Yonggang Nie

Obligate herbivory in an ancestrally carnivorous lineage: the giant panda and bamboo from the perspective of nutritional geometry

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.

Ecological scale and seasonal heterogeneity in the spatial behaviors of giant pandas

We report on the first study to track the spatial behaviors of wild giant pandas (Ailuropoda melanoleuca) using high-resolution global positioning system (GPS) telemetry. Between 2008 and 2009, 4 pandas (2 male and 2 female) were tracked in Foping Reserve, China for an average of 305 days (± 54.8 SE). Panda home ranges were larger than those of previous very high frequency tracking studies, with a bimodal distribution of space-use and distinct winter and summer centers of activity. Home range sizes were larger in winter than in summer, although there was considerable individual variability. All tracked pandas exhibited individualistic, unoriented and multiphasic movement paths, with a high level of tortuosity within seasonal core habitats and directed, linear, large-scale movements between habitats. Pandas moved from low elevation winter habitats to high elevation (>2000 m) summer habitats in May, when temperatures averaged 17.5 °C (± 0.3 SE), and these large-scale movements took <1 month to complete. The peak in panda mean elevation occurred in Jul, after which they began slow, large-scale movements back to winter habitats that were completed in Nov. An adult female panda made 2 longdistance movements during the mating season. Pandas remain close to rivers and streams during winter, possibly reflecting the elevated water requirements to digest their high-fiber food. Panda movement path tortuosity and first-passage-time as a function of spatial scale indicated a mean peak in habitat search effort and patch use of approximately 700 m. Despite a high degree of spatial overlap between panda home ranges, particularly in winter, we detected neither avoidance nor attraction behavior between conspecifics.

Giant panda scent-marking strategies in the wild: role of season, sex and marking surface

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.

Giant Pandas Are Not an Evolutionary cul-de-sac: Evidence from Multidisciplinary Research

The giant panda (Ailuropoda melanoleuca) is one of the worlds 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.

Comparative genomics reveals convergent evolution between the bamboo-eating giant and red pandas

Significance The giant panda and red panda are obligate bamboo-feeders that independently evolved from meat-eating ancestors and possess adaptive pseudothumbs, making them ideal models for studying convergent evolution. In this study, we identified genomic signatures of convergent evolution associated with bamboo eating. Comparative genomic analyses revealed adaptively convergent genes potentially involved with pseudothumb development and essential bamboo nutrient utilization. We also found that the umami taste receptor gene TAS1R1 has been pseudogenized in both pandas. These findings provide insights into genetic mechanisms underlying phenotypic convergence and adaptation to a specialized bamboo diet in both pandas and offer an example of genome-scale analyses for detecting convergent evolution. 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.

Effects of season and social interaction on fecal testosterone metabolites in wild male giant pandas: implications for energetics and mating strategies

In the first-ever study of reproductive endocrinology in wild male giant pandas (Ailuropoda melanoleuca), we provide new insights into the reproductive ecology of the species. We tracked and observed pandas in Foping Nature Reserve of the Qinling Mountains for 3 years, collecting fecal samples for testosterone metabolite analysis and data on reproductive activity. Males encountered multiple potential mates and competed for reproductive access to females. Male testosterone metabolites increased in February, peaked in March and April, and fell back to baseline after the mating season. However, males did not maintain a high testosterone level throughout the mating season. Male testosterone instead peaked during encounters with potential mates and declined between encounters. These results indicate that testicular activity is typically dormant until mobilized by interactions with females and potentially by interactions with male competitors. This suggests that male pandas may be energetically constrained, elevating testosterone levels only when necessary to meet the demands of intrasexual competition and courtship and fertilization of females. Maintaining a high testosterone level is metabolically expensive and male pandas enter the mating season during a period of low food availability. If this hypothesis is correct, male panda body condition may be an important determinant of reproductive outcome, and anthropogenic activities that diminish foraging resources may have significant impacts on the mating ecology of the species, affecting its conservation.

Withered on the stem: is bamboo a seasonally limiting resource for giant pandas?

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.

Seasonal variation in nutrient utilization shapes gut microbiome structure and function in wild giant pandas

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 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.

DENTAL ABNORMALITIES OF EIGHT WILD QINLING GIANT PANDAS (AILUROPODA MELANOLEUCA QINLINGENSIS), SHAANXI PROVINCE, CHINA

Abstract 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.