Kathy Carlstead

Behavioral and physiological correlates of stress in laboratory cats

Abstract Sixteen domestic cats were used to investigate the pituitary-adrenal, pituitary-gonadal and behavioral consequences of an unpredictable handling and husbandry routine. After a 10-day baseline period of standard laboratory procedures, eight cats (‘stressed cats’, STR) were subjected to a 21-day period of altered caretaking characterized by irregular feeding and cleaning times, absence of talking and petting by humans, and daily unpredictable manipulations. Eight control cats (CON group) were maintained for 21 days on the standard caretaking schedule. Behavior was recorded on time-lapse video 24 h day −1 , urine was collected daily for cortisol analyses, and hormone stimulation tests with synthetic adrenocorticotropic hormone (ACTH) and luteinizing hormone-releasing hormone (LHRH) were conducted before and after the 3-week treatment period. Results indicate that the STR cats were chronically stressed by the altered caretaking routine. Urinary cortisol concentrations were consistently elevated throughout the 3-week period, adrenal sensitivity to ACTH was enhanced and pituitary sensitivity to LHRH was reduced. Active exploratory and play behavior was suppressed, and STR cats spent more time awake/alert and attempting to hide. Hiding was negatively correlated with cortisol concentration and, therefore, may be an important behavior for coping with uncontrollable and unpredictable captive environments. These results indicate that qualitatively poor caretaking is a potent psychological stressor for confined cats that may eventually compromise reproduction through behavioral or physiological mechanisms. To promote well-being, caged cats should be provided with appropriate places for concealment.

Black rhinoceros (Diceros bicornis) in U.S. zoos: I. individual behavior profiles and their relationship to breeding success

2 Disneys Animal Kingdom, Lake Buena Vista, FL This is the first part of a multi-zoo study to analyze the effects of captive envi- ronments on black rhinoceros (Diceros bicornis) behavior, breeding success, and well-being. We estimated the reliability and validity of a standardized method of cross-institutional assessment of the behavior of individual rhinoceros. In 1994 and 1995, we asked zookeepers at 19 zoos to rate their black rhinoceros (a total of 60 animals) on 52 behavior elements using a questionnaire. At 14 zoos, at least two keepers rated all the black rhinoceros at their zoo. We used average differences in their ratings of the 52 behavior elements to determine the most reliably rated behavior elements. Fourteen elements were retained for further analysis. Based on their inter-correlations, we grouped these 14 behaviors into six behavior traits: olfactory behaviors, chasing/stereotypy/mouthing, friendly to keeper, fearful, patrolling and dominant (to conspecifics). A behavior profile of each animal consisted of scores on these six traits that were the sum of the pri- mary keepers ratings for each element in the group. To test the validity of these profiles, we compared scores on the six traits to the behavior of each rhinoceros during a standardized test of reactivity to a novel object and a novel conspecific scent. Tests were videotaped and analyzed by one researcher. Frequencies and durations of behaviors observed during the tests were correlated with scores on all six rated behavior traits. Scores on friendly to keeper, dominant, and olfac- tory behaviors described differences between black rhinoceros of captive/wild caught origin, age,and sex, respectively. Among successfully breeding males, scores on dominant and olfactory behaviors were negatively correlated with re- productive success, as was chasing/stereotypy/mouthing for females. To test the repeatability of these results, during 1996-1997, we used a modified question- naire to re-survey 70 black rhinoceros at 24 zoos. Results of the second survey were also similar to those of the first with respect to the behaviors that distin- guish rhinoceros of different origin, age, sex, and reproductive success. We con- clude that ratings by keepers of behavior and temperament attributes can be used as reliable and valid cross-institutional descriptions of individual differences be- tween black rhinoceros. Zoo Biol 18:17-34, 1999.

Black Rhinoceros (Diceros bicornis) in U.S. Zoos: II. Behavior, Breeding Success, and Mortality in Relation to Housing Facilities

The captive population of black rhinoceros (Diceros bicornis) is not self-sustaining. The reasons for suboptimal reproduction and high mortality need to be investigated. This can only be achieved by cross-institutional analyses of environments, behavior, and performance. In this study, we collected data on 23 zoos with black rhinoceros to compare zoo environments with reproductive success, mortality, and behavior. Institutional variation was characterized by enclosure area, percentage of walls around enclosure perimeter, percentage of public access along enclosure perimeter, climate, noise level, number of years zoo has maintained black rhinoceros, frequency of chlorine use, and number of male and female black rhinoceros at a zoo simultaneously. Birth and death rates for each institution were calculated from studbook records. We found that the breeding success of a zoo since 1973 correlated positively with enclosure area, and zoos with two or more females had a lower reproductive rate than zoos with only one female. Females residing during their pre-reproductive years at a zoo with another reproductive female gave birth for the first time on average 3 years later than sole females. Mortality since 1973 correlated positively with percentage of public access. In Part I, we developed behavior profiles of 29.31 individual black rhinoceros from keeper ratings. Scores for males on the behavior trait Fear also correlated positively to percentage of public access, and we suggest that this aspect of black rhinoceros exhibits is a stressor for this species, especially the males. We found that different aspects of captive environments are associated with male and female black rhinoceros behavior. Male scores on the behavior trait dominant were higher in smaller enclosures, and female scores for a group of behaviors suggesting agitation (chasing/stereotypy/mouthing) were positively correlated with percentage of walls in their enclosure. These two behavior traits were found in Part I to be negatively correlated with the breeding success of an individual male or female. We re-surveyed the behavior and husbandry of 29 black rhinoceros pairs in zoos 2 years after the original data were collected. The re-survey confirmed that compatible black rhinoceros pairs are those with assertive females and submissive males, and that enclosure area and a low percentage of concrete walls around the enclosure are positive predictors of a pairs reproductive success. We conclude that temperament traits of individuals and characteristics of their captive environments both have an impact on a pairs breeding success. Our study demonstrates that cross-institutional comparisons of zoo facilities, when integrated with behavioral assessments of individual animals, are a valuable tool for investigating potential causes of poor reproduction and well-being in zoo animals. Zoo Biol 18:35–52, 1999.

Seasonal variation in stereotypic pacing in an American black bear Ursus americanus.

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.

Predictability of feeding: Its effect on agonistic behaviour and growth in grower pigs

Abstract Predictability of feeding was experimentally manipulated in Experiment I by changing the reliability of signals announcing the arrival of food for 32 female grower pigs. Results indicated that competition for places at the feed-pan increased when feeding time was unreliably signalled. Experiment II offered a total of 36 pigs, the R group, reliable signals throughout a 13-week period, and another 36 pigs, the UNR group, only unreliable signals. The frequency of aggression in the latter group was higher between meals when no signals were given, mainly after disturbances from in or outside of the pig-shed. Analysis of the behaviour of individual pigs indicates that the higher aggression is frustration-induced. The UNR group also showed a trend for greater variation in weight gain than the R group. The behavioural mechanisms through which unpredictable management practices affect the behaviour and growth of grower pigs are discussed.

An Epidemiological Approach to Welfare Research in Zoos: The Elephant Welfare Project

Multi-institutional studies of welfare have proven to be valuable in zoos but are hampered by limited sample sizes and difficulty in evaluating more than just a few welfare indicators. To more clearly understand how interactions of husbandry factors influence the interrelationships among welfare outcomes, epidemiological approaches are needed as well as multifactorial assessments of welfare. Many questions have been raised about the housing and care of elephants in zoos and whether their environmental and social needs are being met in a manner that promotes good welfare. This article describes the background and rationale for a large-scale study of elephant welfare in North American zoos funded by the (U.S.) Institute of Museum and Library Services. The goals of this project are to document the prevalence of positive and negative welfare states in 291 elephants exhibited in 72 Association of Zoos and Aquariums zoos and then determine the environmental, management, and husbandry factors that impact elephant welfare. This research is the largest scale nonhuman animal welfare project ever undertaken by the zoo community, and the scope of environmental variables and welfare outcomes measured is unprecedented.

Evaluation of Demographics and Social Life Events of Asian (Elephas maximus) and African Elephants (Loxodonta africana) in North American Zoos.

This study quantified social life events hypothesized to affect the welfare of zoo African and Asian elephants, focusing on animals that were part of a large multi-disciplinary, multi-institutional elephant welfare study in North America. Age was calculated based on recorded birth dates and an age-based account of life event data for each elephant was compiled. These event histories included facility transfers, births and deaths of offspring, and births and deaths of non-offspring herd mates. Each event was evaluated as a total number of events per elephant, lifetime rate of event exposure, and age at first event exposure. These were then compared across three categories: species (African vs. Asian); sex (male vs. female); and origin (imported vs. captive-born). Mean age distributions differed (p<0.05) between the categories: African elephants were 6 years younger than Asian elephants, males were 12 years younger than females, and captive-born elephants were 20 years younger than imported elephants. Overall, the number of transfers ranged from 0 to 10, with a 33% higher age-adjusted transfer rate for imported African than imported Asian elephants, and 37% lower rate for imported females than males (p<0.05). Other differences (p<0.05) included a 96% higher rate of offspring births for captive-born females than those imported from range countries, a 159% higher rate of birthing event exposures for captive-born males than for their imported counterparts, and Asian elephant females being 4 years younger than African females when they produced their first calf. In summarizing demographic and social life events of elephants in North American zoos, we found both qualitative and quantitative differences in the early lives of imported versus captive-born elephants that could have long-term welfare implications.

Reproductive Health Assessment of Female Elephants in North American Zoos and Association of Husbandry Practices with Reproductive Dysfunction in African Elephants (Loxodonta africana)

As part of a multi-institutional study of zoo elephant welfare, we evaluated female elephants managed by zoos accredited by the Association of Zoos and Aquariums and applied epidemiological methods to determine what factors in the zoo environment are associated with reproductive problems, including ovarian acyclicity and hyperprolactinemia. Bi-weekly blood samples were collected from 95 African (Loxodonta africana) and 75 Asian (Elephas maximus) (8–55 years of age) elephants over a 12-month period for analysis of serum progestogens and prolactin. Females were categorized as normal cycling (regular 13- to 17-week cycles), irregular cycling (cycles longer or shorter than normal) or acyclic (baseline progestogens, <0.1 ng/ml throughout), and having Low/Normal (<14 or 18 ng/ml) or High (≥14 or 18 ng/ml) prolactin for Asian and African elephants, respectively. Rates of normal cycling, acyclicity and irregular cycling were 73.2, 22.5 and 4.2% for Asian, and 48.4, 37.9 and 13.7% for African elephants, respectively, all of which differed between species (P < 0.05). For African elephants, univariate assessment found that social isolation decreased and higher enrichment diversity increased the chance a female would cycle normally. The strongest multi-variable models included Age (positive) and Enrichment Diversity (negative) as important factors of acyclicity among African elephants. The Asian elephant data set was not robust enough to support multi-variable analyses of cyclicity status. Additionally, only 3% of Asian elephants were found to be hyperprolactinemic as compared to 28% of Africans, so predictive analyses of prolactin status were conducted on African elephants only. The strongest multi-variable model included Age (positive), Enrichment Diversity (negative), Alternate Feeding Methods (negative) and Social Group Contact (positive) as predictors of hyperprolactinemia. In summary, the incidence of ovarian cycle problems and hyperprolactinemia predominantly affects African elephants, and increases in social stability and feeding and enrichment diversity may have positive influences on hormone status.

Determining Connections between the Daily Lives of Zoo Elephants and Their Welfare: An Epidemiological Approach

Concerns about animal welfare increasingly shape people’s views about the acceptability of keeping animals for food production, biomedical research, and in zoos. The field of animal welfare science has developed over the past 50 years as a method of investigating these concerns via research that assesses how living in human-controlled environments influences the behavior, health and affective states of animals. Initially, animal welfare research focused on animals in agricultural settings, but the field has expanded to zoos because good animal welfare is essential to zoos’ mission of promoting connections between animals and visitors and raising awareness of conservation issues. A particular challenge for zoos is ensuring good animal welfare for long-lived, highly social species like elephants. Our main goal in conducting an epidemiological study of African (Loxodonta africana) and Asian (Elephas maximus) elephant welfare in 68 accredited North American zoos was to understand the prevalence of welfare indicators in the population and determine the aspects of an elephant’s zoo environment, social life and management that are most important to prevent and reduce a variety of welfare problems. In this overview, we provide a summary of the findings of the nine papers in the collection titled: Epidemiological Investigations of North American Zoo Elephant Welfare with a focus on the life history, social, housing, and management factors found to be associated with particular aspects of elephant welfare, including the performance of abnormal behavior, foot and joint problems, recumbence, walking rates, and reproductive health issues. Social and management factors were found to be important for multiple indicators of welfare, while exhibit space was found to be less influential than expected. This body of work results from the largest prospective zoo-based animal welfare study conducted to date and sets in motion the process of using science-based welfare benchmarks to optimize care of zoo elephants.

Elephant Management in North American Zoos: Environmental Enrichment, Feeding, Exercise, and Training.

The management of African (Loxodonta africana) and Asian (Elephas maximus) elephants in zoos involves a range of practices including feeding, exercise, training, and environmental enrichment. These practices are necessary to meet the elephants’ nutritional, healthcare, and husbandry needs. However, these practices are not standardized, resulting in likely variation among zoos as well as differences in the way they are applied to individual elephants within a zoo. To characterize elephant management in North America, we collected survey data from zoos accredited by the Association of Zoos and Aquariums, developed 26 variables, generated population level descriptive statistics, and analyzed them to identify differences attributable to sex and species. Sixty-seven zoos submitted surveys describing the management of 224 elephants and the training experiences of 227 elephants. Asian elephants spent more time managed (defined as interacting directly with staff) than Africans (mean time managed: Asians = 56.9%; Africans = 48.6%; p<0.001), and managed time increased by 20.2% for every year of age for both species. Enrichment, feeding, and exercise programs were evaluated using diversity indices, with mean scores across zoos in the midrange for these measures. There were an average of 7.2 feedings every 24-hour period, with only 1.2 occurring during the nighttime. Feeding schedules were predictable at 47.5% of zoos. We also calculated the relative use of rewarding and aversive techniques employed during training interactions. The population median was seven on a scale from one (representing only aversive stimuli) to nine (representing only rewarding stimuli). The results of our study provide essential information for understanding management variation that could be relevant to welfare. Furthermore, the variables we created have been used in subsequent elephant welfare analyses.