Identification of potential suitable areas and conservation priority areas for representative wild animals in the Greater and Lesser Khingan Mountains.

Species geographic distribution and conservation priority areas are important bases for in situ biodiversity conservation and conservation decision-making. In view of the urgency of endangered species protection, eight representative endangered species in the typical forest ecosystem of the Greater and Lesser Khingan Mountains were studied. Based on 1127 occurrence points and environmental data collected from 2016 to 2021, used BIOMOD2 and Zonation to reconstruct the potential distribution area and identify conservation priority areas of eight species (Tetrao parvirostris, T. tetrix, Gulo gulo, Alces alces, Martes zibellina, Moschus moschiferus, Lynx lynx, Lutra lutra). The results showed potential distribution areas for almost all species concentrated in the northern part of the Greater Khingan Mountains (GKM) and the central part of the Lesser Khingan Mountains (LKM). The potential distribution areas of each species were as follows: black-billed capercaillie, 102,623 km2; black grouse, 162,678 km2; wolverine, 63,410 km2; moose, 140,287 km2; sable, 112,254 km2; Siberian musk deer, 104,787 km2; lynx, 139,912 km2; and Eurasian otter, 49,386 km2. Conservation priority areas (CPAs) clustered in the north GKM and central LKM and totaled 220,801 km2, and only 16.94% of the CPAs were currently protected by nature reserves. We suggest that the Chinese government accelerate the integration of existing protected areas in the northern GKM and establish a larger GKM National Park based on cost-effective multi-species protection.

Historical changes in the distribution of the Sichuan golden snub-nosed monkey (Rhinopithecus roxellana) in Sichuan Province, China.

The Sichuan golden snub-nosed monkey (Rhinopithecus roxellana) is a rare and endangered primate species endemic to China. Conducting research on the population distribution changes of the Sichuan golden snub-nosed monkey holds paramount importance for its conservation. Our study represented a comprehensive investigation into the population distribution of the Sichuan snub-nosed monkey by integrating data acquired from field surveys, protected areas, and historical records and using Geographic Information Systems (GIS) to explore changes in distribution across various time periods, including the historical (the Mid-to-Late Pleistocene), recent (1980-2000), and current (2001-2023). The research findings demonstrate a significant shift in the distribution range of the Sichuan golden snub-nosed monkey compared to historical time frames. Notably, between 1980 and 2000, there was a sharp decline in distribution area. Analyses revealed that the southernmost distribution county for the Sichuan golden snub-nosed monkey in Sichuan Province has shifted northward from Huili to Kangding. Furthermore, distribution changes in Sichuan Province are not solely characterized by a reduction in habitat area but also by a decrease in vertical distribution zones. Regions in the northeastern part of Sichuan with elevations below 1000 m, such as Guang'an City, Bazhong City, Dazhou City, and Nanchong City, no longer support the presence of the Sichuan golden snub-nosed monkey. At present, the distribution range is confined to elevations between 1000 and 4000 m in the two major mountain ranges of Qionglai and Minshan. A holistic approach is required to safeguard this species. The establishment of movement corridors can play a critical role in enhancing the overall connectivity of current distribution areas. Additionally, we propose implementing a hierarchical approach to protect current habitats. Spatially differentiated conservation measures should be implemented to prioritize the protection of key habitats while simultaneously monitoring anthropogenic activities in non-key habitats to prevent further fragmentation and isolation of the monkey's distribution areas.

Spatial-temporal shifting patterns and in situ conservation of spotted seal (Phoca largha) populations in the Yellow Sea ecoregion.

Understanding the habitat shifting pattern is a prerequisite for implementing in situ conservation of migratory species. Spotted seals (Phoca largha) inhabiting the Yellow Sea ecoregion (YSE) comprise a small population with independent genes and represent a charismatic flagship species in this region. However, this population has declined by 80% since the 1940s, and increased support from the countries around the YSE is urgently needed to address the potential local extinction risk. A time-series niche model and life-history weighted systematic conservation planning were designed on the basis of a satellite beacon tracking survey (2010-2020) of the YSE population. The results showed clustering and spreading shifting patterns during the breeding and migratory seasons, respectively. The closed-loop migration route formed in the YSE indicated that this population might be geographically isolated from populations in other breeding areas around the world. The conservation priority area (CPA), with an area of 19 632 km2 (3.58% of the total YSE area), was the most effective response to the potential in situ risk. However, nearly 80% of the CPA was exposed outside the existing marine protected areas (MPAs). Future establishment of MPAs in China should strategically consider the conservation gap identified herein, and it is recommended for Korea's closed fishing season to be spatially set in the western Korean Peninsula from May to August. This study also exemplified that the lack of temporal information would lead to the dislocation of niche modeling for migratory species represented by spotted seals. Attention should be paid to protecting small and migratory populations in marine biodiversity conservation planning.

The putatively high-altitude adaptation of macaque monkeys: Evidence from the fecal metabolome and gut microbiome.

Animals living in high-altitude environments, such as the Tibetan Plateau, must face harsh environmental conditions (e.g., hypoxia, cold, and strong UV radiation). These animals' physiological adaptations (e.g., increased red cell production and turnover rate) might also be associated with the gut microbial response. Bilirubin is a component of red blood cell turnover or destruction and is excreted into the intestine and reduced to urobilinoids and/or urobilinogen by gut bacteria. Here, we found that the feces of macaques living in high-altitude regions look significantly browner (with a high concentration of stercobilin, a component from urobilinoids) than those living in low-altitude regions. We also found that gut microbes involved in urobilinogen reduction (e.g., beta-glucuronidase) were enriched in the high-altitude mammal population compared to the low-altitude population. Moreover, the spatial-temporal change in gut microbial function was more profound in the low-altitude macaques than in the high-altitude population, which might be attributed to profound changes in food resources in the low-altitude regions. Therefore, we conclude that a high-altitude environment's stress influences living animals and their symbiotic microbiota.

Research on Space Occupancy, Activity Rhythm and Sexual Segregation of White-Lipped Deer (Cervus albirostris) in Forest Habitats of Jiacha Gorge on Yarlung Zangbo River Basin Based on Infrared Camera Technology.

The white-lipped deer (Cervus albirostris) is a rare and endangered species found in the Qinghai-Tibet Plateau in China. To understand the space occupancy, activity rhythm, and sexual segregation of the white-lipped deer, 24,096 effective photos and 827 effective videos were captured using infrared cameras from February 2020 to January 2022. The ecology and behavior of the white-lipped deer in Jiacha Gorge were studied in more detail using site occupancy models, relative abundance index, and other technologies and methods. The results show that The occupancy predicted by the model exceeds or approaches 0.5. The occupancy increases with greater altitude and with larger EVI values, while the detection rate increases with altitude only during spring and decreases with EVI values only in summer. The daily activity peaks for white-lipped deer were observed from 7:00 to 11:00 and 17:00 to 22:00, with annual activity peaks occurring from April to June and from September to November. From July to the following January, white-lipped deer mostly move in mixed-sex groups, while during the remainder of the year, they predominantly associate with individuals of the same sex. Climate, vegetation coverage, food resources, and human disturbance collectively influenced the behavior and habitat utilization of white-lipped deer. The foundational research conducted on white-lipped deer over the past two years is expected to enhance the basic understanding of white-lipped deer in the Qinghai-Tibet Plateau and contribute to future protection and management decisions.

Food provisioning results in functional, but not compositional, convergence of the gut microbiomes of two wild Rhinopithecus species: Evidence of functional redundancy in the gut microbiome.

The consumption of similar diets has led to the convergence of gut microbial compositions and functions across phylogenetically distinct animals. However, given the functional redundancy in gut microbiomes, it remains unclear whether synchrony occurs in their functions only and not in their composition, even within phylogenetically close animals consuming a similar diet. In this study, we collected fresh fecal samples from a Rhinopithecus roxellana population in April 2021 (before food provisioning) and June and December 2021 (after food provisioning) and used high-throughput sequencing methods (full-length 16S rRNA gene sequencing and metagenomes) to investigate changes in the gut microbiome due to food provisioning. Combining the results from our previous studies on a wild Rhinopithecus bieti population, we found that the artificial food provisions (e.g., apples, carrots, and peanuts) affected the gut microbiome, and synchrony occurred only in its functions and antibiotic resistance gene community in both Rhinopithecus species, reflecting its ecological functional redundancy. Given the current findings (e.g., depletion in probiotic microbes, dysbiosis in the gut microbial community, and changes in the antibiotic resistance gene profile), anthropogenic disturbances (e.g., food provisioning) would have potential negative effects on host health. Therefore, human activity in animal conservation should be rethought from the standpoint of gut microbial diversity.

Suitable Habitats of Chrysolophus spp. Need Urgent Protection from Habitat Fragmentation in China: Especially Suitable Habitats in Non-Nature Reserve Areas.

Over the past few years, the wild population of Chrysolophus spp. has decreased remarkably. Habitat fragmentation is a significant cause for this serious threat to the survival of Chrysolophus spp. population. In order to further understand the distribution of potentially suitable habitats of Chrysolophus spp., we used the maximum entropy model to predict the potentially suitable habitats of C. pictus and C. amherstiae in China based on the known distribution. According to the prediction results of the model, we calculated the landscape pattern index to compare the fragmentation of the two species' potential suitable habitats in nature reserves and non-nature reserves. The results showed that the potentially suitable habitat for Chrysolophus spp. only accounted for a small area of China. The suitable habitats for C. pictus were mainly in Sichuan, Shaanxi, Hubei, and other provinces, and the model predicts a total area of 359,053.06 km2. In addition, the suitable habitats for C. amherstiae were mainly distributed in the three-parallel-river area, with a potential total area of 215,569.83 km2. The model also showed that there was an overlap of suitable habitats between the two species in the western edge of the Sichuan Basin. Previously, hybrids of the two pheasants have already been found in this same overlapping area predicted by the model. The landscape pattern index showed that in the potentially suitable habitat for Chrysolophus spp., the fragmentation of non-nature reserve areas was higher than that of nature reserve areas. The results revealed the distribution of potentially suitable habitats for Chrysolophus spp. in China and highlighted that the suitable habitats in non-nature reserve areas were in urgent need of conservation, thereby providing a key reference for the conservation of the Chrysolophus spp. population in the future.

Dispersal patterns in Yunnan snub-nosed monkeys.

Sex-biased dispersal is common in group-living animals. Due to differences in local demographic and environmental factors, sex-biased dispersal presents many irregular patterns. In this study, a habituated, individually identified Yunnan snub-nosed monkey Rhinopithecus bieti group was observed over 9 years; 192 dispersal events, including 97 male dispersal events (25 natal dispersal and 72 secondary dispersal) and 95 female dispersal events (34 natal dispersal and 61 secondary dispersal) were observed. Males and females showed different dispersal paths, dispersal ages, and dispersal patterns. Females had 2 dispersal paths, whereas males had 4 paths. In terms of age of dispersal, the male age of natal dispersal was younger than for females. Males prefer single dispersal, whereas females prefer parallel dispersal. Our study indicates that the dispersal pattern of R. bieti should be classified as a bisexual dispersal pattern. The differences in dispersal path, average age at dispersal, and dispersal path pattern indicate that Yunnan snub-nosed monkeys may still retain a loose matrilineal social system.

Functional convergence of Yunnan snub-nosed monkey and bamboo-eating panda gut microbiomes revealing the driving by dietary flexibility on mammal gut microbiome.

The gut microbiomes of non-human primates have received a great deal of attention due to their close relationship to humans. In recent years, these studies have mainly focused on the gut microbiome of wild primates, which will be helpful to understanding the evolution of primates and their gut microbiomes (e.g., gut microbiome plasticity and diet flexibility). However, there is still a lack of basic information on the gut microbiomes from wild populations. Here, we investigated the gut microbial composition (16S rRNA gene) and function (metagenome and metagenome-assembled genomes (MAGs)) of Yunnan snub-nosed monkey populations in Weixi County, Yunnan Province, China, that had diets either completely based on wild-foraging or were regularly supplemented with human provisioned food. We found a significant difference in the gut microbiome between these two populations: the gut microbiome of the wild-foraging (no food provision) population was enriched genes involved in the detoxification of bamboo cyanide (high proportion of bamboo shoot intake) and chitin (from insect diet) digestion, while the gut microbiome of the food provisioned (e.g., fruits) wild populations were enriched genes involved in carbohydrate metabolism. Moreover, the gut microbiome of the wild-foraging population shared a putatively functional convergence with the gut microbiome of wild bamboo-eating pandas: such as microbes and genes involved in the cyanide detoxification. Therefore, the gut microbiome of the Yunnan snub-nosed monkey displayed the potential plasticity in response to diet flexibility. Long-term food-provisioning of the wild population has led to dramatic changes in gut microbial composition, function, and even antibiotic resistance. The antibiotic resistance profile for the wild Yunnan snub-nosed monkey population could be considered the baseline and an important piece of information for conservation.

Identification of Conservation Priority Areas and a Protection Network for the Siberian Musk Deer (Moschus moschiferus L.) in Northeast China.

Species conservation actions are guided by available information on the biogeography of the protected species. In this study, we integrated the occurrence data of Siberian musk deer (Moschus moschiferus L.) collected from 2019 to 2021 with species distribution models to estimate the species' potential distribution in Northeast China. We then identified conservation priority areas using a core-area zonation algorithm. In addition, we analyzed core patch fragmentation using FRAGSTATS. Lastly, we identified potential connectivity corridors and constructed a potential protection network based on the least-cost path and the circuit theory. The results showed concentrations of M. moschiferus in the northern Greater Khingan Mountains, the southeastern Lesser Khingan Mountains, and the eastern Changbai Mountains, with a potential distribution area of 127,442.14 km2. Conservation priority areas included 41 core patches with an area of 106,306.43 km2. Patch fragmentation mainly occurred in the Changbai Mountains and the Lesser Khingan Mountains. We constructed an ecological network composed of 41 core patches and 69 linkages for M. moschiferus in Northeast China. The results suggest that the Greater Khingan Mountains represent the most suitable area to maintain the stability of M. moschiferus populations in Northeast China. Considering the high habitat quality requirements of M. moschiferus and its endangered status, we propose that the Chinese government accelerates the construction of the Greater Khingan Mountains National Park and the Lesser Khingan Mountains National Park and enlarges the Northeast China Tiger and Leopard National Park to address the fragmentation of protected areas and the habitat of M. moschiferus.

Invasion and defense of the basic social unit in a nonhuman primate society leads to sexual differences in the gut microbiome.

Multilevel society is one of the most complex social systems in natural ecosystems and is a typical feature among some primates. Given the potential connection between social behavior and gut microbiome composition, the multilevel social system could affect the primate gut microbiome. Here, based on long-term observation (e.g. social unit dynamics, transfer, and behavior), we investigated this potential integrating 16S rRNA gene amplicon sequencing and behavior data in Yunnan snub-nosed monkeys (Rhinopithecus bieti), which possess a multilevel social group based on one male units (OMUs, each unit with several breeding females and their offspring) and all-male unit (AMU, several bachelor males residing together). We found that the mean unweighted Unifrac distance between adult males from different OMUs was significantly lower than that between adult females from different OMUs (paired Wilcoxon test, P = 0.007). There was no significant difference in the mean unweighted Unifrac distance between females within the same OMU or between females from different OMUs. These findings indicated the potential connection between the defense and invasion of social units and the gut microbiome community in wild Yunnan snub-nosed monkeys. We speculated that the resident males of OMUs displaying a significantly higher similarity in the gut microbial community than that of adult females in separate OMUs might be associated with the sexual differences in their interactions and from previously having cohabitated together in the AMU. Therefore, this study suggested that multilevel societies might have an effect on the gut microbial community in this wild nonhuman primate species.

Determinants of Harem Size in a Polygynous Primate: Reproductive Success and Social Benefits.

We used long-term data on the variation in harem size in Yunnan snub-nosed monkeys to research the effects of harem size on reproductive success and the ratio of grooming received to given (RGRG). The results suggest that harem holders derive reproductive benefits commensurate with harem size, whereas the females' reproductive success is unaffected by harem size. Males of larger harems groomed less and had higher RGRG than males of smaller harems. In the case of females, grooming given increased, and RGRG decreased with an increase in harem size. The males' reproductive success seems to be a driver of harem size maximization. From the females' perspective, dwindling social benefits appear to set the upper limit for harem enlargement. We also showed that males of monogamous units ('single-female harems') invested more into grooming their female, presumably to prevent unit disintegration and loss of mating privileges.

Reproductive Parameters of Wild Rhinopithecus bieti.

Animal life activities are rhythmic and affected by seasonal periodicity. Based on 9 years of observations, we estimated the reproductive parameters of a wild, but provisioned Yunnan snub-nosed monkey (Rhinopithecus bieti) group at Xiangguqing in Baimaxueshan National Nature Reserve, Yunnan Province, China. We observed 84 infants (43 males and 41 females) from 41 females between 2010 and 2018. We found the birth sex ratio was 1:1, the female age at first birth was 6.13 years and infant mortality was about 15.5%. Nine years of data showed that the maximum birth season lasted 126 days, and the average length per year was 98.57 ± 18.71 days. R. bieti,characterized by strictly seasonal reproduction, started giving birth on February 1, and this ended on June 7, with a peak reached from March 4 to March 11 (10th week). The mean birth date was March 20 (79.21 ± 29.54 days), and the median birth date was March 11 (71st day). The mean interbirth interval (IBI) was approximately 2 years, and the IBIs among females whose infants had survived for 1 year were found to be significantly longer than those found in females who lost their infant within 1 year. Comparing the reproduction parameters among Asian and African colobines, we concluded that Asian and African colobines tend to have an IBI of 2 years or more, females tend to give birth at the age of 5-6 years, Rhinopithecus species had a strict seasonal reproductive pattern concentrated in February to April. Seasonal changes in food resources and climatic factors may be the main reasons for the variation in reproductive parameters in intraspecific and interspecific comparisons of Asian and African colobines.

Proximate causes of dispersal for female Yunnan snub-nosed monkeys.

Individual dispersal trends, unquestionably important for species ecology and evolution, are affected by multiple factors. Understanding the factors that influence female dispersal strategies offers important insight into primate dispersal mechanisms and female choice. To investigate the proximate causes of dispersal in female Yunnan snub-nosed monkeys (Rhinopithecus bieti), we observed and analyzed nine years of detailed dispersal and demographic data from a population of R. bieti in Xiangguqing, Baimaxueshan Nature Reserve, Yunnan Province, China. Results showed that females who lived long-term in a one-male unit (OMU), without giving birth and with few or no relatives, were more likely to leave that OMU. In addition, an OMU led by an outgroup male and containing more female relatives was significantly more likely to be chosen for immigration. Conversely, greater male age, longer male tenure, and more potentially fertile females discouraged immigration into an OMU. These results suggest that reproduction, male quality, and kin cooperation play the largest roles in female Yunnan snub-nosed monkey dispersal.

Behavioural Responses of Yunnan Snub-Nosed Monkeys (Rhinopithecus bieti) to Tourists in a Provisioned Monkey Group in Baimaxueshan Nature Reserve.

The appearance of tourists brings about behavioural changes in some primates. Primate behavioural responses to human activities can reflect their survival strategy. Little is known about how the behaviour of Rhinopithecus bieti changes in the presence of tourists. Here we provide the first detailed description of interactions between a provisioned group of R. bieti and tourists at Xiangguqing in Baimaxueshan Nature Reserve from July 2012 to June 2013. We found that R. bieti had different response rates to the 5 most common human actions (shout, photograph, offer food, clap, and wave). Results indicated that R. bieti expresses 10 behavioural reactions (threat, escape, vigilance, warning, panic, alliance, attack, foraging, approach, and staring) to tourists' actions. On the whole, most of the monkeys' responses were unfriendly or hostile; a small number were neutral and affiliative. Behavioural responses were also significantly different among the different age/sex classes. Immature individuals engaged in more affiliative behaviours than adult individuals, and adult males tended towards more hostile behaviours. The behaviour of R. bieti towards tourists showed both tension and adaptability. Scientific management of provisioned monkey groups and strict regulation of tourist behaviour is needed in order to protect the animals from the negative effects of tourism-related disturbance.