) compare datasets statistically; (3) establish effects of visitors, temperature, and weather on behavior; and (4) assess the influence of visitors on similarity of researcher/keeper datasets. Activity budgets were similar to the wild and the single previous study from a traditional (nondrive-through) enclosure. There was some discrepancy in activity budgets between researcher and keeper data due to significant differences in recorded frequency of two rare behaviors (horn rub; social interaction) and two behaviors that could be easily confused (grazing vs. standing with head-down): recording of other behaviors matched well. Weather and temperature affected behavior, with rhino becoming more sedentary (-locomotion, grazing; +resting, standing, and sedentary eating of hay) on hot/sunny days compared to cool/wet days. The number of visitor vehicles had a fairly negligible effect but resting was lower on busy days, possibly as vigilance increased. The match between researcher/keeper datasets was lowest when visitor numbers were high, suggesting visitors might affect keeper ability to accurately record behavior.

Do zoo-housed primates retreat from crowds? A simple study of five primate species.

An animal's welfare state is directly influenced by the mental state, which is shaped by experiences within the environment throughout the animal's life. For zoo-housed animals, visitors to the zoo are a large part of that environment and a fluctuating influence within it. This study examines the impact of zoo visitors on the space use of five species of zoo-housed primates (Eastern black-and-white colobus monkeys, Colobus guereza, n = 5, Allen's swamp monkeys, Allenopithecus nigroviridis, n = 2, DeBrazza's monkeys, Cercopithecus neglectus, n = 3, Bolivian gray titi monkeys, Callicebus donacophilus, n = 3, and crowned lemurs, Eulemur coronatus, n = 3). Specifically, we considered whether primates' distance from visitor areas changed as crowd sizes increased. Data were collected using the ZooMonitor app. Observers recorded spatial coordinates for each animal over periods ranging from 12 to 32 months. Data were analyzed using two types of regression models (linear and logistic) to examine the influence of visitors on the location of the primates. Both analyses revealed a statistically significant but small decrease in primate distance from visitor viewing glass as the number of visitors increased. Behavioral indicators of welfare were also unaffected by the presence of visitors. These results suggest that, with additional validation, distance from visitors may be one promising, simple way to evaluate the influence of visitors on primate welfare.

The effects of Zoo Lights on animal welfare: A case study of great Indian hornbills at Denver Zoo.

Popular evening events, such as Zoo Lights, increase the exposure of animals in managed care to stressors such as artificial light and noise, which may alter their behavior and negatively affect animal well-being. The pair of great Indian hornbills (Buceros bicornis) at Denver Zoo provided an opportunity to study the impacts of these stressors because their exhibit was open every evening during Zoo Lights 2017. We expected the hornbills to display increased aggressive behaviors during Zoo Lights due to more exposure to stressors compared to the periods before and after the holiday event. Alternatively, if behavioral changes were associated with hornbills' breeding season which runs from December-March, we expected the hornbills to engage in more affiliative behaviors, and to increase conspecific and nest proximity, during and after Zoo Lights compared to before it due to the onset and progression of the breeding season. The hornbills did not engage in significantly more aggressive behavior during Zoo Lights than before or after it. By contrast, the hornbills engaged in significantly more affiliative behaviors and increased conspecific proximity during and after Zoo Lights compared to before the event. These results are consistent with the timing of the hornbills' breeding season and not with the increased exposure to stressors during Zoo Lights. This case study provides an early step in assessing the impact of Zoo Lights on animals whose exhibits are part of these holiday events. Studies like this will help inform best practices for Zoo Lights events such that they are positive experiences for the zoo, visitors, and animals.

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.

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.

The effects of zoo visitors on Quokka (Setonix brachyurus) avoidance behavior in a walk-through exhibit.

The behavior of zoo animals may be influenced by visitors, with possible implications on animal welfare. We examined the effects of the presence of visitors on the presence and visibility of free-ranging quokkas (Setonix brachyurus) in preferred areas of a walk-through enclosure at Melbourne Zoo, Australia. In a controlled experiment, two visitor treatments were randomly imposed: (1) enclosure open to visitors as normal ("Open") and (2) enclosure closed to visitors ("Closed"). Treatments were imposed for 2-day periods, with five replicates of each treatment (10 2-day periods in total). Instantaneous point sampling of camera footage at 1-min intervals from 09:00 to 16:00 hr each day recorded the location and visibility of quokkas. Data were analyzed using a two-factor ANOVA (visitor treatment and study area), with 2-day summary values as the unit of analysis. While the presence of quokkas in the study areas was not affected by treatment, fewer (p < 0.05) quokkas were visible from the visitor paths and more (p < 0.05) quokkas were obscured from the visitor paths in the "Open" treatment than the "Closed" treatment. Number of quokkas differed between study areas across treatments (p < 0.01), but there was no interaction (p > 0.05) between visitor treatment and study area. The reduction in quokka visibility when visitors were present indicates that visitors were at least moderately fear provoking for the quokkas in this experiment, but further research is required to examine the effects of visitor presence and behaviors on the behavior and stress physiology of quokkas in walk-through enclosures, as there may be possible welfare implications.

The effects of environmental and visitor variables on the behavior of free-ranging ring-tailed lemurs (Lemur catta) in captivity.

The effect of the zoo environment on captive animals is an increasingly studied area of zoo research, with visitor effects and exhibit design recognized as two of the factors that can contribute to animal welfare in captivity. It is known that in some situations, visitors may be stressful to zoo-housed primates, and this may be compounded by environmental factors such as the weather, the time of day, and zoo husbandry routines. Exhibit design and proximity of the public are also known to influence behavioral response of primates to visitors; however, there is minimal research on free-ranging zoo animals, even though they are potentially subjected to intense interactions with visitors. The current study explores the effect of the zoo environment, several visitor variables and specific animal-visitor interactions on the behavior of free-ranging ring-tailed lemurs (Lemur catta) at Fota Wildlife Park, Ireland. Data were obtained through scan samples collected over 18 months (n = 12,263) and analyzed using a range of statistical tests, including general estimating equations (GEE). Results demonstrate that the free-ranging lemurs' behavior at Fota Wildlife Park is affected by season, weather and time of day. Similarities in feeding behavior exist between the free-ranging group and lemurs in the wild when resources are plentiful. Visitor variables had a limited effect on lemur behavior and behavioral diversity level. Lemurs rarely reacted to visitors when specific interactions were considered. Generally, the results indicate that the ring-tailed lemurs in this study have adapted well to the zoo environment and habituated to visitors.

Effects of visitor numbers on captive European red squirrels (Sciurus vulgaris) and impacts on visitor experience.

Visitors to zoological collections can have substantial effects on captive animals that vary according to species, enclosure design, visitor proximity, and husbandry methods. One particularly intense form of visitor interaction occurs in immersive exhibits such as walk-through enclosures. Such enclosures are increasingly common but effects on animal behavior are currently understudied. Here, the behavior of captive European red squirrels (Sciurus vulgaris) is studied in relation to visitor numbers in a walk-through enclosure. We also quantify the correlation between squirrel encounters and visitor experience. Interaction with humans increased significantly as the number of visitors inside the enclosure increased. The number of children present significantly increased locomotion and decreased eating, possibly due to disturbance and squirrels moving away from busy areas. By contrast, the number of adults significantly increased eating and decreased inactivity due to squirrels approaching visitors. The positive reinforcement training used by the keepers (offering food rewards to the squirrels for coming to them to allow routine medical checks) meant that squirrels associated adults with food opportunities. Squirrel encounter rate (number of squirrels seen by each group of visitors) was significantly affected by the number of adults and visitor duration (positive relationships) and noise as perceived by visitors (negative relationship). Encounter rate was positively correlated with overall visitor experience. Our results indicate that visitors affect behavior but this effect is influenced by husbandry methods. It is vital that visitors, especially children, minimize noise, and move slowly in the enclosure, both for the sake of the animals and their own experience.

Impacts of visitor number on Kangaroos housed in free-range exhibits.

Free range exhibits are becoming increasingly popular in zoos as a means to enhance interaction between visitors and animals. However very little research exists on the impacts of visitors on animal behaviour and stress in free range exhibits. We investigated the effects of visitor number on the behaviour and stress physiology of Kangaroo Island (KI) Kangaroos, Macropus fuliginosus fuliginosus, and Red Kangaroos, Macropus rufus, housed in two free range exhibits in Australian zoos. Behavioural observations were conducted on individual kangaroos at each site using instantaneous scan sampling to record activity (e.g., vigilance, foraging, resting) and distance from the visitor pathway. Individually identifiable faecal samples were collected at the end of each study day and analysed for faecal glucocorticoid metabolite (FGM) concentration. When visitor number increased, both KI Kangaroos and Red Kangaroos increased the time spent engaged in visitor-directed vigilance and KI Kangaroos also increased the time spent engaged in locomotion and decreased the time spent resting. There was no effect of visitor number on the distance kangaroos positioned themselves from the visitor pathway or FGM concentration in either species. While there are limitations in interpreting these results in terms of fear of visitors, there was no evidence of adverse effects animal welfare in these study groups based on avoidance behaviour or stress physiology under the range of visitor numbers that we studied.

Behavioral Assessment of Six Reptile Species during a Temporary Zoo Closure and Reopening.

Although reptiles are commonly housed in zoos and aquariums, their welfare is understudied for the diversity of species housed and the taxon's current captive population size. The sensory abilities of reptiles have adapted to the varied ecological niches they inhabit, and these evolutionary adaptations impact how reptiles perceive the stimuli around them-including zoo visitors. This study aimed to assess visitor effects on small groups of six reptile species during a temporary zoo closure due to COVID-19 by measuring behavioral diversity, use of space (measured by a spread of participation index), and select behaviors. The species assessed showed diverse responses. The Catalina Island rattlesnakes (Crotalus catalinensis) demonstrated increased investigation and behavioral diversity after the zoo reopened compared to when the zoo was closed, but the European glass lizards (Pseudopus apodus) showed decreases in the amount of time spent exposed to the observers' view and in their evenness of space use after the zoo was reopened to visitors. The other species, including beaded lizards (Heloderma horridum), Sonoran spiny-tailed iguana (Ctenosaura macrolopha), Arrau turtles (Podocnemis expansa), and dwarf caimans (Paleosuchus palpebrosus), had intermediate changes in their responses to visitor presence.

Behavioral Implications of the Complete Absence of Guests on a Zoo-Housed Gorilla Troop.

Research conducted on the effects that zoo visitors have on primate behavior has yielded inconsistent patterns. This study aims to contribute to the growing body of literature regarding visitor effects on zoo-housed primate's activity budgets, with the purpose of quantifying the behavioral variability under two conditions: guest presence and guest absence. Due to the COVID-19 pandemic, many zoos were closed to the public for varying lengths of time. The Buffalo Zoo was closed to guests for an 18-week period including the summer of 2020, which allowed us to effectively control for zoo guest presence. This case report compares data on the zoo's gorilla troop from the same time period in 2019. We found inconsistent results, similar to prior studies conducted with zoo-housed gorilla troops. Most gorillas were observed foraging less and exhibiting more inactivity in 2020, whereas the adult male silverback showed the opposite pattern. Abnormal or undesirable behaviors were performed less frequently when guests were absent however, these differences were not significant. We encourage others to compare behavior patterns during the pandemic shutdown to add to our knowledge base of visitor effects. We suggest that researchers do not try and generalize their individual and troop results to the entire population of gorillas in managed care, as both intrinsic and extrinsic factors contribute to individual differences in behavioral response.

The Effect of Behind-The-Scenes Encounters and Interactive Presentations on the Welfare of Captive Servals (Leptailurus serval).

The serval (Leptailurus serval) is a small African felid that is well represented in zoos and often serves as an animal ambassador in encounter programs with zoo visitors. The impact on serval welfare in relation to such programs has not been investigated to date, and the aim of this study was to assess short-term welfare effects of varying levels of visitor interaction in two captive servals. Weekly blocks of four different treatments were imposed three times on each animal over 12 weeks, and the treatments involved (1) Presentations (serval undertaking a routine training session in a designated presentation space, typically attracting high visitor numbers), (2) Behind-the-scenes (BTS, a close encounter allowing a small group of visitors to interact closely with the cat in its enclosure), (3) Presentations and BTS combined, and (4) No visitor interaction. Serval activity budgets as well as behavioural diversity were created from behaviours observed from Close Circuit Television (CCTV) footage during four daily recording sessions per animal over three consecutive days per treatment, using instantaneous scan sampling every 60 s. Individual faecal samples were collected daily to monitor changes in faecal glucocorticoid metabolite (FGM) concentration. Results indicate that the mean number of scans with stereotypic pacing was significantly reduced (p = 0.01) during Treatments 1 and 3, when cats participated in presentations only, or the two activities combined. Conversely, a significant reduction in behavioural diversity (p < 0.001) was observed when cats participated in Treatment 3, i.e., cats expressed fewer behaviours when interaction with visitors was more frequent. FGM concentrations did not vary significantly with treatment (p > 0.05). Given the reduction in stereotypic pacing, these findings suggest that involvement in an encounter program appears to exert an overall positive short-term welfare effect on the individual servals in this study. Although a reduction in behavioural diversity was not considered a negative welfare effect in the short term, potential long-term negative welfare effects resulting from a more frequent encounter program could not be ruled out in the present study.

The Visitor Effect on Zoo Animals: Implications and Opportunities for Zoo Animal Welfare.

Achieving and maintaining high standards of animal welfare is critical to the success of a modern zoo. Research has shown that an animal's welfare is highly dependent on how various individual animal factors (e.g., species traits, genetics, temperament and previous experience) interact with environmental features (e.g., social grouping, enclosure design and sensory environment). One prominent feature of the zoo environment is the presence of visitors. Visitor contact can be unpredictable and intense, particularly in terms of auditory and visual interaction. Depending on an animal's perception of this interaction, visitors can have either negative, neutral or positive impacts on zoo animal behaviour and welfare. This paper reviews the literature on the implications and potential opportunities of human-zoo animal interactions on animal behaviour and welfare, with the aim of stimulating interest, understanding and exploration of this important subject. The literature to date presents a mixed range of findings on the topic. It is possible this variation in the responses of zoo animals to visitors may be due to species-specific differences, the nature and intensity of the visitor interactions, enclosure design, and individual animal characteristics. Analysing these studies and better understanding animal preferences and motivations can provide insight into what animals find negatively and positively reinforcing in terms of visitor contact in a specific zoo setting. This understanding can then be applied to either safeguard welfare in cases where visitors can have a negative impact, or, conversely, it can be applied to highlight opportunities to encourage animal-visitor interaction in situations where animals experience positive emotions associated with visitor interaction.

The Social Rank of Zoo-Housed Japanese Macaques is a Predictor of Visitor-Directed Aggression.

The effect that visitors have on the behavior and welfare of animals is a widely-studied topic in zoo animal welfare. Typically, these studies focus on how the presence or activity levels of visitors affect animals. However, for many species, and particularly primates, social factors, such as social rank, can also have a large impact on behavior. Here, we considered the influence of both the role of visitors (crowd size and activity levels) and rank on the occurrence of visitor-directed aggression by zoo-housed Japanese macaques (Macaca fuscata, N = 12). We conducted 52 weeks of observation (443.8 hours) of macaques living in a large outdoor habitat and recorded 1574 events of visitor-directed behavior, 94.2% of which was characterized as aggressive. We calculated rank using the Elo-rating method. GLMM comparisons indicate that rank was a significant predictor of visitor-directed aggression, with lower-ranked individuals displaying more frequent aggression towards visitors. Additionally, visitor-directed aggression differed by crowd activity levels, but not crowd size. These results support our prediction that rank is associated with differences in visitor-directed aggression, and we interpret this pattern as lower-ranking macaques redirecting aggression toward zoo visitors as safe targets. This work emphasizes how factors emanating from the zoo environment can combine with social dynamics to influence primate response to human presence in the zoo setting.

Zoo Playgrounds: A Source of Enrichment or Stress for a Group of Nearby Cockatoos? A Case Study.

There is increasing evidence that in some circumstances, zoo visitors may be aversive stimuli to nonhuman animals housed in zoos. Yet, most previous research has focused on primates with little attention given to numerous other species who are housed in zoos. The focus animal of this project was the cockatoo, a species who has received minimal attention in zoo-based research. Furthermore, although the influence of the zoo setting has become increasingly important in visitor effect studies, this is the 1st study to quantify the effect of activity at a children's playground on zoo animals. There was an investigation on the effect of a zoo playground on the behavior of citron-crested and Moluccan cockatoos (Cacatua sulphurea citrinocristata and Cacatua moluccensis), as well as the effect of children standing in front of the birds' aviaries. The results showed that in some circumstances, the Moluccan cockatoos retreated from visitors, while the citron-crested cockatoos did not retreat from visitors and became more social in the presence of visitors. These findings highlight the importance of careful selection of species and individual animals to be housed near zoo playgrounds.