Environmental influences on stereotypy and the activity budget of Indian leopards (Panthera pardus) in four zoos in Southern India

To eliminate abnormal behaviors in leopards (Panthera pardus), such as stereotypic pacing, by utilizing environmental enrichment techniques, a proper understanding of their behavior in captive environments is required. Hence there is a need for animal welfare studies in Indian zoos. The activity budgets of 16 leopards were recorded across four southern Indian zoos: Thiruvananthapuram Zoo, Arignar Anna Zoological Park, Shri Chamarajendra Zoological Gardens, and the Guindy Children's Park. Of the 16 study animals, 14 were studied on‐exhibit on zoo holidays as well as on days with visitors present, and all 16 individuals were studied off‐exhibit on other days with visitors present. The 11 behaviors recorded were categorized into active, resting, and stereotypic behaviors. Leopards exhibited higher levels of activity in the on‐exhibit enclosures on days with no visitors. Feeding time influenced the behavioral repertoire of all 14 leopards studied on‐exhibit. Lower proportions of resting were exhibited during the hours before feeding. The proportion of active behaviors differed significantly across zoos. Stereotypic pacing levels were not influenced by the presence of visitors or by feeding time, but was significantly influenced by enclosure features. Higher levels of stereotypic pacing were exhibited in off‐exhibit than on‐exhibit enclosures. Our study shows that the behavior of captive leopards is influenced by enclosure type, feeding regime, and the presence of visitors. Zoo Biol 21:585–595, 2002. © 2002 Wiley‐Liss, Inc.     

Feeding enrichment and stereotypic behavior in spectacled bears

The effect of feeding enrichment on the behavior of three spectacled bears (Tremarctos ornatus) was investigated in a large, complex zoo exhibit. Feeding enrichment significantly extended the time bears spent foraging, but no delayed effect on other behaviors was found. The frequency of stereotypic behaviors performed by an old female and a young adult male was not influenced outside the morning feeding period. As yet, a young adult female has not developed stereotypic behaviors. In the old female, the frequency of stereotypic behavior was inversely correlated with the frequency of resting. In the male, the frequency of stereotypic behavior was inversely correlated with the frequency of social interactions with either female. Zoo Biol 18:363–371, 1999. © 1999 Wiley‐Liss, Inc.     

Tongue twisters: feeding enrichment to reduce oral stereotypy in giraffe

Stereotypic behavior has been well‐studied and documented in a variety of animals including primates, carnivores, and domesticated ungulates. However, very little information is known about stereotypic behavior of captive exotic ungulates. Giraffe have been found to perform a wide range of stereotypic behaviors. According to a survey of zoological institutions, oral stereotypies, specifically the licking of nonfood objects are the most prevalent stereotypic behaviors observed in giraffe. Their performance appears to be related to feeding and rumination and may be a result of the inability of a highly motivated feeding behavior pattern, tongue manipulation, to be successfully completed. To test this hypothesis, the indoor and outdoor feeders for three giraffe housed at Zoo Atlanta were modified to require the giraffe to perform more naturalistic and complex foraging behaviors. Data were collected using instantaneous scan sampling in both exhibit and holding areas. Our results showed that, for the giraffe that engaged in the highest rates of oral stereotypic behavior in the baseline, more complex feeders that required tongue use to access grain or alfalfa had the greatest effect on behavior. For the giraffe that performed low baseline rates of oral stereotypic behavior, adding slatted tops to the alfalfa feeders indoors virtually eliminated the behavior. Although some changes in ruminating and feeding behavior were observed, the decreases in stereotypic behavior were not associated with the changes in ruminating or feeding behavior. These results provide evidence for the hypothesis that oral stereotypy in herbivores can be reduced by encouraging giraffe to engage in more naturalistic foraging behavior. Zoo Biol 27:200–212, 2008. © 2008 Wiley‐Liss, Inc.     

Behavioral effects of environmental enrichment on harbor seals (Phoca vitulina concolor) and gray seals (Halichoerus grypus)

Zoos and aquariums have been incorporating environmental enrichment into their animal care programs for the past 30 years to increase mental stimulation and promote natural behaviors. However, most attempts to document the effects of enrichment on animal behavior have focused on terrestrial mammals. Staff at the National Aquarium in Baltimore conducted an investigation of the behavioral effects of enrichment on the seven harbor seals and two gray seals housed in the aquarium's outdoor seal exhibit. We expected that enrichment would change the amount of time the animals spent engaged in specific behaviors. The behaviors recorded were: resting in water, resting hauled out, maintenance, breeding display, breeding behavior, aggression, pattern swimming, random swimming, exploration, and out of sight. Activity levels (random swimming and exploration) were expected to increase, while stereotypic behaviors (pattern swimming) were expected to decrease. The frequency and duration of behaviors were documented for 90 hr in both the control phase (without enrichment) and the experimental phase (with enrichment). Statistically significant differences (P<0.05) in the time spent in pattern swimming, random swimming, exploration, and out of sight were observed between the two phases. With enrichment, pattern swimming and out of sight decreased, while random swimming and exploration behavior increased. These findings demonstrate that enrichment can promote behaviors (random swimming and exploration) that are likely to be normal for phocids in the wild, and that may contribute to the behavioral complexity of these seals in captivity. Zoo Biol 21:375–387, 2002. © 2002 Wiley‐Liss, Inc.     

To hunt or not to hunt? A feeding enrichment experiment with captive large felids

It is often difficult to promote the successful performance of feeding behaviors in zoos, especially for carnivores. Feeding enrichment provides these opportunities and often improves behavioral indications of an animal's well‐being and the experience of the zoo visitor. The effectiveness of two different feeding enrichment techniques was evaluated on five subjects in two species of felids: African lions and Sumatran tigers. The activity budgets of each cat were compared before, during, and after enrichment, focusing on activity levels, frequency and variety of feeding behaviors, and occurrence of stereotypic behaviors. The presentation of live fish increased the variety and frequency of feeding behaviors, while presentation of horse leg bones increased the frequency of these behaviors. Fish reduced the tigers' stereotypic behavior from 60% of scans to 30% of scans on the day of presentation, and this change was maintained for 2 days following enrichment. Bone presentation also reduced stereotypic behavior and increased nonstereotypic activity in both species. Both of these techniques appear to have sustained effects on behavior lasting at least 2 days after presentation, which may indicate their ability to alter the animals' underlying activity patterns. Zoo Biol 22:189–198, 2003. © 2003 Wiley‐Liss, Inc.     

A work‐for‐food enrichment program increases exploration and decreases stereotypies in four species of bears

Zoo‐housed bears are prone to exhibiting stereotypic behaviors, generally considered indicators of negative welfare. We explored the effects of a variable‐time feeding enrichment schedule on behavioral indicators of welfare in four bear species at Cleveland Metroparks Zoo. We distributed the diets of eight bears in one of five enrichment items, for two consecutive days each, and monitored behavior throughout the day. In Experiment 1, we compared variable‐time to fixed‐time presentation of enrichment over two, 10‐day periods. Overall, bears performed more exploratory behavior when enriched (p < 0.0001). Furthermore, variable‐time enrichment was associated with a greater increase in exploratory behavior than fixed‐time enrichment when compared to baseline (p < 0.001). Both fixed‐time (p_unadjusted <0.05, p_adjusted = 0.07) and variable‐schedule (p_unadjusted <0.05, p_adjusted = 0.09) enrichment were also associated with similar decreases in abnormal behavior compared to baseline. For Experiment 2, we tested habituation to enrichment over 30 days using multiple items and a semi‐variable presentation schedule. Again during the enrichment period, bears exhibited increased exploratory behavior (p < 0.0001) and decreased abnormal behaviors compared to baseline (p_unadjusted = 0.05, p_adjusted = 0.09). We observed no habituation during the 30‐day sustained enrichment period for these behaviors. Collectively, these results suggest that daily, variable‐schedule feeding enrichment, with intermittent presentation of unique enrichment items, increases behavioral indicators of positive welfare and decreases behavioral indicators of negative welfare.     

The effects of physical characteristics of the environment and feeding regime on the behavior of captive felids

The behavior of captive felids is influenced by enclosure design and management regime. The behavior of nine felid species housed in 11 enclosures was recorded using instantaneous scan sampling. Stereotypic pacing was observed in 15 out of 19 individuals. Size of enclosure did not affect pacing behavior, but edges of enclosures were found to be used specifically for pacing behavior. Cats in relatively larger enclosures had a higher level of apparent movement, but only about 50% of enclosure space was used. Raised areas such as tree branches were found to be preferred sites in enclosures, particularly for observation of surroundings. The feeding regime was found to affect stereotypic pacing levels. Cats fed on a 3 day cycle paced more on fast days than on days they were fed. Although not statistically significant, 6 out of 7 of these cats paced more in the hour after feeding, whereas the cats fed daily paced more in the hour before feeding. Further research is required to understand the relationship between feeding and stereotypic behavior. Zoo Biol 16:71–83, 1997. © 1997 Wiley-Liss, Inc.     

First experiences with free‐ranging giant day geckos (Phelsuma madagascariensis grandis,Gray 1870) in the masoala rainforest exhibit in Zurich Zoo,Switzerland

Sixty giant day geckos (Phelsuma madagascariensis grandis) have been introduced into the Masoala rainforest exhibit of Zurich Zoo. Eighteen geckos were monitored during a 3‐month study using the telemetry method. In general, the geckos were able to adapt well under these semi‐natural conditions of the exhibit. The geckos accessed to nearly all locations in the exhibit; some of the animals remained stationary, whereas others covered dozens of meters within a week. They preferred four species of plants as well as the artificial structures supporting the walls and roof of the exhibit, and displayed natural behaviors. Animals were observed feeding on all kind of arthropods and nectar substances, and also on food items dropped from feeding stations for other species. Deliberate feeding targeted at the geckos was finally reduced to a calcium‐rich squash along the visitor's main path. Reproduction was observed frequently within the exhibit. These findings suggest that the geckos will be able to build up a self‐sustaining population and contribute to a nearly‐authentic experience for zoo visitors. Zoo Biol 0:1–7, 2006. © 2006 Wiley‐Liss, Inc.     

Visitor Behaviors and Perceptions of Jaguar Activities

ABSTRACT

Zoo animals serve an important function in helping educate the public about their conservation needs. Despite this important function, little is understood about how visitors perceive different zoo exhibits and the animals that reside within them. In the present study, the behaviors displayed by two jaguars located at the Woodland Park Zoo were correlated with visitor behaviors and perceptions. Overall, visitors perceived their enjoyment to be lower when a jaguar was out of sight and rated the behavioral welfare of the jaguar to be lower when it was engaged in stereotypic behaviors. In addition, visitors who described a jaguar's behavior as stereotypic were significantly more likely to give lower ratings than those who perceived the jaguar to be active. It is suggested that by understanding how visitors perceive exhibited animals, zoos can address these perceptions in order to create more positive experiences for their visitors.     

Feeding live prey to zoo animals: response of zoo visitors in Switzerland

In summer 2007, with the help of a written questionnaire, the attitudes of more than 400 visitors to the zoological garden of Zurich, Switzerland, toward the idea of feeding live insects to lizards, live fish to otters, and live rabbits to tigers were investigated. The majority of Swiss zoo visitors agreed with the idea of feeding live prey (invertebrates and vertebrates) to zoo animals, both off‐ and on‐exhibit, except in the case of feeding live rabbits to tigers on‐exhibit. Women and frequent visitors of the zoo disagreed more often with the on‐exhibit feeding of live rabbits to tigers. Study participants with a higher level of education were more likely to agree with the idea of feeding live invertebrates and vertebrates to zoo animals off‐exhibit. In comparison to an earlier study undertaken in Scotland, zoo visitors in Switzerland were more often in favor of the live feeding of vertebrates. Feeding live prey can counter the loss of hunting skills of carnivores and improve the animals' well‐being. However, feeding enrichments have to strike a balance between optimal living conditions of animals and the quality of visitor experience. Our results show that such a balance can be found, especially when live feeding of mammals is carried out off‐exhibit. A good interpretation of food enrichment might help zoos to win more support for the issue, and for re‐introduction programs and conservation. Zoo Biol 29:344–350, 2010. © 2009 Wiley‐Liss, Inc.     

Technology at the Zoo: The Influence of a Touchscreen Computer on Orangutans and Zoo Visitors

A computer‐controlled touchscreen apparatus (hereafter referred to as “touchscreen”) in the orangutan exhibit at Zoo Atlanta provides enrichment to the animals and allows cognitive research to take place on exhibit. This study investigated the impact of the touchscreen on orangutan behavior and visibility, as well as its impact on zoo visitors. Despite previous research suggesting that providing a single computer system may negatively affect orangutan behavior, there was not a significant increase in aggression, stereotypic, or distress‐related behaviors following the activation of the on‐exhibit touchscreen. We also investigated the possibility that zoo visitors may be negatively affected by technology because it deviates from naturalism. However, we did not find a change in stay time or overall experience rating when the computer was turned on. This research was the first to assess visitor attitudes toward technology at the zoo, and we found that visitors report highly positive attitudes about technology for both animals and visitors. If subjects visited the exhibit when the computer was turned on, they more strongly agreed that orangutans benefit from interacting with computerized enrichment. This study is the first investigation of an on‐exhibit touchscreen in group‐housed apes; our findings of no negative effects on the animals or zoo visitors and positive attitudes toward technology suggest a significant value of this practice. Zoo Biol 31:27;–39, 2012. © 2011 Wiley Periodicals, Inc.     

Meta‐analytic review of the effects of enrichment on stereotypic behavior in zoo mammals

This meta‐analysis reports the effect enrichment has on the occurrence of stereotypic behavior exhibited by captive zoo mammals. The analysis also identifies which types of enrichment are most effective, which groups of animals benefit the most, and which types of stereotypes are most affected by environmental enrichment. The analysis included 54 studies that yielded 63 effect size statistics. Fifty‐seven of sixty‐three effect sizes went in the predicted direction (90%), with the animals participating in less stereotypic behavior during the enrichment condition than in the baseline condition. The mean effect size (correlation coefficient r) was 0.46. The combined P‐value using both fixed and random effects methods was reveled to be <0.0000001. A file drawer N‐value was calculated to identify the number of unretrieved studies (with a combined effect size of zero) that would be needed to nullify the results of this analysis. The file drawer N‐value was 1,726, suggesting that it is highly unlikely that the significant results reported in this analysis are nullified by studies that remain in file drawers. Based on these results it was concluded that enrichment substantially reduces the frequency of stereotypic behavior exhibited by mammals living in zoo environments. Zoo Biol 0:1–21, 2006. © 2006 Wiley‐Liss, Inc.     

Activity‐based exhibition of five mammalian species: Evaluation of behavioral changes

Activity‐based management of captive animals involves the training and movement of animals among several exhibits and holding areas. We studied the effectiveness of this system in producing variation in behavior, controlling stereotypies, and eliciting natural behaviors. Twelve animals representing five species of mammals (orangutans, siamangs, tapirs, babirusa, and Sumatran and Siberian tigers) were the subjects of focal observations measuring activity levels, stereotypies, natural behaviors, and space utilization. Statistical analysis was used to assess the association between variation in behavior and the movement among the four exhibits. For several animals, the persistence of behavioral changes was studied over a period of 3 years. We also examined the influence of the previous animal in the exhibit on the focal animal. Moving animals among the exhibits affected activity levels and/or space utilization in all animals in the activity‐based management system. In cases for which 3‐year data were available, there was evidence of habituation to the novelty of changing exhibits. Stereotypies, usually in the form of pacing, were affected by exhibits, providing the opportunity to manipulate these behavior patterns by exhibit placement. Natural behaviors in the form of urine‐spraying by the female tapir and the Sumatran tiger were affected by which animal had previously been in the exhibit. The results support the conclusion that exposure to varying exhibits produces variation in the behavior of the animals and elicits natural behaviors that would be unlikely to occur in a traditional single‐species exhibit. Activity‐based management provides unique opportunities for the behavioral enrichment of captive animals. Zoo Biol 22:269–285, 2003. © 2003 Wiley‐Liss, Inc.     

Improving the Welfare of a Zoo-Housed Male Drill (Mandrillus leucophaeus poensis) Aggressive Toward Visitors

Improving the welfare of nonhuman animals in captivity and maintaining behavioral competence for future conservation purposes is of the highest priority for zoos. The behavior of an aggressive male drill (Mandrillus leucophaeus poensis) was assessed in Barcelona Zoo. The 2-year study presented in this article examined the effects of introducing changes in the exhibit of the drill to improve his welfare by analyzing scan behaviors. First, a partial visual barrier was applied and proved to be insufficient to decrease the long-term stress indicators assessed. Next, a feeding enrichment program was implemented. The results supported the hypothesis that feeding and explorative activities would increase, whereas apathetic and stereotypic behaviors would decrease. However, visitor-directed aggression did not vary, indicating that more profound structural modifications were needed to reduce the negative impact of the agonistic interactions between the drill and the public. The study emphasized the usefulness of environmental enrichment evaluations in assessing captive animal welfare.     

Comparison of several types of enrichment for captive felids

Enrichment can increase the complexity of the captive environment and possibly enhance captive animals' well‐being by stimulating active behaviors and reducing stereotypical behaviors commonly seen in zoo felids. In this study, three different enrichment items were added to outdoor enclosures of felids at the Montgomery Zoo to test their effects on activity levels and stereotypic pacing. Bones, frozen fish, and spices (cinnamon, chili powder, and cumin) were presented over a 3‐month period to six species of felids: cheetah, cougar, jaguar, lion, ocelot, and tiger. Proportion of time spent engaging in active behaviors and stereotypic pacing were compared before, during, and after treatments. All treatments resulted in a significant increase in activity level from baseline (bones: +15.59%; frozen fish: +35.7%; spices: +12.38%). Effects of enrichment items on activity levels were not sustained 7 days after removal. Proportion of time spent pacing significantly decreased during presentation of spices (?21.25%) and frozen fish (?26.58%), but not with the addition of bones. However, only the effect of frozen fish on stereotypic behavior was sustained 7 days after removal of the enrichment item. In conclusion, bones, spices, and frozen fish are inexpensive and easy‐to‐administer enrichment items that may be used to increase active behaviors of captive felids. Zoo Biol 26:371–381, 2007. © 2007 Wiley‐Liss, Inc.     

Tailored Enrichment Strategies and Stereotypic Behavior in Captive Individually Housed Macaques (Macaca spp.)

The welfare of nonhuman animals in captivity is widely dependent on the natural psychological, physical, and behavioral needs of the animals and how adequately these needs are met. Inability to engage in natural behaviors can lead to chronic stress and expression of stereotypic behavior. The majority of research on decreasing stereotypic behavior in captivity addresses problems at the group level and does not account for individual variability in each animal's needs, history, and preferences. This study combined physiological and behavioral measures of well being to comprehensively assess the unique needs of individually housed captive macaques (Macaca spp.) with the aim of developing tailored welfare strategies. Behavioral and hormonal data were collected under 2 conditions: baseline and individualized enrichment. The results showed a significant decrease in stereotypic behavior under the enrichment condition. Additionally, 7 out of 9 individuals showed a decrease in fecal glucocorticoid (stress hormone) levels, indicating a reduction in hypothalamic-pituitary-adrenal activity. Addressing welfare on an individual, rather than group, level allows for a better overall characterization of well being and maximizes the probability of improving the welfare of each animal.     

Effect of housing and environmental enrichment on adrenocortical activity,behavior and reproductive cyclicity in the female tigrina (Leopardus tigrinus) and margay (Leopardus wiedii)

The objective of this study was to evaluate the effects of different captive housing conditions on reproductive cyclicity and adrenocortical activity in adult females of two small‐sized felid species, the tigrina (Leopardus tigrinus; n = 3) and margay (Leopardus wiedii; n = 2). Females were housed as singletons and subjected to three enclosure conditions over successive time periods: Phase I—large, enriched enclosures for 3 months; Phase II—small, empty enclosures for 5.5 months; Phase III—the same small enclosures enriched with branches and nest boxes for 6.5 months. Fecal samples were collected five times weekly throughout the study for analysis of progestagen, estrogen, and corticoid metabolites. On the basis of observed behaviors, stereotypic pacing was more frequent before feeding for all cats, regardless of enclosure conditions. Both species displayed a bimodal activity pattern, with peaks occurring at nightfall and dawn. All animals exhibited agitated behavior, characterized by a high frequency and duration of stereotypic pacing, primarily during the first 3 days after moving to the small empty enclosures. On the basis of hormonal analyses, ovarian follicular activity decreased and corticoid concentrations increased in tigrinas after transfer to the small barren cages compared to the patterns observed in the initial large, enriched enclosures. Corticoid concentrations in tigrinas then declined after small cage enrichment. Margay females exhibited increased corticoid excretion during Phases II and III, but in contrast to tigrinas, concentrations remained high even after cage enrichment. It was further showed that enriching the small enclosures was insufficient to reestablish normal ovarian activity within the time frame of the study for both species. In summary, margay and tigrina females exhibited distinct elevations in corticoid concentrations after transfer from large enriched enclosures to smaller barren cages that corresponded with agitated behavior, especially immediately after transfer. Fecal corticoid concentrations were reduced after cage enrichment in tigrinas, but not in margays. Although only a few individuals were evaluated, data suggest there may be species differences in response to captive environmental conditions. Overall results emphasize the importance of enclosure dimensions and enrichment when designing species appropriate environments for improving the health and reproductive fitness of threatened species. Zool Biol 26:441–460, 2007. © 2007 Wiley‐Liss, Inc.     

Stereotypic behavior in wild marine carnivores?

Stereotypic behavior is observed in many species within zoological institutions. Attempts to reduce such behavior typically involve some form of environmental enrichment that provides opportunities for species appropriate behavior or some degree of control within the environment. However, environmental enrichment has never been completely successful in eliminating stereotypic behavior for an entire group of animals within a zoological facility. In the wild, stereotypic behavior is rarely observed. Documenting the occurrence of stereotypic behavior in the wild, and circumstances in which it occurs, could help provide insight into the causes of such behavior within zoological institutions. The following commentary details the observations of wild lemon sharks (Negaprion brevirostris) engaging in a stereotyped swimming pattern behind a research vessel north of Grand Bahama Island, Bahamas. We consider a possible explanation for the sharks' behavior and hope to stimulate conversation as well as increase examination of animal management routines in zoological facilities. Zoo Biol 30:365–370, 2011. © 2010 Wiley‐Liss, Inc.     

Activity budgets and the relationship between feeding and stereotypic behaviors in Asian elephants (Elephas maximus) in a Zoo

Activity budgets were studied in eight Asian elephants (Elephas maximus) at Chester Zoo (UK) for 35 days, between January and November 1999. Recordings were made between 10:00 and 16:00 hr (with most behavior frequencies calculated between 10:00 and 14:00 hr). The elephants exhibited variation in activity depending on their age, sex, the time of day and the time of year. Only the five adult cows exhibited stereotypic behavior, with frequencies ranging from 3.9 to 29.4% of all observations. These elephants exhibited individual, diurnal and seasonal variation in stereotypic behavior. This has implications for studies that use short sampling periods and may make comparisons of data collected at different times of the day or year invalid. The six adult elephants spent 27.4–41.4% of the time feeding (between 10:00 and 14:00 hr), 22.9–42.0% standing still, 6.1–19.2% walking and 3.9–9.6% dusting. The hypothesis that the frequency of stereotypic behavior in adult cow elephants was negatively correlated with the frequency of feeding behavior was tested and was found to be true. Stereotypic behavior increased in frequency toward the end of the day—while waiting to return to the elephant house for food—and elephants spent more time stereotyping during the winter months than during the summer months. Elephants were inactive (i.e. exhibited behaviors other than locomotion) for between 70.1 and 93.9% of the time. Creating more opportunities for elephants to exhibit foraging behavior and the introduction of greater unpredictability into management regimes, especially feeding times, may reduce the frequency of stereotypic behavior and increase general activity levels. Zoo Biol 28:79–97, 2009. © 2008 Wiley-Liss, Inc.