Survival improvements of marine mammals in zoological institutions mirror historical advances in human longevity.

An intense public debate has fuelled governmental bans on marine mammals held in zoological institutions. The debate rests on the assumption that survival in zoological institutions has been and remains lower than in the wild, albeit the scientific evidence in support of this notion is equivocal. Here, we used statistical methods previously applied to assess historical improvements in human lifespan and data on 8864 individuals of four marine mammal species (harbour seal, Phoca vitulina; California sea lion, Zalophus californianus; polar bear, Ursus maritimus; common bottlenose dolphin, Tursiops truncatus) held in zoos from 1829 to 2020. We found that life expectancy increased up to 3.40 times, and first-year mortality declined up to 31%, during the last century in zoos. Moreover, the life expectancy of animals in zoos is currently 1.65-3.55 times longer than their wild counterparts. Like humans, these improvements have occurred concurrently with advances in management practices, crucial for population welfare. Science-based decisions will help effective legislative changes and ensure better implementation of animal care.

Assessing the effectiveness of protected areas for panda conservation under future climate and land use change scenarios.

While the relatively stable land use and land cover (LULC) patterns is an important feature of protected areas (PAs), the influence of this feature on future species distribution and the effectiveness of the PAs has rarely been explored. Here, we assessed the role of land use patterns within PAs on the projected range of the giant panda (Ailuropoda melanoleuca) by comparing projections inside and outside of PAs for four model configurations: (1) only climate covariates, (2) climate and dynamic land use covariates, (3) climate and static land use covariates and (4) climate and hybrid dynamic-static land use covariates. Our objectives were twofold: to understand the role of protected status on projected panda habitat suitability and evaluate the relative efficacy of different climate modeling approaches. The climate and land use change scenarios used in the models include two shared socio-economic pathways (SSPs) scenarios: SSP126 [an optimistic scenario] and SSP585 [a pessimistic scenario]. We found that models including land-use covariates performed significantly better than climate-only models and that these projected more suitable habitat than climate-only models. Static land-use models projected more suitable habitat than both the dynamic and hybrid models under SSP126, while these models did not differ under SSP585. China's panda reserve system was projected to effectively maintain suitable habitat inside PAs. Panda dispersal ability also significantly impacted outcomes, with most models assuming unlimited dispersal forecasting range expansion and models assuming zero dispersal consistently forecasting range contraction. Our findings highlight that policies targeting improved land-use practices should be an effective means for offsetting some of the negative effects of climate change on pandas. As the effectiveness of PAs is projected to be maintained, we recommend the judicious management and expansion of the PA system to ensure the resilience of panda populations into the future.

Factors influencing terrestriality in primates of the Americas and Madagascar.

Among mammals, the order Primates is exceptional in having a high taxonomic richness in which the taxa are arboreal, semiterrestrial, or terrestrial. Although habitual terrestriality is pervasive among the apes and African and Asian monkeys (catarrhines), it is largely absent among monkeys of the Americas (platyrrhines), as well as galagos, lemurs, and lorises (strepsirrhines), which are mostly arboreal. Numerous ecological drivers and species-specific factors are suggested to set the conditions for an evolutionary shift from arboreality to terrestriality, and current environmental conditions may provide analogous scenarios to those transitional periods. Therefore, we investigated predominantly arboreal, diurnal primate genera from the Americas and Madagascar that lack fully terrestrial taxa, to determine whether ecological drivers (habitat canopy cover, predation risk, maximum temperature, precipitation, primate species richness, human population density, and distance to roads) or species-specific traits (body mass, group size, and degree of frugivory) associate with increased terrestriality. We collated 150,961 observation hours across 2,227 months from 47 species at 20 sites in Madagascar and 48 sites in the Americas. Multiple factors were associated with ground use in these otherwise arboreal species, including increased temperature, a decrease in canopy cover, a dietary shift away from frugivory, and larger group size. These factors mostly explain intraspecific differences in terrestriality. As humanity modifies habitats and causes climate change, our results suggest that species already inhabiting hot, sparsely canopied sites, and exhibiting more generalized diets, are more likely to shift toward greater ground use.

Long-term increases in pathogen seroprevalence in polar bears (Ursus maritimus) influenced by climate change.

The influence of climate change on wildlife disease dynamics is a burgeoning conservation and human health issue, but few long-term studies empirically link climate to pathogen prevalence. Polar bears (Ursus maritimus) are vulnerable to the negative impacts of sea ice loss as a result of accelerated Arctic warming. While studies have associated changes in polar bear body condition, reproductive output, survival, and abundance to reductions in sea ice, no long-term studies have documented the impact of climate change on pathogen exposure. We examined 425 serum samples from 381 adult polar bears, collected in western Hudson Bay (WH), Canada, for antibodies to selected pathogens across three time periods: 1986-1989 (n = 157), 1995-1998 (n = 159) and 2015-2017 (n = 109). We ran serological assays for antibodies to seven pathogens: Toxoplasma gondii, Neospora caninum, Trichinella spp., Francisella tularensis, Bordetella bronchiseptica, canine morbillivirus (CDV) and canine parvovirus (CPV). Seroprevalence of zoonotic parasites (T. gondii, Trichinella spp.) and bacterial pathogens (F. tularensis, B. bronchiseptica) increased significantly between 1986-1989 and 1995-1998, ranging from +6.2% to +20.8%, with T. gondii continuing to increase into 2015-2017 (+25.8% overall). Seroprevalence of viral pathogens (CDV, CPV) and N. caninum did not change with time. Toxoplasma gondii seroprevalence was higher following wetter summers, while seroprevalences of Trichinella spp. and B. bronchiseptica were positively correlated with hotter summers. Seroprevalence of antibodies to F. tularensis increased following years polar bears spent more days on land, and polar bears previously captured in human settlements were more likely to be seropositive for Trichinella spp. As the Arctic has warmed due to climate change, zoonotic pathogen exposure in WH polar bears has increased, driven by numerous altered ecosystem pathways.

Climate change and landscape-use patterns influence recent past distribution of giant pandas.

Climate change is one of the most pervasive threats to biodiversity globally, yet the influence of climate relative to other drivers of species depletion and range contraction remain difficult to disentangle. Here, we examine climatic and non-climatic correlates of giant panda (Ailuropoda melanoleuca) distribution using a large-scale 30 year dataset to evaluate whether a changing climate has already influenced panda distribution. We document several climatic patterns, including increasing temperatures, and alterations to seasonal temperature and precipitation. We found that while climatic factors were the most influential predictors of panda distribution, their importance diminished over time, while landscape variables have become relatively more influential. We conclude that the panda's distribution has been influenced by changing climate, but conservation intervention to manage habitat is working to increasingly offset these negative consequences.

Assessing the Effectiveness of China's Panda Protection System.

Protected areas form the backbone of biodiversity conservation, yet their effectiveness is often not known nor even evaluated [1-3]. China-best known for its record of ecological degradation in the face of rapidly increasing gross domestic product and resource consumption [4]-has in recent years enacted a series of policies and programs to conserve its natural resources. Chief among them is an ambitious protected area system covering 17% of its terrestrial land mass [4, 5]. An important early impetus for the establishment of this reserve system was the protection of the giant panda (Ailuropoda melanoleuca) [5-8]. Using data from two previous large-scale surveys [9, 10] separated by a decade, and including over 50,000 habitat plots, we examined the panda population and habitat trends inside and outside reserves. Despite ambitious ecocompensation programs in panda habitat outside reserves [11-13], the protection provided by reserves reduced most classes of human disturbance compared to outside reserves, and most disturbances decreased through time more strongly inside than outside reserves. Reserves also contained more and increasing suitable panda than found outside reserves [14, 15]. Comparing reserve performance, reserves with increasing older forests and bamboo correlated with increasing panda populations. Together these findings indicate that China's panda reserves have been effective and that they are functioning better over time, conserving more and better habitats and containing more pandas. While China's protected area system still has much room for improvement [4, 5], including to support pandas [16], these findings underscore the progress made in China's nascent environmental movement.

Influence of season and social context on male giant panda (Ailuropoda melanoleuca) vocal behaviour.

Documenting the different social and behavioural contexts that vocalisations are produced in remains an important step towards understanding the functional relevance of specific call types in a given species' vocal repertoire. In this study we investigated whether seasonal differences and the presence or absence of male and female conspecifics influence the production of male giant panda vocal signals. To this end, captive male giant pandas were observed during and outside of the breeding season in three social contexts: only male conspecific neighbours, only female conspecific neighbours, and a context with no neighbours. We found that males were more likely to bleat, chirp, honk and moan during the breeding season, and showed a tendency to growl more outside of the reproductive period. The contextual analysis revealed that bleats were more likely to be produced by males when opposite-sexed conspecifics are in close attendance during the breeding season. Conversely, males were more likely to chirp when neighboured by males than females or no neighbours. In addition, males were more likely to honk in the absence of neighbouring conspecifics during the breeding season, raising the possibility that these calls function to signal location and gain the attention of potential mates. Moans were produced more often when male giant pandas had male than female neighbours during the breeding season, which may reflect mild aggression towards these same-sexed rivals, whereas the production of barks and growls did not vary according to season or the sex of conspecific neighbours. Our findings underscore the importance of male giant panda bleats for coordinating reproduction and promoting contact with potential mating partners in this non-gregarious species, and yield fresh insights into the function of male honks that warrant further investigation. They also provide a basis for comparison with free-ranging giant panda vocal behaviour that could potentially inform conservation efforts.

Comprehensive Breeding Techniques for the Giant Panda.

The dramatic growth of the captive giant panda (Ailuropoda melanoleuca) population exemplifies how the application of scientific findings to animal care and reproductive management can improve conservation breeding outcomes. Detailed behavioral studies of giant panda estrus, pregnancy and cub rearing have demonstrated the importance of husbandry management that supports natural reproductive behavior to enhance breeding success. Natural breeding has been valuably augmented by the development of assisted reproductive techniques founded through detailed studies of the reproductive physiology of the giant panda and outlining fundamental information about reproductive seasonality, male fertility and characterization of the estrous cycle. The resultant holistic understanding of giant panda reproduction has improved reproductive success in the captive population to such an extent that it is now self-sustaining and provides surplus animals for reintroduction. Despite these significant advances, there are knowledge gaps and remaining challenges to be addressed. Pregnancy detection remains the single biggest challenge when determining if natural mating or assisted breeding have been successful. Because pregnancy can only be determined in the few weeks prior to parturition, there are gaps in understanding and detecting delayed implantation and early embryonic loss. Additionally, dynamic management practices and standard of care for reproductive assistance needs to be developed. Only large breeding centers in China have the ability to promote normal reproductive behaviors and allow mate choice for the giant panda. These challenges need to be addressed in the near future in order to maintain a self-sustaining, genetically diverse and behaviorally competent captive population. This chapter documents the development of successful giant panda managed breeding programs by focusing on three key areas, (1) the development of science-driven reproductive techniques to improve fecundity in a species where the mating system was poorly understood, (2) how targeted research and adaptive management of social settings surrounding estrus and breeding improved reproductive success, and (3) insights and solutions to challenges faced across the program's history with future directions for research.

The Andean bear alopecia syndrome may be caused by social housing.

The Andean bear alopecia syndrome is a progressive and chronic condition documented in ex situ populations. Recent advances focus on treating symptoms, not preventing future cases. We therefore explored the epidemiology of this syndrome through an analysis of husbandry and veterinary conditions of 63 Andean bears (26M:37F) housed in North and South American zoos and other ex situ circumstances. We had the most complete information for the North American population and found that 29% of females (n = 24) were affected. No males (n = 26) were affected. An analysis of generalized linear models indicated that three models were competitive in describing the occurrence of the condition (i.e., ΔAICc ≤ 2): the model including only the individual's sex (χ2 = 13.41, df = 1, p < .001), the model including both individual sex and social housing status (χ2 = 1.36, df = 2, p < .001), and the model including both individual sex and the expression of stereotypical behaviors (χ2 = 13.82, df = 2, p = .001). Stereotypical behaviors were common among both males (50%, n = 26) and females (51.9%, n = 27) whether or not they were affected, but the syndrome was seen only in females who had been socially housed. Therefore, we suggest that the Andean bear alopecia syndrome is a symptomatic response to the long-term social housing of bears that would otherwise not live socially. To prevent new cases, we recommend that female Andean bears be housed with adult conspecifics only when females choose to cohabitate.

Coevolution of vocal signal characteristics and hearing sensitivity in forest mammals.

Although signal characteristics and sensory systems are predicted to co-evolve according to environmental constraints, this hypothesis has not been tested for acoustic signalling across a wide range of species, or any mammal sensory modality. Here we use phylogenetic comparative techniques to show that mammal vocal characteristics and hearing sensitivity have co-evolved to utilise higher frequencies in forest environments - opposite to the general prediction that lower frequencies should be favoured in acoustically cluttered habitats. We also reveal an evolutionary trade-off between high frequency hearing sensitivity and the production of calls with high frequency acoustic energy that suggests forest mammals further optimise vocal communication according to their high frequency hearing sensitivity. Our results provide clear evidence of adaptive signal and sensory system coevolution. They also emphasize how constraints imposed by the signalling environment can jointly shape vocal signal structure and auditory systems, potentially driving acoustic diversity and reproductive isolation.

Acoustic recordings provide detailed information regarding the behavior of cryptic wildlife to support conservation translocations.

For translocated animals, behavioral competence may be key to post-release survival. However, monitoring behavior is typically limited to tracking movements or inferring behavior at a gross scale via collar-mounted sensors. Animal-bourne acoustic monitoring may provide a unique opportunity to monitor behavior at a finer scale. The giant panda is an elusive species of Ursid that is vulnerable to extinction. Translocation is an important aspect of the species' recovery, and survival and recruitment for pandas likely hinge on behavioral competence. Here we tested the efficacy of a collar-mounted acoustic recording unit (ARU) to remotely monitor the behavior of panda mothers and their dependent young. We found that trained human listeners could reliably identify 10 behaviors from acoustic recordings. Through visual inspection of spectrograms we further identified 5 behavioral categories that may be detectable by automated pattern recognition, an approach that is essential for the practical application of ARU. These results suggest that ARU are a viable method for remotely observing behaviors, including feeding. With targeted effort directed towards instrumentation and computing advances, ARU could be used to document how behavioral competence supports or challenges post-release survival and recruitment, and allow for research findings to be adaptively integrated into future translocation efforts.

Approaches to studying behavior in captive sloth bears through animal keeper feedback.

Animal keepers at zoos and wildlife rescue centers often possess in-depth knowledge of the health and behavior of the individuals under their care. While it is often not feasible for keepers to regularly collect behavior data through formal scientific methods, efforts should be made to find alternative means to capture this knowledge. We investigated the use of keeper feedback to study the behavior of sloth bears at the Agra Bear Rescue Facility (ABRF; Agra, India). We prepared a survey with 5 questions focused on behaviors indicative of playfulness, boldness, aggressiveness, and the tendency to express self-directed behaviors (SDB). We asked keepers to rate bears on a Likert scale from 1 (least likely to exhibit a behavior) to 5 (most likely) for 44 adult female bears (5-21 years of age). We validated this method by comparing keeper ratings of SDB with formal behavior observations, finding that time of day had an influence on the accuracy of keeper assessments. We found a significant negative correlation between housing bears in larger groups (>15) and SDB. In addition, we correlated ratings given by keepers for all study behaviors. Social play had significant negative correlation with aggression toward people. There was no correlation between social play and aggression toward other bears, possibly due to the existence of cohesive social groups in group housing or high dimensionality of the data. We found that keeper feedback is an efficient tool to gather behavior data on captive sloth bears and recommend its use in future studies.

Vocal behaviour predicts mating success in giant pandas.

Surprisingly little is known about how mammal vocal signals are used to achieve behavioural synchrony in the lead up to copulation. The ability to signal short-term fluctuations in arousal levels and behavioural intention is likely to be particularly important for synchronizing mating behaviour in asocial species, which must overcome their natural avoidance and aggressive tendencies to mate. Here, we examined vocal behaviour during breeding encounters in captive giant pandas (Ailuropoda melanoleuca) to gain a greater understanding of how close-range vocal signalling mediates reproduction in this asocial, and conservation-dependent species. Our results revealed that the occurrence of different giant panda vocalizations and acoustic variation within these calls is predictive of successful encounters leading to copulation, as opposed to unsuccessful encounters that do not. In addition, key differences were detected between vocalizations produced during and just prior to copulation. These findings illustrate that vocal exchanges are crucial for achieving behavioural synchrony and signalling intention to mate in giant pandas, and could also provide a valuable tool for breeding programmes, helping conservation managers to assess the likelihood of breeding introductions leading to copulation or potentially injurious failure.

Sound transmission in a bamboo forest and its implications for information transfer in giant panda (Ailuropoda melanoleuca) bleats.

Although mammal vocalisations signal attributes about the caller that are important in a range of contexts, relatively few studies have investigated the transmission of specific types of information encoded in mammal calls. In this study we broadcast and re-recorded giant panda bleats in a bamboo plantation, to assess the stability of individuality and sex differences in these calls over distance, and determine how the acoustic structure of giant panda bleats degrades in this species' typical environment. Our results indicate that vocal recognition of the caller's identity and sex is not likely to be possible when the distance between the vocaliser and receiver exceeds 20 m and 10 m, respectively. Further analysis revealed that the F0 contour of bleats was subject to high structural degradation as it propagated through the bamboo canopy, making the measurement of mean F0 and F0 modulation characteristics highly unreliable at distances exceeding 10 m. The most stable acoustic features of bleats in the bamboo forest environment (lowest % variation) were the upper formants and overall formant spacing. The analysis of amplitude attenuation revealed that the fifth and sixth formant are more prone to decay than the other frequency components of bleats, however, the fifth formant still remained the most prominent and persistent frequency component over distance. Paired with previous studies, these results show that giant panda bleats have the potential to signal the caller's identity at distances of up to 20 m and reliably transmit sex differences up to 10 m from the caller, and suggest that information encoded by F0 modulation in bleats could only be functionally relevant during close-range interactions in this species' natural environment.

Energetic costs of locomotion in bears: is plantigrade locomotion energetically economical?

Ursids are the largest mammals to retain a plantigrade posture. This primitive posture has been proposed to result in reduced locomotor speed and economy relative to digitigrade and unguligrade species, particularly at high speeds. Previous energetics research on polar bears (Ursus maritimus) found locomotor costs were more than double predictions for similarly sized quadrupedal mammals, which could be a result of their plantigrade posture or due to adaptations to their Arctic marine existence. To evaluate whether polar bears are representative of terrestrial ursids or distinctly uneconomical walkers, this study measured the mass-specific metabolism, overall dynamic body acceleration, and gait kinematics of polar bears and grizzly bears (Ursus arctos) trained to rest and walk on a treadmill. At routine walking speeds, we found polar bears and grizzly bears exhibited similar costs of locomotion and gait kinematics, but differing measures of overall dynamic body acceleration. Minimum cost of transport while walking in the two species (2.21 J kg-1 m-1) was comparable to predictions for similarly sized quadrupedal mammals, but these costs doubled (4.42 J kg-1 m-1) at speeds ≥5.4 km h-1 Similar to humans, another large plantigrade mammal, bears appear to exhibit a greater economy while moving at slow speeds.

Urinary profiles of progestin and androgen metabolites in female polar bears during parturient and non-parturient cycles.

Due to the environmental and anthropogenic impacts that continue to threaten the reproductive success of polar bears, a more detailed understanding of their reproductive cycle is needed. Captive populations of polar bears provide an excellent opportunity to learn more about the reproductive physiology of the species. Progestin (P4) and androgen (T) metabolites in urine, and their ratio (P4:T), were examined during 11 reproductive cycles of captive female polar bears (n = 4) to characterize the steroid hormone profile during pregnancy and determine possible variations related to reproductive failure. The concentration of hormone metabolites in urine were determined through enzyme immunoassay. Reproductive cycles were classified as pregnant (n = 3), anovulatory (n = 4) and ovulatory-non-parturient (n = 4) based on the changes in urinary hormone metabolite values and cub production. In the absence of a lactational suppression of estrus, elevated androgen concentrations suggested resumption of follicular development within 3 weeks of parturition. Breeding behaviours were most often observed when androgen values were at their highest or in decline. Ovulation was identified by a return to basal androgen concentration and elevation of progestins within 1-4 weeks after breeding. As a result, urinary concentrations of progestins were greater than androgens (P4:T ratio ≥ 1.0) during ovulatory cycles whereas the P4:T ratio was <1.0 when females were anovulatory. Progestins and the P4:T ratio of parturient cycles were greatest beginning in June/July (17-20 weeks after breeding) and reached a peak at 24-37 weeks (mid-October/mid-November, 4-9 weeks before birth of cubs). Non-invasive monitoring of hormone metabolites in urine provided a rapid determination of endocrine function for improved husbandry and reproductive management of polar bears in captivity. Further research is warranted to understand the reproductive endocrinology of polar bears and its impact on conservation and management of this species in captivity and the wild.

Contextual influences on animal decision-making: Significance for behavior-based wildlife conservation and management.

Survival and successful reproduction require animals to make critical decisions amidst a naturally dynamic environmental and social background (i.e. "context"). However, human activities have pervasively, and rapidly, extended contextual variation into evolutionarily novel territory, potentially rendering evolved animal decision-making mechanisms and strategies maladaptive. We suggest that explicitly focusing on animal decision-making (ADM), by integrating and applying findings from studies of sensory ecology, cognitive psychology, behavioral economics and eco-evolutionary strategies, may enhance our understanding of, and our ability to predict how, human-driven changes in the environment and population demography will influence animal populations. Fundamentally, the decisions animals make involve evolved mechanisms, and behaviors emerge from the combined action of sensory integration, cognitive mechanisms and strategic rules of thumb, and any of these processes may have a disproportionate influence on behavior. Although there is extensive literature exploring ADM, it generally reflects a canalized, discipline-specific approach that lacks a unified conceptual framework. As a result, there has been limited application of ADM theory and research findings into predictive models that can enhance management outcomes, even though it is likely that the relative resilience of species to rapid environmental change is fundamentally a result of how ADM is linked to contextual variation. Here, we focus on how context influences ADM, and highlight ideas and results that may be most applicable to conservation biology.

Giant pandas use odor cues to discriminate kin from nonkin.

Sociality is an important factor in both the mechanism and function of kin recognition, yet it is little explored in solitary species. While there may be future opportunities for nepotistic functions of kin discrimination among solitary species, the ability to discriminate kin from nonkin may still have important roles in social regulation. The solitary giant panda Ailuropoda melanoleuca offers a good model system to explore kin discrimination in a solitary mammal. As kin discrimination in many other mammals is olfactorily mediated, we investigated whether giant pandas are able to discriminate odor cues from daughters even after months and years of separation. Our results indicate that giant pandas are capable of discriminating between kin and nonkin using odor cues available in urine and body odor. Daughters preferentially investigated the odors of unrelated adult female pandas over the odors of their mothers, and mothers spent more time investigating the odors of unrelated age-matched female pandas over those from their daughters. Because these studies were conducted months or years after the mother-daughter period of dependency ended, it is still unclear what mechanism is used for recognition. Long-term olfactory memories and phenotype matching should both be considered, and further studies are required for such determination.

A systematic survey of the integration of animal behavior into conservation.

The role of behavioral ecology in improving wildlife conservation and management has been the subject of much recent debate. We sought to answer 2 foundational questions about the current use of behavioral knowledge in conservation: To what extent is behavioral knowledge used in wildlife conservation and management, and how does the use of animal behavior differ among conservation fields in both frequency and types of use? We searched the literature for intersections between key fields of animal behavior and conservation and created a systematic heat map (i.e., graphical representation of data where values are represented as colors) to visualize relative efforts. Some behaviors, such as dispersal and foraging, were commonly considered (mean [SE] of 1147.38 [353.11] and 439.44 [108.85] papers per cell, respectively). In contrast, other behaviors, such as learning, social, and antipredatory behaviors were rarely considered (mean [SE] of 33.88 [7.62], 44.81 [10.65], and 22.69 [6.37] papers per cell, respectively). In many cases, awareness of the importance of behavior did not translate into applicable management tools. Our results challenge previous suggestions that there is little association between the fields of behavioral ecology and conservation and reveals tremendous variation in the use of different behaviors in conservation. We recommend that researchers focus on examining underutilized intersections of behavior and conservation themes for which preliminary work shows a potential for improving conservation and management, translating behavioral theory into applicable and testable predictions, and creating systematic reviews to summarize the behavioral evidence within the behavior-conservation intersections for which many studies exist.