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.

Adapting conservation breeding techniques using a data-driven approach to restore the 'Alala (Hawaiian crow, Corvus hawaiiensis).

For some critically endangered species, conservation breeding is a vital steppingstone toward re-establishing wild populations. The 'Alala (Hawaiian crow, Corvus hawaiiensis), currently extinct in the wild, exists today only in a conservation breeding program, which, for many years, utilized successful hands-on husbandry approaches such as separating and resocializing pairs, providing partially manmade nests, artificially incubating eggs, and puppet rearing nestlings. Yet, a top priority of any conservation breeding program is to retain natural behaviors essential to postrelease survival and reproduction, to achieve successful reintroduction and restoration to the wild. We describe how we are adapting 'Alala husbandry techniques to strengthen pair bonds through full-time socialization, enable pairs to build robust nests, encourage females to incubate eggs to hatch, and provide pairs and their offspring with vital parental rearing experiences. We discuss the use of standardized, data-driven methods to objectively track our progress towards successful parental breeding and to select release candidates based on their likelihood to survive and breed in the wild. The information shared in this report can be applied to other conservation breeding programs, particularly those implementing or transitioning to husbandry techniques geared towards preparing species to thrive in the wild.

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.

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.

Improving the sustainability of ex situ populations with mate choice.

Many breeding programs managed by the Association of Zoos and Aquariums' (AZA) Species Survival Plans® (SSPs) are not meeting goals for population size and genetic diversity due to failure of recommended pairs to breed successfully. According to AZA Population Management Center analyses, as many as 80% of recommended breeding pairs fail to produce young before the next breeding and transfer plan is issued. Determining reasons for failure and ensuring that a specific pairing produces offspring can be challenging. Mate incompatibility, one possible reason for failure, might be addressed by allowing mate choice. Although many SSP® coordinators and breeding managers, who implement breeding recommendations at their institutions, recognize the potential benefits of mate choice, examples and models for presenting and assessing choice are lacking. Here we review examples from birds, rodents, lagomorphs, marsupials, carnivores, fishes, and insects where mate choice has been incorporated. These examples provide strong evidence that free mate choice and mating with preferred partners increase a variety of reproductive success measurements when compared to assigned mate pairings. We suggest innovative housing and breeding arrangements for better incorporating mate choice into the management strategies for species held ex situ. Further, we discuss the fitness consequences and welfare implications of allowing choice. We advocate for a more systematic use of behavioral research in cooperative breeding programs. Behavioral management for mating can yield more successful programs, thus ensuring SSP® genetic and demographic goals are met, while simultaneously improving welfare.

Inbreeding and inbreeding avoidance in wild giant pandas.

Inbreeding can have negative consequences on population and individual fitness, which could be counteracted by inbreeding avoidance mechanisms. However, the inbreeding risk and inbreeding avoidance mechanisms in endangered species are less studied. The giant panda, a solitary and threatened species, lives in many small populations and suffers from habitat fragmentation, which may aggravate the risk of inbreeding. Here, we performed long-term observations of reproductive behaviour, sampling of mother-cub pairs and large-scale genetic analyses on wild giant pandas. Moderate levels of inbreeding were found in 21.1% of mating pairs, 9.1% of parent pairs and 7.7% of panda cubs, but no high-level inbreeding occurred. More significant levels of inbreeding may be avoided passively by female-biased natal dispersal rather than by breeding dispersal or active relatedness-based mate choice mechanisms. The level of inbreeding in giant pandas is greater than expected for a solitary mammal and thus warrants concern for potential inbreeding depression, particularly in small populations isolated by continuing habitat fragmentation, which will reduce female dispersal and increase the risk of inbreeding.

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.

The acoustic structure of male giant panda bleats varies according to intersexual context.

Although the acoustic structure of mammal vocal signals often varies according to the social context of emission, relatively few mammal studies have examined acoustic variation during intersexual advertisement. In the current study male giant panda bleats were recorded during the breeding season in three behavioural contexts: vocalising alone, during vocal interactions with females outside of peak oestrus, and during vocal interactions with peak-oestrous females. Male bleats produced during vocal interactions with peak-oestrous females were longer in duration and had higher mean fundamental frequency than those produced when males were either involved in a vocal interaction with a female outside of peak oestrus or vocalising alone. In addition, males produced bleats with higher rates of fundamental frequency modulation when they were vocalising alone than when they were interacting with females. These results show that acoustic features of male giant panda bleats have the potential to signal the caller's motivational state, and suggest that males increase the rate of fundamental frequency modulation in bleats when they are alone to maximally broadcast their quality and promote close-range contact with receptive females during the breeding season.

The influence of ambient noise on maternal behavior in a Bornean sun bear (Helarctos malayanus euryspilus).

Anthropogenic noise has become a pervasive feature of both marine and terrestrial habitats worldwide. While a comprehensive understanding of the biologically significant impacts of noise on wildlife is lacking, concerns regarding its influence persist. Noise is also a common feature in the zoological setting, and much can be learned regarding the species-typical response to ambient noise by studying animals in captivity. Here we correlate behavioral and vocal patterns in a Bornean sun bear (Helarctos malayanus euryspilus) mother and cub with ambient noise levels during the 6-month post-partum period. We hypothesized that loud ambient noise would be correlated with changes in behavior, and predicted that noise would be negatively correlated with maternal care behavior, potentially masking cub vocalizations or providing a distraction to the mother. Contrary to expectation, we found that the mother spent significantly more time attending to her cub (P=0.03) on loud days. We also found that she tended to spend less time feeding (P=0.08); however her time spent resting was not affected. The cub was approximately twice as vocal on loud days, although these results were not statistically significant (humming: P=0.10; squawks/cries: P=0.14). Taken together, these results suggest that the behavioral response to ambient noise may have potential energetic costs, and as a result efforts should be made to reduce ambient noise exposure during the post-partum period.

Social learning in captive African elephants (Loxodonta africana africana).

Social learning is a more efficient method of information acquisition and application than trial and error learning and is prevalent across a variety of animal taxa. Social learning is assumed to be important for elephants, but evidence in support of that claim is mostly anecdotal. Using a herd of six adult female African bush elephants (Loxodonta africana africana) at the San Diego Zoo's Safari Park, we evaluated whether viewing a conspecific's interactions facilitated learning of a novel task. The tasks used feeding apparatus that could be solved in one of two distinct ways. Contrary to our hypothesis, the method the demonstrating animal used did not predict the method used by the observer. However, we did find evidence of social learning: After watching the model, subjects spent a greater percentage of their time interacting with the apparatus than they did in unmodeled trials. These results suggest that the demonstrations of a model may increase the motivation of elephants to explore novel foraging tasks.

Stable seasonal migration patterns in giant pandas.

A critical function of animal movement is to maximize access to essential resources in temporally fluctuating and spatially heterogeneous environments. Seasonally mediated resource fluctuations may influence animal movements, enabling them to track changing resource distributions, resulting in annual migration patterns. The conservation-dependent giant panda ( Ailuropoda melanoleuca) displays seasonal movement patterns; however, the key factor driving these seasonal migration patterns remains poorly understood. Here, we used GPS tracking collars to monitor the movements of six giant pandas over a 12-year period across different elevations, and performed statistical analysis of seasonal migration directions, routes, habitat revisitation, home range overlap, first arrival events, and stability. Our results revealed a compelling pattern of seasonal migrations that facilitated the ability of the pandas to forage at the appropriate time and place to maximize nutritional intake. Our results indicated that pandas utilize spatial memory to locate reliable food resources, as evidenced by their annual return to the same or similar winter and summer home ranges and the consistently maintained percentage of home range overlap. These novel insights into giant panda foraging and movement ecology not only enhance our understanding of its ability to adapt to nutritionally poor dietary resources but also provide important information for the development of resource utilization-based protection and management strategies.

Signal detection theory applied to giant pandas: Do pandas go out of their way to make sure their scent marks are found?

Inter-animal communication allows signals released by an animal to be perceived by others. Scent-marking is the primary mode of such communication in giant pandas (Ailuropoda melanoleuca). Signal detection theory propounds that animals choose the substrate and location of their scent marks so that the signals released are transmitted more widely and last longer. We believe that pandas trade-off scent-marking because they are an energetically marginal species and it is costly to generate and mark chemical signals. Existing studies only indicate where pandas mark more frequently, but their selection preferences remain unknown. This study investigates whether the marking behavior of pandas is consistent with signal detection theory. Feces count, reflecting habitat use intensity, was combined with mark count to determine the selection preference for marking. The results showed that pandas preferred to mark ridges with animal trails and that most marked tree species were locally dominant. In addition, marked plots and species were selected for lower energy consumption and a higher chance of being detected. Over 90% of the marks used were the longest-surviving anogenital gland secretion marks, and over 80% of the marks were oriented toward animal trails. Our research demonstrates that pandas go out of their way to make sure their marks are found. This study not only sheds light on the mechanisms of scent-marking by pandas but also guides us toward more precise conservation of the panda habitat.

Local intensity of artisanal gold mining drives mercury accumulation in neotropical oxbow lake fishes.

Driven by surges in global gold prices and additional socio-economic factors, artisanal small-scale gold mining (ASGM) in the Global South is increasing and driving emissions of significant quantities of mercury (Hg) into the air and freshwater. Hg can be toxic to animal and human populations and exacerbate the degradation of neotropical freshwater ecosystems. We examined drivers of Hg accumulation in fish that inhabit oxbow lakes of Peru's Madre de Dios, a region with high biodiversity value and increasing human populations that depend on ASGM. We hypothesized that fish Hg levels would be driven by local ASGM activities, by environmental Hg exposure, by water quality, and by fish trophic level. We sampled fish in 20 oxbow lakes spanning protected areas and areas subject to ASGM during the dry season. Consistent with previous findings, Hg levels were positively associated with ASGM activities, and were higher in larger, carnivorous fish and where water had lower dissolved oxygen levels. In addition, we found a negative relationship between fish mercury levels associated with ASGM and the occurrence of the piscivorous giant otter. The link between fine-scale quantification of spatial ASGM activity and Hg accumulation, as indicated by the result that in the lotic environment, localized effects of gold mining activities are stronger drivers (77 % model support) of Hg accumulation than environmental exposure (23 %) constitutes a novel contribution to a growing body of literature on Hg contamination. Our findings provide additional evidence of high Hg exposure risks to neotropical human and top carnivore populations subject to the impacts of ASGM, which depend on freshwater ecosystems undergoing gradual degradation. The documented spatial variation in Hg accumulation and increased Hg levels in carnivorous fish should serve as a warning to human communities in Madre de Dios to avoid the proximity of high-intensity gold mining areas and minimize local carnivorous fish consumption.

Fitness costs of neighborhood disruption in translocations of a solitary mammal.

Translocation is used to reestablish wild populations of animals, but translocation projects often do not meet their objectives because postrelease mortality of animals is high. One reason for translocation failure is that the behavioral or ecological requirements of released animals are unmet. Maintaining founder-group social relationships during release can affect reestablishment of social species. Solitary territorial species with stable neighbors (restricted dispersal and lifetime occupation of a home range) of the same species may also benefit from the maintenance of these social relationships during translocation. We translocated Stephens' kangaroo rats (Dipodomys stephensi), a solitary species listed as endangered under the U.S. Endangered Species Act, with and without neighboring kangaroo rats. We compared the settlement (establishment of a stable home range) decisions and fitness of kangaroo rats between the 2 treatments. Kangaroo rats translocated with neighbors traveled shorter distances before establishing territories, had higher survival rates, and had significantly higher reproductive success than kangaroo rats translocated without neighbors. Number of offspring was 24-fold higher for kangaroo rats translocated with neighbors than those translocated without neighbors. Differences in behavior following release may partially explain differences in survival between the 2 groups. Immediately following release, animals translocated with neighbors fought less and spent significantly more time foraging and digging burrows than animals translocated without neighbors. Our results indicate that even for solitary species, maintaining relationships among members of a translocated group of animals can influence translocation success. This study is the first empirical demonstration of the fitness consequences of disrupting social relationships among territorial neighbors.

Vocal cues to male androgen levels in giant pandas.

Little is known about the potential of non-human mammal vocalizations to signal information on the hormonal status of the caller. In the current study, we used endocrine data and acoustic analyses to determine whether male giant panda bleats provide reliable information about the caller's current androgen levels. Our results revealed significant relationships between acoustic features of male giant panda bleats and the caller's faecal androgen metabolite concentrations. To our knowledge, this constitutes the first demonstration that the acoustic structure of a non-human mammal call has the potential to yield information about the caller's current androgen levels. We go on to discuss the anatomical basis for our findings and the potential functional relevance of signalling information on male androgen levels in giant panda sexual communication.

Old-growth forest is what giant pandas really need.

Giant pandas (Ailuropoda melanoleuca) are an iconic conservation species, but despite significant research effort, do we understand what they really need? Estimating and mapping suitable habitat play a critical role in conservation planning and policy. But if assumptions about ecological needs are wrong, maps with misidentified suitable habitat will misguide conservation action. Here, we use an information-theoretic approach to analyse the largest, landscape-level dataset on panda habitat use to date, and challenge the prevailing wisdom about panda habitat needs. We show that pandas are associated with old-growth forest more than with any ecological variable other than bamboo. Other factors traditionally used in panda habitat models, such as topographic slope, are less important. We suggest that our findings are disparate from previous research in part because our research was conducted over a larger ecological scale than previous research conducted over more circumscribed areas within individual reserves. Thus, extrapolating from habitat studies on small scales to conservation planning on large scales may entail some risk. As the Chinese government is considering the renewal of its logging ban, it should take heed of the panda's dependency on old growth.

Symbiotic bacteria mediate volatile chemical signal synthesis in a large solitary mammal species.

Mammalian chemosignals-or scent marks-are characterized by astounding chemical diversity, reflecting both complex biochemical pathways that produce them and rich information exchange with conspecifics. The microbiome of scent glands was thought to play prominent role in the chemical signal synthesis, with diverse microbiota metabolizing glandular products to produce odorants that may be used as chemosignals. Here, we use gas chromatography-mass spectrometry and metagenomic shotgun sequencing to explore this phenomenon in the anogenital gland secretions (AGS) of the giant panda (Ailuropoda melanoleuca). We find that this gland contains a diverse community of fermentative bacteria with enzymes that support metabolic pathways (e.g., lipid degradation) for the productions of volatile odorants specialized for chemical communication. We found quantitative and qualitative differences in the microbiota between AGS and digestive tract, a finding which was mirrored by differences among chemical compounds that could be used for olfactory communication. Volatile chemical compounds were more diverse and abundant in AGS than fecal samples, and our evidence suggests that metabolic pathways have been specialized for the synthesis of chemosignals for communication. The panda's microbiome is rich with genes coding for enzymes that participate in the fermentation pathways producing chemical compounds commonly deployed in mammalian chemosignals. These findings illuminate the poorly understood phenomena involved in the role of symbiotic bacteria in the production of chemosignals.

Exploiting common senses: sensory ecology meets wildlife conservation and management.

Multidisciplinary approaches to conservation and wildlife management are often effective in addressing complex, multi-factor problems. Emerging fields such as conservation physiology and conservation behaviour can provide innovative solutions and management strategies for target species and systems. Sensory ecology combines the study of 'how animals acquire' and process sensory stimuli from their environments, and the ecological and evolutionary significance of 'how animals respond' to this information. We review the benefits that sensory ecology can bring to wildlife conservation and management by discussing case studies across major taxa and sensory modalities. Conservation practices informed by a sensory ecology approach include the amelioration of sensory traps, control of invasive species, reduction of human-wildlife conflicts and relocation and establishment of new populations of endangered species. We illustrate that sensory ecology can facilitate the understanding of mechanistic ecological and physiological explanations underlying particular conservation issues and also can help develop innovative solutions to ameliorate conservation problems.

Female giant panda (Ailuropoda melanoleuca) chirps advertise the caller's fertile phase.

Although female mammal vocal behaviour is known to advertise fertility, to date, no non-human mammal study has shown that the acoustic structure of female calls varies significantly around their fertile period. Here, we used a combination of hormone measurements and acoustic analyses to determine whether female giant panda chirps have the potential to signal the caller's precise oestrous stage (fertile versus pre-fertile). We then used playback experiments to examine the response of male giant pandas to female chirps produced during fertile versus pre-fertile phases of the caller's reproductive cycle. Our results show that the acoustic structure of female giant panda chirps differs between fertile and pre-fertile callers and that male giant pandas can perceive differences in female chirps that allow them to determine the exact timing of the female's fertile phase. These findings indicate that male giant pandas could use vocal cues to preferentially associate and copulate with females at the optimum time for insemination and reveal the likely importance of female vocal signals for coordinating reproductive efforts in this critically endangered species.

Giant panda conservation science: how far we have come.

The giant panda is a conservation icon, but science has been slow to take up its cause in earnest. In the past decade, researchers have been making up for lost time, as reflected in the flurry of activity reported at the symposium Conservation Science for Giant Pandas and Their Habitat at the 2009 International Congress for Conservation Biology (ICCB) in Beijing. In reports addressing topics ranging from spatial ecology to molecular censusing, from habitat recovery in newly established reserves to earthquake-induced habitat loss, from new insights into factors limiting carrying capacity to the uncertain effects of climate change, this symposium displayed the vibrant and blossoming application of science to giant panda conservation. Collectively, we find that we have come a long way, but we also reach an all-too-familiar conclusion: the more we know, the more challenges are revealed. While many earlier findings are supported, many of our assumptions are debatable. Here we discuss recent advancements in conservation science for giant pandas and suggest that the way forward is more direct application of emerging science to management and policy.