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30 January 2023, Volume 43 Issue 1

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ORIGINAL PAPERS

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Effect of temperature acclimation on thermosensitive transient receptor potential channels of liver in Brandt’s voles (Lasiopodomys brandtii)

LYU Jinzhen, TANG Liqiu, ZHANG Xueying, WANG Dehua

2023, 43(1):  1-10.  DOI: 10.16829/j.slxb.150674

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Liver is a key organ of basal metabolic thermogenesis in mammals. Thermosensitive transient receptor potential channels (Thermo-TRPs) are involved in the regulation of various physiological functions of hepatocytes. In order to understand whether Thermo-TRPs are involved in liver metabolic thermogenesis, we measured the expressions of six types of Thermo-TRPs in liver of adult Brandt's voles (Lasiopodomys brandtii) acclimated at different temperatures, and assessed the relationship between Thermo-TRPs and liver thermogenesis related proteins and signaling pathway proteins. Results showed that:(1) Compared with the hot (30℃) group, cold (4℃) acclimation increased the expression of uncoupling protein 1 (UCP1) in liver but cold acclimation decreased the expression of UCP3 in liver compared with the warm (23℃) group. (2) Six types of Thermo-TRPs were expressed in liver. Compared with the hot group, cold acclimation decreased the expression of TRP vanilloid 4 (TRPV4) and increased AMP-activated protein kinase (AMPK) in liver. (3) The level of serum thyroid hormone (T₃) and the ratio of T₃/T₄ were significantly higher in the cold than other groups. Ratio of T₃/T₄ was positively correlated with UCP1 and AMPK in liver, and UCP1 was positively correlated with TRPM2 and AMPK in liver. These results suggest that liver TRPV4 and AMPK may be involved in the regulation of physiological functions such as metabolic thermogenesis under cold conditions.

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Effects of a high-fiber diet on energy metabolism in Niviventer lotipes

CHI Qingsheng, LUO Huining, YAO Xiaogang, LI Guangrong, YANG Changqian, ZHANG Qiang, LIU Yuhang, LIU Quansheng

2023, 43(1):  11-20.  DOI: 10.16829/j.slxb.150700

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Small mammals usually show physiological adaptations to cope with seasonal changes in food quality. To examine the adaptive strategy in energy metabolism of Niviventer lotipes responding to varying dietary quality, we acclimated Niviventer lotipes to high-fiber standard rabbit pellets for 4 weeks with a group of animals fed with standard rat pellets as control. Body mass, parameters of energy intake, and expenditure were measured during the experiment. At the end of the experiment, animals were sacrificed to analyze the body composition. The results show that body mass of Niviventer lotipes fed with rabbit pellets decreased continuously and reached 62. 8% of that in control at the end of the experiment. Basal metabolic rate and nonshivering thermogenesis decreased significantly to 55. 1% and 63. 4% of the control respectively after the food treatment of 4 weeks. Food intake, digestive energy, and apparent digestibility also decreased to 63. 7%, 38. 8%, and 71. 8% of that in control, respectively. Body composition analysis showed that the mass and/or length of most vital organs and digestive tracts significantly decreased in animals fed with high-fiber rabbit pellets. Taken together, apparent digestibility decreased in Niviventer lotipes fed with a high-fiber diet, however, neither the mass/length of digestive tracts nor food intake increased to compensate for the decrease in digestive efficiency. Although the basal metabolic rate and nonshivering thermogenesis were down-regulated in animals fed with rabbit pellets, the energy balance cannot be maintained thus the body mass decreased significantly. This might be explained by the low selection pressure related to the utilization of a high-fiber food in the subtropical habitats of Niviventer lotipes.

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Effects of exogenous leptin injection on adaptive thermogenesis in Eothenomys miletus between Kunming and Dali regions

CHEN Huibao, JIA Ting, ZHANG Di, ZHANG Hao, WANG Zhengkun, ZHU Wanlong

2023, 43(1):  21-32.  DOI: 10.16829/j.slxb.150667

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Small mammals respond to environmental stress by adjusting their thermogenic capacity. To investigate the effect of exogenous leptin on the induction of adaptive thermogenesis in Eothenomys miletus from Kunming (KM) and Dali (DL), 14 voles were selected from each region and placed at 25℃ ± 1℃ with a photoperiod of 12L:12D, and daily intraperitoneal leptin injection last for 28 days. LT502 electronic balance was used to measure the body mass every two days in E. miletus, the food intake was measured by the food balance method every two days, and the resting metabolic rate (RMR) and nonshivering thermogenesis (NST) were measured by a portable respiratory metabolic measurement system every seven days. After the animals were killed on day 28, mitochondrial protein content (MtP), mitochondrial cytochrome c oxidase (COX) activity and uncoupling protein 1 (UCP1) content, serum levels of triiodothyronine (T₃), thyroxine (T₄), leptin, thyrotropin-releasing hormone (TRH) and adrenal corticotropin-releasing hormone (CRH) were determined by enzyme-linked immunosorbent assay (ELISA). The results showed that leptin injection significantly reduced body mass and food intake, enhanced RMR and NST, increased MtP and COX activity in liver, COX activity and UCP1 content in brown adipose tissue (BAT), and serum T₃, T₄, T₃/T₄ ratio, TRH and CRH concentrations in E. miletus from KM and DL. Leptin levels were negatively correlated with body mass and food intake, and serum T₃ levels were positively correlated with NST and UCP1 levels. Moreover, body mass and food intake were higher in voles from KM region than those from DL region before injection, but RMR and NST were lower in animals from KM region. The changes in body mass in E. miletus from KM after exogenous leptin injection were higher than those from DL, while the changes in food intake, RMR, and NST were lower in KM voles than those in DL. In conclusion, exogenous injection of leptin reduced body mass and food intake and increased thermogenic capacity and energy metabolism in the two regions, suggesting that leptin was involved in their body mass and thermogenic regulation. Furthermore, E. miletus in the DL region was more sensitive to exogenous leptin injection, which may be related to low habitat temperature or poor food quality in DL.

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Isolation, identification, and miRNAs enrichment analysis of exosomes derived from giant panda umbilical cord mesenchymal stem cells

AN Junhui, LI Yuan, WANG Donghui, CHEN Jiasong, LI Hongyan, LIANG Xiaohu, FENG Tongying, CAI Zhigang, HOU Rong, ZENG Changjun, LIU Yuliang

2023, 43(1):  33-40.  DOI: 10.16829/j.slxb.150664

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The exosomes released by giant panda umbilical cord mesenchymal stem cells (UC-MSCs) through paracrine mechanisms have application prospects in giant panda veterinary care and disease treatment. The aims of this study were to explore a method of separating exosomes secreted by giant panda UC-MSCs, identify their biological and molecular characteristics, and study the miRNA expression profile and distribution characteristics. Ultracentrifugation was used to successfully isolate exosomes from the supernatant of giant panda UC-MSCs culture medium. The morphological observation was performed by transmission electron microscopy, particle size was detected by nanoparticle tracking analyzer, and the expression of specific molecular markers was detected by western blotting. In addition, the small RNA sequencing technology was used to explore the expression profile and function of exosomal miRNAs. The results showed that the exosomes obtained from giant panda UC-MSCs displayed a circular cup-shaped structure with a particle size of (79. 15 ± 4. 81) nm. These exosomes were positive for CD81 and TSG101 but negative for CALNEXIN. The miRNAs in exosomes were mainly composed of miR-148-3p (30. 28%) and miR-21-5p (21. 72%). In this study, we harvested exosomes from the supernatant of giant panda UC-MSCs culture medium for the first time and conducted the enrichment analysis and functional prediction of UC-MSCs miRNAs. This study lays the foundation for follow-up studies of UCMSCs exosomes and their clinical application in giant pandas.

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Genetic diversity of wapiti in northeast China based on fecal DNA

TIAN Xinmin, ZHANG Minghai

2023, 43(1):  41-49.  DOI: 10.16829/j.slxb.150677

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As an endangered species listed in the Class Ⅱ protected species of the national government of China, wapiti (Cervus canadensis xanthopygus) in northeast China has been experiencing population contraction and gene flow block between populations in recent years, and it is hard to find its traces in many areas. It is an urgent need to further evaluate the genetic changes of the population, especially the genetic diversity and inbreeding decline, so as to enhance the pertinence of conservation and management. In this study, 409 suspected fecal samples of wapiti were collected from six key research areas in Daxing'an, Xiaoxing'an, and Changbai Mountains. Firstly, species identification was carried out based on mtDNA Cyt b gene sequencing technology, and the positive samples were supplied for further individual identification by microsatellite technology. Finally, 172 wapiti individuals were identified from the 409 fecal samples. The results showed that there were 14 variation sites and 11 haplotypes in the Cyt b sequence of wapiti. In the populations, the haplotype diversity and nucleotide diversity of Cyt b gene were 0.849 (0.105-0.732) and 0.678% (0.099%-0.775%), respectively. Based on 10 microsatellite loci, we found that the mean number of alleles was 5.7 (5.2-7.2), the effective number of alleles was 3.3 (2.5-4.1), the average observed heterozygosity was 0.687 (0.644-0.725), the average expected heterozygosity was 0.619 (0.564-0.689), and the inbreeding coefficient was -0.113 (-0.160 to-0.037) in the populations. The results showed that the genetic diversity was at a medium level for populations, among which the Shuanghe and Tieli populations were the highest, followed by the Gaogestai and Huangnihe populations, and the Fangzheng and Muling populations were the lowest. The population decline and isolation of the distribution area affected the genetic diversity pattern of the six local populations. The high proportion of rare haplotypes and alleles suggested a risk of decreasing genetic diversity in the future. The Gaogestai and Huangnihe populations displayed significant differences in haplotype diversity and nucleotide diversity, which may be the result of rapid growth after the population decline. The negative inbreeding coefficients of populations showed no risk of inbreeding. It is suggested that individuals with rare haplotypes and alleles should be key targets in monitoring and protection. Additionally, promoting exchanges of individuals with nearby populations and releasing artificially bred populations in the field at the appropriate time may improve the gene exchange between individuals and accelerate population restoration.

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A comparison of two methods of leopard cat food content analysis

TENG Yang, GAI Lixin, LI Jian, FANG Xinmin, YANG Nan, BAO Weidong

2023, 43(1):  50-58.  DOI: 10.16829/j.slxb.150665

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As a top predator, the leopard cat (Prionailurus bengalensis) plays an important role in maintaining the structure of the food web and ecosystem stability. For the study of the diet composition of predators, a relatively simple method is the fecal sample contents analysis, while the DNA metabarcoding technology on fecal residues has the advantages of being more accurate and detailed, but it also has shortcomings. Therefore, exploring the complementary advantages of different methods will help to improve their application effectiveness. In this study, 71 fecal samples of leopard cats collected from four areas in Beijing were analyzed by using the DNA metabarcoding technique and fecal content analysis with the aims of understanding the food resources utilization of leopard cats and assessing the complementary results of these two approaches. The results showed that the DNA metabarcoding identified 36 prey species, belonging to 22 families and 10 orders. The small mammals were the main prey, among which the rats comprise the highest percentage and birds in second place in Baihuashan, Songshan, and Yunmengshan sampling areas. In Yunfengshan area, the highest percentage of prey was birds followed by rats and mice in second place. The fecal content analysis identified 9 types of prey, including insects and plants which were not detected by the DNA metabarcoding. Furthermore, this approach detected the prey numbers of three rats and two birds in scat samples, respectively, and the secondary food is plants and insects. Both methods showed that Niviventer confucianus, Apodemus draco, and A. agrarius were the most frequently preyed rodents. This study identified more prey species by DNA metabarcoding while the fecal content analysis revealed the numbers of the prey, indicating complementary results between these two methods. In addition, the diet composition characteristics of leopard cats provid baseline information for further detecting the inter-species coexistence among the sympatric predators.

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Effects of olfactory enrichment using logs used by baboons on behaviors of captive carnivores

CAO Yani, HUANG Xinrui, ZHANG Yuanyuan, ZHANG Yizhuo, HE Shaochun, ZHAO Jing, MA Jun, ZHANG Tao, ZHANG Chenglin, LIU Dingzhen

2023, 43(1):  59-68.  DOI: 10.16829/j.slxb.150651

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The monotonous environment is thought to be one of the causes of the stereotypic behavior in captive carnivores. It is a challenging work for zoo managers to explore and use a simple, economical and effective method to conduct enrichment to prevent those carnivores from displaying stereotypic behavior. Here, we conducted an olfactory enrichment study using logs formerly used in baboon playgrounds in small (9 species), medium (4 species) and large (7 species) carnivores at Beijing Zoo. We used the scan sampling and instantaneous recording method to observe those carnivores'behavior and compared the five main behaviors of 28 animals before and after enrichment during the non-feeding period. The results showed that the relative ratio of using old enrichment items in small and medium carnivore groups decreased significantly after the enrichment (small:P=0.026; medium:P=0.038), but no significant changes were detected in large carnivores. In addition, small carnivores showed less stereotypic pacing, resting, and watching behavior than those before the enrichment (stereotypic pacing:P=0.023; resting:P=0.023; watching:P=0.017). There were no significant behavioral changes in other behaviors of medium and large carnivores (both P>0.05). Moreover, the behavioral diversity index in small carnivores decreased significantly after enrichment by displaying more exploring behavior to the newly added logs (P=0.008). No similar change was found in medium and larger carnivores (both P>0.05). Our results suggest that using items containing body odors of other animals like baboons in the zoo as environmental enrichment materials is only effective for reducing stereotypic behavior in small carnivores, but not for medium and large carnivores. It is a low-cost, simple and effective way to exploit items used in other animals'enclosures to conduct environmental enrichment for small captive carnivores and should be recommended to other zoos and wildlife parks.

REVIEWS

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Advances and prospects of the gut microbiome in non-human primate

Qiuyan GUO, Xiao WEI, Meijing LU, Penglai FAN, Qihai ZHOU

2023, 43(1):  69-81.  DOI: 10.16829/j.slxb.150669

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The gut microbiome is the second set of animal genomes and interacts with hosts in development, nutrition metabolism, physiological function, and immunity. Non-human primates (NHPs) are close to humans in terms of ecological niche, social structure, geographical distribution and evolution. The research of NHPs gut microbiome not only contributes to understanding primate ecology, conservation, and evolution but has also important reference value for in-depth understanding of the role of the gut microbiome in human evolution. This paper summarizes the factors influencing the composition of the gut microbiome in NHPs, including host species and phylogeny, diet, habitat fragmentation, age/sex, captivity, and community life. We also explore the application of gut microbiome research in NHPs ecology, behavior, conservation, and adaptive evolution. Future studies of the gut microbiome of NHPs will offer new insight into primate ecology and evolution as well as human health. They will also provide a new theoretical basis and means for primate conservation.

METHOD AND TECHNOLOGY

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Giant panda head image segmentation based on dual model fusion

ZHOU Zhangyu, HOU Jiaping, LIU Peng, CHEN Peng, DUAN Chang

2023, 43(1):  82-88.  DOI: 10.16829/j.slxb.150635

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In the ex situ conservation and population management of giant pandas (Ailuropoda melanoleuca), timely and rapid individual identification and behavior monitoring play a crucial role in health supervision. The health status of captive giant pandas is usually observed by specialized breeders, which have high labor costs, low efficiency, and lack of timeliness. Therefore, efficient and cheap image-based identity recognition and behavior analysis has become a new development trend. Existing studies have proposed to realize it by detecting and analyzing facial images of giant pandas. However, this type of method still has the problem of insufficient detection accuracy, which makes it difficult to improve the recognition performance. We propose a dual model fusion method based on YOLOv3 and Mask R-CNN to achieve the segmentation and accurate detection of giant panda head images. It includes three parts:YOLOv3 completes head detection, Mask R-CNN completes panda contour segmentation, and then fuses the outputs of the two models. Experimental results show that the accuracy of head detection, giant panda and head contour segmentation are 82. 6%, 95. 2%, and 87. 1%, respectively. Our method has high detection and segmentation accuracy for the giant panda head images. It provides help for individual identification and gender classification of giant pandas and provides technical reference for behavior analysis.

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Diversity of birds and mammals in Laojunshan region, Wenshan National Nature Reserve based on infrared cameras

HAN Keguo, LI Kai, SUN Jing, RAO Jingqiu, ZHOU Jia, YANG Yun, CUI Liangwei, GUAN Zhenhua

2023, 43(1):  89-101.  DOI: 10.16829/j.slxb.150588

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Wildlife resources are a vital part of biodiversity and their composition and structure directly relate to the function of the ecosystem. Investigating the current situation of wildlife supports biodiversity conservation and management. To further comprehend the diversity of birds and mammals in Mt. Laojun, Wenshan National Nature Reserve, Yunnan Province, we deployed 73 camera monitoring sites from August 2019 to March 2020 to observe the activity rhythm of common species and their relationship with humans and livestock. After adjusting for lost, damaged, and invalid cameras, we detected a total of 62 species of birds and mammals at 59 camera sites, including 21 species of mammals in 17 genera, 11 families, and five orders, and 41 species of birds in 31 genera, 14 families, and five orders. This list included 12 National Level Ⅱ Key protected mammals, including the Assam macaque (Macaca assamensis), stumptailed macaque (M. arctoides), spotted linsang (Prionodon pardicolor), Lady Amherst's pheasant (Chrysolophus amherstiae), rusty-naped pitta (Pitta oatesi) and so on. Among these 12 species, four were distributed only in the core zone and two are endemic to China, namely Forrest's rock squirrel (Rupestes forresti) and red and white giant flying squirrel (Petaurista alborufus). Ultimately, we added new records for four species of mammals and 17 species of birds. Among birds, the species with the highest relative abundance index were the rufous-throated partridge (Arborophila rufogularis) and silver pheasant (Lophura nycthemera). Among mammals, the species with the highest relative abundance index were the red-hipped squirrel (Dremomys pyrrhomerus) and Forrest's rock squirrel. There were significant differences in activity rhythm between the rufous-throated partridge and silver pheasant, and between the red-hipped squirrel and Forrest's rock squirrel. There was also a significant differentiation between human daytime activity and the activity time of silver pheasant and the red-hipped squirrel. The results showed that the activity rhythm of terrestrial birds and animals was affected not only by the activities of species in the same region with similar niches, but also by human activities.

SCIENTIFIC NOTES

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Wild camel space use as determined by different home range estimators

Yongxiang ZHOU, Yadong XUE, Shaochuang LIU, Jianquan LIU, Duoliang ZHOU

2023, 43(1):  102-108.  DOI: 10.16829/j.slxb.150672

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Satellite tracking and positioning technology has been widely used to estimate species home ranges, habitat selection, and migration behavior, which can provide the scientific basis necessary for endangered species conservation and management. In this study, the home ranges of two wild camels (Camelus ferus) were determined using minimum convex polygons, Kernel density estimators, and dynamic Brownian Bridge Movement Models (dBBMM).The advantages, disadvantages, and applicable scenarios of these methods were discussed and key habitats and conservation priority areas of wild camels were identified. The dBBMM home range was the most accurate in relation to the distribution of the camels studied. The average home range (95% dBBMM) and the average core home range (50% dBBMM) were 300.11 km² and 7.02 km², respectively. The average monthly home range (95% dBBMM) of the two wild camels was 164.98 km² and 39.67 km², respectively, and the average monthly core home range (50% dBBMM) was 4.69 km² and 2.71 km², respectively. The northern and western regions of the nature reserve harbored key habitats for wild camels, and should be regarded as conservation priority areas. We propose the use of a multi-method estimation to comprehensively and holistically identify key habitats. The dBBMM home range calculations of wild camels at different life history stages can identify their stopover sites and corridors, which is helpful for the development of management measures and fine-scale conservation actions.

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Temporal niche relationship between snow leopard (Panthera uncia) and its sympatric large carnivores in Qilian Mountains, Gansu Province

ZHANG Changzhi, MA Teng, Wuliji, LIU Xiaomin

2023, 43(1):  109-115.  DOI: 10.16829/j.slxb.150632

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Large mammalian carnivores are at the top of the food chain and nutritional level, and they play an important role in maintaining the stability of ecosystem structure and function. Exploring the interspecific interaction and coexistence mechanism of large carnivores is of great significance to understanding how biotic communities assemble, species population dynamics, and endangered species conservation and management. In this study, we seleted the Yanchiwan National Nature Reserve in the west of Qilian Mountains, Gansu Province as our study area. We collected temporal data of snow leopards (Panthera uncia) and their sympatric large carnivores from a camera-trapping survey in the alpine ecosystem and conducted kernel density estimation and coefficient of overlap to explore temporal niche differentiation. We found that the daily activity patterns of snow leopards showed a sub-peak and a peak at 04:00-08:00 and 16:00-20:00, respectively, indicating that snow leopards tended to be crepuscular. The sub-peak and the highest peak of the daily activity patterns of brown bears (Ursus arctos) are from 03:00 to 05:00 and from 19:00 to 21:00 respectively, which are more nocturnal. Dhole (Cuon alpinus) has the highest peak and sub-peak from 06:00 to 10:00, which are concentrated in the daytime and mainly active in the morning, making it a typical diurnal animal. The daily activity patterns of lynx(Lynx lynx) and wolf (Canis lupus) were both bimodal. The two activity peaks of lynx are 01:00-03:00 and 18:00-20:00, which are more nocturnal, while the two activity peaks of wolves are about 09:00-11:00 and 18:00-19:00, which are more diurnal. The overlap of daily activity patterns of snow leopard and wolf (Δ1=0. 70), snow leopard and lynx (Δ1=0. 78), and snow leopard and brown bear (Δ1=0. 82) were higher, while snow leopard and dhole (Δ1=0. 39) showed low overlap of daily activity pattern. The results preliminarily revealed the temporal niche relationship between the snow leopard and its sympatric large carnivores and, provide basic information for a further in-depth understanding of the coexistence mechanism of large carnivores in the alpine ecosystem.

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Growth curve fitting and comparative analysis of hand-rearing cubs of African lion, Bengal tiger and leopard

OU Qianyun, ZHANG Xueli, CHEN Siming, LUO Shenghui, FANG Jing, ZHANG Peng, DONG Guixin

2023, 43(1):  116-121.  DOI: 10.16829/j.slxb.150574

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In order to understand the growth patterns of African lion (Panthera leo leo) cubs, Bengal tiger (Panthera tigris tigris) cubs, and leopard (Panthera pardus) cubs, we analyzed the body weight of 17 hand-rearing African lion cubs, 15 hand-rearing Bengal tiger cubs and 10 hand-rearing leopard cubs. We found that their growth curve fitted the Logistic, Gompertz and Von Bertalanffy models, respectively. We also compared the growth and development trend of different species and the sexual difference of the same species based on the growth curve with ideal fitting effect. The results show that the Logistic model may ideally fit the growth curve of lion and tiger cubs from birth to about 100-day old and leopard cubs from birth to about 200-day old. The growth curves of African lion and Bengal tiger are similar, but there are significant differences between the growth curves of the two and the leopard. The growth curves of female and male African lion cubs are similar, but there are significant differences between the growth curves of female and male Bengal tiger and leopard cubs. These results summarize the early growth and development of African lions, Bengal tigers, and leopards, suggesting that the time of male-female difference in feline body weight growth might be related to the survival strategies and rearing methods of the species. This study could provide an important theoretical and practical basis for the conservation of large cat populations.

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Rediscovery of Theobald's tomb bat (Taphozous theobaldi, Chiroptera, Emballonuridae) from Guangdong, China

LI Yannan, LIANG Xiaoling, XIE Huixian, DENG Wenpu, HE Minyi, YU Wenhua, WU Yi

2023, 43(1):  122-128.  DOI: 10.16829/j.slxb.150680

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A series of tomb bats were captured in a cave by using harp traps in Longmen County, Guangdong Province, China (23o35'18″N, 114o17'53″E, 91 m a. s. l.), between 2007 and 2020. The bats were similar in appearance but of different sizes. Six of them are morphologically and morphometrically similar to Taphozous theobaldi rather than Taphozous melanopogon. Both principal component analysis and discrimination analysis suggested the separation between T. theobaldi and T. melanopogon. T. theobaldi exhibits an elongated posterior orbital process and a well-developed pterygoid bone. Such identifications are also supported by the phylogenetic inferences using a segment of of Cyt b mitochondrial gene. Given that no traceable T. theobaldi specimens were reported since the first records in 1984, our finding represents the field rediscovery of this species after nearly 40 years.