Wing condition does not negatively impact time budget, enclosure usage, or social bonds in a flock of both full-winged and flight-restrained greater flamingos.

Zoo management techniques for captive birds, such as flight restraint and enclosure type, may affect behavioral performance and are consequently worthy of investigation. Flamingos are amongst the most popular of zoo-housed birds and, as such, research into their captive management and associated behavioral responses are widely applicable to many thousands of individuals. As a highly social species, understanding social bonds and behavior of the individual bird and the flock overall can help inform decisions that support husbandry and population management. In this project, 41 greater flamingos at Bristol Zoo Gardens were observed for 49 days across spring and summer 2013 to assess the following: (i) social associations within the flock, (ii) overall activity patterns, and (iii) distribution of time within specific enclosure zones for both full-winged and flight-restrained birds living in the same enclosure. Results showed that pinioning interacted with age in regard to flamingo time-activity patterns, but wing condition did not significantly influence association patterns, performance of social interactions, or performance of breeding behavior. Social network analysis revealed that associations were nonrandom and flamingos, of either wing condition, displayed different roles within the network. Birds of similar age formed the strongest bonds. Enclosure usage was not even, suggesting that the flamingos favored specific areas of the enclosure during the observation period. This study showed that wing condition does not affect flamingo behavior, social bonds, or space use, and that age and sex have more of an overall influence on what flamingos do, and with whom they chose to do it. Further research should extend this study into other, larger captive flocks to further refine behavioral measures of welfare for these popular zoo birds.

The Animal-Visitor Interaction Protocol (AVIP) for the assessment of Lemur catta walk-in enclosure in zoos.

Animal-Visitor Interactions (AVI) are activities offered by zoos and other tourism facilities, in which visitors come into close contact with animals. These activities can promote conservational and educational content, raise conservation mindedness and responsibility for the environment and animal welfare, but if not properly managed can jeopardize visitors' and animals' well-being and conservation efforts. The Animal-Visitor Interaction assessment Protocol (AVIP) has been designed to perform an integrated and multidisciplinary assessment of these activities, encompassing the "One Health, One Welfare" approach. AVIP throughout six different steps allows to assess the effects of AVIs both on animals, visitors, and the staff involved. Results can assist zoos to improve management decisions, ensure a transparent evaluation of their activities and promote conservation education goals. Lemurs walk-in enclosures have become increasingly popular among zoos, nevertheless studies focused on their assessment are still scarce. To validate AVIP to this particular AVI, we applied it to assess a walk-in enclosure hosting five Lemur catta in an Italian zoo. Results of behavioural and physiological analyses suggested no changes in animal welfare level and the Animal Welfare Risk Assessment showed low animal welfare risks. Two Visitor Experience Surveys were used to interview 291 visitors, showing that the assessed AVI could help promote the zoo's conservation objectives and visitor education. Risk Assessment found low and medium risks to the health and safety of visitors. Results were then combined to perform a final ethical assessment. Some potential ethical concerns were detected, but the outcomes indicated that these conflicts were well managed. In the context of recent findings AVIP demonstrated its potential for application also in assessing AVIs involving primates. Our findings confirmed the usefulness of AVIP in assessing and monitoring AVIs, allowing to gain key information in a single process on multiple welfare-related parameters, educational impact, safety of the main stakeholders involved, and ethical concerns.

Activity Budget and Postural Behaviors in Orangutans on Bukit Merah Orang Utan Island for Assessing Captive Great Ape Welfare.

Assessments of the welfare status of captive and semi-captive animals often compare how their expression of natural behaviors differs from that of free-ranging conspecifics. From December 2015-2016, we recorded and analyzed the activity budget and postural behaviors of three orangutans in Bukit Merah Orang Utan Island (BMOUI) to evaluate their welfare status. The orangutans' activity budget was dominated by resting (60%), feeding (13%), playing (14%), and moving (9%). Behavioral categories followed a similar trend: resting > feeding > moving > playing, except that the subadult male spent significantly more time playing than the two adults. The most predominant posture was sitting (47.0%), followed by pronograde standing (29.4%), lying (10.5%), and clinging (4.5%). Our results suggest that orangutans on BMOUI engage in less feeding but more resting, and show less postural diversity than free-ranging individuals. We propose that appropriate interventions to shift activity budgets, especially feeding vs. resting, and postural behaviors of captive orangutans toward those found in free-ranging orangutans might be beneficial for their welfare and survival.

INVESTIGATION INTO CARDIOVASCULAR ASSESSMENT OF CAPTIVE ADULT SCARLET IBIS (EUDOCIMUS RUBER).

Cardiovascular lesions are commonly diagnosed postmortem in scarlet ibis (Eudocimus ruber), but antemortem diagnosis is rare. The aim of this study was to evaluate the cardiovascular health of a zoo population (n = 44) of apparently healthy, adult, scarlet ibis. A cross-sectional study design was employed whereby each animal was manually restrained for physical examination, phlebotomy, and echocardiographic examination performed with a 12-MHz transducer and a ventromedial approach, and observed intervals were calculated for 12 parameters. Seven individuals from the study population had high left-sided mid-ventricular velocities (2.59-5.89 m/sec) compared with values in other species. Follow-up examination suggested that these mid-ventricular obstructive lesions were dynamic and transient in nature rather than caused by fixed lesions within the outflow tract and may therefore be associated with stress. Conscious echocardiography proved to be feasible, although, unsurprisingly, the stress response in nonhabituated birds appeared to increase blood flow velocities. Handling protocols likely have a significant effect on echocardiographic parameters and should be taken into consideration when interpreting findings. Serum cholesterol concentrations were generally high (7.4-13.0 mmol/L), and further work is required to investigate the relationship between circulating cholesterol and the development of atherosclerosis in scarlet ibis. Serum cardiac troponin I concentrations were measured, and four animals were identified with suspected elevated levels, likely indicative of myocardial damage.

Activity budget and spatial distribution of Bennett's wallabies (Macropus rufogriseus) in open versus closed exhibit designs.

Although many studies investigating the impacts of zoo exhibit designs on captive animals exist, none have been performed on how they influence the behavior and welfare of captive Bennett's wallabies (Macropus rufogriseus). Here, we assess the impact of exhibit design on the activity budget and spatial distribution of Bennett's wallabies. We compared animal behavior in two open exhibits (i.e. physical interaction between animals and visitors permitted) to two closed exhibits (i.e. physical interaction between animals and visitors prohibited). Behavioral data were collected using focal sampling, and spatial distribution was recorded on exhibit maps at regular time intervals. We found a significant increase in feeding and interactive behaviors in closed exhibits in comparison to open exhibits. However, other behaviors such as resting, locomotion, and vigilance did not vary with design. Functional use of space was similar between both designs; however, the effect of habituation may be relevant to consider in future studies. Although some support for visitor effects were present, our study provided no evidence for strong impacts of exhibit design on Bennett's wallaby welfare. Our study emphasizes the need for additional research into the impacts of how zoo environments affect Bennett's wallaby behavior and welfare.

Interacting circadian and homeostatic processes with opportunity cost: A mathematical model of sleep with application to two mammalian species.

This paper introduces a new model of sleep for mammals. It extends the classic 'two-process' model of sleep to account for differences in external circumstances. We apply this model to previously-collected data on elephants and sloths, comparing sleep patterns in the wild with sleep patterns in captivity. We find that the model does very well in explaining sleeping patterns for both types of animals, in both the captive state and in the wild state.

Evaluating the Contribution of North American Zoos and Aquariums to Endangered Species Recovery.

The challenge of recovering threatened species necessitates collaboration among diverse conservation partners. Zoos and aquariums have long partnered with other conservation organizations and government agencies to help recover species through a range of in situ and ex situ conservation projects. These efforts tend to be conducted by individual facilities and for individual species, and thus the scope and magnitude of these actions at the national level are not well understood. Here we evaluate the means and extent to which North American zoos and aquariums contribute to the recovery of species listed under the U.S. Endangered Species Act (ESA), by synthesizing data from federal recovery plans for listed species and from annual surveys conducted by the Association of Zoos and Aquariums. We found that in addition to managing ex situ assurance populations, zoos frequently conduct conservation research and field-based population monitoring and assessments. Cooperatively managed populations in zoos tend to focus on species that are not listed on the ESA or on foreign listings, and thus it may be beneficial for zoos to manage more native threatened species. Our results highlight the existing contributions, but also identify additional opportunities for the zoo community to help recover threatened species.

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.

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.

Captive-breeding of captive and wild-reared Gunnison sage-grouse.

Gunnison sage-grouse (Centrocercus minimus) distribution in North America has decreased over historical accounts and has received federal protection under the Endangered Species Act. We investigated captive-breeding of a captive-flock of Gunnison sage-grouse created from individuals reared in captivity from wild-collected eggs we artificially incubated. We also introduced wild-reared individuals into captivity. Our captive-flock successfully bred and produced fertile eggs. We controlled the timing and duration of male-female breeding interactions and facilitated a semi-natural mating regime. Males established a strutting ground in captivity that females attended for mate selection. In 2010, we allowed females to establish eight nests, incubate, and hatch eggs. Females in captivity were more successful incubating nests than raising broods. Although there are many technical, financial, and logistic issues associated with captive-breeding, we recommend that federal biologists and managers work collaboratively with state wildlife agencies and consider developing a captive-flock as part of a comprehensive conservation strategy for a conservation-reliant species like the Gunnison sage-grouse. The progeny produced from a captive-rearing program could assist in the recovery if innovative approaches to translocation are part of a comprehensive proactive conservation program.

Behavioural Repertoires and Time Budgets of Semi-Free-Ranging and Captive Groups of Wedge-Capped Capuchin Monkeys, Cebus olivaceus, in Zoo Exhibits in Venezuela.

The behavioural repertoires and time budgets of 2 captive groups and 1 semi-free-ranging group of Cebus olivaceus were determined with the aim to assess the impact of the zoo environment on behaviour. The repertoires were qualitatively similar between groups and to those reported for wild troops, but the captive groups showed self-directed and stereotyped behaviours not reported in the wild. The differences in repertoires between groups were easily associated with the opportunity to interact directly with the visitors, with particularities of the enclosure and with the severity of confinement. Overall, females spent more time foraging than males in the 2 captive groups, and adults rested and watched more than subadults in all the groups. Time budgets were dominated by foraging, resting, movement and affiliative interactions, but their relative importance varied between groups, with foraging being especially prominent in the most confined group. The time budgets also varied qualitatively from those reported for wild troops. We conclude the species is behaviourally able to adjust to captivity, but the slight differences along the continuum from wild to semi-free to captive are suggestive of mild stress or social tension probably due to unstimulating environmental conditions, high visitor pressure and deviations from typical sex-age group composition.

Short-term costs and benefits of grooming in Japanese macaques.

This study investigated the short-term consequences of giving grooming in Japanese macaques (Macaca fuscata) in order to obtain information on its immediate costs and benefits. Giving grooming was associated with increased aggression received from groomees and decreased aggression received from third parties (but only as long as the groomer maintained proximity to the groomee). Grooming was also associated with decreased scratching rates. These results emphasize the unpredictable outcome of individual grooming interactions and the difficulties of social decision-making for monkeys living in despotic societies.

Diurnal and nocturnal activity budgets of zoo elephants in an outdoor facility.

The present study examined the activity budgets of 15 African elephants (1 bull, 6 cows, 2 male juveniles, 2 female juveniles, and 4 male calves) living at the San Diego Zoo Safari Park during the summers of 2010 and 2011. Onsite behavioral data (n = 600 hr) were collected for approximately 12 weeks from 0400 to 0830 and 1100 to 2400 during the 2010 and 2011 summer season. Foraging was the most common behavior state during the day followed by resting, and walking. During the evening hours, the elephants spent majority of their time foraging, resting, and sleeping. The average rate of self-maintenance behavior events (dust, wallow, etc.) increased from 0600 to 0700, 1100 to 1500, and from 1700 to 1900. Positive social behavior events (touch other, play, etc.) remained high from 0500 to 2300, with peaks at 0600, 1300, 1500, and 1900. Negative social events occurred at low rates throughout the day and night, with peaks at 0600, 1900, and 2200. The majority of positive behavior events during the daylight and nighttime hours involved the mother-calf pairs. Furthermore, the calves and juveniles initiated approximately 60% of all social events during the daytime and 57% of all social interactions at night. The results of this study demonstrate the differences between diurnal and nocturnal activity budgets of a multi-age and sex elephant herd in a zoological facility, which highlights the importance of managing elephants to meet their 24 hr behavioral needs.

Assessment of ovarian cycles in the African elephant (Loxodonta africana) by measurement of salivary progesterone metabolites.

Monitoring ovarian cycles through hormonal analysis is important in order to improve breeding management of captive elephants, and non-invasive collection techniques are particularly interesting for this purpose. However, there are some practical difficulties in collecting proper samples, and easier and more practical methods may be an advantage for some institutions and/or some animals. This study describes the development and validation of an enzymeimmunoassay (EIA) for progestins in salivary samples of African elephants, Loxodonta africana. Weekly urinary and salivary samples from five non-pregnant elephant cows aged 7-12 years were obtained for 28 weeks and analyzed using EIA. Both techniques correlated positively (r = 0.799; P < 0.001), and the cycle characteristics obtained were identical. The results clearly show that ovarian cycles can be monitored by measuring progestins from salivary samples in the African elephant. This is a simple and non-invasive method that may be a practical alternative to other sampling methods used in the species.

Multidisciplinary approaches and assessment techniques to better understand and enhance zoo nonhuman animal welfare.

Nonhuman animal welfare is a complex concept that encompasses an animal's biological functioning, emotional states, and opportunities to experience a natural life, including the performance of natural behaviors. Further, animal welfare can be viewed as quality of life from the perspective of the animal and thus must consider the animal's subjective experiences. Therefore, assessing and enhancing animal welfare should include multidisciplinary, scientific ventures that strive to create a complete picture of how animals' bodies and minds respond to both aversive and pleasant situations. Practical assessment of animal welfare should include outcome-based measures from the animal that provide information about the individual's welfare as well as resource-based measures that can help identify causes of or risk factors for poor welfare. Increasingly, scientists are examining the emotional states of animals as well as the impact of pain, pleasure, and consciousness on animal welfare. This article discusses approaches such as preference testing, instrumental learning, examination of space and resource use, and qualitative assessments of animal welfare that might be useful and practical for assessing and enhancing welfare in zoo settings.

Circadian rhythm of salivary cortisol in Asian elephants (Elephas maximus): a factor to consider during welfare assessment.

Elevated glucocorticoid levels during an extended time period might be a stress indicator in nonhuman animals. Therefore, knowledge of the circadian pattern of cortisol secretion is very important to correctly interpret data obtained for welfare assessment of animals in captivity through salivary cortisol. In order to define the circadian rhythm of salivary cortisol secretion in the Asian elephant (Elephas maximus), morning and evening saliva samples of 3 Asian elephants were collected and analyzed by radioimmunoassay. Significantly higher salivary cortisol concentrations were found in the morning than in the evening in all individuals. These results show that salivary cortisol of Asian elephants follows a diurnal pattern of secretion, which could be taken into account when using this methodology to assess welfare in captive Asian elephants.

Tri-axial dynamic acceleration as a proxy for animal energy expenditure; should we be summing values or calculating the vector?

Dynamic body acceleration (DBA) has been used as a proxy for energy expenditure in logger-equipped animals, with researchers summing the acceleration (overall dynamic body acceleration--ODBA) from the three orthogonal axes of devices. The vector of the dynamic body acceleration (VeDBA) may be a better proxy so this study compared ODBA and VeDBA as proxies for rate of oxygen consumption using humans and 6 other species. Twenty-one humans on a treadmill ran at different speeds while equipped with two loggers, one in a straight orientation and the other skewed, while rate of oxygen consumption (VO2) was recorded. Similar data were obtained from animals but using only one (straight) logger. In humans, both ODBA and VeDBA were good proxies for VO2 with all r(2) values exceeding 0.88, although ODBA accounted for slightly but significantly more of the variation in VO2 than did VeDBA (P<0.03). There were no significant differences between ODBA and VeDBA in terms of the change in VO2 estimated by the acceleration data in a simulated situation of the logger being mounted straight but then becoming skewed (P = 0.744). In the animal study, ODBA and VeDBA were again good proxies for VO2 with all r(2) values exceeding 0.70 although, again, ODBA accounted for slightly, but significantly, more of the variation in VO2 than did VeDBA (P<0.03). The simultaneous contraction of muscles, inserted variously for limb stability, may produce muscle oxygen use that at least partially equates with summing components to derive DBA. Thus, a vectorial summation to derive DBA cannot be assumed to be the more 'correct' calculation. However, although within the limitations of our simple study, ODBA appears a marginally better proxy for VO2. In the unusual situation where researchers are unable to guarantee at least reasonably consistent device orientation, they should use VeDBA as a proxy for VO2.

Science-based assessment of animal welfare: wild and captive animals.

Science-based assessment of animal welfare in wild and captive animals has, during the past ten years, benefited from increased interest in and research into consciousness, emotions, stress and pain. Because it is impossible to make a detailed physiological study in free-living animals, reliance must be placed on behaviour and Darwinian fitness, which have been shown to correlate to welfare. Only in captive animals can more detailed physiological studies be made, and then not without difficulty. In short, the welfare of an animal is shown to be compromised if the animal exhibits similar behaviour to that of animals whose physiological responses have been confirmed as indicating poor welfare, and if its Darwinian fitness is compromised in similar ways to such animals.