Effects of feeding enrichment on behavior of three species of captive bears

Bears are extremely popular among the zoo-going public, yet while many zoo exhibits have undergone dramatic design changes in recent years, most bears continue to be housed in moated grottos constructed largely of gunite. In these traditional exhibits they frequently demonstrate stereotypic locomotor patterns and are often encouraged by the public to beg. Thus, the manner in which most captive bears are exhibited does not facilitate conservation education. It is possible, however, to provide bears with opportunities to demonstrate species-typical feeding and foraging behaviors, even in standard exhibits. Subjects were four individuals of three bear species. Feeding enrichment was provided to one bear per week during three mornings during the summers of 1989 and 1990. Overall, animals were more active, less passive and less often engaged in abnormal behaviors during sessions with enrichment. Effects showed individual variation and were more profound during the second year of the study, when a greater variety of enrichment items was presented. These results suggest that simple and inexpensive methods of enrichment may have a significant, positive influence on the behavior of captive bears. © 1992 Wiley-Liss, Inc.     

Animal Activity and Visitor Learning at the Zoo

ABSTRACT

This study investigated the effect animal activity had on information visitors attended to at three bear exhibits. Attention was used as an indirect measure of what information visitors are consciously processing, or learning. It was hypothesized that visitors would be more likely to attend to specific information about animal behavior when bears were active rather than when inactive or out of sight. Visitor conversations were recorded during observations of polar, sloth and spectacled bears. Conversation was coded according to its content (animal-directed, human-focused, behavior, other) and to the corresponding behavior of the bear (active, inactive, pacing, not visible). The energy level of the activity was also considered. The hypothesis was supported for the polar bears, but less so for the other two bears. Behavior conversation was highest and human-directed conversation was lowest in the presence of highly animated polar bears. Behavior content was limited in the presence of the less animated sloth and spectacled bears. However, it was still significantly less frequent, and human content more frequent, when the sloth and spectacled bears were pacing and/or not visible. Therefore, what visitors attended to was influenced by what the bears were doing. The findings suggest that animated activity (rather than the more broadly defined ‘activity’) elicits the most visitor attention to behavior, and this in turn potentially facilitates visitor learning.     

Behavioral development of a polar bear cub (Ursus maritimus) in captivity

The difficulty of observing polar bears (Ursus maritimus) in the wild has prohibited the gathering of behavioral data necessary to develop a baseline set of milestones for monitoring cub development. This study describes and quantifies previously undocumented trends in behavior observed in a captive cub–information that will be useful both in future comparative studies and in the implementation of husbandry improvements. Nearly 400 hr of behavioral data were collected, 100 hr of which were video recordings from the maternity den during the first 3 months of life. Den videos were scored to determine activity budgets and levels of maternal contact. For the remainder of the first year, mother and cub were observed in the outdoor enclosure. The onset and relative frequency of 40 discrete cub behaviors were tracked, as were patterns of mother–cub contact, including nursing and weaning. This study revealed that environmental conditions, habitat enrichment, and conditioning procedures influenced the patterns of developmental behavior exhibited by a polar bear cub. Both climatic and developmental factors had significant effects on the time the bears spent swimming. Management practices, such as environmental enrichment, and a conditioning procedure involving separation of mother and cub caused transient changes in several tracked behaviors. As the cub aged, the longest time between consecutive maternal contacts increased. Nursing bouts recorded per hour of observation decreased, and the duration of individual nursing bouts and pre‐nurse begging periods increased. Zoo Biol 22:507–514, 2003. © 2003 Wiley‐Liss, Inc.     

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.     

Assessing the Welfare of Dairy Cattle

This article attempts to determine the effects of environment (captive or wild) and a simple form of environmental enrichment on the behavior and physiology of a nonhuman animal. Specifically, analyses first compared behavioral budgets and stereotypic behavior of captive coyotes (Canis latrans) in kennels and pens to their counterparts in the wild. Second, experiments examined the effect of a simple form of environmental enrichment for captive coyotes (food-filled bones) on behavioral budgets, stereotypies, and corticosteroid levels. Overall, behavioral budgets of captive coyotes in both kennels and pens were similar to those observed in the wild, but coyotes in captivity exhibited significantly more stereotypic behavior. Intermittently providing a bone generally lowered resting and increased foraging behaviors but did not significantly reduce stereotypic behavior or alter corticosteroid levels. Thus, coyote behavior in captivity can be similar to that exhibited in the wild; in addition, although enrichment can affect proportions of elicited behaviors, abnormal behaviors and corticosteroid levels may require more than a simple form of environmental enrichment for their reduction.     

Golden-bellied mangabeys (Cercocebus galeritus chrysogaster) at the Sacramento Zoo: Adult heterosexual pairs

The behaviors of three different adult male–adult female pairs of golden-bellied mangabeys (Cercocebus galeritus chrysogaster) were compared. Correlates of restricted social conditions and of the presence of offspring on adult behavior and direction of aggressive behaviors were noted. A captive pair displayed self-biting and other aberrant behaviors, a lone wild-caught pair showed redirected aggression related to sex, and a pair housed with its offspring showed close social proximity and protection of an infant. The implications of housing and experience for space and visitor exposure are discussed. Observer- vs. visitor-directed displays are seen as important measures of group and visitor effects.     

Contextual impacts on individual and synchronous breathing rate variations in three captive odontocete groups

Breathing rates are often collected both in the wild and in captivity to inform on cetaceans' internal state. However, few studies have investigated the effect of various factors on this breathing rate. We investigated the variations of individual and synchronous breathing rates depending on individual features (species, sex, age), displayed behavior, social parameters (social grouping), and environmental parameters (diurnal variation, presence of enrichment, unusual events, and presence of visitors in three groups of captive odontocetes (Yangtze finless porpoises, Neophocaena asiaeorentalis asiaeorientalis, East‐Asian finless porpoises, Neophocaena asiaeorentalis sunameri, bottlenose dolphins, Tursiops truncatus). Both individual and synchronous breathing rates were the highest when animals engaged in energetic or social behaviors. Individual breathing rate decreased but synchronous breathing rate increased with the presence of enrichment. Both rates increased during unusual events (e.g., pool cleaning, presence of a diver in the pool, noise, transport) and when public was present for Yangtze finless porpoises. Finally, synchronous breathing rate increased for Yangtze finless porpoises when experiencing social separation. We suggest that individual and synchronous breathing rates are useful parameters to measure, both in wild and captive animals, to obtain information on their arousal/stress state. However, these rates should be interpreted with caution and should be used together with other parameters to allow more accurate inferences.     

Variation in visitor perceptions of a polar bear enclosure based on the presence of natural vs. un-natural enrichment items

A debate exists among modern zoo staff as to whether or not the addition of un-naturalistic enrichment takes away from, or even defeats, the educational messages designers are trying to incorporate in naturalistic exhibits. A visitor study was conducted at the Central Park Zoo's polar bear exhibit in order to determine whether or not the type of enrichment in an enclosure actually alters guest perceptions. Visitors were exposed to one of two enrichment treatments in the bear enclosure: Naturalistic or Un-naturalistic. The results of this study suggest that enrichment type did not alter the perceptions of visitors. However, it did identify some of the different ways adults and youths perceive animals and zoos. Additionally, the study highlighted the varying perceptions individuals have of the concept of polar bears vs. their perceptions of the captive individuals at the Central Park Zoo. Implications for enrichment usage and exhibit design are discussed. Zoo Biol 28:292–306, 2009. © 2008 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.     

Stimulus enhancement and spread of a spontaneous tool use in a colony of long-tailed macaques

In a captive group of long-tailed macaques, tool-using behavior by a single competent individual had a significant effect on the synchronous manipulative behavior of naïve animals. Group members engaged in manipulations on the same object class more frequently during times when the model was working than when it was not. The form of their behavior, however, in no way resembled the technique used by the model. All three animals that later became successful tool users were among the few subjects that exhibited a significant increase in manipulations on the same object class while the model was working. Possible causal relationships between this stimulus enhancement and the transmission of the new behavior to other group members are analyzed and discussed.     

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.     

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.     

Animal‐borne video systems provide insight into the reproductive behavior of the Asian black bear

Previous studies on the mating system of the Asian black bear (Ursus thibetanus) have been limited to observations of captive populations and estimations of multiple paternities. Hence, the mating system of wild bears remains poorly understood. Animal‐borne camera systems (i.e., cameras mounted on animals) provide novel tools to study the behavior of elusive animals. Here, we used an animal‐borne video system to record the activities of wild bears during the mating season. Video camera collars were attached to four adult Asian black bears (male “A” and “B,” and female “A” and “B”) captured in Tokyo, central Japan, in May and June 2018. The collars were retrieved in July 2018, after which the video data were downloaded and analyzed in terms of bear activity and mating behavior. All the bears were found to interact with other uniquely identifiable bears for some of the time (range 9–22 days) during the deployment period (range 36–45 days), and multiple mating in males was documented. Both males and females exhibited different behaviors on social days (i.e., days when the bear interacted with conspecifics) compared with solitary days (i.e., days with no observed interactions with conspecifics). Compared with solitary days, the bears spent a lower proportion of time on foraging activities and higher proportion of time on resting activities on social days. Our results suggest that Asian black bears have a polygamous mating system, as both sexes consort and potentially mate with multiple partners during a given mating season. Furthermore, bears appeared to reduce their foraging activities on social days and engaged more in social interactions.     

Contrafreeloading in grizzly bears: implications for captive foraging enrichment

Although traditional feeding regimens for captive animals were focused on meeting physiological needs to assure good health, more recently emphasis has also been placed on non‐nutritive aspects of feeding. The provision of foraging materials to diversify feeding behavior is a common practice in zoos but selective consumption of foraging enrichment items over more balanced “chow” diets could lead to nutrient imbalance. One alternative is to provide balanced diets in a contrafreeloading paradigm. Contrafreeloading occurs when animals choose resources that require effort to exploit when identical resources are freely available. To investigate contrafreeloading and its potential as a theoretical foundation for foraging enrichment, we conducted two experiments with captive grizzly bears (Ursus arctos horribilis). In Experiment 1, bears were presented with five foraging choices simultaneously: apples, apples in ice, salmon, salmon in ice, and plain ice under two levels of food restriction. Two measures of contrafreeloading were considered: weight of earned food consumed and time spent working for earned food. More free than earned food was eaten, with only two bears consuming food extracted from ice, but all bears spent more time manipulating ice containing salmon or apples than plain ice regardless of level of food restriction. In Experiment 2, food‐restricted bears were presented with three foraging choices simultaneously: apples, apples inside a box, and an empty box. Although they ate more free than earned food, five bears consumed food from boxes and all spent more time manipulating boxes containing apples than empty boxes. Our findings support the provision of contrafreeloading opportunities as a foraging enrichment strategy for captive wildlife. Zoo Biol 29:484–502, 2010. © 2009 Wiley‐Liss, Inc.     

The Effects of Visitor Density and Intensity on the Behavior of Two Captive Jaguars (Panthera onca)

Several researchers have reported significant effects of visitor density and intensity on captive animal behavior. This study determined whether this was the case for 2 captive jaguars housed at the Woodland Park Zoo, Seattle, WA. Subjects were monitored for changes in behavior as a function of visitor density and intensity. The jaguars were observed for 8 hr per week for 29 weeks—March 31 until October 11, 1998—for a total of 230 hr. Continuous frequency sampling was used, and visitor density and intensity were recorded every minute. Parametric statistics were used to test for correlations between behavior and density, intensity, or a combination of the two. Both density and intensity were significant for time spent non-visible for both cats, and intensity showed a significant effect on the female's pacing behavior. In addition, the male cat exhibited a trend for increased aggression based on both visitor density and intensity and a trend of intensity affecting his social behavior. In conclusion, both density and intensity had a significant effect on behavior, with intensity showing a larger effect.     

The effects of visitor density and intensity on the behavior of two captive jaguars (Panthera onca)

Several researchers have reported significant effects of visitor density and intensity on captive animal behavior. This study determined whether this was the case for 2 captive jaguars housed at the Woodland Park Zoo, Seattle, WA. Subjects were monitored for changes in behavior as a function of visitor density and intensity. The jaguars were observed for 8 hr per week for 29 weeks—March 31 until October 11, 1998—for a total of 230 hr. Continuous frequency sampling was used, and visitor density and intensity were recorded every minute. Parametric statistics were used to test for correlations between behavior and density, intensity, or a combination of the two. Both density and intensity were significant for time spent non-visible for both cats, and intensity showed a significant effect on the female's pacing behavior. In addition, the male cat exhibited a trend for increased aggression based on both visitor density and intensity and a trend of intensity affecting his social behavior. In conclusion, both density and intensity had a significant effect on behavior, with intensity showing a larger effect.     

Seasonal shifts in giant panda feeding behavior: relationships to bamboo plant part consumption

The giant panda (Ailuropoda melanoleuca) is classified as a carnivore, yet subsists on a diet comprised almost exclusively of bamboo. Wild and captive giant pandas use highly selective foraging behaviors for processing and consuming bamboo. These behaviors are for the first time quantified in captive giant pandas over a 5‐year period of time showing highly specific seasonal trends. Giant panda feeding behavior was recorded using live video observations of two giant pandas housed at the Memphis Zoo from November 2003 to June 2008. Leaf was the primary plant part consumed from June to December, whereas culm was consumed primarily from February to May, with both bears displaying similar seasonal shifts in plant part consumption. From May to June, leaf consumption increased significantly (P‐values<0.001); from June to August, leaf consumption remained high and stable. From December to March, leaf consumption decreased significantly (P‐values<0.001). Specific behaviors for bamboo leaf and culm consumption were also observed. Both bears formed wads of leaves before ingestion while feeding on leaf, but the male employed this feeding behavior more often than the female (54 and 33%, respectively). Both bears used similar culm‐stripping behavior (26 and 25%), used to remove the outer layer and isolate the pith for consumption. This study indicates that unique seasonal foraging behaviors observed in wild pandas are also apparent in captive animals in relation to plant part selectivity and feeding behaviors. Zoo Biol 29:470–483, 2010. © 2009 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.     

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.     

Behavior of giant pandas (Ailuropoda melanoleuca) in captive conditions: Gender differences and enclosure effects

The behavior of giant pandas (Ailuropoda melanoleuca) was studied under captive conditions. Both male and female pandas spent similar amounts of time engaged in eating and locomotion. Males performed anogenital‐marking more but rested less than females, which suggests a sexually dimorphic pattern of behavior. Furthermore, females housed in the seminatural environment spent significantly less time engaged in stereotyped behavior than did females housed in the traditional enclosure, indicating that an enclosure environment affects the behavior of giant pandas. These data illustrate the importance of careful management and facility design for captive giant pandas. Zoo Biol 22:77–82, 2003. © 2003 Wiley‐Liss, Inc.