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.     

环境丰容对笼养川金丝猴日常行为以及粪便皮质醇水平的影响

在笼养条件下,由于有限的空间和单调的笼舍结构,川金丝猴行为和生理指标发生变化,包括出现刻板行为和产生较高的粪便内应激激素。本论文旨在研究环境丰容对笼养川金丝猴日常行为以及粪便皮质醇水平的影响。于2013年8月1日至11月1日对杭州动物园内7只川金丝猴进行环境丰容后的行为观察。采用瞬时扫描法记录上午08:30-10:30和下午14:00-16：00的动物行为,并统计15种行为的发生频率。比较丰容前后每种行为的发生频率,结果表明环境丰容降低了川金丝猴的不活跃行为（P=0.021）和刻板行为（P=0.034）,增加了其活跃行为频率（P=0.018）。环境丰容后,动物表现出更多的攀爬（P = 0.012）、探究（P = 0.014）和环顾行为（P = 0.010）。粪便皮质醇激素的结果表明,除1只雄性个体激素上升外,其余6只个体的粪便皮质醇含量显著下降（P=0.028）。以上结果提示环境丰容可改善川金丝猴的福利状况。     

Frustrated appetitive foraging behavior, stereotypic pacing, and fecal glucocorticoid levels in snow leopards (Uncia uncia) in the Zurich Zoo

This study hypothesized that permanently frustrated, appetitive-foraging behavior caused the stereotypic pacing regularly observed in captive carnivores. Using 2 adult female snow leopards (Uncia uncia), solitarily housed in the Zurich Zoo, the study tested this hypothesis experimentally with a novel feeding method: electronically controlled, time-regulated feeding boxes. The expected result of employing this active foraging device as a successful coping strategy was reduced behavioral and physiological measures of stress, compared with a control-feeding regime without feeding boxes. The study assessed this through behavioral observations and by evaluating glucocorticoid levels noninvasively from feces. Results indicated that the 2 snow leopards did not perform successful coping behavior through exercising active foraging behavior or through displaying the stereotypic pacing. The data support a possible explanation: The box-feeding method did not provide the 2 snow leopards with the external stimuli to satisfy their appetitive behavioral needs. Moreover, numerous other factors not necessarily or exclusively related to appetitive behavior could have caused and influenced the stereotypic pacing.     

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.     

圈养马麝刻板行为表达与粪样类固醇激素的关系

2017年7月1日-8月31日及2018年6月1日-7月31日,在甘肃兴隆山保护区马麝繁育中心,采用焦点取样法和连续记录法进行了圈养马麝的刻板行为取样,采集同期粪样,并用放射免疫分析法（RIA）检测粪样中肾上腺皮质醇、睾酮及雌二醇激素的水平,分析了圈养马麝刻板行为表达与上述3种激素水平的关系。结果显示,展现刻板行为的圈养马麝的皮质醇水平（111.099 ± 16.231）ng/g略高于无刻板行为表达的马麝（95.640± 9.738） ng/g,差异未达显著（P> 0.05）;展现刻板行为雄麝的睾酮水平（135.900± 21.582）ng/g略高于无刻板行为的雄麝（108.182 ± 9.689） ng/g,差异也不显著（P> 0.05）;展现刻板行为雌麝的雌二醇水平（0.445 ± 0.116）ng/g显著低于无刻板行为雌麝（10.843 ± 1.142）ng/g（P< 0.05）。研究结果表明,圈养雄性马麝的刻板行为表达与其类固醇激素水平不相关;而雌麝的刻板行为表达与雌二醇分泌显著负相关,这与其繁殖及健康状况有关。在麝类驯养实践中,可将粪样类固醇激素水平（尤其是雌二醇）作为其受胁迫水平及行为健康的监测指标。     

The effects of physical characteristics of the environment and feeding regime on the behavior of captive felids

The behavior of captive felids is influenced by enclosure design and management regime. The behavior of nine felid species housed in 11 enclosures was recorded using instantaneous scan sampling. Stereotypic pacing was observed in 15 out of 19 individuals. Size of enclosure did not affect pacing behavior, but edges of enclosures were found to be used specifically for pacing behavior. Cats in relatively larger enclosures had a higher level of apparent movement, but only about 50% of enclosure space was used. Raised areas such as tree branches were found to be preferred sites in enclosures, particularly for observation of surroundings. The feeding regime was found to affect stereotypic pacing levels. Cats fed on a 3 day cycle paced more on fast days than on days they were fed. Although not statistically significant, 6 out of 7 of these cats paced more in the hour after feeding, whereas the cats fed daily paced more in the hour before feeding. Further research is required to understand the relationship between feeding and stereotypic behavior. Zoo Biol 16:71–83, 1997. © 1997 Wiley-Liss, Inc.     

Stereotypic behavior in wild marine carnivores?

Stereotypic behavior is observed in many species within zoological institutions. Attempts to reduce such behavior typically involve some form of environmental enrichment that provides opportunities for species appropriate behavior or some degree of control within the environment. However, environmental enrichment has never been completely successful in eliminating stereotypic behavior for an entire group of animals within a zoological facility. In the wild, stereotypic behavior is rarely observed. Documenting the occurrence of stereotypic behavior in the wild, and circumstances in which it occurs, could help provide insight into the causes of such behavior within zoological institutions. The following commentary details the observations of wild lemon sharks (Negaprion brevirostris) engaging in a stereotyped swimming pattern behind a research vessel north of Grand Bahama Island, Bahamas. We consider a possible explanation for the sharks' behavior and hope to stimulate conversation as well as increase examination of animal management routines in zoological facilities. Zoo Biol 30:365–370, 2011. © 2010 Wiley‐Liss, Inc.     

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.     

Failure of a chemical spray to significantly reduce stereotypic licking in a captive giraffe

The repetitive licking of nonfood substrates is a common stereotypic behavior in captive giraffes. In this study we attempted to reduce stereotypic licking in a Masai giraffe (Giraffa camelopardalis tippelskirchi) by applying a bitter chemical (marketed as a taste deterrent to prevent the unwanted licking and chewing of substrates) to the areas of the fence licked most frequently by the giraffe. We hypothesized that this treatment would reduce stereotypic licking. However, there were no significant overall changes in stereotypic licking following treatment with the chemical spray. Although licking of the treated area was observed to decrease, the behavior increased in nontreated areas. These results suggest that the underlying motivation driving the behavior was not affected by the aversive stimulus. Because stereotypic licking in giraffes may be based on a motivation to use their tongues in foraging, more effective techniques for reducing stereotypic fence‐licking in giraffes may include increasing feeding duration by increasing the quantity, processing time, or distribution range of food. Zoo Biol 22:601–607, 2003. © 2003 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.     

Tailored Enrichment Strategies and Stereotypic Behavior in Captive Individually Housed Macaques (Macaca spp.)

The welfare of nonhuman animals in captivity is widely dependent on the natural psychological, physical, and behavioral needs of the animals and how adequately these needs are met. Inability to engage in natural behaviors can lead to chronic stress and expression of stereotypic behavior. The majority of research on decreasing stereotypic behavior in captivity addresses problems at the group level and does not account for individual variability in each animal's needs, history, and preferences. This study combined physiological and behavioral measures of well being to comprehensively assess the unique needs of individually housed captive macaques (Macaca spp.) with the aim of developing tailored welfare strategies. Behavioral and hormonal data were collected under 2 conditions: baseline and individualized enrichment. The results showed a significant decrease in stereotypic behavior under the enrichment condition. Additionally, 7 out of 9 individuals showed a decrease in fecal glucocorticoid (stress hormone) levels, indicating a reduction in hypothalamic-pituitary-adrenal activity. Addressing welfare on an individual, rather than group, level allows for a better overall characterization of well being and maximizes the probability of improving the welfare of each animal.     

Technology at the Zoo: The Influence of a Touchscreen Computer on Orangutans and Zoo Visitors

A computer‐controlled touchscreen apparatus (hereafter referred to as “touchscreen”) in the orangutan exhibit at Zoo Atlanta provides enrichment to the animals and allows cognitive research to take place on exhibit. This study investigated the impact of the touchscreen on orangutan behavior and visibility, as well as its impact on zoo visitors. Despite previous research suggesting that providing a single computer system may negatively affect orangutan behavior, there was not a significant increase in aggression, stereotypic, or distress‐related behaviors following the activation of the on‐exhibit touchscreen. We also investigated the possibility that zoo visitors may be negatively affected by technology because it deviates from naturalism. However, we did not find a change in stay time or overall experience rating when the computer was turned on. This research was the first to assess visitor attitudes toward technology at the zoo, and we found that visitors report highly positive attitudes about technology for both animals and visitors. If subjects visited the exhibit when the computer was turned on, they more strongly agreed that orangutans benefit from interacting with computerized enrichment. This study is the first investigation of an on‐exhibit touchscreen in group‐housed apes; our findings of no negative effects on the animals or zoo visitors and positive attitudes toward technology suggest a significant value of this practice. Zoo Biol 31:27;–39, 2012. © 2011 Wiley Periodicals, Inc.     

Non‐invasive fecal hormone analysis and behavioral observations for monitoring stress responses in captive western lowland gorillas (Gorilla gorilla gorilla)

Non‐invasive techniques for monitoring the stress response in captive western lowland gorillas (Gorilla gorilla gorilla) were investigated. Fecal samples for cortisol measurement and concurrent behavioral data were collected from six individuals in a socially housed gorilla group (one adult male, three adult females and their three offspring) over a 7‐month period. Despite inter‐individual variation in the dynamics of fecal cortisol concentrations over time, several major secretory peaks coincided across individuals. High cortisol concentrations in feces were correlated with induced stressors or behavioral observations indicating high social tension, with a 1–2 day lag period. Entry progression order of the gorillas into a den complex and a supplant‐based dominance index were suitable indicators of overall dominance hierarchies, and fluctuations over time reflected periods of instability. Diurnal variation in fecal cortisol was not apparent when comparing afternoon and morning samples, however the sample collection interval was relatively short (3–5 hr). These results demonstrate the feasibility of monitoring stress responses based on the dynamics of both fecal cortisol excretion and behavior. This non‐invasive approach may be used for gauging responses to changes in husbandry, environment and group structure of captive gorillas. Zoo Biol 0:1–15, 2005. © 2005 Wiley‐Liss, Inc.     

Effects of construction noise on behavior and cortisol levels in a pair of captive giant pandas (Ailuropoda melanoleuca)

Studies of the effects of ambient noise on animals have found variable results. A study was conducted at the Smithsonian's National Zoological Park to determine what effect short‐term demolition work would have on the behavior and cortisol excretion of giant pandas. Behavioral and endocrine differences were examined during the presence and absence of demolition work being conducted on an adjacent exhibit complex. High frequency noise was significantly louder on work days compared to non‐work days. Panda activity budgets differed significantly between work and post‐work periods, although in different ways. The male's use of substrates and locations that might be associated with refuge or shelter changed during the study; the female did not show similar changes. He spent more time in the enclosure adjacent to the work site rather than a more distant enclosure during the demolition period whether work was occurring or not. The behavior of both animals was more often characterized as “restless” during, as opposed to before or after the work period. In general, cortisol excretion increased during the study in both animals but this was likely a seasonal effect in the male. In many cases, significant short‐term increases in cortisol were temporally associated with certain kinds of construction noises or specific physiological events. Variability in cortisol secretion fluctuated during the study for both animals but in differing patterns. These results demonstrate that demolition noise was associated with behavioral and some physiological changes in giant pandas, and these changes were individual‐specific. Zoo Biol 0:1–18, 2006. © 2006 Wiley‐Liss, Inc.     

Behavioral and adrenocortical responses to environmental changes in leopard cats (Felis bengalensis)

Indicators of environmental adequacy relevant to the well-being of small felids are developed by examining, in 4 captive leopard cats, interrelationships between behavioral and adrenocortical responses to changes in housing conditions. Singly housed cats were moved from their barren home cage (Cage 1, baseline) sequentially to 2 new, barren housing situations (Cages 2 and 3; ≈ 10 weeks/cage). Urinary cortisol concentrations, stereotypic pacing, and hiding frequencies were transiently increased for 1 week after translocation to Cage 2. After translocation to Cage 3, cortisol concentrations and hiding also were increased for the first week. However, conditions in Cage 3 were determined to be aversive to the cats, as evidenced by cortisol concentrations that remained chronically elevated for the entire 10-week period. Exploratory behavior was suppressed during this period. When Cage 3 was enriched with a complex of branches and hiding places, urinary cortisol concentrations and stereotypic pacing decreased, and exploration increased. Concealment locations that camouflage were more often used for lying down when urinary cortisol was elevated. These results suggest that reduced exploratory behavior is an indicator of chronic exposure to aversive environmental conditions. Stereotypic pacing may not necessarily increase when adrenocortical activity increases. The results also suggest that enrichment facilitates coping with aversive stimulation by providing behavioral options to confined felids. To promote the welfare of small felids, appropriate camouflaged hiding places should be provided and enrichment programs developed to stimulate exploratory behavior. © 1993 Wiley-Liss, Inc.     

Comparison of several types of enrichment for captive felids

Enrichment can increase the complexity of the captive environment and possibly enhance captive animals' well‐being by stimulating active behaviors and reducing stereotypical behaviors commonly seen in zoo felids. In this study, three different enrichment items were added to outdoor enclosures of felids at the Montgomery Zoo to test their effects on activity levels and stereotypic pacing. Bones, frozen fish, and spices (cinnamon, chili powder, and cumin) were presented over a 3‐month period to six species of felids: cheetah, cougar, jaguar, lion, ocelot, and tiger. Proportion of time spent engaging in active behaviors and stereotypic pacing were compared before, during, and after treatments. All treatments resulted in a significant increase in activity level from baseline (bones: +15.59%; frozen fish: +35.7%; spices: +12.38%). Effects of enrichment items on activity levels were not sustained 7 days after removal. Proportion of time spent pacing significantly decreased during presentation of spices (?21.25%) and frozen fish (?26.58%), but not with the addition of bones. However, only the effect of frozen fish on stereotypic behavior was sustained 7 days after removal of the enrichment item. In conclusion, bones, spices, and frozen fish are inexpensive and easy‐to‐administer enrichment items that may be used to increase active behaviors of captive felids. Zoo Biol 26:371–381, 2007. © 2007 Wiley‐Liss, Inc.     

The Effects of Husbandry Training on Stereotypic Pacing in Captive African Wild Dogs (Lycaon pictus)

To examine the effects of operant conditioning on stereotypic pacing in 3 female African wild dogs located at the Franklin Park Zoo in Boston, this study made recordings of pacing behavior immediately following individual sessions of husbandry training and 2 no-training conditions. The study found significant differences in the percentage of observations spent in stereotypic pacing behaviors for all 3 dogs among the 3 different conditions. The authors discuss the data in terms of the contribution of motivated tasks to the effects and the role of food deprivation in the expression of stereotypic pacing. The study suggests that even short periods of training may improve the African wild dogs' welfare by reducing stereotypic pacing following the conditioning sessions.     

黄金周游客干扰对圈养大熊猫应激影响初探

通过非损伤性手段,监测了"五一"黄金周期间北京动物园一雌一雄两只圈养大熊猫粪样中的皮质醇水平变化.结果显示,随着客流量的明显上升,雌雄个体粪样中的皮质醇水平均出现了明显的升高.其中雄性大熊猫粪样中皮质醇含量的变化与前一日的客流量存在显著性相关,而雌性个体粪样中的皮质醇水平则与前一日客流量存在极显著的相关性.     

Physiological and Behavioral Effects of Capture Darting on Red Colobus Monkeys (Procolobus rufomitratus) with a Comparison to Chimpanzee (Pan troglodytes) Predation

Understanding how human activities affect wild primates is critical to the design of effective conservation strategies. Despite this need, few studies have examined the physiological and behavioral effects of field research methods in the wild. Here, we examine how the stress response, i.e., fecal cortisol, and behavior of Ugandan red colobus monkeys (Procolobus rufomitratus) in Kibale National Park are affected by chemical immobilization and collaring, i.e., capture. We compare this anthropogenic stressor to a naturally occurring stressor: a chimpanzee (Pan troglodytes) predation attack. Two adult males had peak cortisol levels of 283 and 284 ng/g 2–3 d after capture, which were 190% and 182% above their baseline levels, i.e., the first sample taken immediately after capture, but these peak levels did not remain elevated. Using long-term data, i.e., 11 mo of data, we found no difference in fecal cortisol levels between 10 darted and collared individuals and 14 individuals living in the same social group that were not darted or collared. For the chimpanzee attack, peak fecal cortisol levels (147–211% above baseline) were recorded 1–4 d after the attack, but these levels also did not remain elevated for long. These data show that darting and collaring and a chimpanzee predation attempt caused an acute stress response, but neither leads to sustained elevated cortisol levels. Thus, in situations in which research contributes significantly to the conservation of primates and cannot be conducted noninvasively, capture darting appears to be a useful technique with minimal long-term effects as long as injury and mortality are avoided. However, we encourage researchers to make similar physiological and behavioral comparisons in other field studies using similar techniques to provide a better understanding of the effects of research practices on the stress physiology and social behavior of wild primates.     

Twenty-four hour activity budgets and patterns of behavior in captive ocelots (Leopardus pardalis)

Activity budgets of captive ocelots (Leopardus pardalis) were assessed from over 547h of observational data obtained from six ocelots; two females at the Dallas Zoo (Dallas, TX), two females at the Caldwell Zoo (Tyler, TX) and a male and female at the Fossil Rim Wildlife Center (Glen Rose, TX). Data were examined for the percentage of active behaviors exhibited during the day and nighttime hours; temporal patterns of active, pace, exploratory and marking behavior, and for significance in pacing behavior between pre- and post-feeding times. The captive cats had a bimodal pattern of active behavior similar to field studies of wild ocelots, except that the timing of the active peaks were closer to the diurnal hours for the captive cats. The captive ocelots were less active than wild ocelots, and more diurnal. Also, the captive cats exhibited stereotypic pacing. When the percentage of time of active behavior was assessed for each cat, a strong variation between individuals and institution was not seen. Pacing behavior was highest prior to the feeding times for the cats. In assessing patterns of behavior, peaks in marking and exploratory behavior in the cats did not occur at the same time as the peaks in active behavior. However, we did see institutional differences in the pattern of exploratory and marking behavior, which may have been influenced by differing management practices.