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13 May 2014, Volume 34 Issue 2

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Seasonal variation in diurnal diet and activity rhythm of cao vit gibbon (Nomascus nasutus) in Bangliang Nature Reserve,Guangxi,China

MA Changyong,FEI Hanlan,HUANG Tao,CUI Liangwei,FAN Pengfei

2014, 34(2):  105-114. 

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Diet and activity rhythms are important aspects of animal behavior. Studying these topics provides valuable insights into how variations of food,temperature and illumination time impact animal behavior and behavioral adaptations. To better understand how these variables affect the endangered cao vit gibbon,we collected behavioral and dietary data using instantaneous scan sampling at 5 -min intervals on two groups in Bangliang Nature Reserve in Guangxi,China from January 2009 to December 2009. Both activity and diet showed an obvious rhythm in rainy and dry seasons. Gibbons sang only before 12:00 in both rainy and dry seasons,but later in dry season. There were two feeding peaks each day,one in the early morning after leaving sleeping trees and the other in the afternoon before entering sleeping trees. Gibbons fed primarily on fruit and figs in the early morning (07:00),and ate more fruit but less figs in the late afternoon (16:00). They consumed more leaves and buds between 13:00 and 15:00. Gibbons spent more time resting and exhibiting social behaviors between 10:00 and 12:00. Seasonality in diet corresponded with availability of preferred foods. In the warm rainy season when fruit and figs were most abundant,gibbons’diet consisted mainly of fruit and figs,as well as more invertebrates.In the cold dry season,their diet mainly comprised leaves and buds. In response to variations of temperature and lower fruit abundance in the dry season,the gibbons spent more time feeding,and decreased their time spent traveling,but increased their resting time,presumably as a mechanism to conserve energy and cope with lower temperatures. In the rainy season, gibbons spent more time exhibiting social behavior,which peaked between 08:00 and 10:00,whereas in the dry season social behavior was predominantly observed between 11:00 and 14:00.There was no obvious resting behavior peak in the rainy season,whereas resting behavior clearly peaked at 10:00 in dry season We suggest the contrasting behavior of gibbons between wet and dry seasons demonstrates the special adaptation this species has to persist in highly seasonal karst forests.

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Social play of Yunnan snub-nosed monkeys (Rhinopithecus bieti) from 0-3 years old

YUAN Xiaoxia,LI Dayong,REN Baoping,LI Yanhong,MA Yonghong,ZHANG Dejun,HU Jie

2014, 34(2):  115-121. 

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We observed the social play behavior of individual Yunnan snub-nosed monkeys (Rhinopithecus bieti)of 0 - 3 years of age at Xiangguqing in Baimaxueshan National Nature Reserve from July 2012 to April 2013. Thirty monkeys (12 males,18 females)from a provisioned monkey group were observed via all-occurrence sampling. We found that the frequency of social play is significantly different among individuals in their first,second,or third years of life,and that play frequency negatively correlates with age. Choice of play partners and types of play also vary between age groups. Individuals are most likely to play with age-mates. The preferred games for individuals in the first year of life are chasing (67.5% ), while individuals in the second year of life most often catch (26.6% ),bite (25.3% ),and chase (40.5% )each other. We found no particular preference in the play of monkeys in their third year of life. On average,males spend more time playing than females. We interpret these patterns in the social play of R. bieti in light of the age/stage hypothesis,sex difference hypothesis,and locomotor development hypothesis.

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Does paedomorphosis contribute to prairie vole monogamy?

Timothy Bushyhead,J. Thomas Curtis

2014, 34(2):  122-128. 

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We examined skull morphology in prairie voles (Microtus ochrogaster)and meadow voles (M. pennsylvanicus),two closely related species with fundamentally different mating systems,to test the hypothesis that paedomorphosis contributes to the evolution of monogamous mating systems. Using several skull measurements,we found that the overall length:width ratio of meadow vole skulls was greater than that of prairie voles suggesting that meadow vole have longer narrower skulls. We then examined which aspects of skull morphology differed between the species and found that the ratio difference was attributable primarily to longer snout length in meadow voles. Finally,we compared adult morphology in both species to that of pups and found the prairie vole,a monogamous species,displays a more juvenile-like skull morphology than does the meadow vole,a promiscuous species. These results suggest that monogamous vole species retain more juvenile-like morphology than do promiscuous species,and thus possibly retain juvenile-like behaviors that may contribute to a monogamous mating system.


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Transcriptomatic determination of convergent evolution between plateau zokors (Eospalax baileyi) and naked mole rats (Heterocephalus glaber)

DENG Xiaogong,WANG Kun,ZHANG Shoudong,SU Jianping,ZHANG Tongzuo,LIN Gonghua

2014, 34(2):  129-137. 

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Subterranean rodents have evolved convergent traits in many of their biological characteristics that allow them to adapt to a similar underground burrowing life style. However,no study has yet been published about this convergent evolution at the molecular level. Here,we use high-throughput next-generation sequencing data (transcriptomes)to identify both amino acid (AA)variations and gene expression levels in order to analyze the convergent evolution of two typical subterranean rodents,the plateau zokor (Eospalax baileyi)and the naked mole rat (Heterocephalus glaber). AA variation analysis detected 54 genes of which each had at least one convergent adaptation site;of these genes 13 were successfully annotated by their relatively obvious phenotypical functions. Within the 13 genes,four (Ptpn6,Sco1,Dhcr 24,and Add2) were related with hypoxia tolerance or adaptation to oxidative stress,four (Mbtps1,Atp1a1,Acsl3,and Ncoa2)were involved in nutrient transport or energy metabolism,fou(Smoc1,Kif1b, Tcap,and Cryab)were involved in limb development or muscle health,and the remaining gene (Myo6)was involved in auditory function. Gene expression level analyses of the two subterranean rodents detected 103 genes that were significantly upregulated (> 3 fold)as compared to mouse (Mus musculus)and guinea pig (Cavia porcellus);20 of these genes could be successfully annotated by their phenotypical functions. Within these 20 genes,12 were related with hypoxia tolerance functions,such as oxygen transport(Dsg2, Tab2, Hp,Rock1,and F5),oxygen metabolism (Tfb1m and Mrpl1),and DNA repair (Tdp2,Rad50,Alkbh2,Hltf, and Plk1),3 were related with the functional integrity of muscle (Sync and Taf3)and bone (Acp5),and the other 5 were involved in immune (Spon2 and Sh2d4a),biological rhythm (Clock),starvation tolerance (Pdk4 ),and reproduction (Clgn). Our results show that the hypoxia tolerance-related genes were the most important adaptation genes found in the two subterranean rodents,followed by the digging apparatus-related genes (especially the skeletal muscle)in addition to the genes important in energy metabolism and energy balance. This paper provides evidence for convergence of subterranean rodents at the molecular level.


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Population survey and genetic diversity of snow leopard (Uncia uncia) in Qinghai-Tibet Plateau as revealed by fecal DNA

ZHOU Yunyun, FENG Jinchao, DUO Hairui, YANG Hailong, LI Juan, LI Diqiang, ZHANG Yuguang

2014, 34(2):  138-148. 

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With noninvasive sampling, 277 fecal samples were collected from dominant distribution areas of snow leopard (Uncia uncia), including Sanjiangyuan National Nature Reserve (Qinghai Province), Qiangtang National Nature Reserve (Tibet Autonomous Region) and Nanshan area (Danghe, Gansu Province). Species identification, individual recognition and genetic diversity were explored by analysing the mtDNA cytb gene fragment and microsatellite loci. The results showed that 190 samples were successfully amplified and sequenced in 277 fecal samples. 89 samples were identified as snow leopard and they belonged to 48 individuals. 9 haplotypes and 13 diversity sites were found in the 48 mtDNA cytb gene fragments. The haplotype diversity was 0.776, the nucleotide diversity was 1.50% and the genetic distance among 9 haplotypes ranged from 0.009 to 0.058. According to the results, we postulate that snow leopards among these areas have significant genetic variation in the mtDNA cytb gene fragments. The samples distributed in Qiangtang National Nature Reserve and Nanshan area have significant genetic distance.

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Seasonal changes in body mass and energy budget in striped hamsters

ZHAO Zhijun, CAO Jing, CHEN Kexin

2014, 34(2):  149-157. 

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The present study was aimed at examining seasonal changes in body mass and energy metabolism in small mammals and the physiological mechanisms underpinning the changes. Seasonal changes in body mass,energy budget,masses of tissues and organs and serum leptin levels were determined in striped hamsters (Cricetulus barabensis)that were acclimated to natural temperature and photoperiod for 12 months Basal metabolic rate (BMR)and non-shivering thermogenesis (NST)were measured using a computerized open-flow respirometry system in summer,autumn,spring and winter,respectively. The hamsters showed significant seasonal changes in energy intake and expenditure. Digestive energy intakes were higher by 73.7% ,137.9% and 69.3% in autumn,winter and spring,respectively,than that in summer. BMR and NST increased by 86.2% and 163.6% in winter compared with those in summer. Body mass was constant over the year,but the masses of tissues and organs differed significantly between the four seasons. In detail,masses of liver,heart
and kidneys,as well as digestive tracts were heavier in winter than those in summer. Body fat content was significantly lower in winter than in summer, autumn and spring (P < 0.01);it reached a maximum in summer,and a minimum in winter. There were significant changes in serum leptin levels over the four seasons,which were higher by 88.2% and 52.4% in summer than that in autumn and winter,respectively (P < 0.05). It suggested that striped hamsters showed constant body mass over the year,which was inconsistent with the prediction of the ‘set-point’hypothesis. However,body fat content and serum leptin levels were significantly different between the four seasons,providing support for the hypothesis.The increased leptin levels may play a role in the inhibition of energy intake. Serum leptin may be also one of the important factors stimulating metabolic thermogenesis in the winter. Further,the role of leptin in the regulation of energy metabolism and body mass may be different in animals that were acclimated to different seasons.

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Growth and thermogenesis in pups of Eothenomys miletus

YU Tingting, ZHOU Qinghong, HE Lijuan, ZHU Wanlong, ZHANG Hao, GAO Wenrong, WANG Zhengkun

2014, 34(2):  158-163. 

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In order to study the growth pattern and thermogenesis in pups of Eothenomys miletus,postnatal data from 1-49 days’for E. miletus pups were collected, including body mass,body temperature,resting metabolic rate (RMR)and nonshivering thermogenesis (NST). Body mass growth in E. miletus pups could be divided into rapid-growing and slowgrowing phases based on the inflection point of a logistic growth curve (24 days). Body temperature of pups increased with age,and approached the adult level at 22 days after birth. RMR and NST increased with age continually,reached the adult level at 28 days of age. BAT thermogenesis was active within the 7 day after birth. These results show the growth pattern and thermogenesis in pups of E. miletus accord with altricial mammal characters;the short gestation period,fewer foetus, and longer feeding term are important adaptation to the special and changeable environment in Hengduan Mountains region.

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Using camera traps to survey wildlife at water sources on the northern slope of the Altun Mountains,China

XUE Yadong, LIU Fang, GUO Tiezheng, YUAN Lei, LI Diqiang

2014, 34(2):  164-171. 

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To examine the diversity and abundance of wildlife at water sources on the northern slope of the Altun Mountains,camera-trapping was conducted at seven sites from 2010 to 2012. A total of 26 species were captured in the survey. There were 11 species of mammal including Camelus ferus,Equus kiang,Uncia uncia,Lynx lynx,and 15 species of birds including Gypaetus barbatus,Aquila chrysaetos,and Gyps himalayensis in the photos. Wild camel (Camelus ferus) was the only species captured at all observation sites and was present in almost 66% of the photographs. This suggests that wild camel is the dominant species of herbivore at water source areas. Wolf (Canis lupus)and red fox (Vulpes vulpes)were the dominant species of carnivores at water sources since they were captured in 123 and 268 photographs respectively. The research suggests that camera-trapping at water sources is a practical approach for animal investigation in arid regions. Moreover,using camera-trapping data of behavior and activity could be a feasible method to study community structures and interspecies competition,or to evaluate overlap or partition of niches. Cameral-trapping at water sources will be beneficial to assess the influence of environment change and human disturbance on how wildlife use water and develop recommendations on how water sources in arid area could be managed and conserved.


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Intestinal parasites prevalence in root voles (Microtus oeconomus) from field enclosures

NIE Xuheng, CAO Yifan, DU Shouyang, HE Hui, BIAN Jianghui

2014, 34(2):  172-180. 

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Parasitism is one of the factors that can regulate fluctuations of small rodent populations. Many biotic and abiotic factors can affect parasite infections. In this study,we examined the types and prevalence of gastrointestinal parasites in root voles (Microtus oeconomus)from field enclosures,and analyzed the effects of the number of founders,sex,age and time on parasite infections. The results showed that intestinal parasites of the root voles are coccidia,cestode and nematodes; and coccidia is the key intestinal parasite;Eimeria wenrichi is a dominant species among the coccidia. We found a positive association between E. wenrichi prevalence and the number of founders;E. wenrichi prevalence significantly increased with time. In addition,E. wenrichi prevalence in juveniles in high density enclosures was higher than that in low density enclosures. E. ochrogasteri prevalence was higher in juveniles than in adults. However,sex-related susceptibility was not found for coccidian species. These results indicate that coccidian infection varied with time and depended on the density of root vole populations. Prenatal stress due to high density and density-dependent effects on the coccidian infection may have a coupling effect on coccidian prevalence to the root vole populations.

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Diagnosis and treatment of squirrel monkeys infected with Yersinia pseudotuberculosis

ZHOU Ziyao, ZHOU Xiaoxiao, PENG Guangneng, TANG Tianliang, PENG Xi, ZHONG Zhijun, LIU Changsong, LIU Junqing, WU Jianglan, SUN Hongyan, DENG Qiao, ZHOU Zhijin

2014, 34(2):  181-187. 

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Six squirrel monkeys died suddenly in an animal park of Ya’an in February 18th to 20th,2013. During that time,～100 squirrel monkeys were infected and had different symptoms which caused significant losses at the zoo. To find the reasons and treatments of this infectious disease,we first examined tissue changes by using anatomy and pathological sections;we then detected pathogens by isolation and culture of bacteria,identified the pathogens by biochemical testing and molecular identification;after that,we searched for the characterizations of pathogenicity and epidemiology through experiments
of animal regression and drug resistance;and finally controlled this disease by a series of emergency measures. The results showed that various monkey’s organs had serious congestion necrosis and severe tissue lesions caused by a large number of bacteria. The pathogen was Yersinia pseudotuberculosis which was similar as Yersinia pestis. The pathogen had strong abilities of pathogenicity,epidemiology and drug resistance,but was sensitive to Amikacin. This is the first study to find and report a case of squirrel monkeys infected with Yersinia pseudotuberculosis in our country,and provides a basis of reference in the diagnosis and treatment,epidemiological studies and pathological model building.

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Effects of storage temperature and duration on cortisol concentration in feces of giant pandas (Ailuropoda melanoleuca)

MA Kai, WU Cunzhe, YIN Feng, LIU Xuefeng, ZHANG Jinguo, LIU Dingzhen

2014, 34(2):  188-192. 

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Noninvasive sampling methods,e.g. collection and analysis of fecal samples,are increasingly used to monitor the stress levels of wild animals,yet the effects of storage temperature and of the duration of transportation and storage of fresh fecal samples on fecal cortisol concentrations remain unclear. We collected one fresh fecal dropping daily from each of two captive giant pandas (Ailuropoda melanoleuca)on three consecutive days at Beijing Zoo. Each dropping was mixed thoroughly and then allocated to a 50 g sample. We took a 5 g sub-sample from each individual fecal sample and froze it at -20℃;  this was used as the pre-treatment baseline. Next,we divided the remainder of each fecal sample into three 15 g sub-samples which were randomly assigned to be stored at 0℃ ,10℃ and 22℃ for six days. The glucocorticoids were extracted from each sub-sample once per day. The fecal cortisol concentrations were finally assayed by using commercial 125 I cortisol radioimmunoassay kits. The results showed that the fecal cortisol concentrations were not significantly affected by storage temperature (F _2,107 = 1.094,P = 0.366),but were affected by the duration of storage (F _5,107 = 7.501,P =0.001). After storage at 0℃ ,10℃ and 22℃ for six days,fecal cortisol concentrations were similar to those of the pretreatment baseline fecal samples (F _6,41 = 1.274,P = 0.290;F _{6 ,41} = 2.027, P = 0.084 and F _6,41 = 1.009,P = 0.434). The results of this study suggest that short-term (no longer than 6 days)transportation or storage of fecal samples at temperatures below 22℃ does not alter radioimmunoassay results for fecal cortisol concentrations in the giant panda. Our results will aid fecal sample collection for monitoring stress hormones in wild pandas,and thus their conservation as well.

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A comparison of live traps and pitfall traps for monitoring the diversity of ground - dwelling small mammals in forests

YAGN Xifu, XIE Wenhua, TAO Shuanglun, LI Junnian, XIAO Zhishu

2014, 34(2):  193-199. 

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Small mammals are among the most important indicators used for monitoring wildlife diversity Live traps and pitfall traps are common methods used to investigate community and population dynamics of ground - dwelling small mammals. However,it is poorly explored which trapping method is more efficient to evaluate diversity patterns of ground -dwelling small mammals. We compared the advantages,limitations and applications of live traps and pitfall traps based on species richness,community diversity and body mass of ground - dwelling small mammals in forest ecosystems. During August and September of 2012,we monitored ground - dwelling small mammals using live traps and pitfall traps in the Banruosi forest in the Dujiangyan City,Southwest China. We found that species composition biodiversity patterns and body mass of small mammals varied greatly between live traps and pitfall traps,though species richness was quite similar between them. In addition,species composition,species diversity indices and evenness indices for small mammals were lower using live traps than using pitfall traps,but the dominance indices and body masses were higher using live traps than using pitfall traps. Our study indicates that live traps can capture more rodents with larger body mass,while pitfall traps are more efficient for monitoring insectivores and rodents with smaller body mass. Live traps had a relatively higher cost and also required bait during trapping compared to non - bait pitfall traps. Since most of the trapped animals are dead using pitfall traps,live traps are better to monitor community and population dynamics of small rodents. We also recommend that both live traps and pitfall traps should be used simultaneously to monitor the whole diversity patterns of ground-dwelling small mammals.

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A new record of Anourosorex squamipes in Jiangxi Province with a discussion of its geographical range

WANG Yumei, LIU Zexin, ZHANG Wenjie, KONG Lingming, Masaharu Motokawa, Masashi Harada, WU Yi, LI Yuchun

2014, 34(2):  200-204. 

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We collected three male individuals of Chinese mole shrew (Anourosorex squamipes) from Suichuan County, Jiangxi Province,in our field survey in August 2013,and this is the first time this species has been recorded in Jiangxi Province. The external and skull measurements are as follows:body weight 15.8 - 21.6 g,total length 107.0 -125.0 mm,head and body length 95.0 - 112.0 mm,tail length 12.0 -13.0 mm,front foot length 10.5 -11.1mm, hind foot length 13.5 - 15.7 mm,greatest length of skull 24.74 - 25.83 mm,median palatal length 11.27 -11.98 mm,basion-staphylion 10.82 -11.33 mm,postpalatal depth 5.51 -5.65 mm,rostrum length 3.55 - 3.70 mm,interorbital breadth 6.28 - 6.62 mm,greatest breath of braincase 13. 53 - 13.96 mm,length of upper toothrow 10.97 -11.94 mm,mandibular length 16.13 -17.63 mm,oral height of the vertical ramus 6.87 -7.17 mm. The dental formula is 1.2.1.3/ 1.1.1.3=26. This new record of A. squamipes in Jiangxi Province greatly expands the eastern line of the historical distribution of this species in mainland China,the authors imply that the historical distribution of A. squamipes was greatly underestimated due to limitations of field survey data,and A. squamipes may occur in middle elevation areas in southern mainland China.

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An SEM observation of the microvascular casts of the lungs of a subadult female leopard (Panthera pardus)in captivity

XIE Mingren, YU Wen, ZHANG Lu, YU Farong

2014, 34(2):  205-208. 

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The present study was conducted to investigate the microvascular structures of a case of subadult female leopard (Panthera pardus)that had died from wound in captivity,by using the microvascular casting method to provide useful information and evidence to the study of respiratory physiology in animals. The results observed through the scanning electron microscope (SEM)indicated that the arterioles of the lung and pleura are formed by the ramification of small arteries (0.3 -1.0 mm diameter),pre-capillary arterioles (11 - 15 μm diameter),and capillaries (4.5 - 7.0 μm diameter). There are extensive connections in capillarity networks of blood vessels,including bridge connections between adjacent alveoli holes that form the irregular alveolar-capillary network. Our findings suggest that the dense and stereo capillary network is an important feature of the lung microvasculature in snow leopard,and is similar to those in human,mouse,rabbit,yak, sheep,Sichuan snub-nosed monkey and bactrian camel,but different from those in birds,reptiles,and amphibians.