Supporting Zoo Asian Elephant (Elephas maximus) Welfare and Herd Dynamics with a More Complex and Expanded Habitat.

Ensuring good health and welfare is an increasingly important consideration for conservation of endangered species, whether free-ranging or managed to varying degrees under human care. The welfare-based design of a new habitat for Asian elephants at the Oregon Zoo focused on meeting the elephants' physical, physiological, psychological, and social needs 24 h a day and across life stages. The habitat was designed to encourage activity, promote species-typical behaviors, support changing social dynamics, offer increased opportunities for choice, and provide biologically meaningful challenges. In this 4-year study, we monitored elephant health and welfare indicators throughout the transition and acclimation from the previous habitat to the new habitat. Several welfare indicators obtained through longitudinal hormone analyses, behavior assessments, and GPS measurement of walking distance and space use provided evidence that these goals were achieved. The elephants were more active and walked farther on a daily basis in the new habitat, with an average walking distance of over 15 km per day. A switch from primarily caretaker-delivered food to seeking food on their own indicates that the disbursement of food with less temporal and spatial predictability increased foraging opportunities, which better satisfies appetitive motivations important for psychological well-being. All individuals showed adaptive and normal adrenal responses to change and challenge, with the highest fecal glucocorticoid metabolite (FGM) concentrations and variability during the construction phase, and a return to previous baseline concentrations in the new habitat, suggesting they acclimated well to the new environment. The elephants expressed a diverse range of species-typical behaviors and demonstrated social dynamics of a healthy herd in both habitats with transitions of individuals through life stages. They exhibited more autonomy in choosing whom to associate with socially and also by choosing different aspects of their environment with regular indoor/outdoor access and extensive resource use in the new habitat. Findings indicate that the complexity and flexibility of the new habitat and habitat management has been effective in improving overall welfare by providing meaningful challenges and the opportunity to express appetitive behaviors, by offering choice in environmental conditions, and by providing the space and resource distribution to support evolving herd dynamics and increased social equity for individuals.

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.

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.

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.

Free mate choice enhances conservation breeding in the endangered giant panda.

Conservation breeding programmes have become an increasingly important tool to save endangered species, yet despite the allocation of significant resources, efforts to create self-sustaining populations have met with limited success. The iconic giant panda (Ailuropoda melanoleuca) embodies the struggles associated with ex situ species conservation. Here we show that behavioural mate preferences in giant pandas predict reproductive outcomes. Giant pandas paired with preferred partners have significantly higher copulation and birth rates. Reproductive rates increase further when both partners show mutual preference for one another. If managers were to incorporate mate preferences more fully into breeding management, the production of giant panda offspring for China's reintroduction programme might be greatly expedited. When extended to the increasing numbers of species dependent on ex situ conservation breeding to avoid extinction, our findings highlight that mate preference and other aspects of informed behavioural management could make the difference between success and failure of these programmes.

Validation of a novel cognitive bias task based on difference in quantity of reinforcement for assessing environmental enrichment.

Cognitive bias tasks purport to assess affective states via responses to ambiguous stimuli. We hypothesized that a novel cognitive bias task based on positive reinforcement using quantity differences would detect changes in affect in captive grizzly bears (Ursus arctos horribilis). We trained bears (n = 8) to respond differently (nose or paw touch) to two stimuli (light or dark gray cue cards), with responses counterbalanced across bears. The two cues signaled a small or large food reward, respectively. Responses to ambiguous probe stimuli (i.e., shades of gray) intermediate to the trained stimuli were classified as either 'optimistic,' appropriate for the larger reward, or 'pessimistic,' appropriate for the smaller reward. In Experiment 1, we explored the contrast in reward size necessary to detect a change in response across probe stimuli (large reward, 3 or 6 apple slices: small reward, 1 slice). We observed a change in response across probe stimuli, with no difference in response between reward-value groups, indicating that a contrast of 3:1 apple slices was sufficient to affect responses. In Experiment 2, we investigated cognitive bias after 2.1 h of exposure to enrichment items varying in attractiveness. Results were unaffected by enrichment type or time spent interacting with enrichments, indicating that the task failed to demonstrate criterion validity for comparing mood following exposure to different enrichment items. However, greater time spent pacing prior to testing was associated with 'optimistic' judgments. The data provide some support for use of cognitive bias tasks based on quantity differences in animal welfare assessments involving captive wildlife.

The value of enrichment to reintroduction success.

Reintroduction attempts have faced low, albeit improving, success rates, especially for threatened and endangered species reintroduced from captivity to the wild. This is not only a concern for conservation, as the low success of reintroduction also implies an animal welfare issue for the individuals concerned. Success rates are particularly low for species that live in complex social structures, require greater training during development, and exhibit higher levels of intelligence. Aside from mitigating the original cause of a species extirpation from an area, behavior factors arguably represent the most important aspect influencing an animal's survival following reintroduction. Indeed, we previously recommended using behavioral indicators for determining relative reintroduction success, especially as practitioners develop and compare protocols or if survivorship is difficult to gauge. Strategic enrichment programs targeted toward developing specific skills important for survival in the wild promise to improve reintroduction success by providing individuals with opportunities to develop and improve behavioral skills, such as avoiding predation, foraging (especially for predators and primates), interacting in social groups, courtship and mating, habitat selection, and learning movement and migration routes. Enrichment also improves the physical condition of most individuals, which should also increase reintroduction success. Last but not least, such programs offer the prospect of improved animal welfare both pre- and post-release. We explore how behavioral enrichment has influenced reintroduction success and welfare in a variety of different species.

Organochlorine contaminants in blubber from stranded marine mammals collected from the Northern Oregon and Southern Washington coasts: implications for re-introducing California Condors, Gymnogyps californianus, in Oregon.

Re-introduction of California Condors into Oregon is currently being considered, but there are concerns about the safety of potential food sources of this species. Condors are opportunistic feeders and a largely available food source for this species will be stranded marine mammal carcasses. We analyzed 37 blubber samples from 7 different marine mammal species collected from the Oregon and Southern Washington coasts for 18 organochlorine (OC) pesticides and 16 polychlorinated biphenyls (PCBs). Dichlorodiphenyldichloroethylene (DDE) was the most prevalent OC contaminant, making up more than 58 % of the total OC concentration measured. There were no significant differences in OC content between species or sexes.

Role of familiarity and preference in reproductive success in ex situ breeding programs.

Success of captive-breeding programs centers on consistent reproduction among captive animals. However, many individuals do not reproduce even when they are apparently healthy and presented with mates. Mate choice can affect multiple parameters of reproductive success, including mating success, offspring production, offspring survival, and offspring fecundity. We investigated the role of familiarity and preference on reproductive success of female Columbia Basin pygmy rabbits (Brachylagus idahoensis) as measured by litter production, litter size, average number of young that emerged from the burrow, and average number of young that survived to 1 year. We conducted these studies on pygmy rabbits at the Oregon Zoo (Portland, Oregon, U.S.A.) and Washington State University (Pullman, Washington, U.S.A.) from February to June 2006, 2007, and 2008. Before mating, we housed each female adjacent to 2 males (neighbors). Female preference for each potential mate was determined on the basis of behavioral interactions observed and measured between the rabbits. We compared reproductive success between females mated with neighbor and non-neighbor males and between females mated with preferred and nonpreferred males. Our findings suggest that mating with a neighbor compared with a non-neighbor and mating with a preferred neighbor compared with a nonpreferred neighbor increased reproductive success in female pygmy rabbits. Litter production, average number of young that emerged, and average number of young that survived to 1 year were higher in rabbits that were neighbors before mating than in animals who were not neighbors. Pairing rabbits with a preferred partner increased the probability of producing a litter and was significantly associated with increased litter size. In captive breeding programs, mates are traditionally selected on the basis of genetic parameters to minimize loss of genetic diversity and inbreeding coefficients. Our results suggest that integrating genetic information with social dynamics and behavioral measures of preference may increase the reproductive output of the pygmy rabbit captive-breeding program. Our findings are consistent with the idea that allowing mate choice and familiarity increase the reproductive success of captive-breeding programs for endangered species.

Characterizing gonadal and adrenal activity by fecal steroid analyses in pygmy rabbits (Brachylagus idahoensis).

In 2001, the sudden collapse of the Columbia Basin population of pygmy rabbits prompted the initiation of a captive breeding program to facilitate reintroduction, but reproductive success in captivity has not met expectations. Therefore, the objective of this study was to characterize the reproductive and adrenal endocrinology of this endangered rabbit species so that appropriate management strategies could be developed to monitor animal welfare and increase reproduction. Fecal samples were collected from 27 female pygmy rabbits over three breeding and non-breeding seasons. HPLC analyses verified the presence of progesterone in the excreta of pygmy rabbits, but the majority of progestagen metabolites were unidentified polar compounds. By contrast, >70% of glucocorticoid immunoactivity was associated with cortisol. Longitudinal fecal hormone profiles during pregnancy were characterized by a large spike in progestagens shortly after mating, a gradual increase in progestagen and glucocorticoid concentrations throughout gestation and a return of hormones to baseline soon after birth (Day 24). The spike in progestagens 1 day after mating was a significant discovery for this species and appears to provide a reliable means of determining if a successful mating has occurred. Seasonal analyses of hormone excretion found that progestagen baselines did not vary between the breeding and non-breeding seasons, but, as expected, were highest during the breeding season in association with pregnancy. Across seasons, the lowest concentrations of glucocorticoids were associated with the highest rates of offspring production and survival, suggesting a possible link between heightened adrenal activity and lowered reproductive fitness in pygmy rabbits.

A survey of elephant husbandry and foot health in North American zoos.

The foot health of elephants in human care is a longstanding concern. In 2001, the AZA Standards for Elephant Management and Care were published recommending husbandry to improve foot health. This article reports the results of a 2006 survey: basic statistics describing facility, husbandry, and foot health attributes are reported and relationships among variables are investigated. Median area available to elephants exceeded Standard recommendations (755 ft(2) per elephant indoor and 10,000 ft(2) outdoor). Concrete makes up 69% of indoor area and natural substrates account for 85% of outdzoor area. Elephants in AZA facilities received an average of 45.5 min/day of exercise, and facilities with a structured exercise plan provided significantly more exercise than did facilities without a structured exercise plan (z=-2.522, P=0.012). Enrichment is important to psychological health and may also stimulate activity beneficial to foot health; 95% of institutions had a structured enrichment program. Preventative foot care was nearly universal, and 100% of facilities performed routine nail and pad trimming. However, foot pathology has not been eradicated; 33% of institutions reported at least one pathology in the previous year. This study found a strong inverse relationship between foot pathology and exercise (chi(2)(3)=24.34, P<0.001). Younger herds were less likely to have a member diagnosed with arthritis (chi(2)(1)=8.90, P=0.003). Lameness was unrelated to age or pathology, and only the presence of arthritis explained lameness (z=-7.81, P<0.001). African elephants seemed to experience lower rates of foot pathology and arthritis than Asian elephants; however, this was explained by differences in age.

Effects of rubberized flooring on Asian elephant behavior in captivity.

Six Asian elephants at the Oregon Zoo were observed to determine the effects of a poured rubber flooring substrate on captive Asian elephant behavior. Room utilization also was evaluated in seven rooms used for indoor housing, including Front and Back observation areas. Data were collected in three phases. Phase I (Baseline Phase) examined elephant behavior on old concrete floors. In Phase II (Choice Phase), elephant behavior was observed in the Back observation area where room sizes were comparable and when a choice of flooring substrates was available. Phase III (Final Phase) examined elephant behavior when all rooms in both observation areas, Front and Back, were converted to rubberized flooring. Room use in both observation areas remained stable throughout the study, suggesting that flooring substrate did not affect room use choice. However, there was a clear pattern of decreased discomfort behaviors on the new rubber flooring. Normal locomotion as well as stereotypic locomotion increased on the new rubber flooring. In addition, resting behavior changed to more closely reflect the resting behavior of wild elephants, which typically sleep standing up, and spend very little time in lateral recumbence. Overall, these findings suggest that the rubber flooring may have provided a more comfortable surface for locomotion as well as standing resting behavior. It is suggested that poured rubber flooring may be a beneficial addition to similar animal facilities. Zoo Biol 0:1-11, 2007. (c) 2007 Wiley-Liss, Inc.