Article

About pace: How variations in method and definition affect quantification of pacing in bears?

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Abstract

Repetitive pacing behavior is exhibited by many species in zoos and is particularly prevalent in carnivores with large home ranges, such as bears. Pacing can be a behavioral indicator of poor welfare, however, understanding this behavior can be challenging. As many bears that pace are singly housed, efforts to systematically examine and ameliorate pacing may be strengthened by multi-institutional studies. However, there is currently no standardized method to quantify pacing, which makes cross-institutional analyses of causal factors and intervening measures challenging. The purpose of this study was to compare multiple sampling methods and definitions for quantifying pacing in bears to understand how they affect outcome measures. We analyzed video recordings of two grizzly and two black bears pacing, using three sampling methods (continuous, instantaneous 30-s interval, instantaneous 1-min interval), and three definitions of pacing (AB—two repetitions of the path, ABA—three repetitions, ABAB—four repetitions). A generalized linear mixed model revealed that continuous and instantaneous 30-s interval methods captured more pacing than instantaneous 1-min methods, and definitions captured a decreasing amount of pacing from AB to ABA to ABAB. AB also captured the highest number of pacing bouts. The importance of comparability across institutions is growing, and a standard methodology and definition for recording pacing would be useful. We suggest that the combination of instantaneous sampling and the ABA definition presents a good balance between capturing the right data and being flexible enough for a variety of institutions to implement. Research Highlights • We found that different sampling methods and definitions used to observe pacing in bears do affect the amount of pacing behavior recorded. • We recommend using instantaneous sampling and the ABA definition of pacing for bear behavior studies.

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This book is comprised of 11 chapters generally discussing different perspectives of stereotypic behaviour in man and animals. The chapters are divided into 3 parts (normal animal and abnormal environment, stereotypic behaviours as pathologies and treating stereotypic behaviours). The first chapter reviews the extent and nature of research into stereotypic behaviour. Chapters 2-4 (part I) focus on the ethological perspective. Behaviour is discussed, including stereotypies, in terms of its motivated basis (stereotyping subjects are normal animals responding in species-typical ways to an abnormal environment). Chapters 5-8 (part II) emphasize clinical psychology, psychiatry and neuroscience. Three assumptions are presented: stereotypies of focus are the products of dysfunction (animal is abnormal); fullest understanding of stereotypies will come from investigating the neurophysiological mechanisms involved; and processes involved at this level have great cross-species generality. Part III (chapter 9 and 10) illustrates how stereotypies can be tackled and reduced by those concerned about their unaesthetic appearance and/or welfare implications. Chapter 11 provides a synthesis of the book and future research and suggestions on how terminology can be improved.
Article
A current focus of zoo-based research aims to identify indicators of animal welfare. Reliable behavioral indicators of welfare are highly desirable as behavioral observation is non invasive and requires little in the way of specialized equipment and other costly resources—save for observer time. Anticipatory behavior is an indicator of an animal's sensitivity to reward and as such, it is a real-time indicator of animals' own perceptions of their well-being. In fact, anticipatory behavior may generate a positive affective state and thus be at least a brief manifestation of good welfare itself. The husbandry conditions of most captive animals are such that food acquisition and other positive outcomes are highly scheduled and easily signaled. These conditions promote the development of anticipatory behavior, yet little research has either documented or interpreted this behavior in zoo and aquarium animals. This commentary suggests that anticipatory behavior could be a useful tool for assessing welfare and calls upon zoo and aquarium researchers to begin to develop this tool by describing the behavior and the circumstances that lead to its modulation. Zoo Biol. XX:XX–XX, 2014. © 2014 Wiley Periodicals Inc.
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Captive bears are prone to developing dental pathology for reasons including longevity in captivity, inappropriate diet, trauma, and stereotypical bar biting. If not detected, this can cause pain and suffering, with negative welfare consequences. As animals cannot verbally express feelings, objective methods are required to detect pain. Some methods of pain assessment can be invasive and impractical but behavioural observations offer a non-invasive alternative. Behavioural assessment for the detection of pain has been described in some domestic species but little published research has applied this to wild animal species. Eight Malayan sun bears (Helarctos malayanus) required dental extractions under anaesthesia. Their behaviour was observed, alongside a control cohort with no visible disease, pre-operatively and at one, two and four weeks post-operatively, when it was assumed the pain had resolved from the original pathology and surgery performed. Behavioural indices measured included general activity, social behaviours, stereotypies, eating-related behaviours and oro-facial behaviours hypothesised to be affected by dental pain. Bears that had received treatment took significantly longer to eat hard sugarcane pre-operatively compared to four weeks post-operatively, and took longer to eat soft porridge one week post-operatively compared to four weeks post-operatively. Untreated bears tended to be more active outdoors one week post-operatively compared to the treatment cohort. Results suggest that using hard foods and assessing the duration of eating behaviours could be useful to indicate dental pain in sun bears. General behavioural assessment of dental pain in sun bears is unlikely to be effective as a single diagnostic tool, but may be combined with other methods of assessment, and further research into this area is warranted.
Article
Although captive bears are popular zoo attractions, they are known to exhibit high levels of repetitive behaviors (RBs). These behaviors have also made them particularly popular subjects for welfare research. To date, most research on ursid welfare has focused on various feeding methods that seek to increase time spent searching for, extracting, or consuming food. Prior research indicates an average of a 50% reduction in RBs when attempts are successful and, roughly, a 50% success rate across studies. This research focused on decreasing time spent in an RB while increasing the time spent active by increasing time spent searching for, extracting, and consuming food. The utility of timed, automated scatter feeders was examined for use with captive grizzly bears (Ursis arctos horribilis). Findings include a significant decrease in time spent in RB and a significant increase in time spent active while the feeders were in use. Further, the bears exhibited a wider range of behaviors and a greater use of their enclosure.
Article
Polar bears are known to exhibit repetitive pacing behaviors, usually described as stereotypic, in zoo environments. However, little quantitative information exists about the prevalence of pacing in the zoo population. Similarly, large, multi-institutional studies conducted to determine the relationship between stereotypic behavior in zoo polar bears and environmental/husbandry variables using corticoids as a measure of stress are lacking. The study reported here includes data from 55 bears housed in 20 North American zoos. Individual and zoo characteristics were collected and behavior and fecal glucocorticoid metabolites were measured over a one-year period. Using an epidemiological approach, individual and facility level multiple linear regression models were constructed to determine the nature, strength and significance of environmental/husbandry variables and temperament (measured using a standardized novel object behavior test) on stereotypic pacing and corticoids. We found zoo polar bears performed stereotypic pacing behavior during 11% of the day; the rate rose to 23% when expressed as a percentage of time engaged in locomotor behavior. However, considerable variation in rate of stereotypy was observed. Variables associated with reduced pacing at zoos were: enrichment, number of bears in the group, bear’s having a view out of their exhibit, and presence of a positive reinforcement training program. Among individuals, bear’s whose temperament measured high on the “interest” axis (defined in terms of behavior directed toward the novel object) tended to display less stereotypic behavior and those that scored high on the “slow to approach” axis displayed more pacing. We found higher fecal glucocorticoid levels were associated with higher rates of stereotypic pacing and smaller dry land exhibit area. These results support other studies suggesting polar bears are particularly prone to stereotypic pacing behavior in zoos and that there is a link between stress (measured as fecal glucocorticoids) and pacing in zoo polar bears. These findings also suggest that some easily available tools, namely environmental enrichment and positive reinforcement training, can effectively reduce the incidence of these behaviors. Exhibit designers should take note that providing bears with a view out of their exhibit and larger land areas are associated with both behavioral and physiological benefits. Finally, certain temperaments are associated with elevated levels of both stereotypic behavior and corticoids. This information may provide a tool for proactively identifying the individuals most likely to develop pacing behaviors and providing appropriately enhanced care before the behavior becomes established.
Article
A 12-year-old, male, brown bear (Ursus arctos) named Abdi exhibited stereotypical pacing behavior. He was kept as a pet for 10 years by local villagers, then he was rescued and taken to the Karacabey Bear Sanctuary in July 2001. His physical condition was extremely poor. Because he had never lived with other bears, he was terrified and refused to integrate with them. After 6 months he was healthy physically but observations by the keepers indicated that he was pacing all day. He was treated with fluoxetine (0.62 mg/kg orally every 24 hours) for 6 months, and had been observed totally for 18 months. After stereotypy ceased completely, he was transferred to the large naturalistic enclosure and did not show any stereotypical behavior during the subsequent observation period (1 year). He was treated successfully using a combination of fluoxetine, the provisioning of extra space, and the addition of novel stimulation in a naturalistic enclosure. The space and stimulation could be sufficient to mimic the therapeutic effect of the pharmacological therapy in the long term.
Article
This paper summarises recent findings on the causation of stereotypic behaviours and other abnormal repetitive behaviours (ARBs) in captive animals: primarily motivational frustration and/or brain dysfunction, with possible contributory roles also being played by habit-formation and ‘coping’ effects. We then review the extent to which ARBs occur in zoos and similar, estimating that at least 10000 captive wild animals are affected worldwide. We argue for ‘zero tolerance’ of such ARBs, because stress and poor welfare raise ethical issues, while abnormal behavioural phenotypes and possibilities of impaired brain development challenge both the indirect (e.g. educational) and the direct, intrinsic conservation value of affected animals. We then consider five potential means by which ARBs may be tackled: genetic selection; pharmacological treatment; the reinforcement of alternative behaviours; punishment; and environmental enrichment. All except punishment have potentially useful roles to play, but enrichment is the preferred approach: it is most likely to tackle the problems underlying stereotypic behaviours, and thence to improve both welfare and behaviour with few unwanted side-effects. Nevertheless, in zoos, environmental enrichment to date has only had partial success, with no study managing to abolish ARBs in all its subjects—suggesting either that the enrichments currently being used are never quite optimal, or that by the time they are tackled, ARBs have become resistant to change. We suggest some ways in which the effectiveness of enrichments may be enhanced; propose that certain properties of ARBs may usefully help evaluate their likely ‘treatability’; and emphasise that if improving welfare is more important than just reducing ARB, then additional measures are needed in order to first, reliably identify those individuals most at risk from poor welfare, and then, to fully evaluate the welfare impact of enrichments. This paper also emphasises, with examples, the enormous potential value of zoo-derived data for helping understand how taxon, ecological niche, rearing history, and current housing together affect animals’ responses to captivity.
Article
In captivity, some species often seem to thrive, while others are often prone to breeding problems, poor health, and repetitive stereotypic behaviour. Within carnivores, for instance, the brown bear, American mink and snow leopard typically adapt well to captivity and show few signs of poor welfare, while the clouded leopard and polar bear are generally hard to breed successfully and/or to prevent from performing abnormal behaviour. Understanding the fundamental source of such differences could enable reproductive success and behavioural normalcy to be improved in zoos and breeding centres, by increasing the appropriateness of the enclosure designs and environmental enrichments offered particular species, and by allowing these to be offered pre-emptively instead of reactively. Here, we demonstrate that a significant proportion of the variation in apparent welfare between captive carnivore species stems from specific aspects of natural behaviour. We tested pre-existing hypotheses that species-typical welfare is predicted by natural hunting behaviour, general activity levels, ranging, or territorial patrolling (all activities that are constrained in captivity), by collating data on median stereotypy levels and infant mortality for multiple captive species, and then regressing these against median values for the relevant aspects of natural behavioural biology (e.g. hunts per day, proportion of flesh in the diet, home-range size, etc.). Our results revealed that instead of relating to foraging (e.g. hunting), as often assumed, carnivore stereotypy levels are significantly predicted by natural ranging behaviour (e.g. home-range size and typical daily travel distances). Furthermore, naturally wide-ranging lifestyles also predicted relatively high captive infant mortality rates. These results suggest that enclosure designs and enrichments focussing on carnivores’ ranging tendencies (e.g. providing more space, multiple den sites, greater day-to-day environmental variability/novelty, and/or more control over exposure to aversive or rewarding stimuli) could be particularly effective means of improving welfare; and also, that targeting such enrichment programmes on wide-ranging species, before problems even emerge, might effectively pre-empt their development. Alternatively, species with relatively small ranges could instead be made the focus of future collections and breeding programmes, zoos phasing out wide-ranging carnivores in favour of those species inherently more suited to current or readily achievable enclosure sizes and enrichment regimes.
Article
Seven major types of sampling for observational studies of social behavior have been found in the literature. These methods differ considerably in their suitability for providing unbiased data of various kinds. Below is a summary of the major recommended uses of each technique: In this paper, I have tried to point out the major strengths and weaknesses of each sampling method. Some methods are intrinsically biased with respect to many variables, others to fewer. In choosing a sampling method the main question is whether the procedure results in a biased sample of the variables under study. A method can produce a biased sample directly, as a result of intrinsic bias with respect to a study variable, or secondarily due to some degree of dependence (correlation) between the study variable and a directly-biased variable. In order to choose a sampling technique, the observer needs to consider carefully the characteristics of behavior and social interactions that are relevant to the study population and the research questions at hand. In most studies one will not have adequate empirical knowledge of the dependencies between relevant variables. Under the circumstances, the observer should avoid intrinsic biases to whatever extent possible, in particular those that direcly affect the variables under study. Finally, it will often be possible to use more than one sampling method in a study. Such samples can be taken successively or, under favorable conditions, even concurrently. For example, we have found it possible to take Instantaneous Samples of the identities and distances of nearest neighbors of a focal individual at five or ten minute intervals during Focal-Animal (behavior) Samples on that individual. Often during Focal-Animal Sampling one can also record All Occurrences of Some Behaviors, for the whole social group, for categories of conspicuous behavior, such as predation, intergroup contact, drinking, and so on. The extent to which concurrent multiple sampling is feasible will depend very much on the behavior categories and rate of occurrence, the observational conditions, etc. Where feasible, such multiple sampling can greatly aid in the efficient use of research time.
Article
We estimate that stereotypies are currently displayed by over 85 million farm, laboratory and zoo animals worldwide. This paper investigates their reliability as welfare indicators, by surveying studies relating stereotypy to other welfare measures and by analysing the mechanisms underlying this behaviour. Where data exist, most (approximately 68%) situations that cause/increase stereotypies also decrease welfare. Stereotypy-eliciting situations are thus likely to be poor for welfare, although exceptions exist. Within such an environment, however, most (approximately 60%) accounts link individual stereotypy performance with improved welfare (cf approximately 20% linking it with reduced welfare). Thus, in a sub-optimal environment, non-stereotyping or low-stereotyping individuals could well have the poorest welfare, although again exceptions exist. Examining the mechanisms underlying stereotypy performance, we discuss four processes that could account for these complex links between stereotypy and welfare. Beneficial consequences from performing the specific source-behaviour of the stereotypy ('do-it-yourself enrichment'), or arising from repetition per se ('mantra effects'), may ameliorate welfare in poor environments. In addition, stereotypies that have become centrally controlled (habit-like), or that arise from autistic-like changes in the control of all behaviour (perseveration), are likely to be unreliable indicators of current state because they can be elicited by, or persist in, circumstances that improve welfare. To refine the role of stereotypy in welfare assessment, we suggest the collection of specific additional data to reveal when any of these four processes is acting. Until such research increases our understanding, stereotypies should always be taken seriously as a warning sign of potential suffering, but never used as the sole index of welfare; non-stereotyping or low-stereotyping individuals should not be overlooked or assumed to be faring well; simple measures of frequency should not be used to compare stereotypies that differ in age, form, or the biological or experiential characteristics of the performing animal; enrichments that do not immediately reduce stereotypies should not be assumed failures with respect to welfare; and finally, stereotypies should not be reduced by means other than tackling their underlying motivations.
Article
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.
Article
Behavioral and hormonal data were compared for four giant pandas in two management conditions: (1) panda confined to exhibit area and (2) panda given choice to move freely between exhibit and off-exhibit bedroom areas. Pandas displayed fewer signs of behavioral agitation and lower urinary cortisol in the free choice condition. Time active did not differ between the two conditions. These results suggest that simply offering pandas free access to alternative locations can improve behavioral and hormonal variables that may be related to well-being. Zoo Biol 0:1–7, 2005. © 2005 Wiley-Liss, Inc.
Article
In the present study we compared 33 enclosures in 28 parks, with a total of 66 bears. We chose direct observation of behaviour rather than surveys. Each enclosure was observed during one day; stereotypies and social relationships were qualitatively noted in types and amount. The connections of behaviour with bears characteristics and types of management were established. Young bears exhibited fewer stereotypies than adult ones, especially if these adults were kept indoor at night. Contrary to stereotyped pacing and circling, head-tossing was more frequent in young subjects. Occurrences of stereotypical behaviour were more numerous during the afternoon, especially if animals received a single main feed in the evening. Whereas circling was observed only in bears kept with related fellows, pacing was more frequent when they were kept with unrelated. Neither social isolation nor sex did influence stereotypies. Keeping more than two bears together was a source of social conflict. These results suggest some recommendations for housing and management of captive brown bears. # 2004 Elsevier B.V. All rights reserved.
Article
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.
Article
The behaviour of a male American black bear Ursus americanus was observed for over 2400 h across all seasons of the year. Stereotypic pacing was most frequent, oriented away from the exhibit, and performed mainly after feeding during the period May–July; from August–November pacing was oriented towards the exhibit and performed mainly around feeding time. Placing bear odors in the enclosure slightly reduced pacing and increased exploring/foraging in the late spring. Hiding small food items in the exhibit almost completely eliminated pacing in the fall and replaced it with foraging. Comparison with seasonal changes in the behaviour of wild bears suggest that the stereotypy of this bear, and probably zoo bears in general, developed from two main primary behaviours that cannot be performed in a barren zoo environment: mate-seeking behaviour predominating in the late spring and foraging behaviour in the late summer and fall.
Article
The benefits to captive animals of environmental enrichment (EE) are widely recognized. Few studies have, however, studied how to maximise the effect of EE. One issue with EE programs seems to be habituation to the enrichment device. To study the effect of habituation to EE, 14 captive sloth bears (Melursus ursinus) were subjected to two different EE treatments. Treatment one presented EE (logs with honey containing holes) for five consecutive days, whereas treatment two presented EE on intermittent days for five days. Intermittent presentations tended to reduce habituation toward the EE. Both consecutive and intermittent presentations significantly reduced stereotypies; however, the consecutive presentations had a longer-lasting effect. Explorative behaviors increased in both treatments, consistent with earlier findings that EE increase levels of natural behaviors. Other behaviors were unaffected by the EE presentations. The results show that intermittent presentation of EE objects may secure the interest of the animals, but continuous access to enrichment may be more efficient in reducing stereotypies in the long run.
Article
We conducted a brief study of the effectiveness of environmental enrichment for a polar bear at the Bronx Zoo with two objectives in mind. First we wanted to determine if a novel method of collecting data that easily fits into a zookeeper's work routine would produce usable data and if so, we wanted to evaluate the effectiveness of some new items that had been purchased for enriching the polar bear in reducing his pacing behavior. Observations were recorded for 119 days over a period of 5 months from April 2007 through August 2007. Five new items and eight previously used items were rotated and presented to the polar bear in the morning and afternoon. We recorded the bear's behavior five times per day as we passed by his exhibit during our regular work routine. Predictably, we found that the newer enrichment items were more effective at increasing play and decreasing pacing, as well as other more subtle effects on his behavior that helped us to design a better enrichment routine. More importantly, we found that this method of "multi-point scan sampling" was effective at producing ample and reliable data that could be used to analyze the bear's behavior without adding significant work to the keepers' daily routine.
Article
This paper proposes a regression model where the response is beta distributed using a parameterization of the beta law that is indexed by mean and dispersion parameters. The proposed model is useful for situations where the variable of interest is continuous and restricted to the interval (0, 1) and is related to other variables through a regression structure. The regression parameters of the beta regression model are interpretable in terms of the mean of the response and, when the logit link is used, of an odds ratio, unlike the parameters of a linear regression that employs a transformed response. Estimation is performed by maximum likelihood. We provide closed-form expressions for the score function, for Fisher's information matrix and its inverse. Hypothesis testing is performed using approximations obtained from the asymptotic normality of the maximum likelihood estimator. Some diagnostic measures are introduced. Finally, practical applications that employ real data are presented and discussed.