Cheryl L. Meehan

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.

Housing and demographic risk factors impacting foot and musculoskeletal health in African Elephants [loxodonta Africana] and Asian elephants [elephas maximus] in North American zoos

For more than three decades, foot and musculoskeletal conditions have been documented among both Asian [Elephas maximus] and African [Loxodonta africana] elephants in zoos. Although environmental factors have been hypothesized to play a contributing role in the development of foot and musculoskeletal pathology, there is a paucity of evidence-based research assessing risk. We investigated the associations between foot and musculoskeletal health conditions with demographic characteristics, space, flooring, exercise, enrichment, and body condition for elephants housed in North American zoos during 2012. Clinical examinations and medical records were used to assess health indicators and provide scores to quantitate conditions. Using multivariable regression models, associations were found between foot health and age [P value = 0.076; Odds Ratio = 1.018], time spent on hard substrates [P value = 0.022; Odds Ratio = 1.014], space experienced during the night [P value = 0.041; Odds Ratio = 1.008], and percent of time spent in indoor/outdoor exhibits during the day [P value < 0.001; Odds Ratio = 1.003]. Similarly, the main risk factors for musculoskeletal disorders included time on hard substrate [P value = 0.002; Odds Ratio = 1.050] and space experienced in indoor/outdoor exhibits [P value = 0.039; Odds Ratio = 1.037]. These results suggest that facility and management changes that decrease time spent on hard substrates will improve elephant welfare through better foot and musculoskeletal health.

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.

Housing and Social Environments of African (Loxodonta africana) and Asian (Elephas maximus) Elephants in North American Zoos.

We evaluated 255 African (Loxodonta africana) and Asian (Elephas maximus) elephants living in 68 North American zoos over one year to quantify housing and social variables. All parameters were quantified for the both the day and the night and comparisons were made across these time periods as well as by species and sex. To assess housing, we evaluated not only total exhibit size, but also individual animals’ experiences based on the time they spent in the unique environments into which the exhibits were subdivided. Variables developed to assess housing included measurements of area as a function of time (Total Space Experience), environment type (Indoor, Outdoor, In/Out Choice) and time spent on hard and soft flooring. Over the year, Total Space Experience values ranged from 1,273 square feet to 169,692 square feet, with Day values significantly greater than Night values (p<0.001). Elephants spent an average of 55.1% of their time outdoors, 28.9% indoors, and 16% in areas with a choice between being in or out. Time spent on hard flooring substrate ranged from 0% to 66.7%, with Night values significantly greater than Day (p<0.001). Social factors included number of animals functionally housed together (Social Experience) and social group characteristics such as time spent with juveniles and in mixed-sex groups. Overall Social Experience scores ranged from 1 to 11.2 and were significantly greater during the Day than at Night (p<0.001). There were few significant social or housing differences between African (N = 138) and Asian (N = 117) species or between males (N = 54) and females (N = 201). The most notable exception was Total Space Experience, with African and male elephants having larger Total Space Experience than Asian and female elephants, respectively (P-value<0.05). The housing and social variables evaluated herein have been used in a series of subsequent epidemiological analyses relating to various elephant welfare outcomes.

Assessment of Body Condition in African (Loxodonta africana) and Asian (Elephas maximus) Elephants in North American Zoos and Management Practices Associated with High Body Condition Scores

Obesity has a negative effect on health and welfare of many species, and has been speculated to be a problem for zoo elephants. To address this concern, we assessed the body condition of 240 elephants housed in North American zoos based on a set of standardized photographs using a 5-point Body Condition Score index (1 = thinnest; 5 = fattest). A multi-variable regression analysis was then used to determine how demographic, management, housing, and social factors were associated with an elevated body condition score in 132 African (Loxodonta africana) and 108 Asian (Elephas maximus) elephants. The highest BCS of 5, suggestive of obesity, was observed in 34% of zoo elephants. In both species, the majority of elephants had elevated BCS, with 74% in the BCS 4 (40%) and 5 (34%) categories. Only 22% of elephants had BCS 3, and less than 5% of the population was assigned the lowest BCS categories (BCS 1 and 2). The strongest multi-variable model demonstrated that staff-directed walking exercise of 14 hours or more per week and highly unpredictable feeding schedules were associated with decreased risk of BCS 4 or 5, while increased diversity in feeding methods and being female was associated with increased risk of BCS 4 or 5. Our data suggest that high body condition is prevalent among North American zoo elephants, and management strategies that help prevent and mitigate obesity may lead to improvements in welfare of zoo elephants.

The Days and Nights of Zoo Elephants: Using Epidemiology to Better Understand Stereotypic Behavior of African Elephants (Loxodonta africana) and Asian Elephants (Elephas maximus) in North American Zoos.

Stereotypic behavior is an important indicator of compromised welfare. Zoo elephants are documented to perform stereotypic behavior, but the factors that contribute to performance have not been systematically assessed. We collected behavioral data on 89 elephants (47 African [Loxodonta africana], 42 Asian [Elephas maximus]) at 39 North American zoos during the summer and winter. Elephants were videoed for a median of 12 daytime hours per season. A subset of 32 elephants (19 African, 13 Asian) was also observed live for a median of 10.5 nighttime hours. Percentages of visible behavior scans were calculated from five minute instantaneous samples. Stereotypic behavior was the second most commonly performed behavior (after feeding), making up 15.5% of observations during the daytime and 24.8% at nighttime. Negative binomial regression models fitted with generalized estimating equations were used to determine which social, housing, management, life history, and demographic variables were associated with daytime and nighttime stereotypic behavior rates. Species was a significant risk factor in both models, with Asian elephants at greater risk (daytime: p<0.001, Risk Ratio = 4.087; nighttime: p<0.001, Risk Ratio = 8.015). For both species, spending time housed separately (p<0.001, Risk Ratio = 1.009), and having experienced inter-zoo transfers (p<0.001, Risk Ratio = 1.175), increased the risk of performing higher rates of stereotypy during the day, while spending more time with juvenile elephants (p<0.001, Risk Ratio = 0.985), and engaging with zoo staff reduced this risk (p = 0.018, Risk Ratio = 0.988). At night, spending more time in environments with both indoor and outdoor areas (p = 0.013, Risk Ratio = 0.987) and in larger social groups (p = 0.039, Risk Ratio = 0.752) corresponded with reduced risk of performing higher rates of stereotypy, while having experienced inter-zoo transfers (p = 0.033, Risk Ratio = 1.115) increased this risk. Overall, our results indicate that factors related to the social environment are most influential in predicting elephant stereotypic behavior rates.

Recumbence Behavior in Zoo Elephants: Determination of Patterns and Frequency of Recumbent Rest and Associated Environmental and Social Factors.

Resting behaviors are an essential component of animal welfare but have received little attention in zoological research. African savanna elephant (Loxodonta africana) and Asian elephant (Elephas maximus) rest includes recumbent postures, but no large-scale investigation of African and Asian zoo elephant recumbence has been previously conducted. We used anklets equipped with accelerometers to measure recumbence in 72 adult female African (n = 44) and Asian (n = 28) elephants housed in 40 North American zoos. We collected 344 days of data and determined associations between recumbence and social, housing, management, and demographic factors. African elephants were recumbent less (2.1 hours/day, S.D. = 1.1) than Asian elephants (3.2 hours/day, S.D. = 1.5; P < 0.001). Nearly one-third of elephants were non-recumbent on at least one night, suggesting this is a common behavior. Multi-variable regression models for each species showed that substrate, space, and social variables had the strongest associations with recumbence. In the African model, elephants who spent any amount of time housed on all-hard substrate were recumbent 0.6 hours less per day than those who were never on all-hard substrate, and elephants who experienced an additional acre of outdoor space at night increased their recumbence by 0.48 hours per day. In the Asian model, elephants who spent any amount of time housed on all-soft substrate were recumbent 1.1 hours more per day more than those who were never on all-soft substrate, and elephants who spent any amount of time housed alone were recumbent 0.77 hours more per day than elephants who were never housed alone. Our results draw attention to the significant interspecific difference in the amount of recumbent rest and in the factors affecting recumbence; however, in both species, the influence of flooring substrate is notably important to recumbent rest, and by extension, zoo elephant welfare.

Walking Behavior of Zoo Elephants: Associations between GPS-Measured Daily Walking Distances and Environmental Factors, Social Factors, and Welfare Indicators

Research with humans and other animals suggests that walking benefits physical health. Perhaps because these links have been demonstrated in other species, it has been suggested that walking is important to elephant welfare, and that zoo elephant exhibits should be designed to allow for more walking. Our study is the first to address this suggestion empirically by measuring the mean daily walking distance of elephants in North American zoos, determining the factors that are associated with variations in walking distance, and testing for associations between walking and welfare indicators. We used anklets equipped with GPS data loggers to measure outdoor daily walking distance in 56 adult female African (n = 33) and Asian (n = 23) elephants housed in 30 North American zoos. We collected 259 days of data and determined associations between distance walked and social, housing, management, and demographic factors. Elephants walked an average of 5.3 km/day with no significant difference between species. In our multivariable model, more diverse feeding regimens were correlated with increased walking, and elephants who were fed on a temporally unpredictable feeding schedule walked 1.29 km/day more than elephants fed on a predictable schedule. Distance walked was also positively correlated with an increase in the number of social groupings and negatively correlated with age. We found a small but significant negative correlation between distance walked and nighttime Space Experience, but no other associations between walking distances and exhibit size were found. Finally, distance walked was not related to health or behavioral outcomes including foot health, joint health, body condition, and the performance of stereotypic behavior, suggesting that more research is necessary to determine explicitly how differences in walking may impact elephant welfare.

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.