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30 September 2024, Volume 44 Issue 5

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SPECIAL SUBJECT ON SPECIES DIVERSITY OF MAMMAL IN THE HIMALAYAS REGION

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Two new species of genus Crocidura(Eulipotyphla: Soricidae) from Xizang, China

CHEN Shunde, YANG Siyu, QING Jiao, FAN Ronghui, TANG Keyi, LIAO Rui, GUO Keji, ZHANG Mengfei, WU Nanfei, LIU Shaoying

2024, 44(5):  529-550.  DOI: 10.16829/j.slxb.150612

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Crocidura is the most speciose mammalian genus. The taxonomy of Chinese taxa remains controversial and unexplored. In this study, a total of 189 specimens of eight large-sized white-toothed shrews (mean condyloincisor length > 19.5 cm) were collected in China, including C. attenuata, C. tanakae, C. anhuiensis, C. dracula, C. lasiura, C. pullata and two undescribed species (Crocidura sp. 1 and Crocidura sp. 3) from Xizang, China. Their fur, skull and tooth morphology were compared with each other. A principal component analysis (PCA) was conducted to assess morphological variation, including cranial characters, on 14 measurements among six Crocidura species and the two undescribed species. A canonical discriminant analysis was also computed for these specimens. For further comparison, we retrieved Cyt b sequences from GenBank, which included 86 Crocidura species from China and adjacent areas. BEAST was used for Byesian Inference (BI) analyses for these Crocidura species and a general mixed Yule-coalescent model (GMYC) was used to delineate species boundaries. Two undescribed species (Crocidura sp. 1 and Crocidura sp. 3) are recognized based on morphological and molecular evidence from Zhada County of Xizang (Western China) and Motuo County of Xizang, respectively. The two new Crocidura species are described as Crocidura zhadaensis Chen, Wu et Liu, sp. nov. and Crocidura medogensis Chen, Wu et Liu, sp. nov. The diagnostic characteristics of Crocidura zhadaensis are headbody length 69 ? 77 mm, tail length 49 ? 56 mm, and condyloincisive length 20.04 ? 20.74 mm. The hair is light in color, and the whole color is brown. Three quarters of the tail is covered with sparse white long hairs, and the tail ends form short hair bundles. Cranium is flattened. There are a pair of large oval foramen on the medial side of the inferior articular surface. Maxillary U³ was significantly greater than U² in size. There is a small depression near the protocone of P⁴. The diagnostic characteristics of Crocidura medoensis are head-body length 67- 76 mm, tail length, 62-65 mm, condyloincisive length 20.33-22.21 mm. The body color is dark, the back hair is dark brown, and the belly hair is dark gray. The tail is long, often more than 85% of the head length. The cranium is full and the parietal bone is protuberant. The U¹ is the largest, two times the height of U² and U³. The lingual surface of hypocone of the M¹ is extended, and appear a half-moon shape. The mastoid process is prominent. This article includes a taxonomic key to these species, which provides basic data for further clarifying the classification and species diversity of the genus Crocidura in China.

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First record of Nepalese brown-toothed shrew (Episoriculus soluensis) in China

LIU Yingxun, PENG Buqing, WANG Xuming, LIAO Rui, PAN Xuan, LIU Shaoying

2024, 44(5):  551-557.  DOI: 10.16829/j.slxb.150877

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In August 2023, four specimens of shrew were collected from the Upper Yadong Township, Yatung, and Chen tang Town, Tingkye, Xizang Autonomous Region. Dorsally, the hair of this species is dark brown, the ventral hair light yellowish brown, the dorsoventral line is indistinct, and the tail two colors divided above and below. The four external measurements and nine skull measurements are basically consistent with the original measurements of Episoriculus soluensis. The parietal bone of the skull protrudes. The specimens have four upper unicuspids, the posterior cusps of the upper incisor are similar in height to the first upper unicuspid, and the cusps are light brown. These characteristics are consistent with those of E. soluensis, as is a phylogenetic analysis of Cyt b sequences based on data for the species in GenBank. The K2P distance between them is merely 3.0%. Thus, morphological and molecular analyses confirm the collected specimens constitute a new species record for the mammalian fauna of China.

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New records of Macroglossus sobrinus and Murina eleryi from Xizang Autonomous Region, China

DIAO Haixin, SU Haohui, SHI Zifan, PEI Xiaoxin, HUANG Qin, YU Chuanting, LI Quan, YU Wenhua, WU Yi, JIANG Xuelong, CHEN Zhongzheng

2024, 44(5):  558-562.  DOI: 10.16829/j.slxb.150915

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In October 2020 and December 2023, two bat specimens were collected in Medog County, Xizang Autonomous Region. Among them, one male specimen is medium in size, with small ears, non-protruding nostrils, and an elongated muzzle. The skull is small and elongated, with a narrow zygomatic width, a pronounced downward turn of the occiput, pointed upper canines, and two pairs of smaller upper and lower incisors, which is consistent with the characteristics of Macroglossus sobrinus. The maximum likelihood tree constructed based on COI gene showed that it was clustered with M. sobrinus specimes, and the genetic distance between them was 0.6%, which supported it to be M. sobrinus. The other specimen is a female with dark yellowish-brown dorsal fur with metallic luster, grayish-white ventral fur, and grayish-black hair bases. The wing membranes are black, the ears are nearly ovoid, and the nasal muzzle protrudes as a short tube, which is consistent with the characteristics of Murina eleryi. Phylogenetic analysis based on the COI gene showed that it was clustered with M. eleryi individuals, which supported it to be M. eleryi. Both M. sobrinus and M. eleryi represent new records for Xizang.

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Three new records of small mammals in Xizang Autonomous Region, China

ZHU Zhongxu, LI Quan, CHEN Zhongzheng, LI Xueyou, PEI Xiaoxin, WANG Hongjiao, PU Changzhe, LUO Kang, LUO Jing, PU Mingjin, JIANG Xuelong

2024, 44(5):  563-573.  DOI: 10.16829/j.slxb.150909

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A series of specimens of small mammals were collected in Nyingchi and Shigatse regions from Himalayas, Xi zang, China during the second comprehensive scientific expedition to the Qinghai-Xizang Plateau and the biological resources survey in key areas of Xizang by researchers from Kunming Institute of Zoology, Chinese Academy of Sciences. The specimens were subsequently identified as Sorex cansulus, Alexandromys limnophilus and Leopoldamys neilli by morphological and genetic analyses, which represented as new mammal records in Xizang. The population of Sorex cansulus in Xizang are similar to the Yunnan population in morphological characteristics, and maximum likehood phyloge netic analyses support the two populations are monophyletic (BS=100) and the K2P genetic distance of Cyt b gene is 0.5%? 0.6%. The Xizang population of Alexandromys limnophilus are similar to the Sichuan population in morphological characteristics, and the two populations are monophyletic (BS=100) and the K2P genetic distance is 1.0%? 1.4%. While Leopoldamys neilli in Xizang is somewhat different from the Yunnan and Thailand population, Molecular analyses supported the three populations are monophyletic (BS=81) and the K2P genetic distance is 5.7%? 6.3%. This study extend the distribution range of those species.

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Petaurista nobilis and Priapomys leonardi found in Xizang Autonomous Region of China

LI Quan, LI Xueyou, ZENG Xiangle, BAI Haotian, Stephen Jackson, HU Zhechang, ZHU Zhongxu, WANG Siyuan, LUO Kang, LUO Jing, PU Mingjin, PU Changzhe, JIANG Xuelong

2024, 44(5):  574-586.  DOI: 10.16829/j.slxb.150923

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Wildlife photographers and researchers from the Kunming Institute of Zoology, Chinese Academy of Scienc es, collected specimens and photographs of Petaurista nobilis from Yadong and Cuona County and Priapomys leonardi from Bayi District, Motuo and Cuona County, Xizang Autonomous Region, China between 2022 and 2023. The pelage, skull, and teeth morphology of the P. nobilis specimens resemble those of P. n. singhei Saha, 1975, and they form the sister group of Petaurista mishmiensis based on the Cytochrome b gene phylogeny analysis, with the genetic distance of 1.85%. Considering the very small genetic distance, continuous distribution range, and similar habitats between P. nobilis and P. mishmiensis, this study recommends that Petaurista mishmiensis be recognized as a subspecies of Petaurista nobilis. The Priapomys leonardi specimens from Xizang are similar to the northwest Yunnan population in terms of pel age, skull, and teeth morphology. However, they are slightly smaller, and their penis glans differ significantly in length, diameter, and shape. Genetically, the Xizang population is a paraphyletic group including the northwest Yunnan popula tion, with a relatively small genetic distance (12S ribosomal RNA:0.45%–0.91%, 16S ribosomal RNA:0.31%–1.05%). The results presented the first recording of P. nobilis in China and Priapomys leonardi in Xizang Autonomous Region, China, and significantly expands the known range of these taxa, highlighting the need for increased monitoring and research of mammal biodiversity in the Himalayan region. Future surveys in the region will probably discover more new species and records.

ORIGINAL PAPERS

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Effects of predation risk stress on the reproductive characteristics of male Brandt’s voles and their offspring

ZHOU Taoxiu, CHEN Lin, WU Yongzhen, YANG Shengmei, WEI Wanhong, WU Ruiyong

2024, 44(5):  587-597.  DOI: 10.16829/j.slxb.150904

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The present study aims to investigate whether predation risk stress can affect the reproductive characteristics of male Brandt’s voles (Lasiopodomys brandtii) and their offspring, and whether this is stage-specific. Adolescence is a crucial period for growth and development, and it is sensitive to external environmental factors. Thus, we speculated that exposure to predation risk stress during adolescence would have a more pronounced impact on the reproductive characteristics of both the males and their offspring. In this study, 90-day-old adult male Brandt’s voles and 28-day-old adolescent male Brandt’s voles were exposed to distilled water, rabbit urine, and cat urine for 1 hour daily for 18 consecutive days. Subsequently, half of each group was randomly selected for sampling to assess reproductive characteristics, including reproductive organ index, sperm quality and quantity. The remaining half was mated with a normal female, and their offspring's reproductive characteristics were evaluated until adulthood. The results indicated that, when compared to the control group, male Brandt’s voles exposed to cat odor during adulthood and adolescence significantly reduced normal sperm rate and increased sperm malformation and mortality rates, while exposure to rabbit odor only reduced the normal sperm rate. Exposure to cat odor during adulthood had no effect on reproductive output, whereas offspring from fathers exposed to cat odor during adolescence showed an increase in the ratio of female offspring at birth. Exposure to cat or rabbit odor during adulthood had no effect on offspring reproductive characteristics, but adult offspring from cat odor-exposed father during adolescence exhibited reduced gonadal index, sperm density, and normal sperm rate, as well as increased sperm deformity and mortality rates, while rabbit odor exposure only reduced sperm density and normal sperm rate in male offspring. These results confirmed our hypothesis that predation risk has a suppressive effect on the repro ductive characteristics of fathers and their offspring, especially during adolescence. The cross-generation transmission induced by paternal predation risk on offspring reproduction is stage-dependent.

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The activity rhythm and space utilization among six species of ungulates in Tangjiahe National Nature Reserve, Sichuan, China

HAN Yimin, XIAO Mei, HE Mengnan, LI Mingfu, HOU Rong, WU Pengcheng, HE Fang, SHEN Limin, HU Jie, CHEN Peng

2024, 44(5):  598-610.  DOI: 10.16829/j.slxb.150844

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Understanding the temporal and spatial distribution of sympatric species with similar niches is a primary focus in community ecology research. In this study, infrared camera technology was used for monitoring large and medium mammals in the forest ecosystem of Tangjiahe National Nature Reserve, Sichuan, China, from January to December 2021. A total of 82 camera-trap sites were deployed, resulting in a total of 18 710 days of camera workdays. Kernel density estimation and occupation model were used to analyze the temporal and spatial distribution of the six ungulates in the reserve during the cold and warm seasons. The results showed that the daily activity rhythms of the tufted deer (Elaphodus cephalophus) and the Reeves’s muntjac (Muntiacus reevesi) showed a high degree of overlap (? ≥ 0.80) in both seasons, while the Chinese takin (Budorcas tibetana), Chinese goral (Naemorhedus griseus), Chinese serow (Capricornis milneedwardsii), and wild boar (Sus scrofa) exhibited moderate overlap (? value between 0.50 and 0.80). The daily activity patterns of the tufted deer, Reeves’s muntjac, Chinese goral, Chinese takin, and wild boar were bimodal, with cre puscular tendencies, whereas the Chinese serow displayed a predominantly nocturnal and multimodal activity pattern. In the cold season, the Chinese takin had the highest occupancy rate (0.70), while in the warm season, the Chinese goral had the highest occupancy rate (0.96). The Chinese serow had the lowest occupancy rates in both seasons, at 0.18 and 0.19, respectively. Elevation, slope, slope direction, distance to water source, and distance from road were significant factors influencing the spatial distributions of these six ungulate species. The study demonstrates that activity rhythms and spatial utilization of the six ungulate species in Tangjiahe National Nature Reserve exhibit seasonal differences. These findings provide preliminary insights into the temporal and spatial distribution characteristics and influencing factors of ungulate species in different seasons, offering a scientific basis for the formulation of targeted conservation management strategies in this region.

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Habitat suitability analysis of Asian badgers (Meles leucurus) in the western Liaoning Province based on MaxEnt model

SHANGGUAN Zhouyi, FENG Chaofan, WANG Jianing, WAN Dongmei, ZHANG Lei

2024, 44(5):  611-621.  DOI: 10.16829/j.slxb.150848

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In order to assess the habitat use and suitable habitat distribution pattern of Asian badgers (Meles leucurus) in western Liaoning, 132 effective distribution points of this species obtained between 2018 and 2022 were used to generate the MaxEnt model. The results showed that topography, climate, vegetation, and water sources were the main environ mental factors affecting the distribution of badger in western Liaoning, while human disturbance factors had little im pact. The occurrence probability of badger in western Liaoning was the highest in the habitat with an altitude of 1 150 m, a slope of 40°, a NDVI of 85%, a maximum temperature (Bio5) of 24.5℃ in the hottest month, a temperature annual range (Bio7) of 39℃, and a distance of about 100 m from the river. The potential suitable habitat area for Asian badgers in western Liaoning is about 12 051.13 km², accounting for 41.63% of the total study area. The distribution of highly suitable habitats was relatively concentrated, mainly in Lingyuan, Jianchang, and Suizhong in the southwest of the study area, and Kazuo and Chaoyang in the central part of the study area. The distribution of low suitability areas is scat tered across all counties and cities in the study area, and the middle suitability area surrounds the high suitability area to form a transition area connecting the low suitability area. This study revealed the distribution pattern of suitable habitats and the dominant environmental factors limiting the distribution of badgers in western Liaoning, which will help clarify the ecological adaptability of badgers in different regions and provide more refined habitat distribution references for the management of Asian badgers in western Liaoning.

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Species diversity and distribution pattern of small mammals along an elevation gradient in the middle and low mountains of Changqing National Nature Reserve

NIE Haijuan, ZHANG Yazu, YAN Xiaodong, BU Shuhai, MA Youjun, ZHENG Xueli

2024, 44(5):  622-631.  DOI: 10.16829/j.slxb.150880

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Vertical distribution patterns across altitudinal gradients are one of the key topics in studying the distribution patterns of species diversity. To understand the vertical distribution pattern of mammals in Changqing National Nature Reserve, this study was carried out from June 2022 to June 2023 along an altitude range of 800 m to 2 423 m. Using the trap-day method and the trap method, 40 sample points were set up in 8 consecutive sites at 200 m intervals from 800 m to 2 423 m above sea level, resulting in a cumulative total of 8 858 trap days and 240 pitfall traps. A total of 357 smallsized species were captured, belonging to 3 orders, 7 families, and 20 species, including 16 species of Rodentia, 2 species of Eulipotyphla, and 2 species of Lagomorpha, including 5 new species recorded to the reserve. Both the Shannon-Wie ner and Simpson indices showed that species diversity was highest in the middle and lower elevations and the small ani mal community consisted mainly of Niviventer huang, Niviventer confucianus, and Apodemus draco. The regression of relative species multiplicity and interpolated corrected richness was fitted to a significant one-dimensional three-curve model (P< 0.01), with peak values (5.55%, 13) occurring around 1 200 m above sea level, indicating that species diver sity was highest at lower elevations. The vertical distribution pattern of small mammal species diversity in the middle and low elevations of Changqing Reserve showed an obvious left-biased center front pattern, suggesting that the reserve should also pay attention to the protection and management of the low-elevation section in the future.

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The conservation of wildlife habitats in the Beijing surrounding areas based on the EES system

XU Huimei, FANG Liang, WANG Lanxin, LIU Chao

2024, 44(5):  632-641.  DOI: 10.16829/j.slxb.150839

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Harmonious coexistence between man and nature is the essential requirement of Chinese modernization, and only through the coordinated development of the ecological-economic-social (EES) systems can a high-quality wildlife habitat, conducive to the harmonious development between humans and nature, be built. Based on the data from various districts around Beijing from 2009 to 2017, we select indicators from the EES system perspective and adopts the objec tive-AHP method (Objective Analytic Hierarchy Process) to assign weights to each indicator. Based on the coefficient of variation coordination development model, we obtain the degree of coordinated development between the EES systems of wild animal habitats in each district. Finally, using Huairou District as an example, we explore the actual impact of the degree of coordinated development on the quality of wild animal habitats. The results show that using objective-AHP for weighting, the Spe-AHP judgment matrix with an AIC value of 505.707 6 is selected based on the principle of mini mum AIC value. The maximum weight of the ecological system is 0.460 9, the weight of the social system is 0.281 7, and the weight of the economic system is 0.257 4. The coordination degree of each district is relatively high, except for the imbalance caused by the significant increase in the ecological system score, the others are in a coordinated state, but with low development, belonging to low development coordination. The degree of coordinated development of EES sys tems shows a gradual increase over time. Among the six districts, Fangshan, Huairou, and Mentougou reached primary coordination in 2016 and 2017, with the quality of wild animal habitats being higher than in other districts. The coordina tion between EES systems within habitats has a negative impact on the frequency of human-wildlife conflicts in the re gion.

METHOD AND TECHNOLOGY

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Preliminary survey of mammals and birds diversity using camera traps in Yaoshan National Nature Reserve, Yunnan Province

ZHAO Chenguang, YANG Wei, ZHONG Qianjuan, WU Minghui, HU Longqin, DOU Wenli, WU Han, DUAN Yubao

2024, 44(5):  642-653.  DOI: 10.16829/j.slxb.150760

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In order to systematically access the species diversity of mammals and birds of Yaoshan National Nature Re serve in Yunnan Province, we deployed 71 infrared cameras from July 2020 to October 2021 in 1 km × 1 km grid area of the reserve according to the altitude zone. During the monitoring period, a total of 17 960 camera days resulted in 8 274 independent and valid photos, including 3 810 mammals, 2 958 birds, 829 livestock, and 677 people. A total of 20 spe cies of mammals, belonging to 6 orders and 12 families, and 72 species of birds, belonging to 7 orders and 20 families, were recorded. Among them, one species is listed as Class Ⅰ and 15 species as Class Ⅱ National Key Protected Wildlife in China, representing 17.39% of total species listed. The five most detected mammal species were Dremomys per nyi, Muntiacus vaginalis, Callosciuru serythraeus, Arctonyx collaris, and Sus scrofa. The five most detected bird species were Chrysolophus amherstiae, Tragopan temminckii, Trochalopteron elliotii, Erythrogenys gravivox, Myophonus caeruleus. Our survey detected 42 species of birds new to the reserve, including Scolopax rusticola, Psittiparus gularis, and Larvivora cyane, and 3 new species of mammals, Martes flavigula, Meles leucurus, and Petaurista caniceps. There are significant differences in bird diversity at different altitudes and habitats (P<0.01), but there are no differences be tween birds in different seasons (P>0.05), and there are significant differences between animals in different seasons (P<0.01). This study provides real image data of birds and mammals from Yaoshan National Nature Reserve, Yunnan Province, not only updates the database of species diversity in this area but also provides an objective basis for scientific protection and precise management of the reserve.

SCIENTIFIC NOTES

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Retention time and remaining percentage of digestive tract seeds in black-and-white snub-nosed monkey

JIANG Yanxian, NIU Xin, LAI Jiandong, LI Yanpeng, HUANG Zhipang, XIAO Wen

2024, 44(5):  654-659.  DOI: 10.16829/j.slxb.150783

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Non-human primates are one of the three main seed dispersing groups, and it is crucial to evaluate the efficien cy of primate seed dispersal via the retention time and remaining percentage of seeds in their digestive tracts. To evalu ate the ability of black-and-white snub-nosed monkey (Rhinopithecus bieti), a rare and endangered primate, disperse seeds in temperate forest environments, we investigate digestive tract retention time and remaining percentage of seeds, and evaluate the relationship with the size of seeds. We fed an adult male R. bieti who just rescued in captivity with four species of fruits, namely Actinidia purpurea, Sorbus scalaris, Sorbus megalocarpa and Cotoneaster horizontalis, at the Tacheng Wildlife Rescue Station of Yunnan Baimaxueshan National Nature Reserve from October to November 2021. All feces excreted by the male R. bieti were collected and recorded, and the seeds remaining in the feces were sorted, and the time of seed excretion and the number of complete seeds were recorded. The mean retention time of the four fruit seeds through the digestive tract of R. bieti was (34.60 ± 8.34) h. The retention time of the fruit seeds through di gestive tract was influenced by the size of the seeds, with the smaller seeds the longer retention time (r_s=?0.519, n=12, P < 0.01). The mean percentage of fruit seeds remaining after passing through digestive tract was 17.7%(6.7%–61.7%), and the percentage of fruit seeds remaining after passing through their digestive tract was not affected by the size of seeds (r_s=0.17, n=12, P=0.957). The retention time of seeds in the digestive tract of R. bieti was less than that of the previous long-term caged individuals (34.6 vs. 47.0), and the retention time of seeds was influenced by seed size. Our results provide a reference for assessing the seed dispersal distance of R. bieti and experiment of germination rate in future. Therefore, as the R. bieti can spread plant seeds to enrich the soil seed bank and promote forest regenera tion, future conservation of this species can be called for in terms of the role of R. bieti in the ecosystem.

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Preliminary study on bipedal walking behavior of Hainan gibbon (Nomascus hainanus)

LI Ping, REN Baoping, DENG Huaiqing, JIN Kun, LI Wenyong, ZHOU Jiang, QI Xuming

2024, 44(5):  660-664.  DOI: 10.16829/j.slxb.150849

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The species in Hylobatidae are specialized arboreal primates that barely move on the ground in the wild. In the previous monitoring studies, no records of bipedal walking behavior of Hainan gibbon (Nomascus hainanus) were re ported. Here, we recorded seven cases of the bipedal walking behaviors of the Hainan gibbon using a combination meth od of infrared cameras and human tracking in Bawangling area of Hainan Tropical Rainforest National Park from Janu ary 2020 to August 2023. The background, duration and activities after each action are described in detail. The behaviors were classified into active bipedal walking and passive bipedal walking, the causes are analyzed, and the topographic fea tures of the possible bipedal walking location are proposed, and the key monitoring regions are delimited. This report can not only protect the Hainan gibbon population more effectively but also provide updated data for compiling the be havior spectrum of Hainan gibbon.