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Five giant panda subpopulations purportedly separated by human disturbance events in the Qionglai Mountains.
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The giant panda is an example of a species that has faced extensive historical habitat fragmentation, and anthropogenic disturbance and is assumed to be isolated in numerous subpopulations with limited gene flow between them. To investigate the population size, health, and connectivity of pandas in a key habitat area, we noninvasively collected a t...
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... Our research is centered in Hetaoping, a region in the Wolong Nature Reserve known for its high giant panda densities. 39 Using molecular biology techniques, we identified 13 individuals from 17 fresh giant panda fecal samples collected exclusively from this area. 40 Extensive field monitoring confirms a stable giant panda population in the study area, ensuring an adequate sample size. ...
... 40 Extensive field monitoring confirms a stable giant panda population in the study area, ensuring an adequate sample size. 9,19,39 In our sampling approach, we targeted scent-marking trees frequented by giant pandas, leveraging their information exchange habits, especially during the breeding season, to increase our chances of collecting scent marks from a larger number of individuals. The distance between each sampling point ranges from 200-600m. ...
Scent marking sites served as a primary means of chemical communication for giant pandas, enabling intraspecific communication. We integrated metabolomics and high-throughput sequencing techniques to examine the non-targeted metabolome and microbial community structure of scent marking sites and feces in the field. Integrative analysis revealed a more comprehensive array of chemical compounds compared to previous investigations, including ketones, acids, heterocycles, alcohols, and aldehydes. Notably, specific compounds such as 2-decenal, (E)-, octanal, decanal, L-α-terpineol, vanillin, and nonanal emerged as potential key players in scent signaling. Intriguingly, our study of the microbial domain identified dominant bacterial species from the Actinobacteria, Bacteroidetes, and Proteobacteria phyla, likely orchestrating metabolic processes at scent marking sites. Comparative analyses showed, for the first time, that feces do not share the same functions as scent markers, indicating distinct functional roles. This research deepens scientific understanding of chemical communication in wild pandas.
... Previous studies showed that the seven fecal samples from wild giant pandas were from seven different animals (19,39). The five wild red panda samples have also been confirmed to be from different individuals via GPS collars. ...
Gut microbiota plays a vital role in obtaining nutrition from bamboo for giant pandas. However, low cellulase activity has been observed in the panda’s gut. Besides, no specific pathway has been implicated in lignin digestion by gut microbiota of pandas. Therefore, the mechanism by which they obtain nutrients is still controversial. It is necessary to elucidate the precise pathways employed by gut microbiota of pandas to degrade lignin. Here, the metabolic pathways for lignin degradation in pandas were explored by comparing 209 metagenomic sequencing data from wild species with different feeding habits. Lignin degradation central pathways, including beta-ketoadipate and homogentisate pathway, were enriched in the gut of wild bamboo-eating pandas. The gut microbiome of wild bamboo-eating specialists was enriched with genes from pathways implicated in degrading ferulate and p -coumarate into acetyl-CoA and succinyl-CoA, which can potentially provide the raw materials for metabolism in pandas. Specifically, Pseudomonas , as the most dominant gut bacteria genus, was found to be the main bacteria to provide genes involved in lignin or lignin derivative degradation. Herein, three Pseudomonas -associated strains isolated from the feces of wild pandas showed the laccase, lignin peroxidase, and manganese peroxidase activity and extracellular lignin degradation ability in vitro . A potential mechanism for pandas to obtain nutrition from bamboo was proposed based on the results. This study provides novel insights into the adaptive evolution of pandas from the perspective of lignin metabolism.
IMPORTANCE
Although giant pandas only feed on bamboo, the mechanism of lignin digestion in pandas is unclear. Here, the metabolic pathways for lignin degradation in wild pandas were explored by comparing gut metagenomic from species with different feeding habits. Results showed that lignin degradation central pathways, including beta-ketoadipate and homogentisate pathway, were enriched in the gut of wild bamboo-eating pandas. Genes from pathways involved in degrading ferulate and p -coumarate via beta-ketoadipate pathway were also enriched in bamboo-eating pandas. The final products of the above process, such as acetyl-CoA, can potentially provide the raw materials for metabolism in pandas. Specifically, Pseudomonas , as the most dominant gut bacteria genus, mainly provides genes involved in lignin degradation. Herein, Pseudomonas -associated strains isolated from the feces of pandas could degrade extracellular lignin. These findings suggest that gut microbiome of pandas is crucial in obtaining nutrition from lignin via Pseudomonas , as the main lignin-degrading bacteria.
... Wolong Nature Reserve is an approximately 2000-km 2 national protected area centrally situated in the panda's extant range ( Figure 1). There are approximately 150 giant pandas in the reserve (Qiao et al. 2019). Panda habitat in the reserve consists of understory bamboo forests below 4000 m elevation (Linderman et al. 2005). ...
... Although a large-scale sampling effort was undertaken, our study system encompassed a proportionally small area of the giant panda range and only a single (2-year) sampling period. For larger scale landscape effects on genetic connectivity, sampling across distinct populations (i.e., separate mountain ranges [Zhao et al. 2013]) would be needed, but our analysis of interindividual genetic distance is a powerful tool to examine gene flow in a continuously distributed population and more valid than attempting to differentiate subpopulations within our study area (Shirk et al. 2018;Qiao et al. 2019). To examine ongoing effects of habitat structure, it will be important to sample genetics over time and conduct stratified analyses (Draheim et al. 2018). ...
Analyses of animal social networks have traditionally been conducted on species that exhibit social behaviors such as group living, whereas relatively less work has been done on species that are thought of as solitary, are cryptic, and that communicate through scent-marking cues. We employed noninvasive fecal genetic sampling, conducted from March 2015 to February 2016, to identify individuals of one such species, the giant panda (Ailuropoda melanoleuca), across a study population in southwestern China. We then used spatiotemporal proximity thresholds to infer scent mark–based association networks and conduct social network analyses of the population. Results show social clustering in which cluster members preferentially associated with each other. Genetic relatedness was a positive predictor of associations outside the mating season but a negative predictor of associations in the mating season (Mar–Jun), potentially indicating a behavioral change that would reduce risk of inbreeding and kin competition that we term “kin-space recognition.” Our findings suggest that associations between individuals in species generally thought of as solitary may be widespread and dependent on complex behavior.
... STRs are abundant, highly polymorphic and inherited codominantly, and have been widely applied to evaluate population genetic diversity, identify kinship, investigate genetic differentiation, individual identification, and analyze population structure in many species (Wang et al., 2022). For example, a standardized microsatellite marker system allows accurate monitoring of genetic diversity in wild giant pandas (Ailuropoda melanoleuca) (Huang et al., 2015;Qiao et al., 2019). ...
An effective genetic marker panel that can be used with noninvasive samples is useful for population genetics and the conservation management of endangered species. We aimed to develop a microsatellite marker panel for Tibetan macaques (Macaca thibetana), with good levels of polymorphism, stability, and repeatability and suitable for use with noninvasive samples. We designed 83 primer pairs to screen for polymorphic loci based on a tetranucleotide microsatellite dataset. We tested the loci using 16 tissue samples from Sichuan, Guangxi, and Anhui Province in China, and then 106 fecal samples from three wild populations (Huangshan: Anhui Province, Labahe Natural Reserve: Sichuan Province, Fanjingshan Natural Reserve: Guizhou Province). We used the resulting marker panel to identify individuals and estimate genetic diversity in the three populations. We found that 37 novel loci were polymorphic when we genotyped tissue samples. Fifteen of these loci were high polymorphic, sensitive and stable, they were suitable for fecal samples, and we could identify individuals effectively using a subset of six loci. Using these 6 loci, we identified 89 individuals from the 106 fecal samples. The three wild populations had relatively high genetic diversity, with polymorphism information content ranging from 0.530 to 0.678. The Huangshan population had the highest genetic diversity and the largest number of alleles, whereas genetic diversity was the lowest in the Fanjingshan population. The marker panel will facilitate future population genetic research on Tibetan macaques.
... Many researches in this region considered roads to be the most significant source of disturbance to the natural environment through indirect speculation from the change of effect variables rather than the direct evidence of empirical data as the study above, which could lead to an overestimation of the effects of roads on plant community (Zheng et al., 2016;He et al., 2019;Zhao et al., 2019). Subsequently, the management suggestions such as abandoning and closing the existing roads, reducing, or forbidding road construction may be put forward to reduce the impacts on biodiversity, though the road (e.g., G350) did not make a clear genetic boundary for the panda populations on both sides of the road (Qiao et al., 2019). The construction of roads in many mountainous areas is regarded as a livelihood project for the development of regional economy. ...
We analyzed the impact of mountain roads on patterns of species richness and community dissimilarity along elevation gradients with linear mixed-effects models, assessed how non-native/annual species modified these patterns of diversity, and explored changes in the effects of road on plant diversity along topographic gradients through the generalized additive model (GAM). Data analysis showed that (i) species richness for all, native and perennial species was unimodal relative to elevation and peaked at middle elevations; these patterns were modified by colonization of non-native and annual species favored by roads; (ii) mountain roads homogenized community compositions by selective extinction of native perennial species and to a lesser extent by colonization of annuals, rather than by colonization of non-native species; roads did not affect beta diversity response to elevation gradient; and (iii) mountain roads only contributed 8.98 % plant diversity at the landscape level; species richness was affected more by roads than by beta diversity. Montane ecosystems showed strong resilience to the influence of road the at landscape level. We suggest that new roads be planned and constructed on northeast-facing slopes and at lower elevations in order to minimize negative impacts on native plant diversity.
... Habitat fragmentation has occurred for a long time in giant panda distribution areas, and human activities are the main cause of this fragmentation [66]. With the intensification of human interference, giant pandas have become isolated in numerous subpopulations, experiencing habitat changes and limited gene flow between different subpopulations [67]. We found that the connectivity in 2015 was better than that in 1995. ...
The giant panda (Ailuropoda melanoleuca) is a symbolic and flagship species in the field of endangered wildlife conservation. We studied the changing and driving factors of landscape patterns in Sichuan giant panda habitats through image interpretation and ecological niche evaluation models. According to land-use and cover-change analysis, we also studied the structural changes in habitat over the past two decades and used empirical analysis to evaluate the relative ecological niche widths and overlap of giant panda distribution areas in 1995 and 2015. It is found the area of non-forested land decreased significantly from 1995 to 2015. It is interesting that the high-quality land-use types tended to decrease but low/middle-quality land-use types tended to increase over the past 20 years. Giant panda conservation projects in China have promoted changes in conservation thought and management, as well as the innovation of technical means over the studied period. The goals of Chinese giant panda conservation projects are not only to facilitate giant panda reproduction but also to alleviate the contradiction between conservation and development and promote the coexistence of humans and giant pandas.
... 共有3种大熊 猫主食竹分布期间，海拔2 600 m以下为拐棍竹林(Fargesia robusta)、海 拔 2 600 -3 200 m为 冷 箭 竹 林(Bashania faberi)， 而短锥玉山竹林(Yushania brevipaniculata)镶嵌分 布在海拔2 300-2 700m的拐棍竹林和冷箭竹林之中. 森林植 物群落的原始性、竹子资源的丰富性和沟壑水系的纵横性使 得该地成为野生大熊猫的最佳栖息地之一，根据红外数码相 机和粪便DNA测定表明， 大约有22只大熊猫生活其中， 是卧龙 自然保护区野生大熊猫数量分布较为集中的地区之一 [25][26] . ...
This study analyzed the characteristics of the bamboo grazing behaviors (food selection, resource intake rate) of wild giant pandas and livestock in Wolong National Nature Reserve to reveal the ecological mechanism of the impact of grazing livestock on giant panda bamboo resources and habitats. The study was analyzed using data from line transect surveys and the sample plot method. The results showed that wild giant panda foraging strategy not only had seasonal migratory characteristics, but also that these animals chose to feed on different species, age classes, and organs of the bamboo plant. However, livestock fed only on bamboo resources in the free-range area, and the branches and leaves of bamboo forest were the main foraging targets. This led to the giant pandas and livestock having different bamboo resource feeding intensities. Statistics
showed that the feeding rates of grazing livestock and wild giant pandas were significantly different (P < 0.001). This study shows that although livestock and giant pandas display foraging behaviors with regard to bamboo species, there are clear differences caused by how these groups select bamboo in certain age classes and prefer particular organs, but because livestock feed mainly on bamboo branches and leaves, the photosynthetic efficiency of the bamboo was affected. This in turn led to a decrease in the growth of the pandas’ staple food, which have a low natural regeneration ability and can even die dry, thereby severely reducing the quality of bamboo resources available. Therefore, prohibiting grazing of livestock in giant panda habitat is an important measure to effectively conserve this species. The adjustment of the industrial structure of rural communities could definitely become an effective way to coordinate the protection of nature and development of communities.
... Wolong Nature Reserve is an approximately 2000-km 2 national protected area centrally situated in the panda's extant range ( Figure 1). There are approximately 150 giant pandas in the reserve (Qiao et al. 2019). Panda habitat in the reserve consists of understory bamboo forests below 4000 m elevation (Linderman et al. 2005). ...
... Although a large-scale sampling effort was undertaken, our study system encompassed a proportionally small area of the giant panda range and only a single (2-year) sampling period. For larger scale landscape effects on genetic connectivity, sampling across distinct populations (i.e., separate mountain ranges [Zhao et al. 2013]) would be needed, but our analysis of interindividual genetic distance is a powerful tool to examine gene flow in a continuously distributed population and more valid than attempting to differentiate subpopulations within our study area (Shirk et al. 2018;Qiao et al. 2019). To examine ongoing effects of habitat structure, it will be important to sample genetics over time and conduct stratified analyses (Draheim et al. 2018). ...
The relationships between habitat amount and fragmentation level and functional connectivity and inbreeding remain unclear. Thus, we used genetic algorithms to optimize the transformation of habitat area and fragmentation variables into resistance surfaces to predict genetic structure and examined habitat area and fragmentation effects on inbreeding through a moving window and spatial autoregressive modeling approach. We applied these approaches to a wild giant panda population. The amount of habitat and its level of fragmentation had nonlinear effects on functional connectivity (gene flow) and inbreeding. Functional connectivity was highest when approximately 80% of the surrounding landscape was habitat. Although the relationship between habitat amount and inbreeding was also nonlinear, inbreeding increased as habitat increased until about 20% of the local landscape contained habitat, after which inbreeding decreased as habitat increased. Because habitat fragmentation also had nonlinear relationships with functional connectivity and inbreeding, we suggest these important responses cannot be effectively managed by minimizing or maximizing habitat or fragmentation. Our work offers insights for prioritization of protected areas.
... Eighteen fresh samples with mucosa were collected from 18 pandas which lived in the Wolong National Nature Reserve (wild group) based on freshness level. Individual genotypes were identified by Qiao et al (Qiao et al., 2019). The identification information is provided in Table 1. ...
Abstract Reintroduction is a key approach in the conservation of endangered species. In recent decades, many reintroduction projects have been conducted for conservation purposes, but the rate of success has been low. Given the important role of gut microbiota in health and diseases, we questioned whether gut microbiota would play a crucial role in giant panda's wild‐training process. The wild procedure is when captive‐born babies live with their mothers in a wilderness enclosure and learn wilderness survival skills from their mothers. During the wild‐training process, the baby pandas undergo wilderness survival tests and regular physical examinations. Based on their performance through these tests, the top subjects (age 2–3 years old) are released into the wild while the others are translocated to captivity. After release, we tracked one released panda (Zhangxiang) and collected its fecal samples for 5 months (January 16, 2013 to March 29 2014). Here, we analyzed the Illumina HiSeq sequencing data (V4 region of 16S rRNA gene) from captive pandas (n = 24), wild‐training baby pandas (n = 8) of which 6 were released and 2 were unreleased, wild‐training mother pandas (n = 8), one released panda (Zhangxiang), and wild giant pandas (n = 18). Our results showed that the gut microbiota of wild‐training pandas is significantly different from that of wild pandas but similar to that of captive ones. The gut microbiota of the released panda Zhangxiang gradually changed to become similar to those of wild pandas after release. In addition, we identified several bacteria that were enriched in the released baby pandas before release, compared with the unreleased baby pandas. These bacteria include several known gut‐health related beneficial taxa such as Roseburia, Coprococcus, Sutterella, Dorea, and Ruminococcus. Therefore, our results suggest that certain members of the gut microbiota may be important in panda reintroduction.
... Demographics for all pandas sampled in this study are shown in Table S1. Seven tetra-microsatellites including GPL-60, gpz-47, gpz-20, GPL-44, GPL-29, GPL-53, and gpz-6 were used to distinguish the wild individuals, and this DNA analysis was performed by Qiao et al., therefore the samples of wild giant pandas were from their research (Table S2) [25]. ...
Captive breeding has been used as an effective approach to protecting endangered animals but its effect on the gut microbiome and the conservation status of these species is largely unknown. The giant panda is a flagship species for the conservation of wildlife. With integrated efforts including captive breeding, this species has been recently upgraded from “endangered” to “vulnerable” (IUCN 2016). Since a large proportion (21.8%) of their global population is still captive, it is critical to understand how captivity changes the gut microbiome of these pandas and how such alterations to the microbiome might affect their future fitness and potential impact on the ecosystem after release into the wild. Here, we use 16S rRNA (ribosomal RNA) marker gene sequencing and shotgun metagenomics sequencing to demonstrate that the fecal microbiomes differ substantially between wild and captive giant pandas. Fecal microbiome diversity was significantly lower in captive pandas, as was the diversity of functional genes. Additionally, captive pandas have reduced functional potential for cellulose degradation but enriched metabolic pathways for starch metabolism, indicating that they may not adapt to a wild diet after being released into the wild since a major component of their diet in the wild will be bamboo. Most significantly, we observed a significantly higher level of amylase activity but a lower level of cellulase activity in captive giant panda feces than those of wild giant pandas, shown by an in vitro experimental assay. Furthermore, antibiotic resistance genes and virulence factors, as well as heavy metal tolerance genes were enriched in the microbiomes of captive pandas, which raises a great concern of spreading these genes to other wild animals and ecosystems when they are released into a wild environment. Our results clearly show that captivity has altered the giant panda microbiome, which could have unintended negative consequences on their adaptability and the ecosystem during the reintroduction of giant pandas into the wild.
