Male elephant management in AZA institutions: Current status and priorities for the future.

Asian elephant (Elephas maximus) and African savanna elephant (Loxodonta africana) populations collectively managed by ex-situ facilities accredited by the Association of Zoos and Aquariums (AZA) face sustainability challenges. Among the priorities to strengthen animal wellbeing and population sustainability is male elephant management. We conducted a survey of AZA facilities currently housing male elephants to assess the status, challenges, and priorities in three areas of male elephant management: musth, socialization, and semen collection. Surveys were administered to elephant care teams at AZA-accredited institutions between November 2022 and February 2023, and we received responses from 34 institutions (91.9% of AZA-accredited facilities holding adult male elephants), housing 32 adult male Asians and 26 adult male Africans. Most facilities prioritized breeding and male socialization over musth management and semen collection (although most facilities acknowledged that all these efforts are important), citing leadership support and staffing as most important to achieve male management goals. Behaviors most commonly accompanying musth included reduced appetite, difficulty training or shifting, human-directed aggression, and interest in females. Musth timing was variable between males and facilities. Most males were well-socialized with females and/or other males, though elephant compatibility and facility design were limiting factors in managing socialization. Although 60.6% of facilities collected semen or were training for semen collection, very few male elephants could reliably provide viable semen samples, challenging assisted reproductive efforts that could bolster population sustainability in both species. Together, our results provide a better understanding of the state of male elephant management, offering specific areas deserving of research and development to enhance wellbeing and sustainability.

Lack of reinforcement is hard to "bear": Assessing judgment bias in grizzly bears (Ursus arctos horribilis).

Cognitive biases reveal underlying affective state by indicating optimism and pessimism. This methodology may permit assessment of positive welfare in animals that have few validated positive welfare indicators, such as bears. Our goal was to validate a judgment bias test for assessing optimism in brown bears, using a touchscreen. After training the bears on a conditional discrimination, we compared responses to an ambiguous stimulus in a 2 × 2 nested design involving four experimental conditions representing presence or absence of a behind-the-scenes tour and presence or absence of a keeper training session with food reinforcement. We recorded bears' behavior during the conditions as a measure of convergent validity. Testing revealed the possibility of pessimism in the absence of reinforcement in one bear. More frustration behaviors were also observed during the no food reinforcement conditions. This is the first experimental demonstration of brown bears using a touchscreen and one of only three reports in which bears have been reported to perform a conditional discrimination. This method of assessing underlying affective state shows promise for the future.

Asian elephants distinguish sexual status and identity of unfamiliar elephants using urinary odours.

Despite the ubiquity of odours in mammals, few studies have documented the natural olfactory abilities of many 'non-model' species such as the Asian elephant. As Asian elephants are endangered, we may apply odours to more effectively manage threatened populations. We implemented a habituation-discrimination paradigm for the first time in Asian elephants to test the ability of elephants to discriminate between unfamiliar male elephant urine, hypothesizing that elephants would successfully distinguish non-musth from musth urine and also distinguish identity between two closely related individuals. We conducted two bioassay series, exposing three female and three male zoo-housed elephants to the same urine sample (non-musth urine in the first series, and urine from an unfamiliar individual in the second) over 5 days. On the sixth day, we simultaneously presented each elephant with a novel sample (either musth urine or urine from a second unfamiliar individual) alongside the habituated urine sample, comparing rates of chemosensory response to each sample to indicate discrimination. All elephants successfully discriminated non-musth from musth urine, and also urine from two unfamiliar half-brothers. Our results further demonstrate the remarkable olfactory abilities of elephants with promising implications for conservation and management.

Postoccupancy evaluation of staff, visitors, and three species of animals in a zoo setting.

Postoccupancy evaluation (POE) was used to assess newly constructed zoo exhibits from the perspective of three user groups: zoo staff, zoo visitors, and the animals. Staff represents a generally understudied user group in zoo-based POEs. We asked staff to rate the animals' space, the visitors' space, and the staff's space at previous and new exhibits. We also compared zoo visitors' ratings of the animals' behavior and environments, overall exhibit impressions, and the time visitors spent viewing previous and new exhibits. Lastly, we compared activity and space use of a Komodo dragon (Varanus komodoensis), two red pandas (Ailurus fulgens), and one rhinoceros (Rhinoceros unicornis) in their previous and new exhibits. Staff rated animal, visitor, and staff areas higher at the new exhibits compared to the previous exhibits. Visitors also rated several factors higher and spent more time at the new exhibits. The most naturalistic exhibit received the most favorable ratings in all categories and animal activity increased visitor stay time. We found that red pandas were less active in their new exhibit, and the Komodo dragon and rhino showed no difference in activity. The red pandas and the Komodo dragon used more available space in their new exhibits; however, we recommend using Electivity index to examine resource preferences for these species, whose enclosure use has been less studied than large mammals. We emphasize the importance of including staff in zoo-based POE, make other recommendations for future POE studies, and discuss various factors that could have influenced our results.

Persistence is key: investigating innovative problem solving by Asian elephants using a novel multi-access box.

Innovative problem solving is considered a hallmark measure of behavioral flexibility as it describes behavior by which an animal manipulates its environment in a novel way to reach a goal. Elephants are a highly social taxa that have demonstrated a remarkable capacity for adapting to changing environments. To understand how individual differences in behavior impact expressions of innovation, we used a novel extractive foraging device comprised of three compartments to evaluate innovation in 14 captive Asian elephants. In the first phase of testing, elephants had an opportunity to learn one solution, while the second phase gave them an opportunity to innovate to open two other compartments with different solutions. We measured the behavioral traits of neophilia, persistence, motivation, and exploratory diversity, and hypothesized that higher levels of each would be associated with more success in the second phase. Eight elephants innovated to solve three compartments, three solved two, and two solved only one. Consistent with studies in other species, we found that higher success was associated with greater persistence, but not with any other behavioral traits when analyzed per test session. Greater persistence and, unexpectedly, lower exploratory diversity, were associated with success when analyzed at the level of each individual door. Further work is needed to understand how innovation varies both within and between species, with particular attention to the potential impact of anthropogenic changes in wild environments.

Performance of Asian elephants (Elephas maximus) on a quantity discrimination task is similar to that of African savanna elephants (Loxodonta africana).

Using an object-choice task, we measured the relative quantity discrimination ability of Asian elephants. Two zoo-housed elephants were given auditory cues of food being dropped into two containers (Nonvisible condition), and in one condition they could also see the food on top of the containers (Visible condition). Elephants received sets of varying ratios and magnitudes. We found that the elephants chose the greater quantity of food significantly above chance in both the Visible and Nonvisible conditions. Additionally, we found the elephants' ability to discriminate between quantities decreased as the ratio, and not the absolute difference, between the quantities increased, which is predicted by the accumulator model. We also compare our findings to those from a study using the same methods with African savanna elephants and found that the two species performed at similar levels, but given our small sample size it is difficult to make strong species-level conclusions. In discussing our results, we consider differences between the two species' wild environments as well as the types of sensory cues provided in human care, and we provide recommendations for extensions of this work.

Use of urinary 13,14, dihydro-15-keto-prostaglandin F2α (PGFM) concentrations to diagnose pregnancy and predict parturition in the giant panda (Ailuropoda melanolecua).

Pregnancy determination is difficult in the giant panda (Ailuropoda melanolecua), representing a challenge for ex situ conservation efforts. Research in other species experiencing pseudopregnancy indicates that urinary/fecal concentrations of 13,14, dihydro-15-keto-prostaglandin F2α (PGFM) can accurately determine pregnancy status. Our objective was to determine if urinary PGFM concentrations are associated with pregnancy status in the giant panda. Urinary PGFM concentrations were measured in female giant pandas (n = 4) throughout gestation (n = 6) and pseudopregnancy (n = 4) using a commercial enzyme immunoassay. Regardless of pregnancy status, PGFM excretion followed a predictable pattern: 1) baseline concentrations for 11-19 weeks following ovulation; 2) a modest, initial peak 14-36 days after the start of the secondary urinary progestagen rise; 3) a subsequent period of relatively low concentrations; and 4) a large, terminal peak at the end of the luteal phase. Pregnant profiles were distinguished by an earlier initial peak (P = 0.024), higher inter-peak concentrations (P < 0.001), and a larger terminal peak (P = 0.003) compared to pseudopregnancy profiles. Parturition occurred 23 to 25 days from the initial PGFM surge and within 24 hours of the start of the terminal increase. These pattern differences indicate that urinary PGFM monitoring can be used to predict pregnancy status and time parturition in the giant panda. Furthermore, this is the only species known to exhibit a significant PGFM increase during pseudopregnancy, suggesting a unique physiological mechanism for regulating the end of the luteal phase in the giant panda.

Giant Panda Maternal Care: A Test of the Experience Constraint Hypothesis.

The body condition constraint and the experience condition constraint hypotheses have both been proposed to account for differences in reproductive success between multiparous (experienced) and primiparous (first-time) mothers. However, because primiparous mothers are typically characterized by both inferior body condition and lack of experience when compared to multiparous mothers, interpreting experience related differences in maternal care as support for either the body condition constraint hypothesis or the experience constraint hypothesis is extremely difficult. Here, we examined maternal behaviour in captive giant pandas, allowing us to simultaneously control for body condition and provide a rigorous test of the experience constraint hypothesis in this endangered animal. We found that multiparous mothers spent more time engaged in key maternal behaviours (nursing, grooming, and holding cubs) and had significantly less vocal cubs than primiparous mothers. This study provides the first evidence supporting the experience constraint hypothesis in the order Carnivora, and may have utility for captive breeding programs in which it is important to monitor the welfare of this species' highly altricial cubs, whose survival is almost entirely dependent on receiving adequate maternal care during the first few weeks of life.

The birth of a giant panda: Tracking the biological factors that successfully contribute to conception through to postnatal development.

Reproducing giant pandas (Ailuropoda melanoleuca) remains the most challenging aspect of managed care of this species. However, advancement in knowledge stemming from basic science research on the giant panda has facilitated a growth in the population. Here, we report the successful application of reproductive technologies, including noninvasive hormone monitoring, behavioral/morphometric observations, ultrasonographic evaluations, and acute phase protein assessment, in an individual female. By applying these approaches to one female, we report the practicality and usefulness of a multidisciplinary approach to reproductive care of the species. In addition, the utilization of various technologies across multiple physiological states also provided us an opportunity to record previously understudied events, such as maternal response to weaning and growth of a conceptus.

Preliminary evidence for color stimuli discrimination in the Asian small-clawed otter (Aonyx cinerea).

Color discrimination ability can be determined through anatomy or perceptual ability. In this study we tested perceptual ability. Three Asian small-clawed otters (Aonyx cinerea), one male and two females, were trained via operant conditioning to discriminate stimuli within a training task. If they passed criteria for this task, they were tested on as many as six delayed matching-to-sample experimental tasks. These experimental tasks involved comparing varying saturations of the colors blue, green, and red against varying shades of gray, as well as against each other. The male reached criterion on five of the experimental tasks, indicating an ability to discriminate the stimuli. One female participated in only two tasks and did not achieve the criteria as set. The second female did not pass the training task, and thus was not experimentally tested. This study overall showed some early evidence that Asian small-clawed otters may have the ability to learn to discriminate different stimuli on the basis of color cues. Sensory studies conducted on two other otter species and the results of this study indicate that color vision may be a common trait across Lutrinae species.

Behavioral and hormonal consequences of transporting giant pandas from China to the United States.

Zoological institutions strive to ensure the welfare of nonhuman animals in captivity. Part of this effort involves reducing the level of distress experienced by an animal to the greatest extent possible. However, some necessary zoo management practices such as transportation induce stress responses. An extensive literature exists concerning the animal welfare implications of road transportation for farm and laboratory animals. There has, however, been little focus on the effects of air transportation on wild animals in captivity. Because many endangered species are transported by air for breeding purposes, it is especially important to study the effects of stress on these species. This study investigated the behavioral and hormonal consequences of transporting 4 giant pandas (2 male-female pairs) by air from China to the United States. An autoregressive test revealed that urinary cortisol measures were highest for 2 subjects, Lun Lun and Tian Tian, during the flight than during the remainder of the 30-day period posttransport (p < .01). No long-term behavioral changes or problems emerged as a result of the transport. The study found that more research is needed to develop a complete understanding of transportation stress and welfare in captive wildlife.

Rising fecal glucocorticoid concentrations track reproductive activity in the female giant panda (Ailuropoda melanoleuca).

To better understand the adaptive significance of adrenal glucocorticoid (GC) variation in the giant panda, we assessed patterns of fecal GC excretion over time as well as during estrus, parturient and non-parturient luteal phases, lactation and acyclicity in 17 adult females. Fecal estrogen and GC patterns were positively correlated (P<0.05) in four of five periestrual females (r = 0.57-0.92). Among all reproductive states, fecal GC was highest (P<0.05) during periestrus (non-parturient, 495.9 ± 100.7 ng/g [mean ± SE]; parturient, 654.1 ± 10 6.5 ng/g; P>0.05). Concentrations of GC metabolites were lower (P<0.05) during the later stage of the luteal phase in non-parturient (334.8 ± 24.8 ng/g) compared to parturient (470.4 ± 54.0 ng/g) females. Although fecal GC concentrations in cyclic, non-parturient females did not differ (P>0.05) across all seasons, there were seasonal variations (P<0.05) in females that were acyclic and non-lactational. However, the overall lack of difference (P>0.05) in GC values between reproductively cyclic and acyclic females did not support the hypothesis that ovarian acyclicity is due to increased adrenal activity (related or unrelated to physiological stress). Furthermore, GCs may play an important role in the normal endocrine milieu associated with sexual receptivity and late pregnancy. These data demonstrate that both reproductive status and seasonal factors are important modulators of adrenal function in this endangered species.

Sex differences in spatial ability: a test of the range size hypothesis in the order Carnivora.

Sex differences in spatial cognition have been reported for many species ranging from voles to humans. The range size hypothesis predicts that sex differences in spatial ability will only occur in species in which the mating system selects for differential range size. Consistent with this prediction, we observed sex differences in spatial ability in giant pandas, a promiscuous species in which males inhabit larger ranges than females, but did not observe sex differences in Asian small-clawed otters, a related monogamous species in which males and females share home ranges. These results provide the first evidence of sex differences in spatial ability in the order Carnivora, and are consistent with the range size hypothesis.

Endocrine milieu of perioestrus in the giant panda (Ailuropoda melanoleuca), as determined by non-invasive hormone measures.

The aim of the present study was to determine the efficacy of faecal hormonal measures for evaluating ovarian activity in a significant sized cohort of giant pandas during the perioestrual period. Faecal excretion of oestrogen and progestagen metabolites corresponded with urinary patterns and receptive behaviours. Longitudinal assessment of 10 females revealed that, on average, faecal oestrogen concentrations started to rise (P < 0.05) above baseline (baseline mean +/- s.e.m.; 64.7 +/- 6.6 ng g(-1)) 5 days before the preovulatory oestrogen peak (484.6 +/- 126.8 ng g(-1)), which was followed by a gradual descent over 4 days to nadir. Mean faecal progestagen metabolite concentrations increased approximately twofold above baseline (from 186.2 +/- 37.7 to 347.2 +/- 75.7 ng g(-1); P < 0.05) during the 20-day interval after the preovulatory oestrogen surge. Variability within and among females precluded the use of a threshold of oestrogen or progestagen metabolites to predict reproductive status, yet faeces collected 2-3 days per week provided sufficient data to recognise that an individual was in the perioestrual period. Finally, in females that were examined for at least 3 consecutive years, there was an 18-53 day variation in the onset and an 8-13 day variation in the duration of perioestrual behaviour from year to year. In summary, these findings indicate that gonadal hormone profiles associated with the period immediately before, during and after oestrus are accurately revealed by analysis of the fibrous faeces of the giant panda. This approach has potential value for providing point-in-time information on the reproductive status of free-living individuals.

Unique biphasic progestagen profile in parturient and non-parturient giant pandas (Ailuropoda melanoleuca) as determined by faecal hormone monitoring.

The luteal phase of the giant panda has been exclusively assessed by studying urinary hormone patterns in a very few individuals. To better understand hormonal dynamics of protracted progestagen excretion in this endangered species, we monitored hormonal metabolites in the fibrous faeces of multiple females in the USA and China. Giant pandas that were anoestrual during the breeding season excreted baseline progestagen throughout the year. In contrast, there were two distinctive periods when progestagen excretion increased in females that experienced behavioural oestrus, the first being modest, lasting for 61-122 days, and likely reflecting presumptive ovulation. This increase was far surpassed by a secondary rise in progestagen excretion associated with a rejuvenated luteal capacity or hormone production from an extra-gonadal source. The duration of this 'secondary' rise in progestagen excretion averaged approximately 45 days and terminated in a decline to baseline coincident with parturition or the end of a non-parturient luteal interval. Data revealed that, even with a complex, biphasic progestagen profile, the longitudinal patterns produced by giant pandas were relatively consistent among animals and across years within individuals. However, progestagen excretion patterns throughout this period could not be used to discriminate among non-pregnant, pregnant or pseudopregnant states.

Vocal cues to identity and relatedness in giant pandas (Ailuropoda melanoleuca).

A range of acoustic characteristics typically carry information on individual identity in mammalian calls. In addition, physical similarities in vocal production anatomy among closely related individuals may result in similarities in the acoustic structure of vocalizations. Here, acoustic analyses based on source-filter theory were used to determine whether giant panda bleats are individually distinctive, to investigate the relative importance of different source-(larynx) and filter-(vocal tract) related acoustic features for coding individuality, and to test whether closely related individuals have similarities in call structure. The results revealed that giant panda bleats are highly individualized and indicate that source-related features, in particular, mean fundamental frequency, amplitude variation per second, and the mean extent of each amplitude modulation, contribute the most to vocal identity. In addition, although individual pairwise relatedness was not correlated with overall acoustic similarity, it was highly correlated with amplitude modulation rate and fundamental frequency range, suggesting that these acoustic features are heritable components of giant panda bleats that could be used as a measure of genetic relatedness. The ecological relevance of acoustically signaling information on caller identity and the potential practical implications for acoustic monitoring of population levels in this endangered species are discussed.

Spatial memory recall in the giant panda (Ailuropoda melanoleuca).

The current study tested spatial memory recall in 1 male and 1 female giant panda (Ailuropoda melanoleuca). The task required subjects to make a delayed response to a previously lighted location, with varying lengths of delay between the observation phase and the test phase. The male subject reached criterion at 2-, 3-, 4-, 5-, 6-, and 10-s delays. The female subject reached criterion at 2-, 3-, 4-, 5-, 6-, 10-, and 15-s delays. The results support the hypothesis that giant pandas demonstrate significant working memory for spatial location in the absence of external cues, which may be an important mechanism for survival in the wild.

Color vision in the giant panda (Ailuropoda melanoleuca).

Hue discrimination abilities of giant pandas were tested, controlling for brightness. Subjects were 2 adult giant pandas (1 male and 1 female). A simultaneous discrimination procedure without correction was used. In five tasks, white, black, and five saturations each of green, blue, and red served as positive stimuli that were paired with one or two comparison stimuli consisting of 16 saturations of gray. To demonstrate discrimination, the subjects were required to choose the positive stimulus in 16 of 20 trials (80% correct) for three consecutivesessions. Both subjects reached criterion forgreen and red. The female subject also reached criterion for blue. The male was not tested for blue. This study is a systematic replication of Bacon and Burghardt's (1976) color discrimination experiment on black bears. The results suggest that color vision in the giant panda is comparable to that of black bears and other carnivores that are not strictly nocturnal.

Behavioral and developmental consequences of early rearing experience for captive giant pandas (Ailuropoda melanoleuca).

Mother-reared (MR) and peer-reared (PR) captive giant panda (Ailuropoda melanoleuca) cubs were compared to evaluate the effects of early removal from mother on behavioral development. Males and females and twins and singletons were compared to assess the effects of social setting on behavioral development. Subjects included 2 PR females, 3 MR females, 3 MR males, and 3 mothers. MR cubs spent more time manipulating bamboo and fell more often than PR cubs. PR cubs spent more time inactive. Male cubs directed more playful behavior at their mothers. Twins spent more time play fighting with their mothers than with their siblings. The results suggest that peer-rearing does not provide young pandas with the same level of social stimulation as mother-rearing.