Table of Content

    30 May 2019, Volume 39 Issue 3
    Recognition of female fertilization and social rank by male golden snub-nosed monkeys (Rhinopithecus roxellana)
    ZHAO Haitao, WANG Xiaowei, HOU Dafu, WANG Chengliang, REN Yi, FU Weiwei, LI Baoguo
    2019, 39(3):  227-233.  DOI: 10.16829/j.slxb.150228
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    Social animals possess important cognitive abilities that help them adapt to complex and variable environments, as well as comprehend their position and that of others within their social groups. Identifying which cognitive behavioral strategies are adopted to maximize reproductive benefits and gain access to resources is an important area of study in primatology. To date, however, research on the recognition of social rank and pregnancy status in golden snub-nosed monkeys (Rhinopithecus roxellana) remains poor. Here we investigated the hierarchical relationships and pregnancy cycles of females from six one-male units (OMUs) located within a provisioned group of golden snub-nosed monkeys from the Guanyinshan Nature Reserve in the Qinling Mountains of China. We used instantaneous scan and focal animal sampling to collect data on spatial position and reproductive behavior to clarify the mating period and analyze differences before and after fertilization. We confirmed significant differences in the rates of sexual solicitation success (t = 4.527, P = 0.001) and found that the rate before fertilization was significantly higher than that after fertilization. Results also demonstrated significant positive correlations between rank status and the rate of solicitation success (R = 0.527, P = 0.006) and time of fertilization (R = 0.556, P = 0.049), which were found to be significantly higher and earlier, respectively, in higher-ranked females than in lower-ranked females. This study revealed that males were able to recognize the pregnancy status and rank of females within their OMUs, which affected their own social and reproductive behavior.
    A new method for determining the age of blue sheep using horn geometric characteristics and computer vision techniques
    SU Mengyu, ZHANG Tongzuo, LIAN Xinming, SU Jianping, DU Yurong
    2019, 39(3):  234-241.  DOI: 10.16829/j.slxb.150223
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    Studies on the population ecology, behaviour and social structure of ungulates often require accurate measurements of the age of individuals. However, to date there is no simple noncontact method of determining the ages of individuals. The horns of ungulates are structurally complex, and grow and change shape as animals age. If 3D models of the horns of individuals of known ages are built, the ages of other individuals can be estimated from photographs of their horns by comparison with the reference models. This paper describes a new age-determining method for blue sheep (Pseudois nayaur) using horn geometric characteristics and computer vision techniques. The procedure consists of three stages: 1) creating 3D reference images based on the horns of individuals of known age (22 individuals, two horns per individual; age range 1.5 to 15.5 years); 2) creating new 3D images of the horns of target individuals, which are then rotated on a computer using an in-house R script to obtain images at stepwise intervals of 1°; and finally, 3) by calculating the similarity between the new and the reference horn images. A final image with the highest similarity to the reference images is generated, and used to determine the actual age of the target individual. Of the 30 photographs used to evaluate our new method the age of the target individual in every picture was correctly determined. Our new method has potential use for studies of all wild/feral sheep and probably also other ungulate species.
    Differences in microhabitat selection between Chinese white-bellied rats (Niviventer confucianus) and Korean field mice (Apodemus peninsulae) in different habitat types and seasons
    HUANG Guangchuan, SI Junjie, MENG Xin, CHEN Zhiwen, ZHANG Hongmao
    2019, 39(3):  242-251.  DOI: 10.16829/j.slxb.150248
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    Microhabitat selection differentiation is an important factor for the coexistence of sympatric animals. Chinese white-bellied rats (Niviventer confucianus CWR) and Korean field mice (Apodemus peninsulae KFM) are common rodent species that share similar habitats (e.g., shrub and forest), rhythms (nocturnal) and diets (e.g., plant seeds) in the Donglingshan area, western Beijing city, China. However, we know little about why they coexist with each other. Here, we studied microhabitat selection of CWR and KFM in different habitats and seasons from May to October in 2016 and 2017. We wanted to know if the two rodent species have different microhabitat preferences that contribute to coexistence. In shrub, in spring, CWR preferred in places with higher arbor density, higher herb coverage and relatively lower litter coverage, while KFM selected higher diameter at breast height (DBH) and litter coverage, but lower herb coverage microhabitats. Principal component analysis showed that surface cover was the key factor affecting microhabitat choices of the two species. In shrub, in autumn, CWR preferred to select microhabitats with more arbor species, higher shrub density and herb coverage microhabitats, while KFM preferred microhabitats with larger DBH, longer shrub distances, higher ratio of open field and litter coverage. Food abundance was the key factor in determining the microhabitat selection. In abandoned farmland, in spring, CWR selected microhabitats with higher shrub density and herb coverage, whereas KFM preferred to select higher canopy coverage, DBH and litter coverage, but lower herb coverage microhabitats. Surface cover was the key factor that affected the microhabitat choices. In abandoned farmland, in autumn, CWR preferred microhabitats with relatively low canopy coverage and litter coverage, while KFM’s selection was on the opposite. Food abundance was the main factor that determined their microhabitatselections. In secondary forests, in autumn, CWR preferred microhabitats with higher shrub density, shrub base diameter and herb coverage, while KFM liked microhabitats with higher DBH and litter coverage, but lower shrub density and herb coverage. Surface cover was the key factor that influenced the microhabitat selections. The case in spring in secondary forest was not analyzed due to small sample sizes. These results suggest that there are different microhabitat preferences between CWR and KFM along habitat types and seasons, therefore promoting their coexistence.
    Vocal plasticity of two sympatric hipposiderid bats in different space openness
    PENG Le, YE Jianping, ZHU Guangjian, LIU Zhixiao, ZHANG Libiao
    2019, 39(3):  252-257.  DOI: 10.16829/j.slxb.150235
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    Two sympatric hipposiderid bats, Hipposideros armiger and H. larvatus were studied to investigate the variation of echolocation calls in different space openness. The echolocation calls were recorded using UltraSound Detector when the bats were in the following three situations: hanging freely, flying in a large cage, and flying in a small cage. The pulse duration (PD), dominant frequency (DF), and inter-pulse interval (PI) were analyzed using BatSound Pro-Sound Analysis software. We used GLM ANOVA to analyze the call differences among different situations. H. larvatus emitted echolocation calls with the highest DF when hanging freely and with the lowest DF when flying in the large cage. The highest PD and PI of calls of both hipposiderid bats were found when they were hanging freely and the lowest values were found in the small cage. Our results indicated that the echolocation calls of bats would change according to the situations and habitats and confirmed the plasticity of echolocation calls in bats.
    Den characteristics and their ecological significance in Himalayan marmots (Marmota himalayana)
    ZHANG Long, GUO Cheng, XIAO Yanhong, XIANG Zuofu
    2019, 39(3):  258-265.  DOI: 10.16829/j.slxb.150218
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     Dens play an important role in the survival of cavernicolous animals. To explore the characteristics and ecological significance of Himalayan marmot (Marmota himalayana) dens, we surveyed the dens of 30 breeding pairs of Himalayan marmots at Duoma Village, Zoige County, Aba Prefecture, Sichuan Province from May to September 2017 and April to May 2018. Ninety dens that were extensively used (sleeping dens and breeding dens) and temporarily used (temporary dens) were selected, and seven physical characteristics of each den were measured to analyze the differences between those types of dens. We found that the average outer diameter of the den long axis is 59.3 ± 21.9 (16-100) cm, and its mean minor axis is 45.8 ± 20.5 (18-100) cm; the average inner diameter of the den is 24.4 ± 4.0 (16-39) cm, and the average inner vertical diameter is 19.7 ± 3.5 (15-39) cm; the average length is 127.3 ± 43.3 (60-240) cm from the ground to the deepest point of the first tunnel; the average angle of the tunnel is 45.7°± 9.5° (20°-72°); the average entrance orientation is 195.8° ± 96.2° (3°-356°). There are no significant differences in physical parameters of different den types except for the inner vertical diameter between sleeping dens and temporary dens that breeding pairs utilized. The physical parameters of the dens used by the Himalayan marmot indicate that they help to avoid natural enemies, resist bad weather conditions, facilitate water drainage, and maintain the stability of microclimate. The physical characteristics of most of the caves are basically the same by combining behavioral observations, illustrate that Himalayan marmot will change their dens in different years.
    Comparative analysis of fecal microbiota of captive musk deer in juvenile and adult
    ZHAO Guijun, FENG Xiaolan, ZHU Jibin, ZHENG Chengli, JIE Hang, ZENG Dejun, ZHANG Chenglu, QI Wenhua
    2019, 39(3):  266-275.  DOI: 10.16829/j.slxb.150255
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    The aim of this study was to analyze the gut microbiota differences of forest musk deer juveniles (n=10) and adults (n=10). To gain insights into this, total DNA was extracted from fresh fecal samples and the microbial composition was characterized by sequencing V3-V4 hypervariable regions of 16SrRNA gene using an Illumina MiSeq 300PE in pair end mode. Sequencing data were processed for quality control and microbial operational taxonomic units (OTUs) were assigned. To access gut bacterial enrichment and differences, alpha-diversity indices were calculated with respect to age. The abundance and diversity of microbes in the adult group were slightly higher than those in the juvenile group, but not statistically significantly so ( P > 0.05). The dominant gut microbiota mainly belonged to the phyla Firmicutes, Bacteroidetes and Proteobacteria in both groups. In particular, a significantly greater proportion of Proteobacteria and a lower proportion of the Firmicutes were found in the adult group. LEfSe analysis revealed 12 distinct bacterial classifications. Both adult and juvenile forest musk deer showed significant differences in the composition of Proteobacteria and Firmicutes. This study shows evidence that there are no signif-icant differences in the abundance and diversity of gut microbiota among adult and juvenile forest musk deer. Further, the composition of bacteria is remains the same, but the proportion of bacteria in the two groups was different which indirectly reflects the different necessity of nutrition ab-sorption at different ages.
    Influence of environmental factors on genetic diversity of Gazella subgotturosa in Xinjiang, China
    Zorigul Ismayil, Shamshinur Muhtar, Buweihailiqiemu Ababaikeri, Arzigul satar, Subinur Eli and Mahmut Halik
    2019, 39(3):  276-284.  DOI: 10.16829/j.slxb.150233
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    Environmental factors play an important role in the evolution and genetic variation of species. To clarify the relationship between genetic diversity and environmental factors of Gazella subgutturosa in Xinjiang, in this study the mitochondrial DNA cytochrome b gene (1140 bp) and control region (1100 bp) sequences of Gazella subgutturosa were analysed from 84 individuals in 11 populations from across the species’natural range within Xinjiang by using PCR and direct sequencing methods. The results showed that the Gazella subgutturosa population in Xinjiang seems to show high haplotype but low nucleotide diversity, these results indicated that the Gazella subgutturosa investigated in this study exhibited low levels of genetic diversity. The results revealed by the analysis of correlation between environmental factors and the genetic diversity of various groups showed that altitude, annual precipitation, annual temperature, population are the main environmental factors affecting the genetic diversity of Gazella subgutturosa in Xinjiang, among which altitude is the key environmental factor. Our results provide a theoretical basis for effective protection and management of Gazella subguttrosa in Xinjiang.
    Genetic diversity and phylogenetic relationships based on mtDNA control region sequences of Marmota himalayana
    MA Ying, LI Hailong, HE Jian, ZHAO Yanmei, YANG Hanqing, LU Liang, LIU Qiyong
    2019, 39(3):  285-294.  DOI: 10.16829/j.slxb.150229
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    The Himalayan marmot (Marmota himalayana) is an exceedingly common species widely-distributed across vast areas of the Qinghai-Tibet Plateau. In order to improve conservation and management strategies of this species, we must understand its genetic structure and genetic diversity at the population level. In this study, 258 Marmota himalayana individuals were collected from 13 geographic populations. The genetic diversity and genetic structures of these populations were analyzed according to the sequence variation of the mitochondrial D-loop sequence. All 258 samples were successfully sequenced for 887 bp of the mitochondrial D-loop sequence. We found 84 sites (22.49%) to be polymorphic and genetic diversity was high overall (mean haplotype diversity 0.968±0.003, mean nucleotide diversity 0.01725±0.01637). The results of AMOVA analysis showed obvious genetic differentiation (Fst=0.62067, P<0.001) and relatively low gene flow among different populations (Nm<1). A neighbor-joining phylogenetic tree produced two main branches; the first branch (A) included 18 haplotypes from the southwestern Qinghai-Tibet Plateau (including Tibet Andu, Qinghai Golmud, Qinghai Nangqian, and Yunnan Diqing), and the second branch (B) included the other 50 haplotypes from the northeastern Qinghai-Tibet Plateau. A similar topology was also found using network diagram methods. Populations of the Himalayan marmot on the Qinghai-Tibet Plateau are separable into two groups, with the Tanggula Mountains serving as a geographic barrier between them. Therefore, geographical isolation via this mountain range appears to be the primary factor enforcing genetic structure of Himalayan marmot populations.
    The characteristics of metabolism and thermoregulation of Microtus gregalis
    CUI Zhiqiang, LIU Xinyu, SONG Shiyi, YANG Ming
    2019, 39(3):  295-301.  DOI: 10.16829/j.slxb.150226
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    In order to study the metabolism and temperature characteristics of the small herbivorous mammal, Microtus gregalis, we measured changes of body weight, resting metabolic rate, heat conduction and other biological indices associated with changes in environmental temperature. The average body weight was (20.8 ± 0.8)g(n = 12), the basal metabolic rate was (1.85 ± 0.05) mLO2/(g・h), the thermal neutral zone was 27.5~35℃, the thermal conductance value was (0.19 ± 0.03) mLO2/(g・h・℃), the thermal adaptability A < 0 (adapt to cold environment), the adaptation pathway index I = 0.8 thermal conductance effect on temperature regulation) ). Microtus gregalis has a low metabolic rate, low thermal conductance and a wide thermal neutral zone, and maintains a low level of energy metabolism in a wide range of temperature changes. This is one of the main survival strategies for Microtus gregalis living in cold regions at higher latitudes during long-term evolution.
    A preliminary study on the maternal behavior of female giant pandas in Shanghai Wild Animal Park
    DING Qiaoqi, YU Jinhua, XIE Chunyu, XU Chunzhong, SUN Qiang, BI Jingzheng, CHU Qingpo, ZHOU Yingmin, WU Feng
    2019, 39(3):  302-310.  DOI: 10.16829/j.slxb.150245
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    In this study, we examine the daily time budgets and activity rhythms of two female giant pandas during their lactation period using continuous recording and focal animal sampling in the Shanghai Wild Animal Park from October 2017 to March 2018. We found that maternal behavior in these two giant pandas was the main activity during the early stage of the lactation period, which accounts for 90% of all behaviors. Furthermore, genetal licking movements and maternal behavior were decreased and other non-maternal behavior such as feeding, resting, moving, grooming showed an increasing tendency across their entire lactation period. We also noticed that the two pandas showed different parental care. The maternal instinct of Qianqian was stronger than that of Sixue, which one has a prolific experience in mother-rearing. Qian qian spent more time on protecting, licking, lactation and interacting of with its cubs than did Si xue at different stages of the lactation period. In conclusion, our study provides a theoretical and scientific basis for the artificial breeding and management of captive giant pandas.
    Social network analysis and its application in animal behavior#br#
    DENG Ke, LIU Wei, WANG Dehua
    2019, 39(3):  311-322.  DOI: 10.16829/j.slxb.150275
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    Social network analysis has been widely used in studies of animal behavior. Application of social network analysis to animal behavior can identify the key individual in a social group, uncover the formation mechanisms of social associations, improves our understanding of the origin of sociality, and identify the links between individual behavior and population-level dynamic patterns by quantifying specific attributes (e.g. centrality, centralization). Here, we first present a brief history of social network analysis, and a description of basic concepts. Then, we discuss different approaches for inferring social networks from observing data, and introduce some social attributes. Thirdly, we highlight the necessity and approach of constructing null models. Finally, we review previous applications to animal behavior, propose that future studies should focus on both the dynamics of physical contact (e.g. fighting, grooming) and nonphysical contact (e.g. vocal communication), and on mixed-species societies, so that it will further our understanding of the ecological function of social behavior and cooperation theory.
    The function analysis of allogrooming in captive Sichuan snub-nosed monkeys (Rhinopithecus roxellanae)
    ZHANG Yuansheng, JIANG Zhigang, BAO Weidong
    2019, 39(3):  323-332.  DOI: 10.16829/j.slxb.150214
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    Grooming behavior is one of the social behaviors commonly found among primates. Such behavior is often associated with particle removal, with the groomers manually brushing away, or sometimes devouring, loose particles . However, the function of allogrooming and the associated particulate matter still remain controversial. In this study, we used all occurrence sampling to record autogrooming and allogrooming behaviors in captive Sichuan snub-nosed monkey (Rhinopithecus roxellanae) in the Endangered Animal Breeding Center of the Beijing Wildlife Park from February to Match 2017. A total of 120 bouts of autogrooming and 259 bouts of allogrooming were recorded to test the hygienic functional hypothesis and the compensation hypothesis of allogrooming. The particulate matter on the hair and skin was checked for ectoparasite, flakes of skin or secretion of salt using microscopy. In addition, we manipulate salt and protein intake via offering the monkeys with drinking water of different concentrations of salts and fresh Populus leaves with high protein, in order to test the nutritional function of allogrooming and particle intake. Our results suggested that the grooming behaviors of the monkeys in general were consistent with the prediction of hygienic functional hypothesis, but in adult males, but not in adult females, were broadly in line with the prediction of compensation hypothesis. No association was noted between grooming and removal of parasites, and neither the functions of obtaining protein, or sodium chloride were confirmed. In conclusion, grooming behavior of captive Sichuan snub-nosed monkeys is more likely to be a semi-ritualized social behavior.
    Preliminary survey of mammal and bird biodiversity using camera traps in the Yading National Nature Reserve of Sichuan Province, China
    HU Xixi, LI Jiaqi, LUO Xu, Zewengtaxu, CHEN Xing, ZHANG Lushui, GUAN Tianpei
    2019, 39(3):  333-343.  DOI: 10.16829/j.slxb.150234
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    To survey the diversity, abundance, and distribution of mammals and birds in the Yading National Nature Reserve we deployed 64 camera traps from May to November 2017. Across 8,394 trapping days, we recorded 56 species belonging to 9 orders and 25 families. Among the recorded species, five were Class Ⅰ and thirteen were Class Ⅱ national protected wildlife, and three were Endangered, five were Vulnerable, and four were Near Threatened on the IUCN Red List. Tufted deer (Elaphodus cephalophus), Perny's long-nosed squirrel (Dremomys pernyi) and macaque (Macaca mulatta) were the three most abundant mammal species according to the relative abundance index. Blood pheasant (Ithaginis cruentus), giant laughingthrush (Garrulax maximus) and buff-throated partridge (Tetraophasis obscurus) were the three most abundant avian species. In addition to providing a preliminary evaluation of mammal and bird species in the Yading Nature Reserve, we also assessed the level of human disturbance. This is the first study to report direct and quantitative data on species occurrences in this reserve. We provide data and guidance to inform further research, wildlife conservation management, and long-term monitoring programs within the reserve. Ultimately, these baseline data are critical for evaluating the long-term population dynamics and developing effective conservation measures of the local wildlife.
    Using auto-trigger camera to observe mating behavior of Hog-badger (Arctonyx collaris)
    GUO Hongxing, CHENG Lin, CHENG Songlin, YUAN Rongbin, MAO Yixian
    2019, 39(3):  344-346.  DOI: 10.16829/j.slxb.150209
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    Mating behavior of the Hog-badger (Arctonyx collaris) was recorded on 463 videos (totally 8053 s) taken with auto-trigger cameras between March 13 and May 13, 2017 in Jiangxi Wuyishan. Males followed and guarded the females for several hours before mating. One mounting behavior, and three mating behaviors were observed from 01:55 to 08:49 on April 18. The durations of mating behaviors lasted for 731s, 1690s and 1494s, respectively. Based on these observations, we found: 1) mating behavior was controlled by the female, including obvious sexual solicitations; 2) females can mate more than one time within one estrous cycle; 3) quickly and repeatedly pumping and inserting behavior was observed in male during mating.