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.     

Effects of positive reinforcement training techniques on the psychological welfare of zoo‐housed chimpanzees (Pan troglodytes)

Captive environments encompass various factors that can elevate stress levels and jeopardize the wellbeing of the captive animals. The use of positive reinforcement training (PRT) techniques enables researchers and caretakers to reduce tension directly associated with potentially stressful procedures and states. The current study tested the general effect of PRT on the wellbeing of zoo‐housed chimpanzees (Pan troglodytes) by measuring behaviors that reflect poor and good welfare and that were not directly connected to the specific aim of the training session. The behavior of a group of twelve chimpanzees was measured throughout the day from the exhibition yard, at baseline (12 weeks) and during the PRT period (10 weeks). The results show a significant decrease in abnormal and stress‐related behaviors and a significant rise in prosocial affiliative behaviors following implementation of the training program. The training was shown to have a greater positive effect on low‐ranking individuals compared with high‐ranking ones. This research shows for the first time that PRT offers an enrichment effect whose general influence lasts throughout the day, irrespective of any direct link to a specific trained behavior. Consequently, it can be claimed that PRT presents an effective enrichment tool that can be implemented with captive animals. Because of the above‐noted differential effect between high‐ and low‐ranking chimpanzees, however, this should be taken into consideration when combining PRT with the non‐human primates' daily routine. Am. J. Primatol. 71:687–695, 2009. © 2009 Wiley‐Liss, Inc.     

Guidelines for developing and managing an environmental enrichment program for nonhuman primates.

Before implementing an environmental enrichment program for nonhuman primates, several issues should be considered. The assignment of enrichment tasks can be made to caretakers, a dedicated "enrichment technician," volunteers, students or individuals with training in behavioral science. Determining the enrichment techniques to be used must take into account personnel time available; the species, age, sex, and individual histories of the nonhuman primates; and experimental protocols for which animals are being maintained. Identifying the most beneficial way to use the available personnel time must be tailored for each institution. To meet federal regulations, records must be kept of the environmental enhancements available to each nonhuman primate. Good record-keeping will allow appropriate evaluation of the program. This evaluation should involve the animals' responses to the enrichment opportunity, cost and durability of enrichment items, human and nonhuman safety considerations, and personnel required. The well-being of captive nonhuman primates will be most improved if well-informed decisions are made in developing and managing environmental enrichment programs.     

Maximizing the effectiveness of environmental enrichment: Suggestions from the experimental analysis of behavior

Environmental enrichment programs provide benefits to both captive animals and the facilities that house them, but cost time and resources to design, implement, and maintain. As yet, there have been few theoretically based guidelines to assist animal care staff in establishing cost-efficient enrichment methods that both elicit the desired behavioral changes and maintain their success over time. We describe several well-studied principles from the field of experimental analysis of behavior, including intrinsic reinforcement, extrinsic reinforcement, habituation, extinction, and schedules of reinforcement that could be very useful for evaluating the short- and long-term effectiveness of enrichment. We use this theoretical framework to generate testable hypotheses and provide examples of enrichment studies relevant to our predictions. In particular, we suggest that enrichment devices that offer extrinsic reinforcement (food, social access, etc. as a result of performing behaviors) should produce greater and more prolonged changes in behavior than devices that rely on the behavior itself being reinforcing to the animal. For techniques that provide no extrinsic reinforcement, using stimuli that are novel, are more different from the environment, have been withheld or altered in some way, or are presented less frequently may help reduce habituation. For techniques that provide extrinsic reinforcement, making reinforcement more difficult to obtain and providing more or higher quality reinforcers may increase the long-term success of the enrichment program. In addition, enrichment may be more effective if animal care staff avoid continuously reinforcing behaviors after they are established, enriching immediately after feeding, and exposing animals to enrichment when reinforcement is no longer available. While the current enrichment literature supports the application of behavior analytic theory, empirical evaluation of many of our predictions is still needed.     

Videotapes as enrichment for captive chimpanzees (Pan troglodytes)

The effectiveness of showing videotapes to captive chimpanzees as an environmental enrichment was quantitatively tested. The responses of 10 subjects (3 adult males and 7 adult females) to videotapes of chimpanzees engaging in a variety of behaviors, to videotapes of other animals and humans, and to television programs were compared. Data collection consisted of 20-minute, continuous sampling tests while various videotapes were shown. A total of 400 tests were conducted. Multivariate analysis of variance was applied to measure differences in the duration of eight categories of behavior across videotapes of varying content. No general behavioral differences in response to the tapes based on sex or housing were revealed. However, with the behavior of monitor-watching analyzed alone, we found that individually housed subjects watched the videotapes more than socially housed subjects. When viewing time was averaged across all videotapes, the chimpanzees watched the monitor a mean of 38.4% of the time available. The chimpanzees' behavior varied significantly only when they were watching the videotapes of various human and chimpanzee activities and not when watching a blank screen. A Pearson's correlation indicated that subjects habituated to repeated presentations of the videotapes, although the effect was small numerically. Although this type of enrichment did not extensively alter behavior, it did occupy a significant portion of the subjects' activity budget; thus, the amount of time spent watching the video stimuli indicated that videotapes may be a useful enrichment for captive chimpanzees. Zoo Biol 19:541-551, 2000. Copyright 2000 Wiley-Liss, Inc.     

Destructible toys as enrichment for captive chimpanzees

The use of destructible objects or toys as enrichment for nonhuman primates has had promising results in terms of increased use and positive behavioral effect. The purpose of this project was to determine the use and durability of a number of inexpensive, destructible toys provided one at a time or several at once. Nine singly caged chimpanzees were provided with 8 different toys made of plastic, vinyl, or cloth, and the frequency of use of the toys was determined during 15 min trials 2 times per day. A toy was removed when it was destroyed or when it was not contacted during 4 trials. The chimpanzees contacted the toys an average of 11 times per trial, and the use of the individual toys was significantly higher when provided 1 at a time rather than all at once. Use of the toys was fairly stable over time, and the toys remained in the cages an average of 3.2 days. The durability of the toys was related to the type of toy (e.g., more flexible cloth and vinyl toys lasted longer than rigid plastic toys). The destructible toys were used significantly more often than other permanent cage toys or televisions. Toy use was not related to age, level of abnormal behavior, or use of existing permanent toys or television. The implications of the results were related to the management of an environmental enrichment program and indicated that the provision of flexible, inexpensive toys 1 at a time can be an effective method of enrichment for captive chimpanzees.     

Den sharing behaviour of captive brushtail possums (Trichosurus vulpecula)

Abstract

Den sharing among wild brushtail possums (Trichosurus vulpecula) has important implications for disease transmission. This study investigated den sharing in captive possums, and measured interactions between possums sharing dens. Thirty‐four sexually mature possums (16 female, 18 male) were housed in single‐sex or mixed‐sex pairs in large enclosures that contained two dens. Daily patterns of den sharing were recorded for each pair over a 69 day period in the breeding or non‐breeding season. Social behaviour within shared dens was sampled using miniature infrared cameras. Male pairs rarely shared dens in the breeding or non‐breeding seasons (4% and 1% of days respectively) and usually engaged in ‘threats’ and ‘fights’ associated with den defence. Pairs of female possums (in both seasons) and mixed‐sex pairs housed together in the breeding season shared dens most frequently (between 84% and 91% of days), and also spent the most time together in dens each night. While sharing dens, affiliative interactions were frequent, including long periods of ‘touching’, and also ‘food sharing’ and ‘allogrooming’. The preference for den sharing and close contact shown by captive possums highlights the importance of den sharing as a potential route for disease transmission.     

Destructible Toys as Enrichment for Captive Chimpanzees

The use of destructible objects or toys as enrichment for nonhuman primates has had promising results in terms of increased use and positive behavioral effect. The purpose of this project was to determine the use and durability of a number of inexpensive, destructible toys provided one at a time or several at once. Nine singly caged chimpanzees were provided with 8 different toys made of plastic, vinyl, or cloth, and the frequency of use of the toys was determined during 15 min trials 2 times per day. A toy was removed when it was destroyed or when it was not contacted during 4 trials. The chimpanzees contacted the toys an average of 11 times per trial, and the use of the individual toys was significantly higher when provided 1 at a time rather than all at once. Use of the toys was fairly stable over time, and the toys remained in the cages an average of 3.2 days. The durability of the toys was related to the type of toy (e.g., more flexible cloth and vinyl toys lasted longer than rigid plastic toys). The destructible toys were used significantly more often than other permanent cage toys or televisions. Toy use was not related to age, level of abnormal behavior, or use of existing permanent toys or television. The implications of the results were related to the management of an environmental enrichment program and indicated that the provision of flexible, inexpensive toys 1 at a time can be an effective method of enrichment for captive chimpanzees.     

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.     

Experimental evaluation of environmental enrichment of sea turtles

Although behavioral studies have been conducted at zoos and aquaria for years, documentation concerning the effectiveness of environmental enrichment has dealt primarily with terrestrial animals and marine mammals. Few enrichment studies have been conducted on reptiles. For this study, behavioral observations were made on four captive sea turtles (three loggerhead, Caretta caretta, and one blind green, Chelonia mydas) with enrichment present and absent. Enrichment devices were modified for the special needs of the blind turtle. Behaviors were classified as Resting, Pattern Swimming, Random Swimming, Focused Behavior, Aggression, Hiding, Orientation, and Noncategorized Behavior. It was hypothesized that, when enrichment was present, a decrease in Resting and stereotypic Pattern Swimming would be seen along with an increase in Random Swimming and Focused Behavior. It was found that, when no enrichment devices were present, 77% of the turtles' time was spent in Resting and Pattern Swimming. When enrichment devices were provided, 88% of their time was spent in Random Swimming and Focused Behavior with only 8% spent in Pattern Swimming and Resting. Statistically, there were significant increases in Random Swimming (three of the four turtles) and Focused Behavior (4/4) and significant decreases in Resting (3/4) and Pattern Swimming (3/4) when enrichment devices were present. These results suggest that environmental enrichment is as effective with marine reptiles as has been found with other animals and should be encouraged for all captive sea turtles. Zoo Biol 26:407–416, 2007. © 2007 Wiley‐Liss, Inc.     

Social and spatial relationships in captive southern white rhinoceros (Ceratotherium simum simum)

Although critical to the conservation of white rhinoceros, captive breeding has proven challenging because of the poor and irregular reproductive health of many captive rhinos, and social interactions may play a significant role. This research investigated the social and spatial relationships of two captive groups of southern white rhinoceros (Ceratotherium simum simum) by examining the frequency of companion changes, the number of space maintenance vocalizations made per hour by each reproductively mature female, and dominant/subordinate interactions. The observed captive rhinos did not change their companionships during the study. They exhibited space maintenance vocalizations and display greater than once per hour, particularly when feeding. Females housed with four calves on 0.033 km² exhibited space maintenance vocalizations more frequently (X±SE = 6.19±0.199/hr) than females housed with one calf and more space (0.06 km², X±SE = 0.55±0.182/hr) and females housed without calves and more space (0.65 km², X±SE = 1.90±0.086/hr). Wider separation of food piles and of females with young calves is suggested to reduce the interpreted spatial stress. The presence of a large number of rhinos in restricted captive space resulted in the formation of herds with dominance hierarchies that were enforced during competition for food and shade. The most subordinate rhino in each of the herds exhibited unusual behaviors such as dung‐kicking and nonestrus urine squirting, and neither has ever reproduced. Suppression of subordinate rhinos might lead to social stress that could negatively impact reproductive success. Zoo Biol 26:487–502, 2007. © 2007 Wiley‐Liss, Inc.     

Assessing the effects of cognitive experiments on the welfare of captive chimpanzees (Pan troglodytes) by direct comparison of activity budget between wild and captive chimpanzees

We investigated the effects of cognitive experiments by direct comparison of activity budgets between wild and captive chimpanzees. One goal of captive management is to ensure that the activity budgets of captive animals are as similar as possible to those of their wild counterparts. However, such similarity has rarely been achieved. We compared the activity budget among three groups of chimpanzees: wild chimpanzees in Bossou (Guinea, n = 10), and captive chimpanzees who participated in cognitive experiments (experimental chimpanzees, n = 6) or did not participate in the experiments (nonexperimental chimpanzees, n = 6) at the Primate Research Institute (Japan). The experimental chimpanzees voluntarily participated in computer‐controlled cognitive tasks and small pieces of fruits were provided as rewards. The data from captivity were obtained on the experimental days (weekdays) and nonexperimental days (weekends). In both study sites, we followed each chimpanzee from about 7 a.m. until the time when chimpanzees started to rest in the evening. The behaviors were recorded every 1 min. The results showed that on weekdays, feeding time and resting time of the experimental chimpanzees were almost the same as those of wild chimpanzees. However, for the nonexperimental chimpanzees, feeding time was significantly shorter and resting time was longer than those of the wild chimpanzees. In contrast, no difference was found in feeding time or resting time of the two groups of captive chimpanzees on weekends. The results suggested that the cognitive experiments worked as an efficient method for food‐based enrichment. Am. J. Primatol. 73:1231–1238, 2011. © 2011 Wiley Periodicals, Inc.     

Accurate measurement of body weight and food intake in environmentally enriched male Wistar rats

Laboratory animals are crucial in the study of energy homeostasis. In particular, rats are used to study alterations in food intake and body weight. To accurately record food intake or energy expenditure it is necessary to house rats individually, which can be stressful for social animals. Environmental enrichment may reduce stress and improve welfare in laboratory rodents. However, the effect of environmental enrichment on food intake and thus experimental outcome is unknown. We aimed to determine the effect of environmental enrichment on food intake, body weight, behavior and fecal and plasma stress hormones in male Wistar rats. Singly housed 5–7‐week‐old male rats were given either no environmental enrichment, chew sticks, a plastic tube of 67 mm internal diameter, or both chew sticks and a tube. No differences in body weight or food intake were seen over a 7‐day period. Importantly, the refeeding response following a 24‐h fast was unaffected by environmental enrichment. Rearing, a behavior often associated with stress, was significantly reduced in all enriched groups compared to controls. There was a significant increase in fecal immunoglobulin A (IgA) in animals housed with both forms of enrichment compared to controls at the termination of the study, suggesting enrichment reduces hypothalamo‐pituitary‐adrenal (HPA) axis activity in singly housed rats. In summary, environmental enrichment does not influence body weight and food intake in singly housed male Wistar rats and may therefore be used to refine the living conditions of animals used in the study of energy homeostasis without compromising experimental outcome.     

Preliminary investigation of social interactions and feeding behavior in captive group-housed Tasmanian devils (Sarcophilus Harrisii)

As the number of Tasmanian devils (Sarcophilus harrisii) in captivity increases, an understanding of captive social dynamics and behavior is becoming increasingly important. In the wild, devils are solitary, although sometimes, they congregate to feed on a large carcass. However, it is common to house devils in groups as a form of social enrichment. This study investigated how behavior at feeding time of captive Tasmanian devils varied in groups of different sizes. Observations were made of individually housed devils and devils in groups of two, three, five, and six, when presented with a carcass on which to feed. Total feeding duration ranged from 6.5 to 47.4 minutes per observation period (70 minutes). There was no significant interaction between feeding duration and group size during the experiment. Feeding duration varied daily and depended on carcass size. Social housing of Tasmanian devils enabled them to display dyadic and agonistic behaviors during feeding. Observing behaviors and learning from the outcomes of these interactions can improve husbandry techniques. Creating a captive environment that encourages natural behaviors may enhance survival in the wild following translocation.     

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.     

Behavioral and physiologic responses to environmental enrichment in the maned wolf (Chrysocyon brachyurus)

The ex situ population of maned wolves is not self‐sustaining due to poor reproduction, caused primarily by parental incompetence. Studies have shown that environmental enrichment can promote natural parental behaviors in zoo animals. The objective of this study was to determine the effects of environmental enrichment on behavioral and physiological responses of maned wolves. During an 8‐week experimental period, daily behavior observations and fecal sample collection were conducted on four adult wolves (2.2) individually housed in environments without enrichment. After 2 weeks, the wolves were chronologically provided with 2‐week intervals of hiding dead mice around the exhibit, no enrichment, and introduction of boomer balls. Responses of the wolves to enrichment were assessed based on activity levels and exploratory rates, as well as the level of corticoid metabolites in fecal samples collected daily throughout the study period. Providing wolves with environmental enrichment significantly increased exploratory behaviors (P<0.05), especially when mice were hidden in the enclosure. Fecal corticoid concentrations were increased during periods of enrichment in males (P<0.05), but not in females. Overall, there were no correlations between behavioral responses to enrichment and fecal corticoid levels. Behavioral results suggest that environmental enrichment elicits positive effects on the behavior of captive maned wolves. There is evidence suggesting that providing animals with ability to forage for food is a more effective enrichment strategy than introducing objects. There is need for a longer term study to determine the impact of environmental enrichment in this species. Zoo Biol 26:331–343, 2007. © 2007 Wiley‐Liss, Inc.     

Behavioral effects of enrichment on singly-housed,yearling rhesus monkeys: An analysis including three enrichment conditions and a control group

Three cohorts of yearling rhesus monkeys (Macaca mulatta) were maintained in single cages for one year as part of a derivation program to produce a breeding colony of specific pathogen-free (SPF) monkeys. During this year of social restriction, subjects were provided with three different types of environmental enrichment (physical, feeding, and sensory) to counteract the known effects of social restriction and to quantify the effects of these different conditions of enhancement on their behavior. Focal animal observations were conducted on enriched and control subjects for all cohorts. Enrichment conditions were presented in a different order to each cohort. Monkeys provided with enrichment spent significantly more time playing and less time self-grooming than did control monkeys in unenriched cages, suggesting that the overall enrichment program was of some benefit to the monkeys, because these changes in behavior were in species-typical directions. Among enriched subjects only, there were significant differences in the amount of time spent drinking, grooming, feeding, playing, exploring, and using enrichment across the three enrichment conditions. Both the physical and feeding enrichment conditions led to species-appropriate changes in behavior, therefore enhancing psychological well-being as some define it. Sensory enrichment was of little benefit. The first cohort was housed indoors, received less stimulation from the environment outside of the single cage, and used enrichment more than did the other two cohorts housed outdoors. This suggests that the external environment influences behavior in the single cage and that enrichment may be most effective for animals housed indoors. © 1995 Wiley-Liss, Inc.     

Objective evaluation of a behavioral enrichment device for captive chimpanzees (Pan troglodytes)

A quantitative evaluation was made of a food puzzle designed to be a behavioral enrichment device for captive chimpanzees. Subjects were two social groups of chimpanzees housed in semifree-ranging conditions at the University of Texas Science Park in Bastrop. Subjects used the device for a mean of 91.6 minutes after it was filled with peanuts. Group levels of agonistic interactions, displays, coprophagy, regurgitation, excessive grooming, and consumption of wood were not significantly altered by the use of the peanut box. However, the data indicate that some of these categories of behavior were significantly increased or decreased in individual animals. Although the food puzzle box appears to be a promising behavioral enrichment tool, the necessity of recognizing individual differences in response to environmental manipulations must be emphasized.     

Chemosensory enrichment as a simple and effective way to improve the welfare of captive lizards

Environmental enrichment has proven to be a useful and effective welfare tool in order to evaluate and enhance the well‐being of captive animals, but only when it is based on detailed knowledge of each species' natural behaviour. Chemoreception is fundamental to many aspects of reptilian biology; however, sensory enrichment with chemical stimuli has rarely been applied to reptiles. In this study, we evaluate the use of chemosensory enrichment as a method to enhance the welfare of Podarcis liolepis. For seven weeks, we exposed field‐caught males to scents from donor conspecific males collected on pieces of filter paper (i.e., “enriched” group, n = 18), and compared their behaviour to that of control males provided with unscented pieces of filter paper (n = 18). We measured the occurrence of normal (e.g., locomotion) and abnormal (escape attempts) behaviours each day for three weeks. In addition, we conducted two exploration tests and a visual barrier test. Compared to controls, enriched lizards showed a consistent long‐term decrease (29%–38%) in the occurrence of escape attempts. During exploration tests, enriched lizards spent less time performing escape attempts and devoted more time to perching than controls. As expected, both control and enriched lizards showed a reduction of time in locomotion and an increase in the time spent perching between the first and second exploration test, but these changes were significantly more pronounced for enriched animals. Taken together, our results suggest improved welfare of enriched animals, as they spent less time engaging in abnormal behaviours, more time in normal behaviours, and showed signs of faster habituation to a novel environment. Chemosensory enrichment is a relatively simple enrichment strategy that could potentially be applied to improve the welfare of a wide range of captive lizards, and reptiles at large.     

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.