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30 March 2024, Volume 44 Issue 2

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ORIGINAL PAPERS

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Ontogeny and the influencing factors of bite force and feeding rate of giant pandas (Ailuropoda melanoleuca)

SUN Mengmeng, YAN Xiao, LI Feng, TANG Yong, ZHANG Xinxing, DONG Chao, HUANG Shengjie, ZHENG Yuanming, LUO Yong, ZHOU Shiqiang

2024, 44(2):  135-145.  DOI: 10.16829/j.slxb.150781

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The biting ability of giant pandas (Ailuropoda melanoleuca) holds significant importance in terms of food acquisition and male-male competition. Their distinctive dietary preferences and masticatory system render them an ideal species for investigating bite forces. Nevertheless, current studies have predominantly relied on theoretical assessments derived from panda skull morphology, with no empirical animal experimentation conducted. The present study designed a force transducer specifically tailored for giant pandas, and measured body weight, bite forces, and feeding rate in a sample of 46 individuals from various age groups, with a particular focus on juvenile development. The results showed that bite forces at the tip of the incisor of juvenile giant pandas increased rapidly during the dental transitional period, as well as the feeding rate of bamboo shoots. At the end of the dental transitional phase, the bite forces exerted at the incisor point of juvenile giant pandas continued to display a growing trend, albeit at a decelerated rate. Concurrently, the feeding rate reached a state of equilibrium. The utilization of a logistic model revealed that age explains 87.56% of the variance observed in the feeding rate among juvenile pandas. As for the comparisons of age groups, the median bite force value exhibited an upward trajectory in tandem with increasing age. The bite force of 8-month to 12-month age group was significantly lower than the bite forces of all the other age groups; the bite force of 13-month to 18-month age group was significantly lower than those of sub-adult, adults and geriatric group; however, there was no significant difference between the latter three groups. The adult group has the highest feeding rate of bamboo shoots and carrots, followed successively by the sub-adult group, the geriatric groups and the juvenile group. In summary, our study confirmed for the first time the feasibility of measuring bite forces of giant pandas by using force transducer, recorded the developmental process of bite forces and feeding rate of juvenile giant pandas during the dental transitional period, and discussed the effect of age on bite forces and feeding rate, all of which laying a good foundation for future work of giant pandas’ feeding ecology.

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Individual identification and genetic diversity of Eurasian otters based on microsatellite markers

ZHENG Kaidan, WANG Qiaoyun, FAN Pengfei, HAN Xuesong, XIAO Mei, SHEN Limin, DONG Zhengyi, ZHANG Lu

2024, 44(2):  146-158.  DOI: 10.16829/j.slxb.150814

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Population size and genetic diversity are important basic information for threatened species conservation. As a Class II protected animal, Eurasian otter (Lutra lutra) was once widely distributed in China, but has experienced severe population decline and range shrinkage over the 20th century. However, only a few studies have been conducted on Eurasian otters in China. Basic research such as population surveys and genetic diversity studies are urgently needed. We collected 270 otter spraints for DNA extraction during 2019-2020 in Yushu City, Qinghai Province and Qingchuan County, Guangyuan City, Sichuan Province. We used 9 microsatellite loci and the SRY gene to genotype individuals and identify sex. Then we estimated the sizes of the two populations based on individual identification and noninvasive capturerecapture method (Capwire). We also assessed their genetic diversity based on the nine microsatellite markers. We successfully genotyped 67 spraints (24. 8%) with 7 - 9 microsatellites and identified 40 otter individuals. Among them, 10 were from Yushu and 30 were from Qingchuan, with a sex ratio of 4F/5M and 15F/14M respectively. Sex identification failed for two individuals. The estimated population of otters within our study area was 13 (95% CI: 7 - 21) in Yushu City and 75 (95% CI: 59-133) in Qingchuan County. The average observed heterozygosity (H_O) and expected heterozygosity (H_E) of the Yushu population were 0. 680 and 0. 611, while those of the Qingchuan population were 0. 664 and 0. 658, revealing a moderate genetic diversity. Otters in Yushu and Qingchuan have been differentiated significantly (F_ST = 0. 238) and no significant inbreeding was found in both populations (F_IS: Yushu -0. 121, Qingchuan -0. 010). As the first study estimating population size and genetic diversity of Eurasian otters based on fecal DNA in Chinese mainland, our work provides important basic information for otter conservation in China.

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Parentage testing and genetic diversity of Tibetan antelope individuals in or among mating groups

Saiqinggaowa, WANG Zihan, LI Quanbang, WANG Dong, LIAN Xinming

2024, 44(2):  159-170.  DOI: 10.16829/j.slxb.150807

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Tibetan antelope (Pantholops hodgsonii), an endemic species of the Qinghai-Tibet Plateau, exhibits group living and sexual segregation behaviors. Outside the rutting season, male and female Tibetan antelope live separately. In this study, a total of 188 fresh fecal samples were collected from 32 groups of Tibetan antelope in the Kekexili region of the Sanjiangyuan National Park in late December 2021. Genetic diversity analysis and parentage testing were conducted using ten highly polymorphic microsatellite loci. The findings revealed that out of the 188 fresh fecal samples, genetic identification confirmed the presence of 145 individual Tibetan antelope. Among them, ten Tibetan antelope individuals (eight females and two males) sequentially appeared in different groups over time. Field observations indicated three mechanisms for recombination among mating groups including group dissolution, male departures or arrivals to/from existing groups, and female departures or arrivals to/from existing groups. Notably, there was considerable genetic differentiation between individuals that changed groups compared to those remaining within their original group composition. Male Tibetan antelopes moved to groups with a higher proportion of females than their previous ones, thereby increasing their potential for acquiring more mates and enhancing opportunities for gene inheritance. The average number of alleles across the ten microsatellite loci was 16. 1, with an average polymorphic information content of 0. 766. Observed heterozygosity (Ho) ranged from 0. 607 to 0. 993 with a mean value of 0. 819. Expected heterozygosity (He) ranged from 0. 575 to 0. 930 with a mean value of 0. 798. These results indicated a high level of genetic diversity within the Tibetan antelope population. At the group level, out of the total parent-child relationships observed (n = 32), fourteen (43. 75%) occurred within the same group, predominantly in mother-daughter relationships (71. 43 %), while only four (28. 57%) involved males (mother-son/father-daughter/father-son). By comparing the average coefficients of relatedness between groups with or without males, our findings suggested that the presence or absence of males had minimal impact on genetic relatedness among group members, indicating that closest genetic relationships within mating groups were primarily among females. Our findings demonstrated that low levels of inbreeding in Tibetan antelope populations and highlight female-female associations as key drivers for forming stable groups and facilitating communication and transmission of migration information due to their higher relatedness compared to males. These results provided scientific evidence supporting further validation of the collective memory conjecture regarding Tibetan antelope migration.

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Cardiomyocyte communication and its gene expression difference between different altitudes yaks based on single cell RNA-seq data

HUANG Nating, CHEN Yibo, SONG Na, LI Jingyi, WEI Qing, CHEN Jiarui

2024, 44(2):  171-182.  DOI: 10.16829/j.slxb.150817

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As the most important organ for blood circulation, the heart plays an important role in the environmental adaptation of animals. Cardiomyocyte is the main functional cell in the animal heart, however, gene expression changes and cellular communication in cardiomyocytes of yaks living at high altitudes are still unclear. To study the effect of yak cardiomyocytes in the process of adaptation to the plateau environment, yaks in high altitude areas (Qilian, Qinghai, altitude 4000 m) and low altitude areas (Xunhua, Qinghai, altitude 2 600 m) were taken as research objects, and the cellular communications and ligand-target gene regulations in cardiomyocytes and other cells were predicted based on the 10× singlecell RNA sequencing data. In addition, the functions of differentially expressed genes (DEGs) between different altitude yak cardiomyocytes were annotated. The results showed that yak cardiomyocytes were most highly correlated with the endothelial cells and epithelial cells. The expression level of ligand and receptor of CD74_COAP and CD74_APP was relatively higher in the cardiomyocyte-dendritic cell and cardiomyocyte-macrophage, the vitality of ligands and receptors was relatively higher in TNF signal pathway; The immune related pathway ligands, such as PTPRC, PECAM1, ITGB2, ANXA1, BDNF had a significant influence on all ‘cell pairs’and the PI3K-Akt signal pathway showed the highest potential score in ligand-target gene regulation; The functions of DEGs between high and low altitude yak cardiomyocytes were mainly enriched in metabolic pathways as the oxidative phosphorylation and glycolysis pathways. These results suggest that yaks may maintain their homeostasis by strengthening the connection between cardiomyocytes and other cells and regulating the processes related to immune action. Meanwhile, high-altitude yaks enhance their aerobic and anaerobic metabolism of cardiomyocytes to acquire more energy to adapt to the harsh environment of high altitude.

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Difference of gut microbial structure between Rhinopithecus brelichi and Macaca thibetana in Fanjingshan Nature Reserve

HUANG Xiaolong, LI Haibo, ZHANG Xu, CHENG Shaochuan, YAN Yuying, YANG Wei, MENG Bingshun, WANG Cheng, YANG Jie, RAN Jingcheng

2024, 44(2):  183-194.  DOI: 10.16829/j.slxb.150837

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Gut microbial are closely related to animal health. Gut microbiota has evolved with the host and formed a complex microecosystem with the gastrointestinal tract of animals. To compare the Rhinopithecus brelichi and Macaca thibetana on gut microbial composition and functions, a total of 42 winter fresh feces samples were collected from Fanjingshan National Nature Reserve in China, and a 16S rRNA gene high-throughput sequencing was performed. The results showed that the gut microbial Chao1 and Shannon indexes of R. brelichi were significantly higher than those in the M. thibetana (P < 0. 05). The β–diversity based on bray-curtis distance matrix found that there were some similarities and differences in the gut microbial community structure between the two groups. At the phylum level, Firmicutes was the dominant phylum, and the relative abundance of R. brelichi was higher than that of M. thibetana. At the genus level, except Acinetobacter and Oscillospira, which were relatively abundant, the other dominant bacterial genera were different between the two species. LEfSe analysis showed that the microorganisms like Coprococcus, Blautia, and Akkermansia related to metabolic pathway had significantly different relative abundance between the two species. Functional prediction of PICRUSt showed that the gut of the two groups of microorganisms were mainly involved in metabolism, genetic information processing, environmental information processing, and cellular processes. At level 2, there were 3 types of metabolic pathways with significant differences (P < 0. 05). Different species and numbers of individuals and different food sources of the two primates resulted in significant differences in gut microbiota composition and characteristics of R. brelichi and M. thibetan in the Fanjingshan. PICRUSt functional prediction showed that there were significant differences in the abundance of functional genes of gut microbiota in the two groups, suggesting that the two groups could adapt to the changes of in food resources by adjusting their gut microbiota. These results can provide a scientific basis for future in-depth study of the gut microbiome of the two primate species with highly overlapping ecological niches, and also have a certain reference value and practical significance for the establishment of artificial protection intervention measures for the two species in the field.

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Effects of artificial feeding on the composition of gut microbiome of longtailed hamster

CAO Kanglin, TAO Mengfan, REN Yue, HOU Yu, JIA Biantao, YANG Xingen

2024, 44(2):  195-208.  DOI: 10.16829/j.slxb.150808

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The alteration in diet is a pivotal factor contributing to modifications in the gut microbiota of small mammals. When transitioning from their natural habitat to captivity, wild animals undergo drastic changes in their lifestyle, however, the succession processes underlying the establishment of intestinal microbial community structure from artificial feeding remain incompletely elucidated. To clarify the effects of artificial feeding on the composition of gut microbiome of small mammals, natural populations of long-tailed hamster (Cricetulus longicaudatus) were captured using cage trapping from Lishi District (LS), Xi County (XX) and Zuoquan County (ZQ) in Shanxi Province in summer (from July to September) of 2022. Based on 16S rDNA high-throughput sequencing, we analyzed the differences of intestinal flora in different ecological environments, and explored the succession process of artificial feeding on the gut microbial composition. The results showed that Firmicutes were significantly enriched in XX and ZQ populations while bacteroides were significantly enriched in LS population. Intestinimonas is a common dominant genus in the three populations. After 35 days of artificial feeding, Bacteroides were significantly enriched in the three populations and their relative abundance tended to be consistent. The relative abundance of Muribaculacea in ZQ population was 48. 85%, which was significantly higher than that in the wild environment. Our study shows that the diversity of the gut microbiota of C. longicaudatus is different in distinct ecological environments. After long-term artificial feeding, the similarity of gut microbiome of different C. longicaudatus populations increased significantly, indicating that diet change has a great impact on the diversity and community composition of gut microbiome, and the composition of gut microbiome of C. longicaudatus may play an important role in nutrition metabolism. The results provided a scientific basis for a better understanding of the ecological adaptability of the intestinal microbiome of C. longicaudatus, and the utilization of food as a means to regulate the population of detrimental.

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Relationship between maternal fecal cortisol levels and mother-infant behaviors in early nursing period of giant panda

ZHOU Xiao, YANG Bo, ZENG Wen, LI Guo, YANG Changjiang, WANG Jing, XIE Qingyang, LIU Huaiting, WANG Rui, LUO Bo, ZHANG Mingchun, HUANG Yan

2024, 44(2):  209-216.  DOI: 10.16829/j.slxb.150741

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Giant panda (Ailuropoda melanoleuca) is an altricial species. The early period of nursing is critical for the survival, growth and development of the cub, and also the most vulnerable period for the young. In order to understand the relationship between maternal cortisol levels and mother-infant behaviors during the early nursing period, and improve the survival rate of cubs in the aspect of behavioral adaptation mechanism, were monitored the concentration of fecal cortisol of 7 mother pandas in the early nursing period (0-75 days) by enzyme-linked immunosorbent assay (ELISA). In addition, we observed the behaviors of 3 pairs of mother and infant using the focal animal sampling method. The results showed that the fecal cortisol concentration of mother panda decreased with the cub’s growth by days (r = -0. 950, P < 0. 001) in the early nursing period. Before and after weaning, there was no significant difference in maternal cortisol concentrations (t = -0. 935, P = 0. 361). The changes in maternal cortisol concentrations had significant positive correlations with communicating (r = 0. 0918, P < 0. 001), cub calling (r = 0. 777, P = 0. 001) and resting (r = 0. 731, P = 0. 002) behaviors. Furthermore, cortisol concentrations were negatively correlated with feeding (r = -0. 608, P = 0. 016) and not correlated with licking (r = 0. 366, P = 0. 179). Results indicated that the cortisol concentration of the mother giant panda was related to the growth and development of the cub during the early nursing period. We hypothesize that the stress intensity of the mother might decrease with the improvement of the cold resistance and independent activity ability of the cub. In addition, cortisol may be involved in the regulation of maternal behavior, which can help the mother respond positively to the demand signals of her cub, enhance maternal behavior, and thus improve the survival rate of her cub at the early stage of nursing.

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Effects of fostering methods on the growth and development of giant panda cubs with different birth weight

WU Kai, LAI Jiaying, WEI Ming, ZHANG Yahui, ZENG Xianyin, WEI Rongping, CAO Xiao-han, HU Zhengquan, ZENG Wen, WANG Chengdong, KONG Fanli

2024, 44(2):  217-223.  DOI: 10.16829/j.slxb.150705

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In this study, 80 giant panda cubs born between 2012 and 2019 were selected to systematically study the effects of birth weight ([50, 100) g, n = 7; [100, 150) g, n = 25; [150, 200) g, n = 37; [200, 250) g, n = 11), fostering method (female feeding, n = 12; artificial feeding, n = 10; artificial and female alternate feeding, n = 58) and fetal litter size (single, n = 14, and twins, n = 66) on the growth and development of the cubs. We collected the daily gain, milk feeding amount, and eye and ear development during the early development of the cubs (from 0 to 120 days). The results showed that the birth weight of singleton pups was significantly higher than that of twin pups (P < 0. 05). We also found that the early growth and development of pups are closely related to their cub-fostering methods and birth weight (R² > 0. 973 7). The greater the birth weight of the pups, the greater the growth rate. The lighter the birth weight of the cubs, the lower the shrinkage, but the higher ratio of shrinkage to its birth weight. In addition, the lighter the birth weight of pups, the lower the developmental status of their ears and eyes. In conclusion, our study provides a theoretical basis on the selection of and the improvement of cub-fostering methods for the giant panda.

REVIEWS

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Research advances on spatial memory on animal movement

GUO Xiaoyi, WANG Wei, GU Jiayin, JIANG Guangshun

2024, 44(2):  224-236.  DOI: 10.16829/j.slxb.150787

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Many animal groups show strong directionality and regularity as they move within home ranges or migrate seasonally over long distances. They can integrate significant spatial cues for destination recognition, navigation, and memory of the types of food available in the habitat, the distribution of food patches and the season of food maturity, and construct spatial cognitive maps, showing a strong spatial memory capacity. This article comprehensively reviews the research methods of captive experiments, field experiments in natural environments, observation and analysis of natural state movement trajectories, and exploration of animal spatial memory in digital virtual experimental environments. The characteristics and application ranges of these research methods are summarized, and future research trends are prospected. The integration of multiple disciplines, multiple application scenarios, and the development of animal spatial memory ecological models have become the main development trends in this field. The study of animal spatial memory can provide new perspectives for in-depth exploration of animal habitat utilization mechanisms, intrinsic movement driving forces, and the maintenance mechanisms of biodiversity. In addition, this research field can also provide scientific basis and reference for wildlife management practices such as endangered species conservation, alleviating human-wildlife conflicts, and improving the welfare of captive animals.

METHOD AND TECHNOLOGY

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Preliminary study on the diversity of medium and large-sized mammals and pheasants at Chuxiong sub-region, Yunnan Ailaoshan National Nature Reserve

YIN Guanghua, QIN Zhongyi, LUO Wenfu, LU Lixiong, LI Han, GAO Wenjun, XU Ping, LI Qianen, YIN Cunquan, LI Genhui, ZHANG Zhiqiang, LI Yuwu, LIU Dong, JI-ANG Xuelong, LI Xueyou

2024, 44(2):  237-246.  DOI: 10.16829/j.slxb.150751

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Between March 2020 and May 2022, we conducted a systematic camera-trapping survey to understand the diversity of medium and large-sized mammals and pheasants at Chuxiong Prefecture sub-region of Yunnan Ailaoshan National Nature Reserve. We set 153 camera traps along 1 km ×1 km grids, with a total trapping effort of 59 623 days, which yielded 9 309 independent records of wildlife species. A total of 23 medium and large-sized terrestrial mammals and seven pheasant species were observed: 14 families of 5 orders for mammals and 1 family of 1 order for pheasants. Of which, three and 14 species were listed as Class One and Class Two protected species respectively by the Chinese muntjac (Muntiacus vaginalis, RAI = 7. 52), tufted deer (Elaphodus cephalophus, RAI = 2. 43),wild boar (Susscrofa, RAI = 2. 39), macaque(Macaca mulatta, RAI = 2. 26) and Malayan porcupine (Hystrix brachyura, RAI = 2. 16). Species rank-abundance curve showed that species in the first three ranks were the northern red muntjac, wild boar, and silver pheasant Lophura nycthemera, which together contributed to 65% of the accumulative abundance of the whole community. In addition, our camera-trapping survey recorded numerous human-related inerference such as livestock grazing, indicating that the reserve is under some levels of anthropogenic disturbance. Overall, our first systematic camera-trapping survey provides basic information on the diversity of medium and large-sized mammals and pheasants at Chuxiong Prefecture sub-region of Yunnan Ailaoshan National Nature Reserve. Such knowledge is important for local wildlife biodiversity management and conservation. Wildlife Conservation Law. The five species with the highest relative abundance indices (RAI) were the northern red

SCIENTIFIC NOTES

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A new method for identifying individuals of François's langur based on observations of white spots on the groin

YAN Xiugang, QI Xiaoguang, GUO Yanqing, ZHANG Peng, WU Ankang, YANG Zhaohui

2024, 44(2):  247-251.  DOI: 10.16829/j.slxb.150732

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The François’s langur (Trachypithecus francoisi) is a nationally protected animal in China. Individual identification of the François’s langurs is essential for monitoring, research, and conservation management. Mayanghe National Nature Reserve in Guizhou Province is the largest habitat for wild populations of the François’s langur. In this study, three groups of wild François’s langurs within the experimental area of Mayanghe Reserve were selected. The instantaneous scan sampling method was used to observe the gibbon groups, and digital cameras were used to photograph the ventral groin patches of 16 adult and sub-adult females. By comparing the results, we found that there were individual differences in the patterns of ventral groin patches among François’s langurs, suggesting that these patterns can be used as a method for identifying individuals. This study provides new insights and research methods for individual identification of François’s langurs and contributes to the fundamental data for studying their behavior in the wild. Furthermore, it offers a scientific basis for the conservation and management of François’s langurs.

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Spatiotemporal variation of composition and diversity of small mammals in Shenzhen Bao’an International Airport

YUAN Daohuan, CHENG Shoujie, YUAN Qianmin, JI Yu, QIN Jiao, LIANG Yitian, LIU Quansheng

2024, 44(2):  252-258.  DOI: 10.16829/j.slxb.150826

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Bird strikes are a serious threat to the safe operation of the global aviation industry, and many birds feed on small mammals. Therefore, understanding the species composition, density, distribution and population dynamics of small mammals inside and outside of airports is of great significance for airport bird control and flight safety. To understand the characteristics and spatiotemporal variation of the species, quantity, and diversity of small mammals in the runway area and peripheral areas of Shenzhen Bao’an International Airport, four small mammal surveys were carried out in Shenzhen Airport from November 2021 to July 2022. A total of 152 small mammals from 6 species, 4 genera, 2 families, and 2 orders were captured by 1 343 effective clips. Rattus losea (37. 50%) and Mus caroli (36. 84%) were the dominant species. The capture rate of the four surveys was 11. 66% ± 2. 42%, and the seasonal variation of the capture rate was not significant. The total capture rate and rodent capture rate in the airport were significantly lower than those outside the airport. Species richness index and Shannon-Wiener index were the highest in November, while Pielou index was the lowest. Species richness index and Shannon-Wiener index inside the airport were slightly lower than outside the airport, while Pielou index was higher than outside the airport. The results indicate that small mammals should be controlled both inside and outside the airport to reduce the attraction of birds such as birds of prey, thereby reducing the risk of bird strikes at the airport.