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30 July 2022, Volume 42 Issue 4

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ORIGINAL PAPERS

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Impacts of human interference on the potential distribution of Yunnan snub-nosed monkeys by MaxEnt model

Tianlu QIAN, Shujie QIN, Zhaoning WU, Changbai XI, Jiechen WANG

2022, 42(4):  349-361.  DOI: 10.16829/j.slxb.150608

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Yunnan snub-nosed monkeys (Rhinopithecus bieti) are rare and precious primates, endemic to China. Predicting the habitat range, evaluating the influence of human activities, and assessing conservation gaps are important for the conservation of this species. Based on 78 occurrence records of Yunnan snub-nosed monkey and 11 environmental variables (including 7 natural variables and 4 human variables), we use the maximum entropy algorithm (MaxEnt) and spatial analysis technology to construct potential suitable habitat models for Yunnan snub-nosed monkeys with and without human interference. Travel big data was used to estimate human travel density and included in the analyses as one of the human variables. The results showed that: (1) The model has achieved an accurate prediction. The human travel density properly reflects the human interferences on habitat. (2) The area of highly suitable habitat for Yunnan snub-nosed monkeys is 3 487.28 km². The four main factors that affect the potential distribution of Yunnan snub-nosed monkeys are altitude, annual precipitation, human travel density, and distance to roads. (3) Human activities have a negative impact on habitat, among which human travel density has the strongest impact. Human interferences lead to a 9.32% decrease of suitable habitats compared to that with natural environment only. 78.8% of the study area is under the influence of human activities. (4) Three of 15 existing habitat patches of Yunnan snub-nosed monkey groups are facing serious human interference while having high suitability, which can be key conservation areas. The habitat suitability curves become stable when the distance to residents and roads is 2 500 m or further, indicating a potential buffer distance in species conservation. It is of practical significance for conservation to reduce the intensity of human disturbance in these areas.

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Density estimation and suitable habitat prediction of Indo-Pacific finless porpoise in the Beibu Gulf

Xiangyao MENG, Huazhi WANG, Yu ZHOU, Hongke ZHANG, Ying QIAO, Bingyao CHEN

2022, 42(4):  362-369.  DOI: 10.16829/j.slxb.150634

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There is little information about the Indo-Pacific finless porpoise (Neophocaena phocaenoides) in China. Between 2018 and 2020, we conducted boat surveys in the inshore of Guangxi Hepu State Dugong National Natural Reserve and offshore of Weizhou Island waters using the line-transect sampling method. The density of finless porpoise estimated using DISTANCE software in Dugong National Natural Reserve was 0.273 (0.133 - 0.561) ind./km², with a population of 88 (95%CI: 43 - 181). The population density in Weizhou Island was 0.100 (0.048 - 0.210) ind./km², with a mean population of 137 (95%CI: 65 - 286). We also used MaxEnt software to analyze the distribution of suitable habitats for finless porpoises in the Beibu Gulf. The AUC values of the MaxEnt model were 0.980 and 0.927 for the training and test sets, respectively, indicating good model performance. The model indicates that offshore distance and water depth are the main factors affecting the habitat distribution of Indo-Pacific finless porpoise. It was predicted that the northeastern coastal area of Beibu Gulf and the western side of Hainan were the most suitable habitat for the finless porpoise. The habitat area with suitability greater than 0.5 was 14 630.62 km². From 2018 to 2020, the area of suitable habitat for Indo-Pacific finless porpoise decreased significantly by 40% compared with that in 2013. According to the density of the two groups and suitable habitat area, it was estimated that there are about 1 463 - 3 994 Indo-Pacific finless porpoises in Beibu Gulf. Thus, the number of finless porpoises in the Beibu Gulf is relatively high. Adequate attention should be paid to the protection of the Indo-Pacific finless porpoise. We suggest strengthening the protection of the marine ecosystem, restoring fish resources, controlling anthropogenic activities, especially fishing boats, and establishing new nature reserves.

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The effects of affiliative relationship on aggressive behavior in Tibetan macaques

Tong ZHANG, Xi WANG, Qixin ZHANG, Jinhua LI

2022, 42(4):  370-378.  DOI: 10.16829/j.slxb.150644

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Affiliative and agonistic behaviors determine the social structure and its systems in animal groups, which are manifested as differences in proximity between individuals. However, it is unclear whether differences in affinity affect the intensity of conflict and aggression. Thus, we conducted a study on one group of Tibetan macaques (Macaca thibetana, Yulinkeng, YA1) from September 2020 to May 2021 in Anhui, China. We used focal animal and behavioral sampling methods to record the proximity, grooming, and aggressive behavior of macaques. We correlated the proximity and grooming with aggressive behavior of those matrices, and ran GLMM models to explore the factors that might affect aggressive interaction among individuals. The results showed that the greater the proximity index was, the longer the grooming duration between group individuals had. The matrix based on the proximity index was positively correlated with the total number of aggression, the number of mild aggression, and the number of intense aggression. Individuals with closer affiliative relationships had more often and more heavily aggression towards each other. When comparing differences between sex, we found the frequency and intensity of aggression among females were less than among males. These results suggest that the close proximity could increase the likelihood of grooming and aggression between macaques and that the social relationship between females is more stable. We did not find that the macaques adjust the intensity of aggression according to their affinity. This study provided theoretical support for understanding the social relationship and social structure of multi-male and multi-female Tibetan macaques.

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Timing and synchrony of births in reintroduced Père David’s deer (Elaphurus davidianus)

Qinghui MENG, Chao BAI, Yuan SONG, Yunfang SHAN, Junfang LI, Shumiao ZHANG, Jiade BAI, Zhenyu ZHONG, Chenglin ZHANG, Xiuxiang MENG

2022, 42(4):  379-386.  DOI: 10.16829/j.slxb.150462

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The sustained reproduction is an important landmark of successful adaptation of reintroduced species to climate recovery in the original extinction area. The study of synchronous population reproduction before and after reintroduction can provide accurate breeding prediction information and scientific basis for reintroduction managers. In this paper, we collected the birthing data of the reintroduced Père David’s deer population in Beijing in 1987, 1997, 2007, and 2017. The earliest birthing day of each year was used as a baseline to evaluate the delay in birth of reintroduced individuals and to measure the synchronization rate. ANOVA was used to analyze the effects of temperature, precipitation, air humidity, and light on the birthing timing pattern of reintroduced Père David’s deer. The results showed that, (1) After reintroduction, the annual birth rhythm of the population initially oscillated, then gradually reverted, and finally remained in a relatively stable state. After 85 years (from extinction to reintroduction), the first birthing of the new population in Beijing was delayed by 35 ? 42 days compared with that of Woburn Abbey population. Reintroduction of colonization stage: the birth rhythm of the new population was advanced annually. Population propagation stage: the rhythm of birth was delayed annually. Population recovery stage: the rhythm of birth was re-back slightly year by year and finally remained stable. (2) Deer parturition has more intense periodic timing and synchronization. In the first year after reintroduction, it took 18, 14, and 5 days to achieve 0 ? 25%, 25% ? 50%, and 50% ? 75% of the delivery rate, respectively. The relocation stage, it took 41, 19, and 11 days to achieve the rate of synchronization 0 ? 25%, 25% ? 50% to 50% ? 75%, respectively. In the re-expanding population stage, it took 45, 10, and 9 days to achieve the rate of synchronization 0 ? 25%, 25% ? 50% to 50% ? 75%, respectively. In the restoration phase, it took 24, 20, and 11 days to achieve the rate of synchronization 0 ? 25%, 25% ? 50% to 50% ? 75%, respectively.(3) Cumulative light and accumulated temperature had significant effects on the birth initiation of Père David’s deer but had no relationship with the birth synchronization. The delivery began when the accumulated temperature reached (2748.34 ± 157.69) ℃ and the accumulated light reached (3684.77 ± 514.26) h. (4) There was a correlation between the peak period of birth and aboveground biomass per unit area of reintroduced land. Judging by the rhythm of birth data, the new population has adapted to the climate of the reintroduction site. The number of non-synchronous birth individuals increased annually, but the total span of the delivery period did not extend. Since 1997, the population has had a 30% non-synchronous delivery average year. Therefore, analysis based on birth data reveals that after 37 years of reintroduction, the new population has recovered its adaptation to the habitation where it went extinct 120 years ago.

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Status of human-Asiatic black bear conflicts in surrounding communities of Baoshan area in Yunnan Gaoligongshan National Nature Reserve

Yunrui JI, Liushuan ZHANG, Xiangyuan HUANG, Jianyan TANG, Zengshuai LIU, Jiahua LI, Weichun YANG, Diqiang LI, Fang LIU

2022, 42(4):  387-397.  DOI: 10.16829/j.slxb.150623

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Conflicts between Asiatic black bear (Ursus thibetanus) and humans are widespread in Asia. In the surrounding communities of Gaoligongshan National Nature Reserve (GLGNR), conflicts between human and Asiatic black bear have seriously threatened the livelihood and safety of residents, thus studying the patterns of human?Asiatic black bear conflicts is the basis for understanding the underlying mechanism of conflicts and proposing mitigation measures. In 2019, we conducted a semi-structured interview survey on human?Asiatic black bear conflicts in the surrounding communities of Baoshan area of GLGNR. The results showed that crop raiding (n = 199 events) was the most common damage caused by Asiatic black bears reported by interviewees based on occurrence frequency, followed by livestock depredation (n = 43), beehives damage (n = 40), and attacking human (n = 5). However, predation of livestock by Asiatic black bear caused the largest economic losses (799 200 RMB), followed by crop damages (309 300 RMB) and beehive damages (298 790 RMB). These conflicts mainly occurred from June to August. The characteristics of human-Asiatic black bear conflicts varied between the eastern and western Gaoligong Mountains. In the eastern area of GLGNR, crop-raiding was the major type of human-Asiatic black bear conflicts, while damage to beehives was the most serious conflict type in the western area. In addition, residents living in the western Gaoligong Mountains had a more negative attitudes towards Asiatic black bears than villagers in the eastern area. However, we found that neither negative attitudes nor occurrence of bear damages led to retaliatory killing of bears by local villagers. Moreover, 72.0% of the interviewees in the surrounding communities in GLGNR reported that they had never heard of the poaching of Asiatic black bears in the local area, while 98.6% of them never heard about bear products trade. Additionally, they had no willingness to use bear products in the future. We analyzed the current situation of human?Asiatic black bear conflicts in the surrounding communities of Baoshan area of GLGNR, and explored the spatial and temporal patterns of human?Asiatic black bear conflicts. Our study provides a scientific basis for future work on mitigation and management of human?Asiatic black bear conflicts in Gaoligongshan Mountains.

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Genetic diversity and demographic history of Siberian flying squirrel (Pteromys volans) population in northern Zhangguangcai Mountains, Heilongjiang, China

Xinmin TIAN, Mingdong LIAN, Yaqi SONG, Xiaohui LIU, Mengping YANG, Hong CHEN

2022, 42(4):  398-409.  DOI: 10.16829/j.slxb.150629

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The Siberian flying squirrel (Pteromys volans) is an arboreal, nocturnal, and gliding rodent. It plays an important role in forest seed dispersal and ecosystem balance maintenance. We used three molecular markers, namely mtDNA Cytb, control region, and nDNA microsatellites, to conduct genetic diversity and demographic history analyses of the flying squirrel population in the north Zhangguangcai Mountains, Heilongjiang Province. The mean haplotype diversity based on the complete sequence of Cyt b gene (1 140 bp) was 0.909 and the mean nucleotide diversity was 0.616%. The mean haplotype diversity based on the complete sequence of the control region (1 066 bp) was 0.945 and the mean haplotype diversity was 1.698%. The mean number of alleles in the population detected by 12 microsatellite loci was 13.167, the observed heterozygosity was 0.727, the expected heterozygosity was 0.864 and the inbreeding coefficient was 0.159. Our results indicated a high level of genetic diversity in the flying squirrel population, but low heterozygosity and some level of inbreeding. No evidence of population genetic bottleneck or within-population genetic differentiation was found. However, high proportion of rare haplotypes (≥ 60%), low frequency of alleles, and inbreeding indicate a risk of declining genetic diversity in the Siberian flying squirrel population in the future. It is suggested that conservation efforts forSiberian flying squirrels in this region should be improved. The phylogenetic relationship of Cyt b haplotypes confirmed that there are three major lineages of Siberian flying squirrel occupying the Far Eastern, northern Eurasia, and the island of Hokkaido. The haplotypes of Zhangguangcai and Daxing’an Mountains in this study are part of the lineage Far Eastern.

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Expression of MTNR1a and MTNR1b genes on HPG axis of male plateau zokor during the breeding and the non‑breeding seasons

Kang AN, Mingfang BAO, Baohui YAO, Yukun KANG, Yuchen TAN, Yanli WANG, Junhu SU

2022, 42(4):  410-419.  DOI: 10.16829/j.slxb.150605

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The plateau zokor (Eospalax baileyi) is an endemic subterranean rodent species with limited exposure light. Previous study has shown seasonal differences in levels of melatonin secretion in plateau zokors. However, the expression pattern of melatonin receptor genes on hypothalamic?pituitary?gonadal (HPG) axis is not clear. In this study, q–PCR was employed to detect the relative expression levels of genes mRNA of melatonin receptor 1a (MTNR1a)and melatonin receptor 1b (MTNR1b) in hypothalamus, pituitary, and testis of male plateau zokors during the breeding (May) and non?breeding seasons (September). The location of MTNR1a and MTNR1b in testis was determined by immunohistochemical technology, and immunohistochemical positive evaluation was conducted in Image Pro Plus software. The results showed that the relative expression levels of MTNR1a in hypothalamus and pituitary were significantly higher during the breeding season (P < 0.05), while there was no significant difference in the relative expression levels of MTNR1b in different seasons (P > 0.05). The relative expression levels of MTNR1a and MTNR1b in testis during the non?breeding season were higher than that during the breeding season (P < 0.01). The positive signal of MTNR1a in testis was observed in all types of cells except elongated spermatid during the breeding season and in Leydig cells, Sertoli cells, and spermatogonia during the non?breeding season. The positive signal of MTNR1b in testis was observed in all types of cells except spermatogonia and elongated spermatid during the breeding season and in Leydig cells and Sertoli cells during the non?breeding season. The average optical density values of immunopositive signals in MTNR1a and MTNR1b during the non?breeding season were significantly higher compared with the breeding season (P < 0.01). The expression patterns of MTNR1a and MTNR1b on the HPG axis of male plateau zokor during the breeding and the non?breeding seasons revealed the potential role of melatonin in seasonal reproduction regulation.

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Effects of hibernation on cecal microbiota in Daurian ground squirrel

Min MAO, Ming YANG, Xinyu LIU

2022, 42(4):  420-431.  DOI: 10.16829/j.slxb.150622

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The diversity and composition of gut microbiota in hibernating mammals are affected by seasonal changes and fasting during hibernation. In order to examine the seasonal changes of the cecal microbiota of Daurian ground squirrel (Spermophilus dauricus), we analyzed the diversity, composition, and function of cecal microbiota from six groups of fattening stage (Initial fattening, Rapid fattening, Finished fattening) and hibernation stage (Early hibernation, Late hibernation, Arousal) using 16S rRNA gene high-throughput sequencing technology. In addition, the relationship between physiological characteristics and the composition and function of cecal microbiota was explored by redundancy analysis (RDA). The cecal microbiota was mainly composed of Firmicutes, Bacteroidetes, and Verrucomicrobia. Compared with other periods, the relative abundance of Firmicutes decreased and that of Bacteroidetes and Verrucomicrobia increased in Early hibernation. The Chao1 and ACE indices in Initial fattening, Rapid fattening, and Early hibernation were significantly lower than those in the Arousal, and the Simpson index in Finish fattening was significantly lower than that in Rapid fattening (P < 0.05) calculated by alpha diversity. Significant seasonal clustering of the cecal microbiota was found through the principal coordinate analysis (PCoA) of the weighted and unweighted UniFrac distance matrix. The butanoate metabolism and other metabolic pathways were enriched in fattening stage, and nitrogen metabolism and other related pathways were concentrated in hibernation stage as shown by PICRUSt analysis. The physiological characteristics at different stages were significantly correlated with the composition and function of cecal microbiota. In conclusion, it is indicated that hibernation profoundly affects the diversity and relative abundance of cecal microbiota. The changes in the composition and function of cecal microbiota play an important role in regulating the physiological metabolism, which can help Daurian ground squirrel adapt to seasonal environmental changes.

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Fecal microbiota diversity analysis of the diarrheal sub-adult Qaidam horses and biomarkers screening

Xiaoqi WANG, Wenjing HAO, Zhichao ZHANG, Jing HAN, Rujing WANG, Ziyuan DUAN

2022, 42(4):  432-441.  DOI: 10.16829/j.slxb.150637

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The study aims to compare the difference in diversity and composition of fecal microbiota between healthy and diarrheal sub-adult Qaidam horses. We analyzed feces of healthy (n = 13) and diarrheal (n = 3) sub-adult Qaidam horses based on 16S rRNA high-throughput sequencing, and determined the absolute abundance of related differential bacteria genera by real-time qPCR. The results indicated that Firmicutes, Bacteroidetes, Verrucomicrobia, Proteobacteria and Spirochaetes were the dominant phyla in feces from both healthy and diarrheal Qaidam horses. Compared to healthy Qaidam horses, the fecal microbial Alpha diversity was significantly lower (P < 0.05), the relative abundance of Firmicutes was relatively lower (P < 0.05), and the ralative abundance of Proteobacteria was significantly higher (P < 0.05) in diarrheal Qaidam horses. It was then deduced that the dysbiosis of these two phyla (Clostridium, Prevotella, Fibrobacter, etc.) in microecology might play an important role in Qaidam horses’ diarrhea. Additionally, 12 biomarkers (feature genera), such as Methanobrevibacter, Fibrobacter, Paludibacter, Carnobacterium and Elusimicrobium, which had significant influence on the difference of fecal bacteria composition between the two groups, were screened by a machine learning algorithm (random forest). The study compared the characteristics of fecal microbial changes in healthy and diarrheal Qaidam horses and provided a data basis for the diarrhea of livestock in the Qinghai-Tibet Plateau.

REVIEWS

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Research progress of interspecies somatic cell nuclear transfer in wild animals

Shigang GU, Yanhui ZHAI, Chao XU, Dawei YU, Zhiqiang HAN, Quanmin ZHAO, Xiangpeng DAI

2022, 42(4):  442-450.  DOI: 10.16829/j.slxb.150642

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Interspecies somatic cell nuclear transfer (iSCNT) is one of the most promising research directions in somatic cell nuclear transfer (SCNT). It has a wide application in the production of transgenic animals, the breeding of improved varieties, the protection of endangered animals, the regeneration of extinct species, as well as the breeding of wildlife and the protection of biodiversity. In this article, we review the research progress and technical barriers of interspecific nuclear transfer technology in cats, canines, bovids, swine and peccaries, and provide theoretical and technical guidance for further improvement of utilization of iSCNT technology in wild animal reproduction, breeding and diversity protection.

METHOD AND TECHNOLOGY

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Giant panda pose estimation method based on high resolution net

Yu QI, Han SU, Rong HOU, Peng LIU, Peng CHEN, Hangxing ZANG, Zhihe ZHANG

2022, 42(4):  451-460.  DOI: 10.16829/j.slxb.150639

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Long-term behavioral monitoring of captive giant pandas (Ailuropoda melanoleuca) can help animal managers better understand the panda’s physiological cycle and health status in a timely manner, and help breeding facilities quickly take corresponding husbandry actions to improve breeding management. At present, neither animal managers nor scientists can monitor giant pandas 24 hours a day and obtain corresponding behavioral information on time. Accurate animal pose estimation is an important factor in animal behavior research and is also the basis for many downstream applications. Understanding the pose of giant pandas can greatly promote the research of panda behavior and improve its conservation and management. In order to improve the accuracy of giant panda pose estimation in complex environments, this paper proposed a pose estimation method based on the high-resolution network HRNet-32. To solve the problem of large-scale differences in different parts of the giant pandas, an atrous spatial pyramid pooling module was introduced in HRNet-32, which used dilated convolution with different dilated rates to form a similar pyramid form, so as to capture multi-scale information while enhancing the feature’s receptive field. Meanwhile, the giant panda pose estimation was regarded as a homogeneous multi-task learning problem, the joint points of the giant panda were grouped, and the part-based multi-branch structure was introduced to learn the representations specific to each part group. The results of several comparison experiments show that the model proposed in this paper, PCK@0.05, had a high detection accuracy (81.51%). The method proposed in this paper can provide technical support for the behavioral analysis and health assessment of giant pandas.

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Camera-trapping survey on large and medium-sized mammal diversity in the Xiaoxiangling Mountains

Hong CHEN, Shengnan JI, Kan ZHANG, Dayong WANG, Jie HU, Yanhong LI

2022, 42(4):  461-470.  DOI: 10.16829/j.slxb.150611

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Regional species diversity monitoring and assessment are an important basis for the design of conservation and management strategies. To assess the status of large and medium-sized mammal diversity in the Xiaoxiangling Mountains, a baseline survey using infrared camera traps was conducted in Sichuan Yele Provincial Nature Reserve (YLPNR), Sichuan Liziping National Nature Reserve (LZPNNR), and their adjacent areas from January 2018 to November 2020. In total, 86 grids (1 km × 1 km each) were selected for monitoring according to habitat type and landform features, with one camera placed in each grid. A total of 19 982 camera-days of data, including 3 304 independent photos, were collected, and 18 mammal species belonging to 4 orders and 12 families were identified. Among them, 3 species are listed as first-class National Key Protected wildlife (Ailuropoda melanoleuca, Moschus berezovskii and Catopuma temminckii), and 10 species are listed as second-class National Key Protected Wildlife, including Ursus thibetanus, Ailurus styani, and Rusa unicolor. Rusa unicolor is a new record in this area. The five species with the highest relative abundance index are Elaphodus cephalophus, Capricornis milneedwardsii, Sus scrofa, Martes flavigula and Arctonyx collaris. Due to differences in area size and altitudinal range, there are some differences in the composition and relative abundance of large and medium?sized mammals between YLPNR and LZPNNR. In addition, grazing is the main human disturbance in the two reserves of the Xiaoxiangling Mountains. We suggest that the nature reserve authorities should strengthen management to minimize the impact of grazing on wildlife.

SCIENTIFIC NOTES

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The first image record of Eurasian lynx (Lynx lynx) in Yunnan Province

Guangxu HUANG, Junjie LI, Yinlei DU, Wen ZHANG, Zhipang HUANG

2022, 42(4):  471-474.  DOI: 10.16829/j.slxb.150640

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In China, Eurasian lynx (Lynx lynx) is mainly distributed in the northeast, north, northwest, and southwest regions. It is one of the second-class national key protected wild animals and is listed as an Endangered species in the Red List of Vertebrates in China. Historically, there was some evidence that Eurasian lynx occurred in Yunnan Province, such as skins, skulls, and community interviews, while there was no field photographic evidence. In order to carry out a survey of animal diversity in Diqing Prefecture, Yunnan, China for the Second Tibetan Plateau Scientific Expedition and Research Program, we set 24 camera traps in Geza Township, Shangri-La City, from August 10, 2020, to September 14, 2021. On February 28, 2021, a video image of a Eurasian lynx was recorded by camera traps in Geza Township, Shangri-La City, Diqing Prefecture, Yunnan. This is the first video image record of a wild Eurasian lynx in Yunnan Province, confirming the species’ presence in Yunnan, which provides the basic data for the distribution of lynx in China.