Cage toys reduce abnormal behavior in individually housed pigtail macaques

As part of a behavioral intervention program that identifies and treats individual nonhuman primates exhibiting abnormal behavior, five individually housed pigtail macaques (Macaca nemestrina) were provided with multiple cage toys in an effort to reduce high levels of abnormal behavior. Ten 30-min observations of each subject were conducted during the baseline condition and again after novel toys were presented, both loose inside the cage and attached to the outside of the cage. The new toys were used during 27% of the observation time. Kong Toys were used most consistently by the macaques during the 5-week observation period. Significant decreases in abnormal behavior and cage-directed behavior, as well as significantly increased enrichment use, were evident after the toys were added. Several of the toys were destroyed quickly, and individual differences were evident in the levels of enrichment use and abnormal behavior. Providing multiple manipulable toys as enrichment for pigtail macaques was effective in reducing abnormal behavior and was an important part of an environmental enrichment program for monkeys who could not be housed socially.     

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.     

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.     

Terrestrial predator alarm vocalizations are a valid monitor of stress in captive brown capuchins (Cebus apella)

The vocal behavior of captive animals is increasingly exploited as an index of well‐being. Here we show that the terrestrial predator alarm (TPA) vocalization, a robust and acoustically distinctive anti‐predation vocal response present in many mammal and bird species, offers useful information on the relative well‐being and stress levels of captive animals. In a 16‐week experiment evaluating the effects of varying levels of physical environmental enrichment (control < toys < foraging box < foraging box and toys) in the cages of eight singly housed adult male brown capuchins, we quantified the 1) emission rate of TPAs, 2) proportions of normal and abnormal behavior sample intervals, and 3) fecal and plasma cortisol levels. Variation in TPA emission across the experimental conditions was significant. We found significant reductions in the mean TPA production rate by the group in the enriched (toys, foraging box, and foraging box and toys) compared to the control condition; pre‐ and post‐experimental conditions, however, did not differ from the control condition. Mean TPA production by the group was also significantly positively correlated to mean group levels of fecal cortisol and proportion of abnormal behavior sample intervals, and significantly negatively correlated to the average proportion of normal behavior sample intervals in the group. Based on group means, plasma cortisol levels were positively, but not significantly, related to increasing TPA rate. At the level of the responses of an individual subject, however, the covariation between the vocal and non‐vocal behavioral measures and the cortisol assays seldom attained significance. Nevertheless, the direction of the relationships among these parameters within individual subjects typically mirrored those correlations based on group means. At both the group mean and individual levels, our results are consistent with the interpretation that in conditions of low environmental enrichment the study subjects were more stressed, and therefore more reactive to the presence of a threatening terrestrial stimulus (human observer), than when in more enriched conditions. We suggest that protocols to evaluate the effectiveness of enrichment for captive species other than brown capuchins could also profitably exploit TPAs as a first‐line monitor or as corroboratory evidence of current well‐being. Zoo Biol 18:295–312, 1999. © 1999 Wiley‐Liss, Inc.     

The effect of housing and environmental enrichment on stereotyped behavior of adult vervet monkeys (Chlorocebus aethiops)

Little information is available on the response of vervet monkeys to different housing conditions or on the suitability of enrichment devices or methods for vervet monkeys. In this study, the authors evaluated the occurrence of stereotyped behavior in adult vervet monkeys under various conditions of housing and enrichment. The variables included cage size, cage level (upper or lower), enrichment with a foraging log, enrichment with an exercise cage and presence of a mate. The authors first determined the incidence of stereotyped behavior in captive-bred, singly housed adult female and male vervet monkeys. They then exposed monkeys to different housing and enrichment situations and compared the incidence of stereotyped behavior among the monkeys. The authors found that more females than males engaged in stereotyped behavior and that females, on average, engaged in such behavior for longer periods of time than males. Stereotyped behavior was most often associated with a small, single cage. The average amount of observed stereotyped activity in monkeys housed in a small cage was significantly lower when the monkeys had access to either a foraging log or an exercise cage. Stereotyped behavior was also lower in female monkeys that were housed (either with a male or without a male) in a larger cage. The least amount of abnormal behavior was associated with the largest, most complex and enriched housing situation. Males and females housed in cages on the lower level of two-level housing engaged in more stereotyped behavior than did monkeys housed in the upper level, regardless of the presence or type of enrichment provided.     

Effect of cage enrichment on the daily use of running wheels by Syrian hamsters

Institutional animal care committees may one day require for the welfare of captive hamsters more floor space and the introduction of tunnels and toys. As hamsters are popular animal subjects in chronobiological research, and as clock phase is usually measured through running wheel activity, it is important to determine what effect cage enrichment might have on daily wheel use. Here the daily number of wheel revolutions, the daily duration of the running activity phase, the phase relationship between lights-off and onset of running activity, and the free-running period of circadian activity rhythms were measured in Syrian hamsters, Mesocricetus auratus, housed in single cages or in multiple cages linked by tunnels and supplied with commercial wooden toys. Free-running periodicity was not affected by cage enrichment. In multiple-cage systems, there were fewer daily revolutions, shorter wheel-running activity phases, and delayed running activity onsets. These effects, however, were small as compared to interindividual and week-to-week variation. They were statistically significant only under a light:dark cycle, not in constant darkness, and only when interindividual variation was eliminated through a paired design or when the number of cages was increased to five (the maximum tested). Daily wheel use is thus affected by cage enrichment, but only slightly.     

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.     

Social buffering in adult male rhesus macaques (Macaca mulatta): Effects of stressful events in single vs. pair housing

Background The purpose of this study was to test whether long‐term pair housing of male rhesus macaques ameliorated negative responses to stressful events that can occur in the course of routine husbandry or research procedures. Methods Twelve singly housed individuals were videotaped during two potentially stressful events before and after social introduction into pairs. During each stressor, abnormal behavior and anxiety‐related behavior were quantified from videotape. Results When visually exposed to the restraint and anesthesia of other monkeys, subjects showed significantly reduced frequencies of abnormal behavior when pair‐housed in comparison to their reactions when housed singly. Noisy and disruptive conversation between technicians standing immediately in front of the subjects’ cage did not elicit the same reduction in abnormal behavior. Neither test showed a significant difference across housing settings for anxiety‐related behaviors. Conclusions These findings suggest that pair housing buffers adult male rhesus macaques against common stressors in the laboratory setting.     

Behavior, appetite, and urinary cortisol responses by adult female pigtailed macaques to cage size, cage level, room change, and ketamine sedation

Pigtailed macaques (Macaca nemestrina) and longtailed macaques (M. fascicularis) show behavioral, ecological, and possible temperament differences, and their responses to the laboratory environment might therefore be quite different. We tested pigtailed macaques under the same conditions that were investigated in a previous study with longtailed macaques, using the same comprehensive set of physiological and behavioral measures of stress. First, eight adult females' adaptation to a new room in regulation-size cages was monitored, and in the third week their responses to ketamine sedation were measured. Then they spent two weeks singly housed in each of four cage sizes (USDA regulation size, one size larger, one size smaller, and a very small cage). Half of the subjects were in upper-level cages and the remainder in lower-level cages for the entire study. Cage size, ranging from 20% to 148% of USDA regulation floor area, was not significantly related to abnormal behavior, self-grooming, manipulating the environment, eating/drinking, activity cycle, cortisol excretion, or biscuit consumption. Locomotion and frequency of behavior change were significantly reduced in the smallest cage, but did not differ in cage sizes ranging from 77% to 148% of regulation size. The only manipulation to produce an unequivocal stress response, as measured by cortisol elevation and appetite suppression, was ketamine sedation. Room change and cage changes were associated with minimal cortisol elevation and appetite suppression. Wild-born females showed more appetite suppression after room change than captive-born females. No differences were related to cage level. Pigtailed macaques strongly resembled longtailed macaques except they showed weaker responses to the new room and cage change, probably because the pigtails had spent more time in captivity. These findings support the conclusion that increasing cage size to the next regulation size category would not have measurable positive effects on the psychological well-being of two species of laboratory macaques.     

环境丰容对圈养灰鹦鹉日常行为的影响

于2008年1、2、6、7月通过改变食物投喂方式、给予玩具、在环境中增加带皮的树干等方式,对两只饲养于成都动物园的灰鹦鹉实施了丰容试验,观察了丰容前、后及丰容期间的行为.结果表明,灰鹦鹉的日常行为有10多种,其中发生最多的行为是休息行为,其次为观望行为以及梳理行为.统计分析表明,灰鹦鹉丰容试验中鸣叫、啃树皮的行为显著高于丰容前、后(P<0.05);丰容期间休息行为显著低于丰容前、后阶段(P<0.01).环境丰容增加了灰鹦鹉行为活动,同时还减少了咬毛、咬脚趾等不良刻板行为的发生,提高了展出效果.     

The effects of two novel objects on the behavior of singly caged adult rhesus macaques.

Six female and six male adult rhesus macaques were given sticks and nylon balls as an attempt at simple cage enrichment. A latin square design was used to compare behavior during separate 4-week periods with each object and during a control period with no object. Frequency and duration of 15 different behaviors were recorded. Resting was the most common activity which decreased slightly in duration when the stick or nylon ball was present (P less than 0.02). The mean duration of stick use was longer than that of the nylon ball (P less than 0.01). No other behaviors changed significantly, including the frequency of abnormal behaviors such as self-abuse, stereotypic acts, and bizarre postures. Generally, these objects were used infrequently and led to few changes in the behavior of singly-caged adult rhesus macaques. However, they did appear to stimulate activity for some individuals.     

Environmental enrichment for nonhuman primates: theory and application

Investigators have an obligation to promote the psychological well-being of nonhuman primates used in research. Considerable emphasis has been placed on providing nonhuman primates with enriched environments as a means to achieve this objective. A framework is provided that consists of a set of hypotheses about well-being, and the extent to which exposure to various enrichment devices and procedures actually promotes well-being is evaluated. Two hypotheses are concerned with fostering species-typical behavior: use (versus nonuse) of the enrichment, and whether use of enrichment helps normalize other aspects of the behavioral repertoire. Two additional hypotheses are concerned with abnormal behavior: whether currently existing enrichment lowers levels of abnormal behavior, and whether it prevents the behavior. This framework is applied to various enrichment strategies ranging from toys and foraging devices to social interaction. Most devices are used by nonhuman primates and thus constitute an important way to enrich the captive environment. However, enrichment devices vary as to their effectiveness in normalizing the behavioral repertoire and eliminating abnormal behavior. Only social contact satisfies the goal of promoting a wide variety of species-typical activities while at the same time reducing or preventing the development of abnormal behavior.     

Increased produce enrichment reduces trauma in socially‐housed captive rhesus macaques (Macaca mulatta)

Due to primate adaptations for sociality, captive rhesus macaques have optimal welfare and utility as a biomedical model when they can be maintained in outdoor social groups. As a despotic species; however, aggression can result in costly injuries and may result in temporary or permanent removal of specific individuals from social housing. Enrichment items, such as toys, climbing structures, and foraging material, are employed to keep captive animals occupied. We hypothesized that produce enrichment that requires more processing to extract may reduce socially‐derived injuries by keeping animals occupied. We tested the effects of additional weekly produce (corn‐in‐husk, whole melon, or whole squash) on trauma incidence in an outdoor social group of rhesus macaques across two distinct seasons (mating and birthing seasons) at the California National Primate Research Center. Aggression and status behavioral data, food resource use and proximity, and trauma incidence were collected over two 16‐week periods, with eight control and treatment conditions alternating biweekly. Mixed‐effects regression modeling was used to determine the best predictors of trauma risk and severe aggression at the group level and at an individual level. We found that food resource use was an important predictor of trauma risk at both group and individual levels; greater use of food resources reduced trauma risk. Produce enrichment did not; however, reduce severe aggression. We suggest that other captive social groups of rhesus macaques with high levels of trauma may benefit from supplemental produce enrichment that increases animal engagement with food resources.     

Pair housing for female longtailed and rhesus macaques in the laboratory: behavior in protected contact versus full contact

Pair housing for caged macaques in the laboratory generally allows unrestricted tactile contact but, less commonly, may involve limited contact via grooming-contact bars or perforated panels. The purpose of using this protected contact housing, which prevents entry into pair-mates' cages, typically is to accommodate research and management requirements. The study used behavioral data collected on 12 pairs of female longtailed macaques (Macaca fascicularis) at the Washington National Primate Research Center and 7 pairs of female rhesus macaques (Macaca mulatta) housed at the Tulane National Primate Research Center to assess the relative benefits of protected versus full protected contact. The study collected data in stable pairs housed first in protected contact followed by full contact. Species combined, the study found the presence of the panel was associated with lower levels of social grooming and higher levels of self-grooming, abnormal behavior, and tension-related behavior. Within species, only the protected- versus full-contact contrasts for abnormal and tension were statistically significant-and only for rhesus macaques. Results suggest that for female rhesus macaques, potential disadvantages or inconveniences of full contact should be balanced against the improved behavioral profile in comparison to protected contact. The use of protected contact among female longtailed macaques does not appear to require the same cost-benefit analysis.     

Environmental enrichment of brown capuchins (Cebus apella): Behavioral and plasma and fecal cortisol measures of effectiveness

No consensus exists about the quantity and variety of environmental enrichment needed to achieve an acceptable level of psychological well‐being among singly housed primates. Behavioral and plasma and fecal cortisol measures were used to evaluate the effectiveness of four levels of toy and foraging enrichment provided to eight wild‐caught, singly housed adult male brown capuchins (Cebus apella). The 16‐week‐long study comprised six conditions and began with a 4‐week‐long preexperimental and ended with a 4‐week‐long postexperimental period during which the subjects were maintained at baseline enrichment levels. During the intervening 8 weeks, the subjects were randomly assigned to a sequence of four 2‐week‐long experimental conditions: control (baseline conditions), toy (the addition of two plastic toys to each cage), box (access to a foraging box with food treats hidden within crushed alfalfa), and box & toy (the addition of two plastic toys and access to a foraging box). Behavioral responses to changes in enrichment were rapid and extensive. Within‐subject repeated‐measure ANOVAs with planned post hoc contrasts identified highly significant reductions in abnormal and undesirable behaviors (and increases in normal behaviors) as the level of enrichment increased from control to toy to box to box & toy. No significant behavioral differences were found between the control and pre‐ and postexperimental conditions. Plasma and fecal cortisol measures revealed a different response to changing enrichment levels. Repeated‐measure ANOVA models found significant changes in both these measures across the six conditions. The planned post hoc analyses, however, while finding dramatic increases in cortisol titers in both the pre‐ and postexperimental conditions relative to the control condition, did not distinguish cortisol responses among the four enrichment levels. Linear regressions among weekly group means in behavioral and cortisol measures (n = 16) found that plasma cortisol was significantly predicted by the proportions of both normal and abnormal behaviors; as the proportion of normal behaviors increased, the plasma cortisol measures decreased. Plasma cortisol weekly group means were also significantly and positively predicted by fecal cortisol weekly group means, but no behavioral measure significantly predicted fecal cortisol weekly group means. In sum, these findings argue strongly that access to a variety of toy and foraging enrichment positively affects behavioral and physiological responses to stress and enhances psychological well‐being in singly housed brown capuchins. Am. J. Primatol. 48:49–68, 1999. © 1999 Wiley‐Liss, Inc.     

The Use of Ice to Enrich the Environment of Pigs Housed Indoors

Pigs used in research are often housed in barren environments. The effects of ice as a simple enrichment tool for newly weaned pigs were investigated. Four replicates of 120 pigs were separated into 3 groups. One group was given free access to blocks of ice (ice group), another group had access to Classic Kong toys (Kong group), and a 3rd group did not receive any enrichment (control group). The behavior of each group was observed every 5 min from 08:00 hr to 12:00 hr during 4 consecutive days. Pigs were motivated to explore the ice blocks (4.85% ± 1.34) over the Classic Kong toys (2.03% ± 0.59). No differences in other behaviors were found between treatments. Ice is an effective and easy-to-replace enrichment device. Blocks of ice can be used as enrichment devices for pigs housed in research facilities.     

Pair Housing for Female Longtailed and Rhesus Macaques in the Laboratory: Behavior in Protected Contact Versus Full Contact

Pair housing for caged macaques in the laboratory generally allows unrestricted tactile contact but, less commonly, may involve limited contact via grooming-contact bars or perforated panels. The purpose of using this protected contact housing, which prevents entry into pair-mates' cages, typically is to accommodate research and management requirements. The study used behavioral data collected on 12 pairs of female longtailed macaques (Macaca fascicularis) at the Washington National Primate Research Center and 7 pairs of female rhesus macaques (Macaca mulatta) housed at the Tulane National Primate Research Center to assess the relative benefits of protected versus full protected contact. The study collected data in stable pairs housed first in protected contact followed by full contact. Species combined, the study found the presence of the panel was associated with lower levels of social grooming and higher levels of self-grooming, abnormal behavior, and tension-related behavior. Within species, only the protected- versus full-contact contrasts for abnormal and tension were statistically significant—and only for rhesus macaques. Results suggest that for female rhesus macaques, potential disadvantages or inconveniences of full contact should be balanced against the improved behavioral profile in comparison to protected contact. The use of protected contact among female longtailed macaques does not appear to require the same cost-benefit analysis.     

Effects of social and inanimate enrichment on the behavior of yearling rhesus monkeys

Certain types of inanimate environmental enrichment have been shown to positively affect the behavior of laboratory primates, as has housing them in appropriate social conditions. While social housing is generally advocated as an important environmental enhancement, few studies have attempted to measure the influence of social conditions on the effects of inanimate enrichment or to compare the relative merits of social and inanimate enhancements. In the present study, inanimate enrichment (predominately physical and feeding enhancements) resulted in increased species-typical behavior for socially restricted subjects. However, social enrichment (living in groups) appeared to be more beneficial for young rhesus monkeys, leading to increased species-typical activities and decreased abnormal activities. The behavior of one cohort of yearling rhesus monkeys (Macaca mulatta) housed in small peer groups was compared with the behavior of four yearling cohorts housed in single cages. Half the animals in each cohort received a three-phase enrichment program and the rest served as controls. Group-housed yearlings spent significantly more time feeding and exploring and significantly less time behaving abnormally, self-grooming, and drinking than did singly housed yearlings. Enriched subjects spent significantly more time playing by themselves, and significantly less time self-grooming and exploring than did controls. Among group-housed subjects only, there were no differences between enriched and control monkeys. Captive primates should be housed socially, whenever appropriate, as the first and most important step in an enrichment program, with the provision of inanimate enhancements being considerably less important. Limited resources for inanimate enrichment programs instead should be focused on those individuals who can not be housed socially. © 1996 Wiley-Liss, Inc.     

A review of environmental enrichment for kennelled dogs,Canis familiaris

Domestic dogs can be housed in a variety of confined conditions, including kennels, shelters and laboratories. Concern over the well-being of dogs housed in human care has prompted much research in recent years into the enrichment of environments for kennelled dogs. This paper highlights the findings and recommendations arising from this work. Two types of general enrichment method are discussed, namely animate (i.e. enrichment through the provision of social contacts with conspecifics and humans) and inanimate (i.e. enrichment through the provision of toys, cage furniture, auditory and olfactory stimulation). The benefits and, where relevant, possible disadvantages, to these various types of enrichment method are highlighted throughout.