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Traits of organisms are shaped by their living environments and also determined in part by their phylogenetic relationships. For example, phylogenetic relationships often affect the geographic distributions of animals and cause variation in their living environments, which usually play key roles in the life history and determine the functional traits of species. As an ancient family of mammals, bears widely distribute and have evolved some specific strategies for survival and reproduction during their long‐term evolutionary histories. Many studies on the ecology of bears have been conducted in recent decades, but few have focused on the relationships between their geographic distributions and ecological adaptations. Here, using bears as a model system, we collected and reanalyzed data from the available literatures to explore how geographic distributions and phylogenetic relationships shape the functional traits of animals. We found a positive relationship between phylogenetic relatedness and geographic distributions, with bears distributed in adjacent areas applying more similar strategies to survive and reproduce: (a) Bears living at high latitudes consumed a higher proportion of vertebrates, which may provide more fat for adaptation to low temperatures, and (b) their reproduction rhythms follow fluctuations in seasonal forage availability and quality, in which bears reach mating status from March to May and give birth in approximately November or later., We used bears as a model system, and collected and reanalyzed data from the available literature to explore how geographical distribution shapes the functional traits of animals. This is the first time to use the species within a family to explore the relationships between geographic distribution and functional traits of animals and demonstrate the ecological adaptations of animals with close phylogenetic relationships.

Attraction to feces in wild mammalian species is extremely rare. Here we introduce the horse manure rolling (HMR) behavior of wild giant pandas (Ailuropoda melanoleuca). Pandas not only frequently sniffed and wallowed in fresh horse manure, but also actively rubbed the fecal matter all over their bodies. The frequency of HMR events was highly correlated with an ambient temperature lower than 15 °C. BCP/BCPO (beta-caryophyllene/caryophyllene oxide) in fresh horse manure was found to drive HMR behavior and attenuated the cold sensitivity of mice by directly targeting and inhibiting transient receptor potential melastatin 8 (TRPM8), an archetypical cold-activated ion channel of mammals. Therefore, horse manure containing BCP/BCPO likely bestows the wild giant pandas with cold tolerance at low ambient temperatures. Together, our study described an unusual behavior, identified BCP/BCPO as chemical inhibitors of TRPM8 ion channel, and provided a plausible chemistry-auxiliary mechanism, in which animals might actively seek and utilize potential chemical resources from their habitat for temperature acclimatization.

Interspecific killing is a primary reason for the low survival rates of some animal species. The giant panda (Ailuropoda melanoleuca) is an altricial eutherian mammal and thus, in comparison to other infants, panda cubs are highly vulnerable, which may significantly influence the selection of breeding sites by females. Here, we used infrared camera traps to monitor giant panda dens for 5.5 years in Foping National Nature Reserve (FNNR) to determine how interspecific factors affect den selection by wild female pandas. Results indicated that Asian black bears (Ursus thibetanus), yellow-throated martens (Martes flavigula), leopard cats (Prionailurus bengalensis), and masked palm civets (Paguma larvata) visited the dens frequently, and the presence of these species negatively influenced den selection by female pandas. Interestingly, the presence of rodents and terrestrial birds appeared to indicate den safety, and female giant pandas were not averse and even preferred dens with a high abundance index of rodents and terrestrial birds. The den suitability index (DSI) was a reliable tool for evaluating whether dens were suitable for female giant pandas to give birth to and rear cubs, with preference for dens with high DSI values. This study increases our understanding of the den selection criteria of female giant pandas and the main threats to the survival of their cubs, thus providing important guidance for the conservation and management of this species.

The giant panda (Ailuropoda melanoleuca) is an iconic bear native to China, famous for eating almost exclusively bamboo. This unusual dietary behavior for a carnivore is enabled by several key adaptations including low physical activity, reduced organ sizes and hypothyroidism leading to lowered energy expenditure. These adaptive phenotypes have been hypothesized to arise from a panda-unique single-nucleotide mutation in the dual-oxidase 2 (DUOX2) gene, involved in thyroid hormone synthesis. To test this hypothesis, we created genome-edited mice carrying the same point mutation as the panda and investigated its effect on metabolic phenotype. Homozygous mice were 27% smaller than heterozygous and wild-type ones, had 13% lower body mass-adjusted food intake, 55% decreased physical activity, lower mass of kidneys (11%) and brain (5%), lower serum thyroxine (T4: 36%), decreased absolute (12%) and mass-adjusted (5%) daily energy expenditure, and altered gut microbiota. Supplementation with T4 reversed the effects of the mutation. This work uses a state-of-the-art genome editing approach to demonstrate the link between a single-nucleotide mutation in a key endocrine-related gene and profound adaptive changes in the metabolic phenotype, with great importance in ecology and evolution.

Competition often occurs between two or more sympatric species that use similar ecological niches. During competition, a superior species may exclude the competitor from parts of its fundamental niche or make it go extinct. Determining the potential competition between two sympatric species including an endangered one has important implications for conservation management. We evaluated potential food competition between the wild boar and the giant panda in a key national nature reserve established primarily for the giant panda protection. We monitored foraging plots for 9 years, conducted food macronutrient analysis, and combined our analysis with long-term population monitoring results for two species. The wild boar population increased dramatically in the past 18 years, benefiting from conservation policies of the Chinese government, whereas the giant panda population decreased. We found evidence for competition for bamboo shoots, an important seasonally limiting resource. The wild boar had a higher utilization rate at foraging plots than giant panda, which also avoided plots used by wild boar. This study indicates key seasonal food competition may exist between wild boar and giant panda. This competition for a key food resource may have negative impacts on giant panda populations, particularly under the substantial increase of the wild boar, yet this possibility has not figured prominently in conservation planning and policy for panda reserves. We suggest long-term monitoring of this competitive relationship across reserves to determine when and where management intervention is needed. And, we might need more flexible policies instead of the current “one size fits all” one.

As certain extreme weather events are becoming frequent and intense, conservationists must identify areas across species' ranges recurrently affected, especially with regard to threatened species. Focusing on the giant panda (Ailuropoda melanoleuca) and historical flood frequency distribution, we determined overlaps between panda distribution affected by floods and nature reserves. We also examined the correspondence between areas subject to high flood exposure densities, areas with high panda habitat use, and areas that exhibit high human density. Of the 67 reserves established for giant panda conservation 7 included areas with the highest flood exposure densities while having a mean exposure ranging between 20 and 75%. In Sichuan province up to 32% of areas of high habitat use were subject to low flood density, and 10% overlapped with areas subject to high flood density. We also found that 40% of the total area with high human density was subject to a high flood density. Our findings indicate that high frequency of flooding is affecting areas of nature reserves where people are rather than areas which pandas are using more intensively. In areas occupied by pandas, strategies should remain focus on mitigating habitat degradation and fragmentation caused by human activities that can also reduce habitat resilience to floods. Management aimed at reducing vulnerability and enhancing resilience in flood-prone areas is warranted if we are to prevent negative indirect impacts on panda habitat driven by human responses to increasingly frequent and intense extreme weather events in the coming decades.

Small features in ecological systems are often underrepresented in conservation monitoring, management and policy. Tree cavities and other forms of refuge play disproportionately large ecological roles due to their importance for shelter and rearing vulnerable offspring. Giant panda (Ailuropoda melanoleuca) cubs are highly altricial, and dependent on dens. In Fengtongzai—a reserve with cavity-containing old growth forest—we measured 19 structural and microhabitat variables in potential tree dens. We also established data loggers in rock cavities in Foping Nature Reserve (which due to logging does not contain old growth) and tree cavities in Fengtongzai to monitor temperature and humidity inside and outside dens to evaluate microclimatic buffering. Fengtongzai pandas selected tree dens that were better concealed, with large interiors and entrances but smaller entrance to interior ratios. Microclimate inside dens differed dramatically from ambient conditions outside: in cold weather dens were warmer, in hot weather dens were cooler, dens were less humid and dens had more stable microclimates. Dens used by maternal pandas were warmer, drier and less variable than tree and rock cavities that were not used. Tree dens showed better capacity to buffer against extremes of temperature and humidity than did cave dens. Our findings have important conservation implications, including the value of den sites and the need for better monitoring and management. Specifically, management practices that preserve large old trees may increase carrying capacity and any experimentation with artificial dens as a conservation intervention should reference our findings on structural and microclimatic characteristics of preferred den sites.

Background Flavonoids are important plant secondary metabolites (PSMs) that have been widely used for their health-promoting effects. However, little is known about overall flavonoid metabolism and the interactive effects between flavonoids and the gut microbiota. The flavonoid-rich bamboo and the giant panda provide an ideal system to bridge this gap. Results Here, integrating metabolomic and metagenomic approaches, and in vitro culture experiment, we identified 97 flavonoids in bamboo and most of them have not been identified previously; the utilization of more than 70% flavonoid monomers was attributed to gut microbiota; the variation of flavonoid in bamboo leaves and shoots shaped the seasonal microbial fluctuation. The greater the flavonoid content in the diet was, the lower microbial diversity and virulence factor, but the more cellulose-degrading species. Conclusions Our study shows an unprecedented landscape of beneficial PSMs in a non-model mammal and reveals that PSMs remodel the gut microbiota conferring host adaptation to diet transition in an ecological context, providing a novel insight into host-microbe interaction.

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Antagonistic coevolution between host and parasite drives species evolution. However, most of the studies only focus on parasitism adaptation and do not explore the coevolution mechanisms from the perspective of both host and parasite. Here, through the de novo sequencing and assembly of the genomes of giant panda roundworm, red panda roundworm, and lion roundworm parasitic on tiger, we investigated the genomic mechanisms of coevolution between nonmodel mammals and their parasitic roundworms and those of roundworm parasitism in general. The genome-wide phylogeny revealed that these parasitic roundworms have not phylogenetically coevolved with their hosts. The CTSZ and prolyl 4-hydroxylase subunit beta (P4HB) immunoregulatory proteins played a central role in protein interaction between mammals and parasitic roundworms. The gene tree comparison identified that seven pairs of interactive proteins had consistent phylogenetic topology, suggesting their coevolution during host–parasite interaction. These coevolutionary proteins were particularly relevant to immune response. In addition, we found that the roundworms of both pandas exhibited higher proportions of metallopeptidase genes, and some positively selected genes were highly related to their larvae’s fast development. Our findings provide novel insights into the genetic mechanisms of coevolution between nonmodel mammals and parasites and offer the valuable genomic resources for scientific ascariasis prevention in both pandas.

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.

Gut microbiota plays a critical role in host physiology and health. The coevolution between the host and its gut microbes facilitates animal adaptation to its specific ecological niche. Multiple factors such as host diet and phylogeny modulate the structure and function of gut microbiota. However, the relative contribution of each factor in shaping the structure of gut microbiota remains unclear. The giant (Ailuropoda melanoleuca) and red (Ailurus styani) pandas belong to different families of order Carnivora. They have evolved as obligate bamboo-feeders and can be used as a model system for studying the gut microbiome convergent evolution. Here, we compare the structure and function of gut microbiota of the two pandas with their carnivorous relatives using 16S rRNA and metagenome sequencing. We found that both panda species share more similarities in their gut microbiota structure with each other than each species shares with its carnivorous relatives. This indicates that the specialized herbivorous diet rather than host phylogeny is the dominant driver of gut microbiome convergence within Arctoidea. Metagenomic analysis revealed that the symbiotic gut microbiota of both pandas possesses a high level of starch and sucrose metabolism and vitamin B12 biosynthesis. These findings suggest a diet-driven convergence of gut microbiomes and provide new insight into host-microbiota coevolution of these endangered species.

Parasitic infection as a form of chronic stress affects the cortisol metabolite levels, and the cortisol levels were consistent with the seasonal variation in parasite infection. Sex, age, reproductive status and diet composition were directly associated with helminth parasite richness of wild giant pandas. Age and diet composition had significant influences on the faecal cortisol levels., Many factors, including the inner status of the individuals and external environment, can influence the parasite infections and stress physiology in mammals. Here, we explored the influence of the sex, age, reproductive season and seasonal food availability on the parasitism and stress physiology in wild giant pandas (Ailuropoda melanoleuca) through nutrient and steroid hormone analysis and parasitic infection measurement. Diet composition had significant influences on the faecal cortisol levels and parasite load of wild giant pandas. The seasonal dynamic of the cortisol levels and parasite load in faeces co-vary with the seasonal nutrient intake levels of the pandas, which concurrently arrived the peaks at the wood bamboo shoot-eating period in May (parasite infection intensity, 41.47 ± 12.11 eggs/g of wet faeces; cortisol levels, 619.34 ± 70.55 ng/g dry faeces) that the nutrition intake by wild pandas was the highest (protein/fibre, 69.23 ± 9.93). Meanwhile, age class is also as an important factor to affect the parasite load and stress physiology of wild giant pandas. Cubs and sub-adults suffered more helminth burden and stress physiology than adults and old individuals. This is the first study to evaluate the inner and external factors influence on parasitism and stress physiology in wild giant pandas. The findings facilitate a better understanding of how environmental factors might influence the physiology, behaviour and health of pandas and other species and have implications for the conservation and management of the endangered species.

Characteristics of the gut microbiome vary synchronously with changes in host diet. However, the underlying effects of these fluctuations remain unclear. Here, we performed fecal microbiota transplantation (FMT) of diet-specific feces from an endangered mammal (the giant panda) into a germ-free mouse model. We demonstrated that the butyrate-producing bacterium Clostridium butyricum was more abundant during shoot-eating season than during the leaf-eating season, congruent with the significant increase in host body mass. Following season-specific FMT, the microbiota of the mouse model resembled that of the donor, and mice transplanted with the microbiota from the shoot-eating season grew faster and stored more fat. Mechanistic investigations revealed that butyrate extended the upregulation of hepatic circadian gene Per2, subsequently increasing phospholipid biosynthesis. Validation experiments further confirmed this causal relationship. This study demonstrated that seasonal shifts in the gut microbiome affect growth performance, facilitating a deeper understanding of host-microbe interactions in wild mammals.

Conservation genetics and genomics are two independent disciplines that focus on using new techniques in genetics and genomics to solve problems in conservation biology. During the past two decades, conservation genetics and genomics have experienced rapid progress. Here, we summarize the research advances in the conservation genetics and genomics of threatened vertebrates (e.g., carnivorans, primates, ungulates, cetaceans, avians, amphibians and reptiles) in China. First, we introduce the concepts of conservation genetics and genomics and their development. Second, we review the recent advances in conservation genetics research, including noninvasive genetics and landscape genetics. Third, we summarize the progress in conservation genomics research, which mainly focuses on resolving genetic problems relevant to conservation such as genetic diversity, genetic structure, demographic history, and genomic evolution and adaptation. Finally, we discuss the future directions of conservation genetics and genomics.

An upsurge in anthropogenic impacts has hastened the decline of the red panda (Ailurus fulgens). The red panda is a global conservation icon, but holistic conservation management has been hampered by research being restricted to certain locations and population clusters. Building a comprehensive potential habitat map for the red panda is imperative to advance the conservation effort and ensure coordinated management across international boundaries. Here, we use occurrence records of both subspecies of red pandas from across their entire range to build a habitat model using the maximum entropy algorithm (MaxEnt 3.3.3k) and the least correlated bioclimatic variables. We found that the subspecies have separate climatic spaces dominated by temperature‐associated variables in the eastern geographic distribution limit and precipitation‐associated variables in the western distribution limit. Annual precipitation (BIO12) and maximum temperature in the warmest months (BIO5) were major predictors of habitat suitability for A. f. fulgens and A. f. styani, respectively. Our model predicted 134,975 km2 of red panda habitat based on 10 percentile thresholds in China (62% of total predicted habitat), Nepal (15%), Myanmar (9%), Bhutan (9%), and India (5%). Existing protected areas (PAs) encompass 28% of red panda habitat, meaning the PA network is currently insufficient and alternative conservation mechanisms are needed to protect the habitat. Bhutan's PAs provide good coverage for the red panda habitat. Furthermore, large areas of habitat were predicted in cross‐broader areas, and transboundary conservation will be necessary.

Reintroduction is an important approach in the conservation of endangered species and in recent decades a number of reintroduction programs have been conducted for conservation purposes. Generally, the success rate of reintroduction is low, but long-term monitoring of most reintroduction programs remains uncommon and this may influence the evaluation of reintroduction. The giant panda is a flagship species of biodiversity conservation. The Chinese government runs a giant panda reintroduction program and here we present reintroduction monitoring data from 2009 to 2015 for three giant pandas released into a small isolated wild population in western Sichuan, China. The results indicate that all three giant pandas display similar activity patterns to wild giant pandas, however, the wild-caught female demonstrated better adaptive ability to the wild environment than the two captive-born individuals in that she established a stable home range in the quickest time and gave birth to a cub. Genetic analysis indicates that new genetic material has been introduced into the local population. Our study provides the latest update on the giant panda introduction program and indicates that it is progressing well.

In response to seasonal variation in quality and quantity of available plant biomass, herbivorous foragers may alternate among different plant resources to meet nutritional requirements. Giant pandas (Ailuropoda melanoleuca) are reliant almost exclusively on bamboo which appears omnipresent in most occupied habitat, but subtle temporal variation in bamboo quality may still govern foraging strategies, with population-level effects. In this paper, we investigated the possibility that temporal variation in the quality of this resource is involved in population regulation and examined pandas' adaptive foraging strategies in response to temporal variation in bamboo quality. Giant pandas in late winter and early spring consumed a less optimal diet in Foping Nature Reserve, as the availability of the most nutritious and preferred components and age classes of Bashania fargesii declined, suggesting that bamboo may be a seasonally limiting resource. Most panda mortalities and rescues occurred during the same period of seasonal food limitation. Our findings raised the possibility that while total bamboo biomass may not be a limiting factor, carrying capacity may be influenced by subtle seasonal variation in bamboo quality. We recommend that managers and policy-makers should consider more than just the quantity of bamboo in the understory and that carrying capacity estimates should be revised downward to reflect the fact that all bamboos are not equal.

For any endangered species, our understanding of the spatial variability in its diet across its distribution range, can be important for its conservation. This study focuses on the feeding habitat of the giant panda. For one full year, we surveyed seasonal foraging behaviors of giant pandas (Ailuropoda melanoleuca) in Foping Nature Reserve, China. The results indicated that giant pandas mainly foraged on new shoots ofBashania fargesiiandFargesia qinlingensisin spring and summer, and leaves constituted the major part of their diet in autumn and winter. Stems only marginally occurred in their diet in late winter and early spring. The general pattern in diet composition of giant pandas across mountains reflected the combined consequence of nutrition quality and food availability. Factors affecting foraging-site selection by giant pandas differed across seasons. In spring, they preferred foraging sites closer to trails, with new shoots ofB. fargesiihigher in basal diameter and less affected by worms. In summer, they foraged at sites with higher density of new shoots and perennial bamboos. Besides overstorey canopy, slope and distance to trails were the other two factors affecting their foraging-site selection in autumn. Temporal variation in diet composition and foraging-site selection exhibited by giant pandas perhaps reflected behaviorally adaptive strategies to changing environmental factors, helping to maximize their energy intake for successful survival and reproduction. Our results, for the first time, support the hypothesized negative effect of some worms on foraging-site selection by giant pandas due to their ingestion of new shoots in spring. Protecting of giant panda foraging sites in these areas where abundant young bamboo resource exist, strengthening management of human activities which can influence giant pandas forage to improve forage habitat quality and widely implementing actions of biological worm pest control during the period when shoot sprouts are eaten can potentially have important implications for habitat conservation for this species.

The scientific and conservation-management value of using camera traps is greatly enhanced if the identity of individual animals ‘captured’ can be assigned. Identification of individuals is necessary to make unbiased estimates of population parameters, and can allow for the generation of more robust inferences from studies of spatial and behavioral ecology. Here we tested the utility of an approach to individually identify wild giant pandas Ailuropoda melanoleuca from camera trap images, by cataloguing and careful scrutiny of numerous traits. We developed our identification strategy first by analyzing images of known (captive) individuals (N = 7). We then deployed camera traps at 23 control sites and at seven camera trap arrays ‘baited’ with conspecific decoys, in Foping Nature Reserve, China. From a sample of 12 871 photographs, and using the method we developed with known individuals, we were able to identify 11 individual giant pandas. We tested the repeatability of this approach using a double blind test with 12 naive volunteers, achieving a relatively high inter-observer agreement of 80%, which was increased to 93% when observers reported a high degree of confidence. We also found that image quality was significantly higher at decoy sites than at control sites. We suggest that this approach will be useful for future field projects, allowing researchers to address a broader array of questions and provide new insights into panda ecology and conservation.

Foraging selection of mammalian herbivores is thought to be not only governed by nutrients, but also influenced by plant secondary metabolites (PSMs) in their diets. Giant pandas (Ailuropoda melanoleuca) are well-known bamboo specialists and little is known about the effects of PSMs in bamboos on their foraging selection. Flavonoids are the most famous bioactive PSMs in bamboo leaves. Here, the spatiotemporal variation of total flavonoids (TF) and four typical carbon glycosides flavonoids (CGFs) (orientin, isoorientin, vitexin and isovitexin) in Bashania fargesii bamboo leaves in a vertical aspect and the association with altitudinal movement pattern of wild giant pandas were investigated. We found: (1) Both the TF and four CGFs in leaves of B. fargesii varied seasonally over elevations. Bamboo leaves in winter at higher elevation range were of the highest content. (2) Evident propensity of giant pandas for habitat selection exhibited in vertical direction. At the whole range of elevations B. fargesii distributed, giant pandas preferred to stay at 1600–1800 m. (3) The altitudinal preference of giant pandas and flavonoids in leaves of B. fargesii had significant positive correlations. The bamboo flavonoids at higher-elevation sites which were preferred by giant pandas were significantly higher than in lower-elevation area. (4) Validation in captive giant pandas showed those bamboo leaves unused in wild were of lower flavonoids especially the (iso)orientin compared to higher-elevation, which showed no differences with those unselected leaves in captivity. Our results indicate that the dietary flavonoids may be one of the driving factors shaping the altitudinal preference and diet selection of giant pandas which may be of significant physiological importance such as being playing key roles in the reproduction of such a dietary specialized species.

Multifaceted approaches are required to monitor wildlife populations and improve conservation efforts. In the last decade, increasing evidence suggests that metagenomic analysis offers valuable perspectives and tools for identifying microbial communities and functions. It has become clear that gut microbiome plays a critical role in health, nutrition, and physiology of wildlife, including numerous endangered animals in the wild and in captivity. In this review, we first introduce the human microbiome and metagenomics, highlighting the importance of microbiome for host fitness. Then, for the first time, we propose the concept of conservation metagenomics, an emerging subdiscipline of conservation biology, which aims to understand the roles of the microbiota in evolution and conservation of endangered animals. We define what conservation metagenomics is along with current approaches, main scientific issues and significant implications in the study of host evolution, physiology, nutrition, ecology and conservation. We also discuss future research directions of conservation metagenomics. Although there is still a long way to go, conservation metagenomics has already shown a significant potential for improving the conservation and management of wildlife.

Seasonally reproducing animals show many behavioral and physiological changes during the mating period, including increased signaling for intrasexual competition and mate attraction. We collected 102 anogenital gland secretions (AGS) from marking trees in Foping Nature Reserve, and used gas chromatography mass spectrometry analyze these chemical composition. Of these marks, all but one were from males, confirmed with DNA analysis. We found that several chemical constituents, especially volatile compounds, is present only during the mating season and that the relative abundance of many compounds changed as a function of breeding season, whereas nonvolatile compounds were lower in the mating season. This seasonal variation in chemical composition of AGS most likely plays an important role in governing giant panda reproduction, including mate location, attraction, and male-male competition. The chemical properties of many of these putative chemosignals-such as volatility and longevity-are suggestive of these roles, and undoubtedly contribute to successful reproduction for this species with a characteristically sophisticated chemical communication system. We also found a number of important differences between the chemical constituents of AGS from wild pandas and those found in previous studies with captive pandas, suggesting that inappropriate chemosignal composition may contribute to poor reproductive success in captive breeding programs.

Major histocompatibility complex genes (MHC), a gene cluster that controls the immune response to parasites, are regarded as an important determinant of mate choice. However, MHC-based mate choice studies are especially rare for endangered animals. The giant panda (Ailuropoda melanoleuca), a flagship species, has suffered habitat loss and fragmentation. We investigated the genetic variation of three MHC class II loci, including DRB1, DQA1, and DQA2, for 19 mating-pairs and 11 parent-pairs of wild giant pandas based on long-term field behavior observations and genetic samples. We tested four hypotheses of mate choice based on this MHC variation. We found no supporting evidence for the MHC-based heterosis, genetic diversity, genetic compatibility and "good gene" hypotheses. These results suggest that giant pandas may not use MHC-based signals to select mating partners, probably because limited mating opportunities or female-biased natal dispersal restricts selection for MHC-based mate choice, acknowledging the caveat of the small sample size often encountered in endangered animal studies. Our study provides insight into the mate choice mechanisms of wild giant pandas and highlights the need to increase the connectivity and facilitate dispersal among fragmented populations and habitats.

Eight adult (six male and two female) wild Qinling giant pandas (Ailuropoda melanoleuca qinlingensis) from China National Foping Nature Reserve were tracked, and their dental data collected and recorded from October 2010 to April 2014. Each panda had dental abnormalities of varying severity. Dental wear and fracture were the most common conditions. Absent teeth were common, with premolars missing most often. Mild caries were present in five molar teeth between two animals. Different degrees of dental plaque and calculus occurred in all animals but without severe periodontal disease. Two animals with severe dental abnormalities died due to intestinal problems. Large segments of bamboo were found in their intestinal tracts, and intestinal perforation and ulcers were evident, indicating dental abnormalities can be an important factor in the health of wild giant pandas and may lead to death. Further research with larger sample sizes of wild and captive giant pandas will be required to substantiate the relationship between dental abnormalities and mortality in giant pandas.

Giant panda (Ailuropoda melanoleuca) conservation is a possible success story in the making. If extinction of this iconic endangered species can be avoided, the species will become a showcase program for the Chinese government and its collaborators. We reviewed the major advancements in ecological science for the giant panda, examining how these advancements have contributed to panda conservation. Pandas' morphological and behavioral adaptations to a diet of bamboo, which bear strong influence on movement ecology, have been well studied, providing knowledge to guide management actions ranging from reserve design to climate change mitigation. Foraging ecology has also provided essential information used in the creation of landscape models of panda habitat. Because habitat loss and fragmentation are major drivers of the panda population decline, efforts have been made to help identify core habitat areas, establish where habitat corridors are needed, and prioritize areas for protection and restoration. Thus, habitat models have provided guidance for the Chinese governments' creation of 67 protected areas. Behavioral research has revealed a complex and efficient communication system and documented the need for protection of habitat that serves as a communication platform for bringing the sexes together for mating. Further research shows that den sites in old-growth forests may be a limiting resource, indicating potential value in providing alternative den sites for rearing offspring. Advancements in molecular ecology have been revolutionary and have been applied to population census, determining population structure and genetic diversity, evaluating connectivity following habitat fragmentation, and understanding dispersal patterns. These advancements form a foundation for increasing the application of adaptive management approaches to move panda conservation forward more rapidly. Although the Chinese government has made great progress in setting aside protected areas, future emphasis will be improved management of pandas and their habitat.

Laid-back bamboo eater Pandas are members of the order Carnivora but are entirely herbivorous, living almost exclusively on bamboo. Unlike most other herbivorous species, however, their digestive tract has not evolved the long twists and turns that facilitate the slower digestion necessary for cellulose-rich plants. Nie et al. measured energy expenditure in both wild and captive pandas, which was extremely low, relative to other mammals. The pandas' thyroid hormone levels are also a fraction of the mammalian norm. Science , this issue p. 171

Food resources are patchily distributed in the environment and carnivores and herbivores have adopted different foraging strategies to maximize feeding efficiency. One interesting strategy is that of the giant panda, a member of the Carnivora that has evolved into a bamboo specialist. Giant pandas forage discriminately, but it remains unknown how nutritional hierarchical levels and landscape configuration heterogeneity affect foraging patch selection. Here, we used global positioning system collars to track wild giant pandas at high resolution (

Wild giant pandas use different parts of bamboo (shoots, leaves and stems) and different bamboo species at different times of the year. Their usage of bamboo can be classified temporally into a distinct leaf stage, shoot stage and transition stage. An association between this usage pattern and variation in the giant panda gut microbiome remains unknown. Here, we found associations using a gut metagenomic approach and nutritional analyses whereby diversity of the gut microbial community in the leaf and shoot stages was significantly different. Functional metagenomic analysis showed that in the leaf stage, bacteria species over-represented genes involved in raw fibre utilization and cell cycle control. Thus, raw fibre utilization by the gut microbiome was guaranteed during the nutrient-deficient leaf stage by reinforcing gut microbiome robustness. During the protein-abundant shoot stage, the functional capacity of the gut microbiome expanded to include prokaryotic secretion and signal transduction activity, suggesting active interactions between the gut microbiome and host. These results illustrate that seasonal nutrient variation in wild giant pandas substantially influences gut microbiome composition and function. Nutritional interactions between gut microbiomes and hosts appear to be complex and further work is needed.

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.

Phenotypic convergence between distantly related taxa often mirrors adaptation to similar selective pressures and may be driven by genetic convergence. The giant panda (Ailuropoda melanoleuca) and red panda (Ailurus fulgens) belong to different families in the order Carnivora, but both have evolved a specialized bamboo diet and adaptive pseudothumb, representing a classic model of convergent evolution. However, the genetic bases of these morphological and physiological convergences remain unknown. Through de novo sequencing the red panda genome and improving the giant panda genome assembly with added data, we identified genomic signatures of convergent evolution. Limb development genes DYNC2H1 and PCNT have undergone adaptive convergence and may be important candidate genes for pseudothumb development. As evolutionary responses to a bamboo diet, adaptive convergence has occurred in genes involved in the digestion and utilization of bamboo nutrients such as essential amino acids, fatty acids, and vitamins. Similarly, the umami taste receptor gene TAS1R1 has been pseudogenized in both pandas. These findings offer insights into genetic convergence mechanisms underlying phenotypic convergence and adaptation to a specialized bamboo diet.

Wild giant pandas use different parts of bamboo (shoots, leaves and stems) and different bamboo species at different times of the year. Their usage of bamboo can be classified temporally into a distinct leaf stage, shoot stage and transition stage. An association between this usage pattern and variation in the giant panda gut microbiome remains unknown. Here, we found associations using a gut metagenomic approach and nutritional analyses whereby diversity of the gut microbial community in the leaf and shoot stages was significantly different. Functional metagenomic analysis showed that in the leaf stage, bacteria species over-represented genes involved in raw fibre utilization and cell cycle control. Thus, raw fibre utilization by the gut microbiome was guaranteed during the nutrient-deficient leaf stage by reinforcing gut microbiome robustness. During the protein-abundant shoot stage, the functional capacity of the gut microbiome expanded to include prokaryotic secretion and signal transduction activity, suggesting active interactions between the gut microbiome and host. These results illustrate that seasonal nutrient variation in wild giant pandas substantially influences gut microbiome composition and function. Nutritional interactions between gut microbiomes and hosts appear to be complex and further work is needed.

The giant panda (Ailuropoda melanoleuca) is one of the world's most endangered mammals and remains threatened by environmental and anthropogenic pressure. It is commonly argued that giant pandas are an evolutionary cul-de-sac because of their specialized bamboo diet, phylogenetic changes in body size, small population, low genetic diversity, and low reproductive rate. This notion is incorrect, arose from a poor understanding or appreciation of giant panda biology, and is in need of correction. In this review, we summarize research across morphology, ecology, and genetics to dispel the idea, once and for all, that giant pandas are evolutionary dead-end. The latest and most advanced research shows that giant pandas are successful animals highly adapted to a specialized bamboo diet via morphological, ecological, and genetic adaptations and coadaptation of gut microbiota. We also debunk misconceptions around population size, population growth rate, and genetic variation. During their evolutionary history spanning 8 My, giant pandas have survived diet specialization, massive bamboo flowering and die off, and rapid climate oscillations. Now, they are suffering from enormous human interference. Fortunately, continued conservation effort is greatly reducing impacts from anthropogenic interference and allowing giant panda populations and habitat to recover. Previous ideas of a giant panda evolutionary cul-de-sac resulted from an unsystematic and unsophisticated understanding of their biology and it is time to shed this baggage and focus on the survival and maintenance of this high-profile species.

Summary Herbivores face various nutritional challenges in their life cycles, challenges that may become increasingly acute under ongoing environmental changes. Here, focusing on calcium, phosphorus and nitrogen, we used nutritional geometry to analyse individual-based data on foraging and extraction efficiencies, and combined these with data on reproduction and migratory behaviour to understand how a large herbivorous carnivore can complete its life cycle on a narrow and seemingly low quality bamboo diet. Behavioural results showed that pandas during the year switched between four main food categories involving the leaves and shoots of two bamboo species available. Nutritional analysis suggests that these diet shifts are related to the concentrations and balances of calcium, phosphorus and nitrogen. Notably, successive shifts in range use and food type corresponded with a transition to higher concentrations and/or a more balanced intake of these multiple key constituents. Our study suggests that pandas obligatorily synchronize their seasonal migration and reproduction with the disjunct nutritional phenologies of two bamboo species. This finding has potentially important implications for habitat conservation for this species and, more generally, draws attention to the need for understanding the nutritional basis of food selection in devising management plans for endangered species.

Biodiversity is the sum total of all life on earth and encompasses genetic diversity, species diversity and ecosystem diversity. Among these three levels of diversity, species diversity reflects not only the relationship between life and the environment, but also the richness of biological resources. The main goal of biodiversity conservation is thought to be the protection of species. Animals play an important role in the processes of material cycling and energy flow in ecosystems through the use of intricate food chains and webs. Thus species diversity, especially animal diversity, directly affects the functioning of ecosystems. However, as a result of the sustained increase in the worlds human population and the rapid development of economic globalization, human society has heavily affected the worlds biodiversity and caused a series of ecological consequences such as habitat loss and fragmentation, pollution, and climate change. These changes have seriously threatened the survival of many species on Earth. In this paper, we reviewed advancements in the research related to this ongoing loss of biodiversity over the past ten years by focusing on the influences of human activities on biodiversity and analyzing the primary drivers, characteristics and impacts of this loss in biodiversity. We also introduce some new biodiversity research methods and raise some important scientific questions that address the future of biodiversity research.

The ancestral panda Ailurarctos lufengensis, excavated from the late Miocene, is thought to be carnivorous or omnivorous [1]. Today, giant pandas exclusively consume bamboo and have distinctive tooth, skull, and muscle characteristics adapted to a tough and fibrous bamboo diet during their long evolution [1, 2]. A special feature, the pseudo-thumb, has evolved to permit the precise and efficient grasping of bamboo [3, 4]. Unlike those of extant pandas, little is known about the diet and habitat preferences of extinct pandas. Prevailing studies suggest that the panda shifted to specialized bamboo feeding in the Pleistocene [5, 6]; however, this remains questionable. Pandas now survive in a fraction of their historical habitat [7], but no specific information has been reported. Stable isotope analyses can be used to understand diet- and habitat-related changes in animals [8]. Isotopic signals in bone collagen reflect dietary compositions of ancient human diets [9, 10] and dietary changes between historical and modern animal populations [11, 12]. Here, we conduct stable isotope analyses of bone and tooth samples from ancient and modern pandas and from sympatric fauna. We show that pandas have had a diet dominated by C3 resources over time and space and that trophic niches of ancient and modern pandas are distinctly different. The isotopic trophic and ecological niche widths of ancient pandas are approximately three times larger than those of modern pandas, suggesting that ancient pandas possibly had more complex diets and habitats than do their modern counterparts. Our findings provide insight into the dietary evolution and habitat contraction of pandas.

Stable isotope analysis is very useful in animal ecology, especially in diet reconstruction and trophic studies. Differences in isotope ratios between consumers and their diet, termed discrimination factors, are essential for studies of stable isotope ecology and are species-specific and tissue-specific. Given the specialized bamboo diet and clear foraging behavior, here, we calculated discrimination factors for carbon and nitrogen isotopes from diet to tissues (tooth enamel, hair keratin and bone collagen) for the giant panda (Ailuropoda melanoleuca), a species derived from meat-eating ancestors. Our results showed that carbon discrimination factor obtained from giant panda tooth enamel (e 13 Cdiet-enamel = 10.0‰) and nitrogen discrimination factors from hair keratin (Δ15 Ndiet-hair = 2.2‰) and bone collagen (Δ15 Ndiet-collagen = 2.3‰) were lower, and carbon discrimination factors from hair keratin (Δ13 Cdiet-hair = 5.0‰) and bone collagen (Δ13 Cdiet-collagen = 6.1‰) were higher than those of other mammalian carnivores, omnivores and herbivores. Such distinctive values are likely the result of a low-nutrient and specialized bamboo diet, carnivore-like digestive system and exceptionally low metabolism in giant pandas.

Scent marking entails significant energetic and opportunity costs that demand efficiency. Signal detection theory offers a theoretical framework that generates testable hypotheses regarding where animals should place scent signals in the environment in a way that maximizes their probability of detection by target receivers while minimizing costs of production and distribution. Solitary and reliant on chemical communication, the giant panda, Ailuropoda melanoleuca, offers an interesting model to test these ideas. We studied scent-marking patterns in wild giant pandas in the Foping Nature Reserve by surveying areas containing a high density of scent posts. Pandas did not deploy scent marks randomly in this environment, but targeted trees with specific characteristics that promoted signal persistence, range and/or likelihood of detection. Variables affecting selection of scent-marking sites included bark roughnesss, presence of moss on the tree trunk, tree diameter and distance to the trail. That pandas should be efficient with their use of chemosignals comes as no surprise, as mounting evidence is suggesting that many aspects of giant panda life history are constrained by their energetically poor diet. We also found seasonal and sex differences in marking patterns, indicating a role for scent marking in reproduction and competition. Males scent-marked throughout the year, whereas females scent-marked predominantly during the mating season, suggesting functional differences in scent marking between the sexes.

The giant panda (Ailuropoda melanoleuca) is notoriously difficult to study in the wild, but its interesting reproductive ecology makes the effort worthwhile. Perhaps more than most species, the panda is energy-limited, which alters the cost/benefit analysis of its reproductive ecology. Using global positioning system/very high frequency radiocollars to locate mating aggregations, we used behavioral observations and fecal testosterone assays to gain insight into male panda reproductive effort and strategies, and test theories relating to reproductive competition. Male pandas initially competed fiercely for access to females that were about to be fertile, but once male competitive status was determined, aggression rates declined. Contact aggression was only observed during the first 2 days of mating aggregations; thereafter, it was replaced with noncontact aggression and avoidance. Agonistic interactions were highly asymmetrical, with contest losers (subordinates) showing less aggression and more avoidance than contest winners (dominants), both before and after contest outcome was established. The competitively superior male displayed mate-guarding tactics and secured all observed copulations. Contrary to theoretical predictions, testosterone levels did not predict aggression levels or contest winners and also were not affected by winning or losing a contest. Body size appeared to be the primary determinant of contest outcome. We discuss our findings in light of theoretical predictions, such as those arising from the “challenge hypothesis,” in the context of the giant panda’s foraging and nutritional ecology.