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30 September 2020, Volume 40 Issue 5

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The effect of coccidian infection on immune function of root voles (Microtus oeconomus) ：a field experiment

SHANG Guozhen, WU Xueqin, ZHU Yahui, CAO Yifan, WU Yan, BIAN Jianghui

2020, 40(5):  413-423.  DOI: 10.16829/j.slxb.150398

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The immune function of animals is an important factor to affect the fitness of animal. In this study, we measured phytohemagglutinin (PHA) response, anti-keyhole limpet hemocyanin immunoglobulin G (anti-KLH IgG) level and hematological parameters of root voles (Microtus oeconomus) by controlling infection of coccidioides in the enclosure to study the effect of coccidian infection on immune function. Our results show that coccidian infection treatment significantly increased the prevalence and intensity of coccidia during the experiment, and significantly reduced the PHA response, serum anti - KLH IgG levels, white leukocyte counts, the percentage of lymphocytes, and plasma protein concentration in root vole. And infection treatment significantly increased the percentage of basophils, the significant difference between both treatments in percentage of eosinophils, neutrophils and monocytes were not found. These results indicate that coccidian infection has negative effects on the cell mediated immune response and humoral immune response of root voles.


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Trophic niche of Brandt’s voles (Lasiopodomys brandtii) and their interspecific relationships with other common rodents in a typical steppe, Inner Mongolia

YUE Chuang, GUO Qianwei, ZHANG Zhuoran, LI Xin, MAN Duhu, YUAN Shuai, FU Heping, WU Xiaodong, JIN Guo, LIU Jianwen, LI Yongshan

2020, 40(5):  424-434.  DOI: 10.16829/j.slxb.150387

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By studying the trophic niche of rodents, we can not only understand the nutrient layer occupied by rodents in the ecosystem, but also reveal their main food sources and their relationships with changes observed in rodents at different growth and development periods. In this study, 81 rodent specimens of 4 species were captured using the snap-trapping method in typical grasslands of Inner Mongolia in July 2018. The trophic niche of Brandt’s voles (Lasiopodomys brandtii) and their interspecific relationship with other three common rodents, i.e., Spermophilus dauricus, Phodopus sungorus and Allactaga sibirica, were analyzed using ¹³C and ¹⁵N stability isotope techniques. We found a marked age-specific trophic niche in the width of bone tissue in Brandt’s voles, i.e., the Ⅲ age group had the widest with 0.802 ‰² Bayesian standard ellipse area,  followed by the Ⅱ age group with 0.699 ‰² ellipse area, and the lowest in the Ⅳ age group with 0.666 ‰².  The trophic niche overlap commonality area among the three age groups was 0.064 ‰², and common food sources accounted for less than 10% of all food sources. Moreover, we did not find that Brandt's voles competed for food sources with the other three rodents in either the short-term or long-term diet. However, compared with the other three rodent species, the niche width of Brandt's voles was narrower and its food selectivity was stronger. These findings suggest that if food source composition changed and was no longer suitable for Brandt's voles in their habitat, the vole might face food shortage and emigration would be a direct and favorable strategy for the development of the voles’ population.

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Morphological features and regulation of seasonal spermatogenesis in plateau zokor (Eospalax baileyi)

AN Xiaoyu, WAND Yujun, LI Yongchang, JIA Gongxue, YANG Qien

2020, 40(5):  435-445.  DOI: 10.16829/j.slxb.150420

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Seasonal reproduction is a life history adaptation that helps animals survive under the changes of their environments. Seasonal reproduction is tightly regulated by the hypothalamus-pituitary-gonad (HPG) axis. Plateau zokor (Eospalax baileyi) is an underground rodent native to the Qinghai-Tibet plateau and they breed only in April to July. How gametogenesis and reproductive activities are regulated in underground mammals remains largely unclear. In the present study, we showed that spermatogenesis in adult male plateau zokor was seasonally regulated. Seminiferous tubules of plateau zokor contained well-developed germ cells including elongated sperm during breeding season (April to June). Based on the cell association and morphological features, the seminiferous epithelium can be divided into 10 stages. During non-breeding season, seminiferous tubules only contained spermatogonia and Sertoli cells, indicating spermatogenesis had been arrested. Levels of gonadotropin-releasing hormone, luteinizing hormone and testosterone were significantly increased in breeding season with notable reduction of melatonin (P < 0.05), while follicle-stimulating hormone level did not show a significant change. Further analysis revealed that biogenesis of retinoic acid, responsible for spermatogonial differentiation, was changed dramatically. As expected, supplementation of retinoic acid induced resumption of spermatogenesis in reproductively dormant animals. Together, these data demonstrated morphological features and key regulatory factors of seasonal spermatogenesis in plateau zokor. This study can provide a reference for understanding similar mechanism existed in other underground rodents.


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Behavior coding and ethogram of the free-ranging giant pandas (Ailuropoda melanoleuca)

HOU Jin, YAN Linlu, LI Liang, LI Yujie, LIAO Yushan, ZHANG Jindong

2020, 40(5):  446-457.  DOI: 10.16829/j.slxb.150392

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Ethograms are the foundation of animal behavior studies. The giant panda is a flagship species for biodiversity protection, and its behavioral ecology is of widespread concern. However, due to their limited population size and avoidance of people, it is difficult to observe giant pandas in the wild. As a result, basic behavioral research, such as the specification of ethograms, has been mainly done by observing captive giant pandas. In order to promote further development of giant panda behavioral research, we constructed an ethogram of giant panda (Ailuropoda melanoleuca) behavior using the PAE (Posture, Act and Environment) coding system based on infrared camera trap data collected in Wolong Nature Reserve during January 2015 to June 2016 and August 2018 to April 2019. In total, we identified and recorded 12 types of postures, 52 acts and 56 behaviors. This study not only recorded the major behaviors of giant pandas, but also discovered unrecorded behaviors of captive pandas in any past research, such as using plant stems to clear snow from the body. In general, our results enriched knowledge of the impact of environmental factors on giant panda behavior. This study provides basic information for behavioral ecology of giant pandas.


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Genetic diversity and structure of the Alashan red deer (Cervus elaphus alashanicus) in Helan Mountains, China

GAO Hui, QIAO Fujie, TENG Liwei, LI Junle, YU Mengqi, LIU Zhensheng

2020, 40(5):  458-466.  DOI: 10.16829/j.slxb.150341

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Alashan red deer (Cervus elaphus alashanicus) is only found in Helan Mountainous areas. It is an isolated population, and has the narrowest distribution range among the eight red deer subspecies in China. Up to now little is known about its genetics. To understand its genetic diversity and variation, and to provide scientific reference for amending its conservation strategies, partial sequences of mitochondrial control region (991 bp), taken from fresh feces samples of 93 wild individuals from Helan Mountains, were amplified and analyzed. The results indicate that, based on 68 polymorphic sites and defined 16 haplotypes, genetic diversity for this species is low; its mean haplotype diversity and nucleotide diversity are only 0.405 and 0.00232, respectively. The analysis of Mismatch distributions and neutral tests demonstrates that the Alashan red deer has experienced a population expansion, and further Bayesin skyline plot (BSP) implies that such an expansion may have occurred during the Last Glacial Maximum (0.028-0.010Ma). The FST test shows that genetic variation of the deer is prominent. The phylogenetic tree constructed with Bayesian method and haplotype network indicates that there is no obvious phylogeographic separation between the two geographic groups. The final conclusion of this study indicates that genetic diversity of the Alashan red deer studied is quite low. Thus, more attentions to increasing its genetic exchanges with  other geographic groups or subspecies is critically required in order to maintain its prosperous prospect.

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Parental testing system for population genetic management of red panda based on microsatellite markers

CHEN Ling, SHEN Fujun, WU Lixia, ZHUO Guifu, HOU Rong, ZHANG Liang

2020, 40(5):  467-474.  DOI: 10.16829/j.slxb.150378

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When the captive red panda population was established in China, individual identity was unclear, breeding and paternity records were incomplete or poorly kept and animal husbandry practices were not standardized. Because of these issues, problems like pedigree errors occurred frequently, which led to inbreeding risks. As the captive population of red panda grows, an accurate pedigree is required especially for the annual breeding plans. To address this issue, an accurate and standardized parentage test is needed. For this study，26 red panda microsatellite loci which were polymorphic and stable were discovered and used for paternity testing. The testing has been applied to several captive populations of red pandas, correcting the previous mistakes in pedigree. Moreover, the combined exclusion probability of these loci could reach 0.9999. Under the condition of one known/unknown parent, the specificity met the international human parental standard (0.9973) when eight or eleven microsatellite loci were applied. Finally, it was found that five loci could be used for the individual identification of red pandas. Thus, the testing can sufficiently improve the inbreeding problem of the captive red panda population. In summary, the application of the paternity testing system could help establish the correct pedigree, implement the scientific breeding plan, and avoid inbreeding. These factors should be an important improvement in the ex-situ conservation of red pandas.


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Transcriptomics analysis of lungs in yaks breeding at different altitudes

FU Fang, GUAN Jiuqiang, QU Xiulong, WANG Li, LUO Xiaolin, AN Tianwu, ZHANG Xiangfei

2020, 40(5):  475-484.  DOI: 10.16829/j.slxb.150414

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This study was aimed to explore the characteristics and regularity of gene expression of yaks adapting to high-altitude hypoxic environment. Transcriptome sequencing was performed in 2.5-3-year-old healthy male Maiwa yaks bred at high and low altitudes for 4 months. The average altitudes were 3 560 m and 478 m, respectively. Lungs of yaks were sequenced by RNA-Seq technology using Illumina II High-throughput Sequencing Platform (HiSeqTM 2500/4000). Then, the expressions of differentially expressed genes in lungs of yaks were verified by qRT-PCR. The results indicated that there were approximately 576, 610 million Clean Reads in lung transcriptome of yaks bred in high and low altitudes, respectively. The numbers of reads mapped to the reference genome accounted for more than 91.74% and 91.28% percentages, respectively. And 2 047 new transcripts were discovered in lung RNA-Seq. There were 199 differentially expressed genes (DEGs) between the two test groups, including 89 up-regulated DEGs and 110 down-regulated DEGs. The differentially expressed genes were enriched in 297 GO terms and 146 KEGG pathways, which contained 62 GO terms and 35 KEGG pathways related to hypoxic adaptation. The cell adhesion, protein complex and calcium ion binding were the largest proportions of biological processes, cellular component and molecular function in hypoxia-related GO terms. Meanwhile, TNF signaling pathway were the largest proportion of KEGG pathways related to hypoxia, followed by HIF-1 signaling pathway. In addition, qRT-PCR results showed that the expressions of HLA-DOA, HLA-DRA, C2 and MASP1 were consistent with those of RNA-Seq. This study will benefit for a global and in-depth understanding of gene expression of yak lung response to high altitude hypoxia.

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The musk secretion rhythm and the influencing factors in captive forest musk deer

WANG Jing, BAI Ruidan, CAI Yonghua, LI Yong, CHENG Jianguo, FU Wenlong, ZHOU Mi, SHENG Yan, MENG Xiuxiang

2020, 40(5):  485-492.  DOI: 10.16829/j.slxb.150374

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From May to August of 2016 to 2017, behavioral and physiological monitoring was conducted on the musk secretion of captive forest musk deer (Moschus Berezovskii) in Maerkang Musk deer farm of western Sichuan, the temporal pattern of musk secretion and its relationships with body weight and age were analyzed by recording the time of prime secretion, the vigorous secretion start, the vigorous secretion finish, the secretion end and the duration of each phase. The results show that, the average date of prime secretion was June 16th [(167.06±7.75)d, n=141], and entered the vigorous secretion in June 17th [(168.52±7.67)d, n=141] on average, then secretion weaken in June 21st [(172.17±7.26)d, n=138], and ended in June 25th [(176.27±8.11)d, n=131]. There were significant negative correlations between body weight and date of prime secretion, finish of vigorous secretion and end musk secretion (r _PS = -0.234，P _PS = 0.028；r _VSF = -0.215，P _VSF = 0.047；r _SE = -0.229，P_SE = 0.043), namely the heavier body weight, the earlier secretion. Secretion periods were significant different (F _17,113 = 3.482, P=0.003) with age groups, among which that at 2 years old was the longest [(13.07±2.08)d, n = 20], and significantly higher than that at 3 years old [(9.38±0.76)d, n=12, P = 0.042] and 4 years old[ (7.80±1.60)d, n=5, P = 0.013]. The average musk production was  (11.85±0.96)g (n=114), and showing an increasing trend with the extension of the secretion period, but was not significant (P = 0.854). Based on the correlations between the musk secretion rhythm and musk production, and the factors such as age and body weight, we can distinguish and predict the capacity and production of musk secretion among captive individuals, as the basis of productivity optimization of captive forest musk deer, it can provide reference for breeding high quality strains of forest musk deer.

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Verification of the vertical distribution pattern of species diversity of non-flying small mammal in the Lebu Valley of Eastern Himalayas, China#br#

WANG Zuobo, HU Yiming, ZHOU Zhixin, LIANG Jianchao, HUANG Zhiwen, ZHENG Shuyang, ZHOU Jiang, HU Huijian

2020, 40(5):  493-502.  DOI: 10.16829/j.slxb.150397

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 Determining the vertical distribution of species diversity along altitudinal gradients is of critical importance in biodiversity and conservation research. Across a broad set of taxa, the hump-shaped pattern of species diversity is the most common one, and the vertical distribution of the small mammal community in the Middle Himalayas best fits a hump-shaped pattern. Since the Eastern Himalayas and Middle Himalays share many geographical and climatological conditions, we hypothesize that the vertical pattern of small mammal diversity in the East Himalayas also fit a mid-peak or humped pattern. Therefore, we conducted field surveys of two mammalian orders, Non-flying Small Mammal at an elevation of 2 300 – 5 000m, in the Lebu Valley of the East Himalayas. 45 sampling sites were set up, with each contained 9 segments distributing along an elevational gradient every 300 m. In total, our 16 200 traps  captured 372 specimens, which belonged to 10 species, 5 families and 3 mammalian orders. Our results indicated that the species richness of Non-flying Small Mammal in the Lebu valley reached a peak at an elevation of 2 600 – 2 900 m, and then decreased at higher elevations, displaying a mid-peak pattern. Based on this study, we hypothesize that the vertical distribution and species diversity of small mammals inhabiting valleys in the southern part of the Himalayas will exhibit a similar pattern in response to similar geographical and climatological conditions. Results suggest that geography and climate are key factors in understanding the vertical distribution of species diversity.

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Comparison of birds’ and mammals’ diversities using camera-trapping survey in Guizhou Chishui Alsophila National Nature Reserve and its surrounding areas

LIU Bangyou, ZHANG Tingyue, LIANG Sheng, BAI Xiaojie, LIU Wei

2020, 40(5):  503-519.  DOI: 10.16829/j.slxb.150425

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The biological inventory within established protected areas is fundamental for biodiversity research and monitoring at both regional and national levels.  Infrared camera- trapping technique has been widely used recently for species inventories and related assessment of terrestrial vertebrates in protected areas across the world.  We conducted a camera-trapping survey to investigate the inventories of mammal and bird within Guizhou Chishui Alsophila Reserve (GCANNR) and its surrounding areas.  We totally deployed 60 camera traps in three sample plots (two in the Reserve and one in outside the Reserve) using continuous1 km×1 km grids.  With a total of 21 234 independent images by an extensive survey effort of 55 029 camera-days during Dec. 2016 to Dec. 2019, we identified that 21 wild mammal species belonging to 4 orders,10 families and 17 genus, and 34 wild bird species belonging to 6 orders,13 families and 29 genus.  Eight species were recorded firstly in GCANNR.  There were 4 mammals and 8 birds categorized as class II nationally protected wildlife, or 8 and 13 species were listed as VU and NT species, according to the Red list of China's Vertebrates.  Based on relative abundance index (RAI), the top three abundant mammal species were Elaphodus cephalophus, Muntiacus reevesi, Macaca thibetana, and the three most abundant bird species were Myophonus caeruleus, Bambusicola thoracicus, Garrulax canorus.  Additionally, we found that the species richness and species diversity Shannon-Wiener index (H) of animals (especially mammals) in GCANNR are greater than those of surrounding areas of GCANNR, and these indexes of birds and mammals in the core zone and buffer zone of the Reserve are higher than those in the outer buffer zone. We also found that the species richness of mammals were higher in 700 – 1 000 m elevation range, while the diversity index (H) of birds and mamamls were highest in > 1 000 m elevation ranges.   Our results provided important baseline information of bird and mammal resources for further biodiversity research, as well as for optimizing management strategies and realizing long-term survey and effective protection in GCANNR.

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The diversity and vertical distribution of summer large and medium-sized mammals and birds in Chadan Township, Sanjiangyuan，Qinghai Province

LIU Zhou, ZHOU Hu, WU Guosheng, CHEN Kangmin, ZHANG Shusheng, CAI Ping, XU Aichun

2020, 40(5):  520-531.  DOI: 10.16829/j.slxb.150395

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The diversity of large and medium-sized mammals and birds in the monitoring area of Chadan in the Sanjiangyuan region was surveyed in July 30 to August 2018.The survey recorded 9 mammals species and including 4 national key protected mammals.These 9 species belonged to 5 orders, 5 families and 8 genera. Equus kiang and Procapra picticaudata are dominant species in the region, with a proportion of 45.5% and 21.6% in mammals. A total of 52 birds species were observed in Chadan.These 52 species belonged to 11 orders, 26 families and 44 genera, including 11 species under national protected. Among birds, Passerine is the dominant species, accounting for 81.0% of the total number of individual birds. The study shows that the number of mammals’ and birds’ species in in different altitude has a significant difference(mammals:P＜0.001;birds: P＜0.001). The vertical distribution of mammals in monitoring area decreased with the increase of altitude, and it’s biodiversity is the highest to altitude from 4800m to 4849 m. The birds’ vertical distribution pattern conforms to the offset to the left ‘mid-domain effect’. The Shannon-Wiener index increases first and then decreases with increasing altitude. This study has mastered the composition of summer birds and mammals in the Chadan area of Sanjiangyuan region, enriched the data of birds and mammals in the Sanjiangyuan region and the Tanggula Mountains, and it provides a case study for the spatial distribution pattern of species at small scales.

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Species identification and morphological measurements of a pregnant minke whale(Balaenoptera acutorostrata acutorostrata)

WANG Zhen, TIAN Jiashen, LEI Liyuan, DU Jing, LIU Weidong, HAN Jiabo, LU Zhichuang

2020, 40(5):  532-538.  DOI: 10.16829/j.slxb.150376

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A dead whale was found by local fishermen on the coast of Zhangzi Island, Changhai County, Dalian, Liaoning on April 16, 2019. According to the following information (1) discovery location, (2) prominent ridges on head, 256 pairs of white baleen in the mouth and the white transverse band on the fin limb, (3) characteristics of Cytochrome b (Cyt b) gene sequence, the whale was identified as the North Pacific minke whale (Balaenoptera acutorostrata acutorostrata). It was found that the whale was in pregnancy. The results showed that the body length of minke whale was 640.0 cm and the body weight was 3350.0 kg. The fetus was a 7-8 months old male, with its body length 123.0 cm and body weight 26.3 kg. The body length of dead minke whale was less than the minimum value of the previous recorded pregnant minke whale. Our study is to record the morphological characteristics of the dead minke whale samples and enrich the basic biological data of large cetaceans in China.