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.     

To hunt or not to hunt? A feeding enrichment experiment with captive large felids

It is often difficult to promote the successful performance of feeding behaviors in zoos, especially for carnivores. Feeding enrichment provides these opportunities and often improves behavioral indications of an animal's well‐being and the experience of the zoo visitor. The effectiveness of two different feeding enrichment techniques was evaluated on five subjects in two species of felids: African lions and Sumatran tigers. The activity budgets of each cat were compared before, during, and after enrichment, focusing on activity levels, frequency and variety of feeding behaviors, and occurrence of stereotypic behaviors. The presentation of live fish increased the variety and frequency of feeding behaviors, while presentation of horse leg bones increased the frequency of these behaviors. Fish reduced the tigers' stereotypic behavior from 60% of scans to 30% of scans on the day of presentation, and this change was maintained for 2 days following enrichment. Bone presentation also reduced stereotypic behavior and increased nonstereotypic activity in both species. Both of these techniques appear to have sustained effects on behavior lasting at least 2 days after presentation, which may indicate their ability to alter the animals' underlying activity patterns. Zoo Biol 22:189–198, 2003. © 2003 Wiley‐Liss, Inc.     

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.     

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.     

Individual Effects of Seasonal Changes,Visitor Density,and Concurrent Bear Behavior on Stereotypical Behaviors in Captive Polar Bears (Ursus maritimus)

Stereotypical behaviors in captive polar bears (Ursus maritimus) can be detrimental to their welfare. These behaviors can be reduced through enrichment programs but are often not completely eliminated, so identifying potential triggers is important. The present study investigated the influences of seasonal changes, visitor density, and concurrent bear activity on stereotypical behaviors exhibited by 3 captive polar bears at the Toronto Zoo. All bears exhibited these behaviors; however, individual differences were found in duration and form. The male exhibited less stereotypical behavior during spring, and the females exhibited less stereotypical behavior during winter. An increase in visitor density was associated with more stereotypical behavior in 1 female but less stereotypical behavior in the other 2 bears. All bears engaged in more stereotypical behaviors when the other bears were inactive, and 1 female engaged in more stereotypical behaviors when the other bears were out of sight. Further, when conspecifics were active, all bears engaged in less stereotypical behaviors. Given the variability among individual bears, future enrichment programs must be tailored to the needs of individuals to maximize efficacy.     

Environmental enrichment for zoo bears

The high incidence of stereotypic behaviors in zoo bears (van Keulen-Kromhout: International Zoo Yearbook 18:177–186, 1978) suggests that the environment of these animals lacks essential stimuli for guiding normal behavior. Three experiments investigated ways in which bear husbandry procedures can be altered to promote normal behavior. In experiments 1 and 2, honey-filled logs were given to a sloth (Melursus ursinus), American black (Ursus americanus), and brown bear (Ursus arctos) to determine 1) the role of food in stimulating investigatory behavior, 2) the rate of habituation to manipulable objects introduced into the exhibit, and 3) effects on locomotory behaviors. Results show specific and general habituation to the introduced objects that can be counteracted by refilling the logs with honey and by providing multiple logs in the exhibit. Investigatory activity directed toward honey-logs replaces pacing and walking in the sloth bear and is most effective in doing so when the log is novel. Experiment 3 examined the behavioral effects of feeding an American black bear in three different ways: 1) once daily in the den, 2) once daily with supplemental food from a mechanical feeder, and 3) once daily with food hidden in the exhibit in manipulatable objects. The latter method reduced stereotypic pacing from a median of 150 min/day to 20 min/day; the mechanical feeder method had no such effect. The results of a survey of 67 zoos concerning the diet and manner of feeding these three species of bears, as well as Asian black bears (Ursus thibetanus) are presented. Results are discussed with respect to the ways in which husbandry procedures can be improved to stimulate functional foraging and feeding behavior in confined bears.     

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.     

Effects of three food enrichment items on the behavior of black lemurs (Eulemur macaco macaco) and Ringtail Lemurs (Lemur catta) at the Henson Robinson Zoo, Springfield, Illinois

This study tested 3 food enrichment items mentioned in a laboratory primate newsletter with 6 adult Eulemur macaco and 3 adult Lemur catta to examine whether the items would affect the behavior of the lemurs. The results suggest that Food Enrichment Item 3 (a wire box filled with whole grapes, apples, or both hidden in straw hung from a branch within the enclosure) caused a significant decrease in the incidence of resting and a significant increase in the incidences of playing and grooming, with no significant effect on the incidence of feeding or foraging. The lemurs' behavior appeared to be most affected by the food enrichment item that required the most manipulation, closely followed by an enrichment that required a moderate amount of manipulation. The order of the exposure to the food enrichment items and the day of the week appear to have an attenuation effect on these behaviors and did affect the incidence of 3 stereotypic behaviors exhibited by a male L. catta such that 3 behaviors declined in occurrence as the study progressed.     

Food transfers in wild and reintroduced golden lion tamarins,Leontopithecus rosalia

We collected data from wild and reintroduced golden lion tamarins (Leontopithecus rosalia) to describe the behavior of donor and recipient during food transfers, evaluate the effect of supplemental feeding on food transfer behavior, and examine various hypotheses concerning the function of food transfers in primates. Behavioral observations were conducted on 12 groups of tamarins with young (N = 30) between the ages of 1 week and 1 year old. Results show that food transfers involve various behaviors, from steals by recipients to offers by donors; transfers mostly derive from adults and are directed at immature weaned young (between 3 and 9 months old); and that most items transferred were prey or fruits that require skill to process. Eleven percent of food transfers were preceded by an adult vocalization specific to that context, whereas 86% were preceded by conspicuous infant vocalizations and begging behavior. The most common vocalizations were loud and atonal (rasps) and broad banded frequency modulated (trills). Infants born to reintroduced parents vocalized less, whereas reintroduced adults vocalized more before transferring food than their wild counterparts. Reintroduced adults and young received more food transfers (4.4 per hr) than did wild‐born adults and young (2.2 per hr). Our findings suggest that food transfer in golden lion tamarins is best understood as provisioning of young that have not fully developed foraging skills to ensure they get the necessary resources for growth and survival. Am. J. Primatol. 48:305–320, 1999. © 1999 Wiley‐Liss, Inc.     

Stereotypic behavior in Asiatic black and Malayan sun bears

The stereotypies of individually caged Asiatic black bears (Ursus thibetanus) and Malayan sun bears (Helarctos malayanus) were studied in detail. Stereotypies were performed by 27 of the 29 subjects, were primarily locomotory in form (e.g., pacing), and occupied on average 18% (standard error of the mean (SEM)=2.5) of daylight hours. Stereotypy levels during the night were almost negligible and were highly correlated with daytime levels. Total stereotypies peaked prior to food arrival, although oral stereotypies were most frequent after feeding. In general, stereotypies were performed in locations from which food arrival could be viewed, although Asiatic black bears were equally likely to exhibit stereotypy near a neighboring bear. Across individuals, stereotypy frequency was inversely correlated with inactivity and increased with age. Older bears also showed less normal activity and a reduced diversity of normal behavior. Stereotypy levels were unrelated to levels of “compulsive” behavior (e.g., hair plucking) or repetitive self‐sucking–a potential deprivation stereotypy. More frequent stereotypies were performed more invariantly (i.e., were more predictable from one repetition to the next) and in more diverse contexts, namely 1) outside the pre‐feeding period, and 2) during the night. Contrary to observations reported elsewhere, higher frequencies of stereotypy were not associated with reduced behavioral diversity, or with a more elaborate repertoire of stereotypy forms and sequences. Although the two species did not differ in overall frequency, the stereotypies of sun bears appeared to be more food‐motivated than those of Asiatic black bears: the sun bears displayed a higher frequency and diversity of oral stereotypies, and higher levels of pre‐feeding stereotypy, and performed significantly more of their total stereotypies in locations from which they could view food arrival. This study demonstrates how analyzing stereotypies in detail can help identify the motivations that underlie these behaviors, and potentially reveal their degree of establishment–both of which are important factors in stereotypy treatment. Zoo Biol 23:409–430, 2004. © 2004 Wiley‐Liss, Inc.     

Long-Term Macroevaluation of Environmental Enrichment in Three Brown Bears (Ursus arctos) at Barcelona Zoo

The evaluation of enrichment programs is important to determine their effect on nonhuman animal welfare. The daily activity pattern and use of space of 3 brown bears (Ursus arctos) were used for long-term macroevaluation of enrichment to compare the baseline and enrichment phases. Focal sampling methods were used for data collection, and instantaneous scans were made at 2-min intervals during 15 sessions of 1 hr for each animal during the 2 study periods. The enrichment devices were categorized as feeding, occupational, and sensorial. The long-term macroevaluation in 3 bears showed statistically significant differences in some types of activity but not in others. There were also statistically significant differences for the use of space in 4 of the 8 zones in which the enclosures were divided. A more homogenous pattern in the use of space was only observed during the enrichment phase in the old female. The 3 brown bears followed different patterns concerning the enrichment program.     

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.     

The structure of feeding behavior in the colorado potato beetle,Leptinotarsa decemlineata (Coleoptera: Chrysomelidae)

Feeding behavior, in an ad libitum situation on potato plants in the laboratory, was continuously observed for approximately 7 h/day on 2 successive days for 18 adult femaleLeptinotarsa decemlineata. Additional behaviors were also recorded including resting, walking, biting, local movements, grooming, defecating, and regurgitating. These data were used to calculate a time budget for the various behaviors. The feeding data were analyzed to describe the structure of feeding for young adult females on their normal host plant. The criterion for a meal (minimum intermeal interval) was determined to be 286 s. This criterion was used to distinguish between intra- and intermeal interruptions in feeding for all subsequent analyses. Meals taken from leaves that were young, medium aged, or old did not differ, but on average beetles took 60% of their meals from young leaves. Meal size and meal duration were equally good predictors of when a meal would end. Feeding from stems was a prominent feature for most beetles. The stem meals had much longer durations than leaf meals, but stem feeding did not affect subsequent leaf feeding. The structure of feeding by these beetles is compared with that found in other insects, especiallyLocusta migratoria.     

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.     

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.     

丰容对圈养雌性岩羊活动时间分配的影响

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

高海拔地区昆明野生动物园大熊猫春季刻板行为探究

2011年2月26日～5月2日,在高海拔地区昆明云南野生动物园,采用连续记录法(Continuous recording) 和焦点动物取样法(Focal animal sampling)记录与分析了3只亚成年雌性大熊猫昼间刻板行为发生频次和持续时间,并就温度、游客流量与刻板行为发生的相关性进行了初步探讨.结果表明,大熊猫刻板行为发生频次(次·h-1)高峰和持续时间( min·h-1)较长的高峰均出现在10:00～11:00和16:00～17:00,各时段行为表达水平存在极显著差异(x2=61.183,P＜0.01;x2 =56.470,P＜0.01).个体间刻板行为持续时间昼间分布无显著差异(x2=3.185,P＞0.05);个体间发生频次在14:00～15:00时段存在显著差异(x2=7.796,P＜0.05),而在其他时段则存在极显著差异(x2=11.536 ～20.212,P＜0.01).温度与刻板行为发生频次、持续时间均无显著相关性(rx=-0.067,P＞0.05;rs=-0.012,P＞0.05);游客流量与持续时间、发生频次有一定的正相关,但不显著(rs =0.187,P＞0.05;rs=0.159,P＞0.05).此外,在刻板行为型时间分配格局中,以刻板踱步最高,占56.78％,其次为爬笼、吮掌,而旋转、摇摆及坐着旋转等其他刻板行为表现较少,其总和仅占1.20％.     

食物丰容对圈养猩猩行为的影响

于2007年2～4月对成都动物园圈养猩猩"铁里"进行了两个食物丰容试验,即用PVC+轮胎和圆木+轮胎试验,每期8 d,观察和记录了猩猩在丰容试验前、后以及两种丰容方式中的各种行为发生次数.结果 表明食物丰容有效地恢复了圈养猩猩的多种摄食行为,增加了猩猩的运动相关行为,减少了休息相关行为;但对刻板行为的影响不明显.     

Behavioral stereotypy in old and young rhesus monkeys

Four old (25 years) and six young (3 years) female rhesus monkeys (Macaca mulatta) were observed individually in a laboratory cage with either an old or a young monkey present as a social partner. The behavioral repertoire was coded into ten mutually exclusive and exhaustive categories. An information analysis of the individual behavior records is presented along with subject and partner age effects on the frequency of bouts and the amount of time spent in each category of behavior. Knowledge of the relative frequencies of the behaviors tells more about the behavior of young than old monkeys; and knowledge of the preceding behavior tells more about the behavior of old than young monkeys. Further, knowledge of the relative frequencies tells more about the behavior of both old and young monkeys with junior or elder partners than with age peers; whereas knowledge of the preceding behavior is more informative for old monkeys than for young ones regardless of the partner's age. Both old and young engaged in more affiliative behaviors with age peers than with junior or elder partners. An hypothesis is proposed which relates this social homophyly to the age difference in behavioral stereotypy.     

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.