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30 July 2021, Volume 41 Issue 4

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ORIGINAL PAPERS

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Diversity and functional characteristics of intestinal microflora of free-living wild boars in the Miaoling Mountain area in Guizhou Province, China

YANG Xiongwei, PENG Caichun, GUO Qunyi, RAN Jingcheng, WANG Yeying, ZHANG Mingming, HU Canshi, LI Shize, SU Haijun

2021, 41(4):  365-376.  DOI: 10.16829/j.slxb.150515

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Wild boars(Sus scrofa), which are widely distributed in southern China, are one of the few large-hoofed species that populations are proliferating.In recent years, an increasing number of studies have been conducted on the intestinal microflora of wild animals, but none have investigated the intestinal microflora of the wild populations of S.scrofa.In this study, total DNA from the gastrointestinal tract(stomach, ileum, colon, and rectum) of four samples of free-living wild boars from the Miaoling Mountain area of Guizhou Province was extracted, and the V3-V4 region of the 16S rRNA gene was amplified using universal primer PCR.The amplification products were sequenced on an Illumina MiSeq platform to assess the community structure, diversity, and flora function of intestinal bacteria of wild boars.A total of 1 268 577 valid sequences remained after the results were filtered for quality, and the low-quality reads were discarded.After drawing out the minimum sample sequence number, 1 019 OTUs were identified at the 97% similarity level.All samples were categorized into 19 phyla and 292 genera.At the level of phylum classification, the key floras in the intestinal tract were Firmicutes, Bacteroidetes, Proteobacteria, and Actinobacteria and there were 15 dominant genera, including Prevotella, Lactobacillus, Escherichia-Shigella, and Bifidobacterium.Rarefaction curves indicated that the sequencing depth had basically covered all bacteria in the sample.Among alpha diversity indices, the Chao1 and Shannon indices of the colon and rectum were significantly higher than those of the stomach and ileum(P<0.05).This fully confirmed that the colon and rectum had a bacterial community structure relatively similar and greater floral richness and diversity to that of the stomach and ileum.The results of principal coordinates analysis(PCoA) and analysis of similarity(Anosim) showed a readily visible difference in distinct parts of the gastrointestinal tracts of wild boars.LEfSe analysis indicated that there were 22 bacterial genera with significant differences in distinct intestinal segments of boars, most of which were attributed to Firmicutes.In addition, PICRUSt showed that different intestinal segments also had unique metabolic functions and pathways.This study preliminarily revealed the characteristics of the intestinal flora of wild boars from Guizhou Province.We found that the intestinal flora of wild boars had a relatively complex structure and that there were significant differences between distinct intestinal segments.

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The relative role of climate, land-use and spatial structure on spatial distribution pattern of species richness of large and medium mammals sympatric with giant pandas

LI Dan, WANG Xiaojun, ZHAO Xuzhe, ZHOU Hong, HONG Mingsheng, WEI Wei, HAN Han, TANG Junfeng, ZHANG Zejun

2021, 41(4):  377-387.  DOI: 10.16829/j.slxb.150512

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Climate and land-use are recognized as the two main driving factors of biodiversity distribution patterns.However, most studies on the effects of climate and land-use have primarily focused on the species level, while their role on community diversity remains poorly understood.In this paper, combining species richness, climate and, land-use data as well as latitude and longitude data, we investigated the relative importance of climate, land-use, and spatial structure vari-ables on the species richness of large and medium mammals sympatric with giant pandas by using model comparison and variation partitioning.Our results show that(1) the number of genera and species of large and medium mammals differs in the five mountains of Sichuan Province.Minshan mountain has the highest number of genera(25) and species(28), while Liangshan mountain has the lowest number of genera(19) and species(20).The top five dominant species in the five mountains are the giant panda, takin, wild boar, Chinese goral, and Chinese serow.(2) We observed high spatial variation in species richness of large and medium mammals sympatric with giant pandas.The number of species in all 10×10 km grids ranged from 1 to 14, with an average of 6.199±3.475.(3) The full model(including all the climatic, land-use, and spatial structure variables, CLS) performed significantly better than all other six models, and the models including land-use covariates performed significantly better than those not including land-use covariates.(4) Climatic, land-use, and spatial structure variables together explained 43.0% of the variation in species richness, among which land-use variables accounted for the largest proportion, explaining 23.0% of the variation in species richness.Climatic and spatial variables explained only 6.3% and 9.3% of the variation in species richness, respectively.These findings indicated that the species richness of large and medium mammals sympatric with giant pandas was predominantly determined by land-use factors.Therefore, good forest stewardship to reduce anthropogenic threats and increase forest cover is the key to achieve comprehensive protection of large and medium mammals sympatric with giant pandas.

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The influence of group size and foraging environment on the daily path length of a critically endangered primate Nomascus nasutus

LI Xingkang, ZHONG Xukai, WEI Shaogan, CUI Liangwei, FAN Pengfei, GUAN Zhenhua, MA Changyong

2021, 41(4):  388-397.  DOI: 10.16829/j.slxb.150495

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Daily path length can reflect animals'foraging efforts and offer insights into their foraging strategy, which is essential for implementing effective conservation plans for endangered species.The Cao Vit gibbon(Nomascus nasutus) is a small, critically endangered arboreal ape living in polygynous social groups(average group size 6.3).Research on its daily path length related to foraging habits is still limited.During two distinct periods, one from April 2008 to December 2009 and the other from October 2016 to August 2017, we followed two gibbon groups(G1 and G4) in Bangliang National Nature Reserve, Guangxi Province, China.We collected feeding behavioral and dietary data using instantaneous scan sampling at 5 min intervals on gibbon groups and mapped the gibbon groups' positions every 30 minutes.A total of 157 full-day observations were used to analyze the dietary changes and calculate the gibbons' daily path lengths.The gibbons changed their diet significantly in the two observation periods, and we found that they traveled on average 1 373 m per day(range:354-2 837 m), similarly to monogamous gibbon species living in low-latitude areas with smaller group sizes(3.8 in average).These findings indicate that, despite Cao Vit gibbons' relatively bigger group sizes, their daily foraging effort is not higher than other species, conflicting with the ecological constraints model.The availability of larger food patches, lower inter-species competition, and low group density might be the main reason for allowing Cao Vit gibbons to survive in bigger groups without increasing foraging efforts.Furthermore, the gibbons fed more fruits and traveled longer distances when anthropogenic disturbances were lower, while they significantly decreased their movements during the fruit-scarce dry season.This points to a potential energy conservation strategy employed by Cao Vit gibbons as an adaptation to cope with limited high-quality food.The large amount of data provided by the present work significantly amplified our understanding of Cao Vit gibbons travel patterns related to their foraging behavior when facing food scarcity, and improved the scientific knowledge that fosters the conservation of critically endangered wildlife.

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Effects of seasonality and social ranks on fecal cortisol levels in male Tibetan macaques(Macaca thibetana)

WU Mingyang, CHEN Shiwang, SUN Binghua, WANG Xi, XIA Dongpo, LI Jinhua

2021, 41(4):  398-405.  DOI: 10.16829/j.slxb.150524

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Many primate species are social, a consequence of long-term evolutionary processes.Despite natural selection favoring sociality, intragroup competition can generate stress for individuals.Cortisol level is one physiological indicator of an individual's stress.Seasonally-breading Tibetan macaques(Macaca thibetana) are ideal candidates for the investigation of the potential relationships between social stressors, cortisol levels, and dominance rank.We collected 325 fresh feces from 13 males in Huangshan, Anhui Province, China, and quantified cortisol levels from the fecal samples.We analyzed individual variation in fecal cortisol levels to test the effects of season(i.e., the mating and non-mating seasons) and position in the dominance hierarchy.Our results show that the macaque subjects had higher fecal cortisol levels in the mating season.There was no significant difference in the cortisol levels of high-ranked, middle-ranked, and low-ranked males in the non-mating season, but in the mating season, cortisol levels of middle-ranked males were significantly higher than those of both high- and low-ranked males.As we have known, this is the first study to investigate the cortisol levels in wild Tibetan macaques, and analyze the effects of seasonality and social ranks on cortisol.

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Comparative on foraging behavior between white-headed langurs(Trachypithecus leucocephalus) and François'langurs(T.francoisi) in Guangxi, China

LIAO Rong, LU Shiyi, HUANG Zhonghao, LI Youbang

2021, 41(4):  406-415.  DOI: 10.16829/j.slxb.150470

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Comparing the foraging behavior of sibling species can reveal similarity in behavioral plasticity and adaptability.White-headed langur(Trachypithecus leucocephalus) and François'langurs(T.francoisi) are sibling species sharing similar body size, social structure and habitat environment.They are neighboring primates distributed in the karst seasonal rain forest of the white-headed Langur National Nature Reserve in Chongzuo, Guangxi.In order to explore whether the two langurs have similar foraging strategies in response to karst habitat, we studied their foraging behavior from January to December 2012 using instantaneous scanning sampling.The results revealed that the feeding habits of the white-headed langur and the François'langur did not vary across day time.Leaves were the main food items for these two species, which accounted for 77.0%±4.4% of annual diet for the white-headed langurs and 68.9%±8.3% of annual diet for the François'langurs.There was no significant change in the eating time of leaves for both langurs(white-headed langur:χ²=6.602, df=11, P=0.830;François'langurs:χ²=11.393, df=11, P=0.411).Foraging behaviors of both species occurred frequently after leaving the sleeping cave in the early morning and before entering the sleeping cave in the later afternoon.Specifically, at 09:00-10:59 and 16:00-17:59, white-headed langur spent 41.7% and 46.3% of day time on feeding, whereas François'langurs devoted 31.3% and 38.0% of day time to feeding at 09:00-10:59 and 16:00-17:59, respectively.In addition, there was no significant difference in foraging time between the two langurs.Our result suggests that the white-headed langur and François'langurs share similar foraging strategy in the limestone forest, implying that the similar conservation efforts based on feeding ecology should be considered for both langurs.

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Effects of visual and olfactory density signals on social stress in Brandt's voles

HE Chen, HUANG Shuli, LIU Jing, SONG Yiran, LU Wei, ZHANG Zhibin

2021, 41(4):  416-430.  DOI: 10.16829/j.slxb.150532

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Rodents have the density-dependent behavior-endocrine regulation mechanism.When their population density increases, it will increase social stress, nervous anxiety, aggression behaviors, as well as alter neuroendocrine in the brain.Social stress caused by increased density may involve different senses such as visual, olfactory, touch, hearing, andtaste, however, their distinct effects on social stress have never been evaluated.Our previous study indicates that high population density decreases the expression of oxytocin(OT) in the brain of male Brandt's voles(Lasiopodomys brandtii), increases the expression of arginine-vasopressin(AVP), and increases serum corticosteroid(CORT), which are linked to the increase of aggressive behavior.However, the role of olfactory and visual signals in triggering social stress is unknown.Because the olfactory signal is involved in marking the territory or dominance of animals, while the visual signal is involved in collective cooperation for defending territory against intruders or predators, the social stress effects may be different.We used nest pads and mirrors to simulate olfactory and visual density.To test the distinct effects of olfactory and visual density signals on social stress of Brandt's voles, we analyzed the behavioral(open-field test, elevated plus-maze test, and three-chamber sociability test), body weight, organs, serum physiological indicators, and brain neurotransmitter expression changes.We found that nest-pads treatment groups with high olfactory density decreased OT expression but increased AVP expression in specific brain regions of Brandt's voles, which is similar to the density effect(except for the OT increase in males).This result generally supported the hypothesis that high-density olfactory is the main signal path of density-dependent social stress.High visual density group treatment increased OT expression in males, but decreased expression of glucocorticoid receptor(GR), serum adrenocorticotropic hormone(ACTH), and anxiety behavior in females, supporting the hypothesis that high-density visual is the main signal path for reducing social stress.Our study suggests that visual and olfactory signals play a different, or even opposite role in the density-dependent behavioral or population regulation of social Brandt's voles, which may be beneficial in maintaining an optimal population density or group size.

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Spatial pattern of plateau pika burrows under different grazing modes

HE Qianyun, WANG Xiaoyi, LUO Gai, ZHANG Pei, RAN Jianghong

2021, 41(4):  431-440.  DOI: 10.16829/j.slxb.150502

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We studied the impacts of grazing on the number and spatial patterns of plateau pika(Ochotona curzoniae) burrows in Zoige County of Sichuan Province, China from April to November, 2019.The grazing mode was categorized as grazing prohibition(GP), winter grazing(WG) and year-round grazing(YG).The average nearest neighbor ratio and the S²/m value(the ratio of variation to mean) were respectively used to assess the spatial patterns of burrows within quadrats(10 m×10 m) and at a larger scale within plots.A nonparametric test was used to evaluate differences in spatial patterns between grazing modes and investigation months.Our results showed that:(1) the total and available burrow numbers of plateau pika were significantly different between grazing modes, and WG plots had the highest number.The number of burrows in the WG plots and YG plots differed significantly between months.(2) There were significant differences in the spatial patterns of burrows between grazing modes in the scale of quadrat and plot.The spatial patterns of all burrows and available burrows showed different distributions.(3) The height and coverage of vegetation were correlated with the number and spatial patterns of pika burrows.(4) The total burrow number was positively correlated with the average nearest neighbor ratio.Our study indicated that grazing mode can affect the spatial patterns of plateau pika and subsequently population dynamics.The utilization and spatial pattern of pika burrows are highly influenced by the height and coverage of vegetation near and around burrows.

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Activity pattern of Transbaikal zokor(Myospalax psilurus) and its relationship with soil temperature and humidity

Manduhu, YUAN Shuai, YANG Suwen, JI Yu, Chaoketu, WEI Jun, FU Heping, WU Xiaodong

2021, 41(4):  441-450.  DOI: 10.16829/j.slxb.150523

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The activity rhythm of animals is a comprehensive adaptation to environmental conditions.Subterranean rodents live in relatively low oxygen and dark environment all year round.How their activity rhythm and intensity are affected by soil temperature and humidity of their habitat, and whether there are gender differences, has received extensive attention.The influence of these factors can objectively reflect the long-term life-history strategies of subterranean rodents to adapt to their habitats.Transbaikal zokor (Myospalax psilurus) is a dominant rodent species in the meadow steppe of northern China.It is very important to study the diurnal and seasonal activity intensity of zokor and their relationships with soil temperature and humidity for understanding its survival and reproductive strategies and ecological controlling factors.This study was conducted in May(spring), July(summer), and September(autumn) of 2016 and 2017 in the meadow grassland of Hulunbeier city, Inner Mongolia, China, using radio-tracking methods to monitor the diurnal and seasonal activity intensity of Transbaikal zokor.We analyzed the daily activity intensity and sex differences among zokor in different seasons, and the relationships between activity intensity and soil temperature and soil relative humidity were analyzed.The results showed that(1) the daily activity rhythm of zokor was unimodal.The activity peak appeared from night to morning in different seasons, and the duration of peak activity varied between seasons:12 hours in spring, 7 hours in summer and 6 hours in autumn.There was no significant difference in the daily and seasonal activity intensity between male and female individuals, which exhibited a high synchronization.(2) The activity intensity of zokor was significantly correlated with soil temperature(P<0.01).The activity intensity of zokor was highest when soil temperature was at 7℃-10℃(20:00 to 08:00 the next day) in spring, 17℃-22℃(20:00 to 03:00 the next day) in summer and 10℃-12℃(22:00 to 04:00 the next day) in autumn, and then gradually decreased with increasing soil temperature.There was no significant correlation between activity intensity and soil relative moisture.

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Effects of repeated exposure to cat odor on anti-predator and anxiety-like behaviors of juvenile Brandt's voles(Lasiopodomys brandtii)

PENG Yan, WU Yongzhen, GU Chen, YANG Shengmei, YIN Baofa, WEI Wanhong

2021, 41(4):  451-458.  DOI: 10.16829/j.slxb.150469

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The predator odor has an important effect on the behavior and physiology of the prey.This paper aimed to investigate the change of anti-predator, anxiety-like behaviors and endocrine level of juvenile Brandt's voles(Lasiopodomysbrandtii) after repeated exposure to cat odor for 18 days.We also discuss the response strategy of juvenile Brandt's voles affected by the cat odor.The results showed that juvenile Brandt's voles significantly increased concealing behavior and decreased the locomotion, jumping, grooming and contact behaviors after exposed to cat odor for one day.However, after repeated exposure to cat odor for 18 days, they developed a behavioral adaptation to the cat odor and their anti-predator behaviors were not significantly different to that of the control group.The open field test showed that the repeated exposure to cat odor significantly reduced the total distance moved and average velocity of juvenile Brandt's voles, while increased their immobility time.In the light-dark box test, female Brandt's vole in the cat-odor group visited more frequently the light area than the male, however, there was no significant difference in time in the light box between genders and treatments.There were no significant changes in plasma corticosterone(CORT) and adrenocorticotropic hormone(ACTH) concentrations for the juvenile Brandt's voles after repeated exposure to cat odor.These findings indicate that when juvenile Brandt's voles are initially exposed to cat odor, their anti-predator behaviors increased, but subsequently diminished over repeated exposures.On the other hand, their anxiety-like behaviors did not vary.

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Melatonin implantation affected annual changes of main reproductive hormones in mink serum

LI Dehe, CUI Kai, GAO Hui, MA Zefang, HU Liangchen

2021, 41(4):  459-467.  DOI: 10.16829/j.slxb.150526

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The purpose of this experiment was to explore the effects of the implanted exogenous melatonin(MLT) on the annual changes of main reproductive hormones in mink serum.A total of 72 female and 72 male minks at 4 months old were randomly divided into four groups:Group A(female) and Group C(male) without any treatment as controls, Group B(female) and Group D(male) were implanted with exogenous MLT from July 7, 2018 to July 7, 2019.During the implantation period, three minks in each group were randomly selected to collect cardiac blood and separate serum samples for every 30 days, resulting in 12 sample collections.The Enzyme-linked immunosorbent assay(ELISA) was used to determine the contents of the main reproductive hormones in the collected sera.The results showed that (1) in Group A, the contents of gonadotropin-releasing hormone(GnRH), prolactin(PRL), and progesterone(P) were at higher levels in January than those in other time.The levels of PRL and P showed a small peak in June and July, respectively.Follicle stimulating hormone(FSH) and luteinizing hormone(LH) first decreased and then increased in autumn and winter and reached a high level in December.In spring and summer, FSH showed a gradual downward trend, while LH decreased at first and then increased.Estradiol(E2) gradually increased in autumn and winter and reached a high level in January, followed by a gradual decrease and fluctuated trends in spring and summer. (2) In Group B, in comparison with Group A, GnRH significantly increased in October(P ≤ 0.05) and January(P ≤ 0.01);PRL decreased in January, February, and June(P ≤ 0.05);P increased in October and June(P ≤ 0.05);FSH increased(P ≤ 0.01) in October, but decreased in both January and February(P ≤ 0.05);and LH significantly increased in March(P ≤ 0.05).(3) The testosterone(T) in Group C increased to the highest level only in January, while in Group D decreased in January(P ≤ 0.01).In summary, the exogenous MLT can increase the content of GnRH, reduce the concentrations of PRL, P and T in January, and induce FSH and LH to reach the peak in October and E2 to peak in November.Implantation of MLT resulted in inconsistent estrus periods between male and female minks, therefore this protocol is not suitable for mink breeding.

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Variation of body weight in all age groups of captive giant pandas(Ailuropoda melanoleuca)

ZHANG Mingchun, ZHOU Xiao, WU Honglin, QIU Jian, ZHANG Yi, HUANG Shan

2021, 41(4):  468-475.  DOI: 10.16829/j.slxb.150491

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Body weight is a key indicator to assess developmental and healthy condition of captive animals.From 2017 to 2019, we weighed 219 pandas kept at China Conservation and Research Center for the Giant Panda(CCRCGP), Dujiangyan, Sichuan, China every 15 days(data collection began in 2013 only in Hetaoping Base of CCRCGP).We found that:(1) the newborn's body weight was(0.16±0.04) kg, and not significantly correlated with its mother's weight;the cub's body weight was(13.74±10.64) kg;sub-adult's body weight was(78.30±27.05) kg;adult's body weight was(112.25±12.04) kg;old-age's body weight was(100.75±15.79) kg.(2) Female newborn's body weight was similar to male's but lighter in all other four age periods(P<0.05).(3) Both female and male giant panda cubs fitted the growth curve of Power, female sub-adult fitted the growth curve of Cubic, and male sub-adult fitted the growth curve of S. Both female and male giant pandas exhibit a linear growth in the period of cub and sub-adult(P<0.05).(4) Body weight of adult giant pandas did not vary significantly in different years and seasons(P>0.05), but became lighter at later age.Especially, there was a dramatic decline for male giant pandas in the later old period(P<0.001).Our study completed the growth patterns of captive giant pandas during their whole life history and provided referential value for husbandry management in ex situ conservation.

SCIENTIFIC NOTES

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Second record of collared sprite(Thainycteris aureocollaris, Chiroptera, Vespertilionidae) from China

XIE Huixian, LI Yannan, LIANG Xiaoling, ZHANG Huiguang, ZHAN Liying, WU Yi, YU Wenhua

2021, 41(4):  476-482.  DOI: 10.16829/j.slxb.150533

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During a chiropteran survey in June 2020 in the Wuyi Mountain National Park, Fujian Province, a male bat was captured by a harp trap on a forest trail.It was a medium-sized vespertilionid bat with a forearm length of 45.9 mm and a distinct broad stripe of buffy hairs running across the top of its head between the bases of the ears.Its skull was robust with the greatest length of 17.42 mm, obvious supraorbital protuberances, and a dental formula of 2113/3123.These characteristics are consistent with those of the Collared sprite Thainycteris aureocollaris, a species rare in China.The morphology-based identification was also verified by phylogenetic inference using the mitochondrial cytochrome C oxidase subunit I gene segment. The calls of the specimen recorded during flight were the frequency modulation type with a dominant frequency of(30.05±0.94) kHz. T.aureocollaris has so far only been recorded in Libo County, Guizhou Province, China, therefore the current record represents the second known occurrence of the species in China, and a new chiropteran record from Fujian Province.