Intact carcasses as enrichment for large felids: Effects on on‐ and off‐exhibit behaviors

Reducing stereotypic behaviors in captive animals is a goal for zoological institutions worldwide, and environmental enrichment is one tool commonly used to meet that end. Behavioral needs associated with feeding, however, are often neglected in large carnivores. To address these needs, I tested the effects of calf carcasses as enrichment for large felids. Over 14 weeks, I provided nine animals with up to seven intact carcasses. The cats were housed at Toledo Zoo, Potawatomi Zoo, and Binder Park Zoo. Animals were observed off and on exhibit for changes in feeding, natural, stereotypic, active, and inactive behaviors. I compared treatment behaviors with behaviors observed during a baseline period in which the animals were fed traditional processed diets. For these nine cats, carcass provision decreased off‐exhibit stereotypic behaviors but had little impact on on‐exhibit behaviors. Zoo Biol 21:37–47, 2002. © 2002 Wiley‐Liss, Inc.     

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.     

Feeding enrichment methods for Pacific walrus calves

In the wild, walrus calves are occupied with many behaviors necessary for survival. In captivity there is usually less to occupy them. Therefore it is necessary to develop other ways to occupy the animals to prevent negative behavior. In the present study, food in four different types of dispensers were tested on two walrus calves: fish in ice, fish in a nine‐hole container, fish in a two‐hole container, and fish in ice in a one‐hole container. All four methods of offering fish had an effect on the animals' behavior. There were differences in the way the two animals responded to each of the four dispensers. The dispensers occupied one animal on average between 32–95% of the 90‐min test periods, and the other animal for between 14–57% of the test periods. Due to the effect of learning and rapid development of the calves, which were shifting from a 100% formula diet to a 100% fish diet during the study period, the four methods cannot be compared. Besides the time feeding methods occupy animals, the practicality of a dispenser determines how often it will be used by the keepers. Of the four dispenser types tested in the present study, the nine‐hole container was the most practical and was still used frequently by the keepers years after the study. Zoo Biol 0:1–12, 2007. © 2007 Wiley‐Liss, Inc.     

Note on optimizing environmental enrichment: a study of fennec fox and zoo guests

Environmental enrichment is widely used to stimulate animal time budgets that seem more natural and diverse than those of unenriched animals. Uncertainty of reward is a suggested means to maintain enrichment's efficacy. Foraging tasks are widely applied in zoo animal enrichment, yet few rely on the logic of optimal foraging theory to help maintain animal motivation. We applied a foraging strategy to zoo housed fennec foxes as enrichment. We varied only the probability of when and where food would occur in the animals' exhibit. Our methods increased behavioral diversity, animal activity, and stimulated guest interest in the exhibit.     

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.     

Successful feeding enrichment for captive chimpanzees

An analysis of a feeding enrichment program for captive chimpanzees was completed to determine the effects of that program on the incidence of agonistic and abnormal behaviors by using 41 adult chimpanzees in six social groups. Four feeding enrichment procedures were implemented simultaneously in the experimental phase of this ABA design study. The procedures were planned to elicit time-consuming, noncompetitive feeding, theorizing a consequent reduction in agonism and detrimental abnormal behaviors typically occurring in captive chimpanzees. The 270 hours of data were collected over a 6-month period. A multivariate analysis of variance result supported the hypothesis, as the barrage of feeding enrichment techniques significantly reduced agonism and abnormal behaviors. This study's significance lies in its application of the scientific method to improving the husbandry of captive primates.     

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.     

Longitudinal study of delayed reproductive success in a pair of white‐cheeked gibbons (Hylobates leucogenys)

Concern over a lack of breeding success in a pair of white‐cheeked gibbons (Hylobates leucogenys) prompted a four‐part study of gibbon behavior and physiology at the Lincoln Park Zoo. Data were collected to determine the female intermenstrual interval (IMI) and identify periods of peak receptivity. Subsequent behavioral data were gathered during both female menses and estrous periods to formulate a behavioral profile for each gibbon. The female experienced a species‐typical IMI of 21.6 days and exhibited heightened levels of behavioral receptivity toward the male during estrus. The male exhibited high levels of human‐directed behavior throughout the day. Closing the exhibit to visitors did not result in higher levels of social proximity or prosocial behavior between the pair, although it did eliminate the male's human‐directed behavior during the experimental condition only. The female exhibited higher levels of social grooming, solicitation of the male, and proximity to the male when the pair was locked indoors. Based on those findings, the pair was moved to an exclusively indoor exhibit. The female's visibility to the public decreased substantially in the alternate exhibit, but there were no other significant behavioral changes. Nearly one year after the exhibit change, the female gibbon was confirmed to be pregnant. Although the results of this study cannot be used to infer causal conditions that resulted in the pregnancy, they do support the notion that systematic documentation of animal behavior and physiology may be used as a tool for monitoring reproductive behavior and informing management decisions. Zoo Biol 21:413–434, 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.     

Object-use in free-ranging white-faced capuchins (Cebus capucinus) in Costa Rica

Chimpanzees and capuchins demonstrate greater varieties and higher rates of tool-use when compared to other non-human primates. Although capuchins have been studied extensively in captivity, data on their tool-using behavior under free-ranging conditions are limited. This is the first long-term field research to systematically study complex object manipulation in capuchins. The aims of this research are 1) to examine the types, rates, and contexts of tool- and object-use in free-ranging capuchins and 2) to determine if free-ranging capuchins' object manipulation behavior is comparable to the behavior exhibited by captive individuals. Data on 3 troops of white-faced capuchins (Cebus capucinus) were collected from February 1995 to January 1996 at Palo Verde, Costa Rica. Data were collected using focal animal and ad libitum sampling techniques. Any observed incident of tool-use and object-use was recorded. No tool-use was observed during the 11-month study. Object-use (pound, rub, and fulcrum-use) occurred at a rate of 0.19/hr and made up less than 1% of the monkeys' time (there were no differences among the age/sex classes). The results indicate that free-ranging capuchins do not exhibit the range of tool-using behavior demonstrated by their captive counterparts. This may be the result of differential motivational responses to objects, arboreal lifestyle, absence of adequate tool material, and/or absence of food resources that require extraction involving tool-use. Am J Phys Anthropol 106:311–321, 1998. © 1998 Wiley-Liss, Inc.     

Variability in food-processing behavior among white-faced capuchins (Cebus capucinus) in Santa Rosa National Park, Costa Rica

Observed patterns of variability in the food-processing behavior of white-faced capuchins (Cebus capucinus) across populations may reflect foraging traditions. However, there has been relatively little attention given to intrapopulation variability in food processing among groups and age/sex classes, making recent cross-population comparisons difficult to interpret. In this paper, we provide data on patterns of object use in foraging that we observed at Santa Rosa National Park, Costa Rica, for comparison with published data from a neighboring research site, Palo Verde National Park. We also describe the techniques used to process two food items consumed by Cebus capucinus at Santa Rosa, and discuss the factors that may underlie observed variability. We conducted a 6-month study on two groups of capuchins in 2001, and collected data on general activity and feeding patterns, rates and forms of object use, and distinctive processing techniques employed for two specific foods (Sloanea terniflora and Luehea candida). Rates of object-use behavior at Santa Rosa were considerably higher than those reported for Palo Verde and showed significant variation between groups and age/sex classes, as did patterns of Sloanea and Luehea processing. Observed differences in feeding rates between groups may reflect food availability or relative profitability, whereas variation between age/sex classes seems to reflect differences in the physical capabilities, foraging strategies, and the relative experience of mature and immature animals. Further research is needed to identify how a social context may influence the acquisition of food-processing techniques in juveniles and the development of foraging traditions in social groups.     

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.     

Foraging enrichment alleviates oral repetitive behaviors in captive red-tailed black cockatoos (Calyptorhynchus banksii)

The relationship between inadequate foraging opportunities and the expression of oral repetitive behaviors has been well documented in many production animal species. However, this relationship has been less-well examined in zoo-housed animals, particularly avian species. The expression of oral repetitive behavior may embody a frustrated foraging response, and may therefore be alleviated with the provision of foraging enrichment. In this study, we examined the effect of different foraging-based enrichment items on a group of captive red-tailed black cockatoos who were previously observed performing oral repetitive behavior. A group of six cockatoos were presented with five foraging enrichment conditions (no enrichment (control), sliced cucumber, fresh grass, baffle cages, and millet discs). Baseline activity budgets were established over a 10-day preintervention period and interventions were then presented systematically over a 25-day experimental period. This study demonstrated that the provision of foraging interventions effectively increased the median percentage of time spent foraging compared to control conditions (range, 5.0–31.7% across interventions vs. 5.0% for control), with two of the interventions; grass and millet discs, significantly decreasing the expression of oral repetitive behaviors (control = 16.6 vs. 8.3% for both grass and millet discs). Finally, a rapid-scoring method utilized by zookeepers during the study proved to be a useful proxy for the amount of time the cockatoos spent interacting with the foraging interventions and overall time spent foraging.     

Stereotypic behavior and fecal cortisol level in captive giant pandas in relation to environmental enrichment

Stereotypic behavior is exhibited by a wide range of captive animals. Its association with hormones, especially elevated cortisol level and lack of naturalistic stimuli in the environment, has been little studied. This study hypothesizes that stereotypic behavior is caused by stress due to lack of appropriate, naturalistic stimuli in the environment. Using four adult pandas (Ailuropoda melanoleuca) in the Beijing Zoo from March–July in 2003, we tested the following predictions: 1) stereotypic behavior and fecal cortisol level will not change associated with the progress of reproductive state; 2) there is a positive correlation between the occurrence of stereotypic behavior and fecal cortisol level; and 3) environmental enrichment by adding a naturalistic stimulus will reduce both stereotypic behavior and fecal cortisol level. We did not find any significant differences in the occurrence of stereotypic behavior and fecal cortisol level but did find a significant difference in the total time engaged in displaying the stereotypic behavior among the three estrous periods. The level of stereotypic behavior was correlated with elevated fecal cortisol level. Enrichment simply by adding a naturalistic stimulus did not show significant effects on stereotypic behavior, or on fecal cortisol level. Our results supported the second prediction, but did not completely support the first and the third ones perhaps because of the small sample size. Additionally, our results showed that stereotypic behavior might be a response to a heightened level of cortisol. Zoo Biol 0:1–15, 2006. © 2006 Wiley‐Liss, Inc.     

斑嘴鹈鹕引入天鹅湖的试验研究

为了确保人工繁育的斑嘴鹈鹕成功引入上海动物园的天鹅湖,于2007年11月至2008年7月对8只2岁的斑嘴鹈鹕在放入天鹅湖前进行了塑料箱取食和天鹅湖水质适应性训练,并在放入天鹅湖后应用所有事件取样法对斑嘴鹈鹕的行为进行观察。取食水质适应性训练结果表明斑嘴鹈鹕生长良好。放入天鹅湖后斑嘴鹈鹕的行为时间分配表明,觅食行为在放入天鹅湖第1个月所占比例最高（44%）,第2、第3个月分别为30%、31%,同时其他主要行为时间分配趋于稳定,与一年后天鹅湖中该斑嘴鹈鹕种群的行为时间分配比较无明显差异（P〉0.05）,表明斑嘴鹈鹕对陌生环境适应期为2-3个月左右。在鹈鹕放入天鹅湖后的第11d和第23d各有1只死亡,引起斑嘴鹈鹕发病并导致死亡的原因是感染棘口吸虫,使用吡喹酮驱虫药进行治疗效果明显。     

The influence of feeding,enrichment, and seasonal context on the behavior of Pacific Walruses (Odobenus rosmarus divergens)

Though some research exists concerning general behavior and activity patterns of Walruses in zoos or aquariums, less is known about how these patterns change in response to various environmental and temporal contexts. This study presents two studies assessing behavioral changes in relation to feeding period, object enrichment (OE), and season in a social group of four Pacific Walruses at the New York Aquarium. Study 1 examined behavior in relation to feeding context (nonfeed, prefeed, postfeed); data were collected over a three‐week period, resulting in 47 observation sessions for each feeding context. Study 2 examined behavior in relation to OE and season; data were collected in two phases resulting in 12 enrichment and 9 no‐enrichment (NE) observation sessions (Phase 1), and 21 enrichment and 18 NE observation sessions (Phase 2). Study 1 showed that after feeding, oral behavior increased while social behavior and total swim frequency decreased. In Study 2, both swim frequency and social behavior were found to interact with OE and phase, while oral behavior remained constant across all conditions. As in the wild, both studies found all animals to be swimming the majority of the time. Though every animal spent much of its swim time engaged in an Individual Swimming Pattern (ISP), both studies showed that the proportion of ISP (in relation to total time swimming) remained stable across all contexts, suggesting a potential functional role of the ISPs. These results are discussed in light of the ongoing debate over the role of stereotypies in welfare assessment. Zoo Biol 29:397–404, 2010. © 2009 Wiley‐Liss, Inc.     

Subterranean termites (Isoptera: Rhinotermitidae): Exploitation of equivalent food resources with different forms of placement

Abstract Coptotermes gestroi and Heterotermes tenuis have been described as important urban pests in Brazil. The establishment of control technologies using baits that consider the social behavior of termites requires a better knowledge of their foraging behavior. Thus, this study analyzed the feeding behavior of these species with three different forms of food placement: food on the surface of a substrate and food either partially or completely buried in the substrate. Experimental arenas were composed of a central chamber connected to three food chambers. Each central chamber contained 550 foragers of C. gestroi or 517 foragers of H. tenuis. Blocks of Pinus elliottii were placed in the different food chambers. After 28 days, the consumption of each wood block and the percentage of foraging individuals recruited for food chambers were verified in relation to the total survival rate obtained for each one of the 20 replicates. Results showed that completely buried food was most consumed for H. tenuis and presented a higher recruitment rate of workers and soldiers for both species. Although the consumption had non‐significant differences for C. gestroi, these termites exhibited a tendency to prefer completely buried food. In these conditions, it can be concluded that the forms of food placement used in the present research influenced the recruitment of individuals for both species. Data also suggests that when the foraging subterranean termites find food resources in the tunneling substrate, they tend to concentrate their efforts on it, a behavior regime that reduces exposure to external environment.