Environmental enrichment for a mixed-species nocturnal mammal exhibit

Environmental enrichment (EE) is an integral aspect of modern zoo animal management but, empirical evaluation of it is biased toward species housed in single‐species groups. Nocturnal houses, where several nocturnal species are housed together, are particularly overlooked. This study investigated whether three species (nine‐banded armadillos, Dasypus novemcinctus; Senegal bush babies, Galago senegalensis; two‐toed sloths, Choloepus didactylus) in the nocturnal house at Paignton Zoo Environmental Park, UK could be enriched using food‐based and sensory EE. Subjects were an adult male and female of each species. EE was deemed effective if it promoted target species‐typical behaviors, behavioral diversity, and increased use of enriched exhibit zones. Results from generalized linear mixed models demonstrated that food‐based EE elicited the most positive behavioral effects across species. One set of food‐based EEs (Kong®, termite mound and hanging food) presented together was associated with a significant increase in species‐typical behaviors, increased behavioral diversity, and increased use of enriched exhibit zones in armadillos and bush babies. Although one type of sensory EE (scented pine cones) increased overall exhibit use in all species, the other (rainforest sounds) was linked to a significant decrease in species‐typical behavior in bush babies and sloths. There were no intra or interspecies conflicts over EE, and commensalism occurred between armadillos and bush babies. Our data demonstrate that simple food‐based and sensory EE can promote positive behavioral changes in a mixed‐species nocturnal mammal exhibit. We suggest that both food and sensory EE presented concurrently will maximize opportunities for naturalistic activity in all species. Zoo Biol 31:397–413, 2012. © 2011 Wiley Periodicals, Inc.     

Activity Budgets of Captive Cape Fur Seals (Arctocephalus pusillus) Under a Training Regime

Ethograms and time budgets are crucial for the behavioral assessment of nonhuman animals in zoos, and they serve as references for welfare research. This study was conducted to obtain detailed time budgets of trained Cape fur seals (Arctocephalus pusillus) in captivity, to evaluate variations of these patterns, and to determine whether abnormal behaviors had been displayed. Behavioral data for 3 Cape fur seals in the Wroclaw Zoo were collected, and more than 300 observation hours (during a 12-month period) per individual were analyzed. The studied animals exhibited a diversified repertoire of natural behaviors with apparent seasonal and daily patterns, and they did not present stereotypic behaviors. Significant differences of interaction rates between individuals suggest more frequent affiliative interactions among related animals. The absence of stereotypic behaviors, good health of individuals, and the presence of diversified natural behaviors indicated relatively good welfare of Cape fur seals kept in the Wroclaw Zoo.     

Human–Ape Interactions in a Zoo Setting: Gorillas and Orangutans Modify Their Behavior Depending upon Human Familiarity

Understanding how human presence influences animal behavior, specifically the behavior of nonhuman primates, has important implications for methodology in cognitive and behavioral studies, for our understanding of human–animal relationships and for animal welfare in captive settings. Conducted in the San Diego Zoo, this study partially replicates an existing study on human–animal relationships, which focused on familiarity effects on the human-directed behavior of great apes residing in the Toronto Zoo. Such a replication in a new location and with different individuals is necessary to expand sample size and to better understand how ontogeny and living environment influence human-directed ape behavior. All-occurrence sampling of human-directed behavior was used to gather data on two gorilla groups and one orangutan group, all housed at the San Diego Zoo. The aim was to compare ape-initiated behaviors toward zoo staff with apeinitiated visitor-directed behavior, in accordance with predictions of the Human–Animal Relationship (HAR) model. Overall, human-directed behaviors were more frequent toward visitors than toward staff, mainly caused by increased visitor-directed visual behavior, specifically brief glances. Given that visual monitoring has been seen as fearful behavior, potentially related to predator monitoring, this would confirm the expectation that lack of familiarity will lead to increased visual vigilance. However, the visitor-directed visual behaviors may not be antagonistic or fearful. Considering the specific behaviors and exhibit designs, curiosity may be an equally likely explanation in this context. Aiming to also understand whether these groups exhibited species differences in human-directed behavior, it was found that orangutans engaged in more affiliative behavior overall than gorillas. Comparing our results with the previous study, we conclude that while effects of familiarity are present, those effects are modulated by both individual ontogeny and exhibit design. While the HAR model is partially supported, additional factors may need to be included to fully interpret the observed behavior. Additional research is needed to further understand the effects of species, sex, and ontogeny on the predictions of the HAR model.     

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.     

Willingness to Pay: Animal Welfare and Related Influencing Factors in China

Personal willingness to pay, an important research aspect on nonhuman animal welfare, is the foundation of animal welfare legislation. As China has no special laws on the issue, it is important to study animal welfare. This article assesses personal willingness to pay for animal welfare in China, using the Contingent Valuation Method. Based on collected data of 229 visitors from Heilongjiang Northeast Tiger Garden (Harbin), Beijing Zoo, Changchun Zoo and Botanical Garden, Dalian Forest Zoo, and Harbin North Forest Zoo, the study researched willingness to pay for animal welfare and associated influence factors in China. Results showed a high rate of personal willingness to pay (89.5%). Factors such as age, education, and income had obvious effects on personal willingness to pay; however, gender and career had only slight effects.     

Willingness to pay: animal welfare and related influencing factors in China

Personal willingness to pay, an important research aspect on nonhuman animal welfare, is the foundation of animal welfare legislation. As China has no special laws on the issue, it is important to study animal welfare. This article assesses personal willingness to pay for animal welfare in China, using the Contingent Valuation Method. Based on collected data of 229 visitors from Heilongjiang Northeast Tiger Garden (Harbin), Beijing Zoo, Changchun Zoo and Botanical Garden, Dalian Forest Zoo, and Harbin North Forest Zoo, the study researched willingness to pay for animal welfare and associated influence factors in China. Results showed a high rate of personal willingness to pay (89.5%). Factors such as age, education, and income had obvious effects on personal willingness to pay; however, gender and career had only slight effects.     

Space Use as an Indicator of Enclosure Appropriateness in African Wild Dogs (Lycaon pictus)

A clear understanding of space use is required to more fully understand biological requirements of nonhuman animals in zoos, aid the design of exhibits, and maximize the animals' welfare. This study used electivity indexes to assess space use of two packs of African wild dogs (Lycaon pictus) and the appropriateness of two naturalistic, outdoor enclosures at the San Diego Zoo and Bronx Zoo. The results identified enclosure features that were both underutilized and overutilized. They suggest that replacing underutilized areas with features similar to areas that were overutilized may provide more preferred opportunities for the animals. Assessing space use of animals in human care may serve as an indicator of enclosure appropriateness and could have welfare implications. By looking at the possible reasons for area preferences, animal managers can get an idea of where improvements could be made. Designing future exhibits accordingly thus can provide possible welfare benefits for the animals concerned.     

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.     

Applying Behavioral Conditioning to Identify Anticipatory Behaviors

The ability to predict regular events can be adaptive for nonhuman animals living in an otherwise unpredictable environment. Animals may exhibit behavioral changes preceding a predictable event; such changes reflect anticipatory behavior. Anticipatory behavior is broadly defined as a goal-directed increase in activity preceding a predictable event and can be useful for assessing well being in animals in captivity. Anticipation may look different in different animals, however, necessitating methods to generate and study anticipatory behaviors across species. This article includes a proposed method for generating and describing anticipatory behavior in zoos using behavioral conditioning. The article also includes discussion of case studies of the proposed method with 2 animals at the San Francisco Zoo: a silverback gorilla (Gorilla gorilla gorilla) and a red panda (Ailurus fulgens). The study evidence supports anticipation in both animals. As behavioral conditioning can be used with many animals, the proposed method provides a practical approach for using anticipatory behavior to assess animal well being in zoos.     

Welfare evaluations of nonhuman animals in selected zoos in the Philippines

This study evaluated 3 zoos in the Philippines: the Wildlife Rescue Center and Mini Zoo, Manila Zoological and Botanical Garden, and Cavite Botanical and Zoological Park to determine the standards of nonhuman animal welfare. The study measured and compared the cage sizes of various animals to the international minimum standards. According to the categories of management and husbandry, the 3 zoos showed a significant difference on the mean scores of ranking. The Wildlife Rescue Center and Mini Zoo ranked first, followed by Manila Zoo and Cavite Zoo. Although most cages in the 3 zoos followed acceptable minimum standards, the study identified several problems related to animal welfare, hygiene, husbandry, and management. Based on the evaluations, the study recommended that the 3 zoos improve animal welfare standards.     

Computer-Aided Pattern Recognition of Large Reptiles as a Noninvasive Application to Identify Individuals

For large species, the capture and handling of individuals in capture–mark–recapture studies introduces nonhuman animal welfare issues associated with handling, physical marking, and possible wounding due to tag loss. The use of photographic identification for these species offers an alternative and less invasive marking technique. This study investigated the opportunity offered by photo identification to individually mark individuals of a large reptile, the perentie (Varanus giganteus), in Australia and therefore avoid the stress of physically capturing and handling. Photographs submitted by a remotely located community were first validated to confirm whether perenties could be individually identified from their spots electronically using a computer program. Computer-aided selection of unique patterns was found to be appropriate for the identification of individuals and confirmed 38 individuals during the sampling period. The value of this approach is 2-fold: There is a benefit to animal welfare in that handling an animal is not required to capture him or her, thus reducing capture-related stress; and confirmation that photo identification of distinctive patterns of the perentie is valid and offers a useful option to identify individuals of this large species.     

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.     

A Comparison of Zoo Animal Behavior in the Presence of Familiar and Unfamiliar People

As recorded in domestic nonhuman animals, regular interactions between animals in zoos and keepers and the resulting relationship formed (human–animal relationship [HAR]) are likely to influence the animals' behaviors with associated welfare consequences. HAR formation requires that zoo animals distinguish between familiar and unfamiliar people. This ability was tested by comparing zoo animal behavioral responses to familiar (routine) keepers and unfamiliar keepers (participants in the “Keeper for the Day” program). Study subjects included 1 African elephant (Loxodonta Africana), 3 Rothschild's giraffes (Giraffa camelopardalis rothschildi), 2 Brazilian tapir (Tapirus terrestris), and 2 slender-tailed meerkats (Suricata suricatta). Different behavior was evident and observed as decreased avoidance behavior toward familiar keepers (t₇ = 6.00, p < .001). This finding suggests the zoo animals have a lower level of fear toward familiar keepers. Keeper familiarity did not significantly affect any other behavioral measure. This finding suggests that in the current study, unfamiliar keeper presence did not appear to have detrimental effects. Furthermore, unfamiliar keeper–animal interactions could provide an increased number of positive human–animal interactions and potentially enhance animal welfare.     

丰容对圈养雌性岩羊活动时间分配的影响

为了探究环境丰容和食物丰容对岩羊行为和活动节律的影响,于2017年3月—7月,以上海动物园的5只雌性岩羊(Pseudois nayaur)为研究对象,设计环境丰容和食物丰容试验,利用瞬时扫描法对岩羊进行行为学观察,分析岩羊丰容前后昼间行为的变化。结果表明:经过环境丰容,岩羊的运动行为和反刍行为显著增加,卧息行为和其他行为显著减少,取食行为无明显变化。在环境丰容基础上,开展食物丰容后,运动行为明显减少,取食行为明显增加。卧息行为有所减少、反刍行为和其他行为有所增加,但变化均不明显。丰容后岩羊的昼间活动节律也发生了变化。取食行为呈现2个高峰期(8:00—11:00和15:00—18:00),取食行为普遍提高;运动行为在13:30—17:30时段较丰容前提前一个小时左右发生;卧息行为有相似的波动规律,但丰容后其昼间发生频次在16:00之前均降低;反刍行为波动最大,呈现出明显的2个高峰期(6:00—9:00和10:00—15:00)。试验表明,在进行环境和食物丰容后,岩羊的活动增加,优化了时间分配,福利状况得到了有效改善。     

Effects of attached data‐loggers on the activity budgets of captive Humboldt penguins

Although they can provide valuable information on at‐sea ecology, data‐loggers may adversely affect energetics, diving performance, and breeding success of equipped birds. With the aim of determining the effects of leg‐attached data‐loggers on the activity budgets of Humboldt penguins (Spheniscus humboldti) while on land, we equipped birds kept at the Landau Zoo, Landau, Germany, with such devices. We followed them during sample periods and recorded the occurrence and length of behaviors. Birds quickly habituated to the devices within 1 day of deployment, and mean rates of device‐pecking were low (0.7–1.7 pecks/hr), with device‐induced behaviors accounting for <1% of the mean daily activity budget. The method of device attachment appears behaviorally less stressful than the traditional tape‐based system in which devices are normally attached to the penguin's back. By facilitating the testing of newly developed data‐loggers on captive birds, or the development of methods for device attachment, zoos and aquaria may strengthen their role in animal conservation by helping research on free‐ranging animals. Zoo Biol 21:365–373, 2002. © 2002 Wiley‐Liss, Inc.     

Habituation to environmental enrichment in captive sloth bears—effect on stereotypies

The benefits to captive animals of environmental enrichment (EE) are widely recognized. Few studies have, however, studied how to maximise the effect of EE. One issue with EE programs seems to be habituation to the enrichment device. To study the effect of habituation to EE, 14 captive sloth bears (Melursus ursinus) were subjected to two different EE treatments. Treatment one presented EE (logs with honey containing holes) for five consecutive days, whereas treatment two presented EE on intermittent days for five days. Intermittent presentations tended to reduce habituation toward the EE. Both consecutive and intermittent presentations significantly reduced stereotypies; however, the consecutive presentations had a longer‐lasting effect. Explorative behaviors increased in both treatments, consistent with earlier findings that EE increase levels of natural behaviors. Other behaviors were unaffected by the EE presentations. The results show that intermittent presentation of EE objects may secure the interest of the animals, but continuous access to enrichment may be more efficient in reducing stereotypies in the long run. Zoo Biol 29:705–714, 2010. © 2010 Wiley‐Liss, Inc.     

Zoo Animal Welfare: The Human Dimension

ABSTRACT

Standards and policies intended to safeguard nonhuman animal welfare, whether in zoos, farms, or laboratories, have tended to emphasize features of the physical environment. However, research has now made it clear that very different welfare outcomes are commonly seen in facilities using similar environments or conforming to the same animal welfare requirements. This wide variation is almost certainly due, at least in part, to the important effects of the actions of animal care staff on animal welfare. Drawing mostly on the farm animal literature, we propose that this “human dimension” of animal welfare involves seven components: (1) positive human–animal interaction, (2) consistency and familiarity of keepers, (3) treating animals as individuals and taking account of their personalities, (4) the attitudes and personalities of keepers, (5) the keepers’ knowledge and experience, (6) the keepers’ own well-being, and (7) the influence of facility design on how keepers and others interact with the animals. We suggest that attention to these human factors provides major scope for improving the welfare of animals in zoos.     

Chimpanzee (Pan troglodytes) responses to caregiver use of chimpanzee behaviors

The relationships between captive primates and their caregivers are critical ones and can affect animal welfare. Friendly relationships can improve quality of life; adversely, agonistic relationships can decrease quality of life. Caregivers in and of themselves should not be stressful to their charges, instead the caregivers' behaviors and the nature of their interactions with captive primates is likely the basis for the stress. One method to promote positive relationships in the captive environment is for caregivers to employ species‐specific behaviors in their interactions with their charges. This study tested the effect of caregivers' use of these behaviors with chimpanzees at The Zoo Northwest Florida in Gulf Breeze. The chimpanzee participants were three males. Data collection occurred during typical interactions between the human participants and the chimpanzees. Some days the caregiver presented chimpanzee behaviors and vocalizations (CB—Chimpanzee Behavior Condition) in the data collection interactions with the chimpanzees. On other days the caregiver presented human behaviors and used speech (HB—Human Behavior Condition) in the interactions with the chimpanzees. The interactions were videotaped. Data coders recorded the behavioral contexts for each chimpanzee as they occurred on the videotape and the time that each context began. Overall they engaged in significantly more friendly behaviors such as play in CB than in HB. They were significantly less interactive in HB than CB. Caregivers should understand and employ species‐specific interactions with chimpanzees to promote friendly interactions and animal welfare. Zoo Biol 27:345–359, 2008. © 2008 Wiley‐Liss, Inc.     

An Empirical Case Study Examining Effectiveness of Environmental Enrichment in Two Captive Australian Sea Lions (Neophoca cinerea)

This case study examined the effect of environmental enrichment on the activity budgets of a male and female Australian Sea Lion (Neophoca cinerea) housed together at Adelaide Zoo. Using non-food-related (intrinsic) and food-related (extrinsic) enrichment objects, the study conducted an ABABA (withdrawal) experimental design over a 30-day period (180 hr). The study expected extrinsically reinforcing objects to be more effective than intrinsically reinforcing objects in reducing pattern swimming. The male sea lion spent more than 45% of scans engaged in pattern swimming during the initial baseline, which was reduced by at least 25% when enrichment items were present. However, there was no evidence of stereotypic behavior in the female sea lion, indicating that individual differences may exist. When enrichment was present, the study observed more active behaviors in both nonhuman animals. They spent more time interacting with the non-food-related objects overall. Therefore, introducing simple enrichment devices offers a cheap, practical, and effective method of adding complexity to the environment, which is likely to benefit the animals' welfare and enhance the zoo-visitor experience.     

Effect of Enclosure Quality on Reactivity and Welfare of Captive Soemmerring's Gazelle (Gazella soemmerringii)

The welfare of nonhuman animals in zoos is a great challenge to the zookeeper. Changes in the behavioral response of captive animals to their immediate environment can be used as a method for evaluating their welfare status. This study evaluates reactive responses of 3 groups of captive Soemmerring's gazelle (Gazella soemmerringii) kept in enclosures of different quality at Giza Zoo, Egypt. The study ascribes variations in observed behaviors to the differences in the living standards of the 3 groups. The group most concealed from visitors' disturbance (Group 3) was the least reactive. With the morning onset of human-nonhuman animal interaction, reactivity reached significantly higher levels. The study noted no difference in reactivity between male and female animals. The main sign of the animals' alertness was their attention to sources of disturbances; vocalization was minimal. Animals in Groups 1 and 2, those most accessible to visitors, had higher agonistic reactions than animals in Group 3.