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30 May 2018, Volume 38 Issue 3

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Opportunities and challenges of fecal DNA technology in molecular ecology researches

SHAN Lei, HU Yibo, WEI Fuwen

2018, 38(3):  235-246.  DOI: 10.16829/j.slxb.150194

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Advances in fecal DNA technology have expanded its usages in molecular ecology, especially in genetic assessment of wild animals. The technology allows researchers to understand ecological issues without contacting, disturbing, or even seeing animals, thus avoided invasions to the animal studied, and greatly promotes studies in molecular ecology of wild animals. Although this technology could yield poor DNA and relatively high genotyping errors in its early stages, these problems have been overcome gradually with the technological achievements being made in the past 25 years. Nowadays, fecal DNA technology yields good DNA and low genotyping errors, allowing researchers to address questions in reliability. Here, we share our knowledge about technological pitfalls on fecal sampling, preservation, DNA extraction, PCR, and genotyping in detail, and discuss opportunities and challenges of its applications, aiming to increase the power and role of the technology in molecular ecology of wild animals.


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Dynamic status of Sichuan snub-nosed monkey in Foping National Nature Reserve, China

HE Gang, GUO Songtao, JIN Xuelin, HE Shujun, LI Fangfang, LI Cai, WU Fan, HOU Rong, HUANG Kang, HE Xiangbo, LIU Xinyu, Ruliang Pan, LI Baoguo

2018, 38(3):  247-259.  DOI: 10.16829/j.slxb.150176

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Foping National Nature Reserve in Shaanxi is characterized by habitats adopted by many rare and endangered animal species including the giant panda and the Sichuan snub-nosed monkey. Since the late 1990s, the State Forestry Administration of the People's Republic of China started implementing a specific protection project, the Natural Forest Protection Project, which, in addition to enhancing reserve protection, featured local governments carriying out a series of supplementary projects aimed at promoting developments in agriculture, industry and economy – which have remarkably upgraded life standards of the locals. In order to assess whether simultaneously such projects have improved conservation status of the Sichuan snub-nosed monkeys (Rhinopithecus roxellana), and perhaps other animals as well, we carried out a broad field survey in order to get the monkeys’ spatial-temporal distribution patterns and census data; and retrospectively reviewed similar records since 1999 from academic publications and the archives kept in the Reserve and by local governments. The results indicate that both population size has increased (from less than 500 to about 671 individuals) and habitat areas have been significantly extended (from 147.8 to 236.5 km2), with an increasing tendency of approaching lower altitude areas, particularly in autumn (1680±304 meters above sea level), getting closer to agricultural regions (less than 1200 meters above sea level); and the monkeys much prefer habitats with evergreen broad-leaf forest (40.11%)  and deciduous broad-leaf forest (38.41%), but less prefer scrub-grassland and bamboo. Thus, the study implies that the implementation of the Natural Forest Protection Project and the improvements of local agriculture, economy and local life standards have significantly reduced the interference of humans with wildlife habitats, and improved the quality of natural habitat conservation and ecological environment adopted by the monkeys. Therefore, what has been done in Foping has established an ideal model showing how nature reserves and wild animals can be effectively protected through integral and systematic endeavours in which local agriculture, economy and life quality, wild habits and animals are mutually considered and improved.


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To disperse or not to disperse: male reproductive success in free-ranging Taihangshan macaques

TIAN Jundong, GUO Weijie, WANG Shuai, DUAN Hongyu, WANG Baishi, WANG Zhenlong，LU Jiqi

2018, 38(3):  260-266.  DOI: 10.16829/j.slxb.150122

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A typical social group of rhesus macaque (Macaca mulatta) is composed of multi-males and multi-females. Females are philopatric, forming kin-bonded subgroups (i.e., matrilines). Males often disperse into non-natal groups during puberty or elder age, while adult males in the social group are mainly immigrants. This is suggested to reduce inbreeding and/or the enhancement of male reproductive success. However, adult males are frequently observed to stay in their natal group after puberty for one or few years. Although complex factors (e.g., social relationship, inbreeding avoidance, reproductive success) could respond to the dispersal, difference in reproductive success could be the main driver. Therefore, it is reasonable to hypothesize that the reproductive success of the natal males would be lower than that of those immigrant males. From March 2010 to January 2014, non-invasive sampling (i.e., fecal DNA) was adopted to test the parentage of the macaques born during 2009 and 2013 in a free-ranging group of Taihangshan macaques (M. m. tcheliensis). This group inhabits Mt. Wangwu area within the Taihangshan Macaque National Nature Reserve, Jiyuan, China. Fecal DNA samples were collected from 76 macaques, including 19 adult females and their offspring, and 6 adult males (4 immigrants and 2 natal males). The results showed that: 1) 36 out of 51 offspring could be assigned to their genetic fathers; 2) the 4 immigrants sired 34 offspring in contrast to 2 offspring sired by a natal male (ZM), and none of the genotyped offspring was assigned to BB; and 3) the average offspring for each immigrant adult males (1.97, 95% CI: [1.02, 2.91]) were higher than that of the natal adult (0.5). The findings demonstrate that the reproductive success of immigrant male rhesus macaques is higher than that of the natal rhesus males, supporting our prediction.

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Interactions between rhesus macaques and visitors at Hainan Nanwan Monkey Islet, China

ZHANG Peng, DUAN Yongjiang, CHEN Tao, ZHANG Jie

2018, 38(3):  267-276.  DOI: 10.16829/j.slxb.150144

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The relationship between tourists and animals in ecotourism has become a research focus among zoologists, anthropologists and sociologists. Primate provisioning is commonly seen at ecotourism sites in China, while monkeys threatening or biting tourists is a rising problem. This study recorded interactions between tourists and macaques on the Nanwan Monkey Islet between 2012 and 2014, and analyzed clinic records on injured tourists. We discuss: (1) the characteristics of visitors who were involved in macaque-human interactions; (2) the characteristics of macaques that were involved in the interactions；(3) the factors which triggered the interactions. This paper aims to understand relationships between tourists and macaques, to find possible solutions to reduce injury risk of tourists, and to improve the management of wildlife tourism in the country.


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Summer habitat selection of sambar deer (Rusa unicolor) in Wolong National Nature Reserve

HU Jie，YAO Gang，LI Dayong， YANG Zhisong，LI Yanhong

2018, 38(3):  277-285.  DOI: 10.16829/j.slxb.150142

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From July to August 2015, the quadrat sampling method was used to investigate summer habitat selection by sambar deer in Wolong National Nature Reserve. Fifteen habitat variables, such as elevation and slope gradient were assessed for 160 quadrats. Of the 160 quadrats, 85 were sites used by Rusa unicolor and 75 were random sites. An optimal model for habitat selection of Rusa unicolor was chosen according to the results of logistic regression analysis and Akaike information criterion (AIC).  The results showed that the key ecological factors affecting the habitat selection of Rusa unicolor in summer were concealment, slope gradient, distance from human disturbance, and distance to water. In summer, Rusa unicolor prefer habitats with good or moderate concealment, gentle slope（< 20 °）, far from human disturbance（> 1000 m ）and near water resources（< 500 m）. Furthermore, the results also suggested that vegetation type affected habitat selection of Rusa unicolor to some extent (χ2= 11.499, df= 4, P= 0.021). Around 92% of the sites used by Rusa unicolor were found in all kinds of forests, and only around 8% were found in the shrubland of Rhododendron sp. and Quercus semecarpifolia located at around 3500 m above sea level.

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Various postnatal developmental patterns of four digestive enzyme activities of small intestine in Swiss mouse#br#

LUO Lijuan, WANG Shengnan, YANG Ming, LIU Quansheng

2018, 38(3):  286-294.  DOI: 10.16829/j.slxb.150204

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We determined the activities of lactase, sucrase, maltase and aminopeptidase-N in small intestine of mice from birth to 27 days of age in order to identify the formation and development model of intestinal digestive enzyme activities in young mice and test the adaptive modulation hypothesis. The lactase specific-mass activity increased initially and then decreased, reachingthe highest levels at 9 days of age in the proximal small intestine and at 12 days of age in the middle and distal small intestine. At 27 days of age, there was weak lactase activity only in the middle small intestine. The sucrase specific-mass activity appeared at 12 days of age, and increased rapidly from 15 days of age, reaching the highest level at 18 days of age in the proximal and distal intestine and at 21 days of age in the middle small intestine, and then declined markedly. The maltase specific-mass activity is weak at birth and remained at this level until 15 days of age. It then increased rapidly and reached the peak at 18 days of age in the proximal and distal intestine and at 21 days of age in the middle intestine, and then decreased. The aminopeptidase-N specific-mass activity of proximal small intestine decline continuously until 27 days of age, but the activity increased continuously from birth to weaning in the middle and distal intestine and then slightly declined. The total lactase activity peaked at 15 days of age and then declined. However, the total activities of sucrase, maltase, and aminopeptidase-N constantly increased through the entire lactation period. All

four enzyme specific-mass activities had remarkable differences among the varied positions of the small intestine. Moreover, the age of mice had significant influence on the distribution of enzyme activity in the different small intestine positions. In sum, the temporal changes of the four kinds of enzymes activities in small intestine could match with the variation of food digestion needs, which partly supported the adaptive modulation hypothesis.

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The anesthetic effects of ketamine on golden snub-nosed monkeys（Rhinopithecus roxellana）

YANG Wanji, ZHANG Bo, XIA Maohua, YAO Hui, LIU Jinpeng, YU Huiliang, XU Haiqing, YANG Jinyuan, XIANG Zuofu

2018, 38(3):  295-301.  DOI: 10.16829/j.slxb.150186

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To evaluate the anesthetic effect of ketamine on golden snub-nosed monkeys (Rhinopithecus roxellana), we observed the reaction of 24 individuals to intramuscular injection of ketamine doses of 5.90-15.71mg/kg when collecting blood for another study. The results indicated that all individuals had a satisfactory anesthetic outcome with no deaths. They exhibited limpness, salivation, slow falling, and occasional idle chewing during incubation which lasted （4.00 ± 1.77） min. They showed good muscle relaxation, smooth breathing, and idle chewing during the anesthesia period which lasted （21.67 ± 5.03 ）min. The recovery period lasted （31.79 ± 6.07 ）mins; golden snub-nosed monkeys began to regain consciousness, tried to sit and walk with frequent idle chewing during the recovery period, and resumed normal activities after the recovery period. A new behavior, idle chewing, i.e. chewing with no food in the mouth, is first reported in the process of anesthesia in this species. Furthermore, our results show that the duration of the recovery period was longer for the male subjects than for the females and that the frequency of idle chewing during the recovery period was lower in the males than in the females. Sex and age dependent differences in behavioral reactions were not detected during the anesthesia or in the recovery period.

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Urinary volatile constituents of tree shrews (Tupaia belangeri) during various reproductive stages

YE Fangyan, ZHU Wanlong, GAO Wenrong, ZHANG Hao, WANG Zhengkun

2018, 38(3):  302-308.  DOI: 10.16829/j.slxb.150111

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Chemical signals in the urine play key roles in recognizing physiological periods in mammals. In our study, gas chromatography-mass spectrometry (GC-MS) was used to analyze the urine compositions in female Tupaia belangeri during estrus, pregnancy and lactation. We found that the chemical compounds were mainly aldehydes and ketones in all three periods. Hexadecane，1,3,6,10-dodecatetraene, 3,7,11-trimethyl-, (Z,E)- and cyclooctane were the special chemical constituents in the urines of Tupaia belangeri in estrus. Acetone，disulfide, dimethyl, 2,3-Hexanedione，(R)-(-)-2-pentanol, 2-buten-1-ol,3-methyl-, 2-nonanol, benzaldehyde,2-methyl, 6-octen-1-ol,7-methyl-3-methylene-, 2,6-octadien-1-ol, 3,7-dimethyl-(Z)-, cyclohexadecanone and dibutyl phthalate were the special chemical constituents in the urines of Tupaia belangeri during pregnancy. 2,5-Octanedione, α-methyl-α-[4-methyl-3-pentenyl]oxiranemethanol, 4-(3,4-Methylenedioxyphenyl)-2-butanone, cyclohexanone,2-methyl-5-(1-methylethenyl)- and benzoic acid,2-ethylhexyl ester were the special chemical constituents in the urines of Tupaia belangeri during lactation. Together, these results indicate that: there were differences in urine volatile compounds

during estrus, pregnancy and lactation in female Tupaia belangeri.

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New record of a rodent genus (Murinae) in China—Tonkinomys daovantieni

CHENG Shi, CHEN Zhongzheng, CHENG Feng, LI Jiaqi, WAN Tao, LI Quan, LI Xueyou, WU Hailong, JIANG Xuelong

2018, 38(3):  309-314.  DOI: 10.16829/j.slxb.150170

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From November 2016 to April 2017, we collected four rodent specimens from Jinchang, Babu and Majie in Malipo County, Yunnan Province, China. They are different from any mammalian species described so far in China and have been identified as Tonkinomys daovantieni Musser et al., 2006, a new record of the genus in China. Its main features are: dorsal pelage grayish black with semi-spinous, dense fur, ventral pelage grayish; a thick, bicolored tail considerably shorter than length of head and body, the distal 1/3 white, the proximal 2/3 of its dorsal and lateral dark brown and ventral white; the first and the second molars consist of tightly pressed rows exposing chunky chewing surfaces in the shapes of two parallel chevrons and a roughly diamond-shaped chewing surface, the third molar consists of a front chevron formed by union of protoconid and metaconid and behind that a large oblong structure likely representing the complete fusion of hypoconid and entoconid. Each lower molar has two roots. The Cyt b sequence is 97.7% identical to the specimens from the type locality and phylogenetic analysis by maximum likelihood algorithm supported the two populations to be monophyletic (BS=100%). This finding is the first recorded distribution of genus Tonkinomys in China and outside of the type locality.

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New record of Murina fanjingshanensis (Chiroptera: Vespertilionidae) in Hunan Province, China#br#

HUANG Taifu, GONG Xiaoyan, WU Tao, PENG Le, ZHANG Youxiang, ZHANG Libiao, LIU Zhixiao

2018, 38(3):  315-317.  DOI: 10.16829/j.slxb.150151

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A hibernating male tube-nosed bat was collected in March, 2016 from Yanzi Cave in the Bamianshan Mountain (28°51′56″N, 109°16′15″E, 1213m asl), Longshan County, Xiangxi Tujia and Miao Nationalities Autonomous Perfecture, Hunan Province. This sample was identified as Murina fanjingshanensis based on both morphology and Cyt b gene sequence. The finding not only adds a new record of Chiroptera for Hunan Province, China, but also is the first report of the species outside its type locality in Fanjingshan Natural National Reserve, Guizhou, China.

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Preliminary camera-trapping survey on wild mammals and birds in Ailaoshan National Nature Reserve, Yunnan Province, China#br#

HE Xuelian, LUO Kang, LU Zhiyun, XIAO Zhishu, LIN Luxiang

2018, 38(3):  318-322.  DOI: 10.16829/j.slxb.150130

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Camera-trapping has been considered as an important method for monitoring large and medium-size mammals and terrestrial birds, and with high applied value to biological inventory for protected areas. From October to December 2014, we set up 40 infrared camera monitoring sites (1 camera for each two ha.) in the northern part of Ailaoshan National Nature Reserve, Yunnan Province, to monitor wild mammals and birds in mid-mountain humid evergreen broad-leaved forest. During the total 1961 camera days, we identified 10 mammals species and 10 bird species from 566 independent images. According to the relative abundance index (RAI), Asian red-cheeked squirrel (Dremomys rufigenis) and wild boar (Sus scrofa) were ranked as two most abundant mammals, while silver pheasant (Lophura nycthemera)、long-tailed thrush (Zoothera dixoni) and spotted forktail (Enicurus maculatus) were ranked as the three most abundant bird species. Among the twenty wild mammal and bird species, four species were categorized as class II state key protected wild animals, two species were listed by the IUCN global red list as Vulnerable, two and three species were classified as Appendix II and III by CITES, respectively. Although several key territorial mammal and bird species were not recorded, this preliminary research still provides basic information of biodiversity for establishing camera-trapping routine

survey and conservation management of the natural reserve.

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Preliminary investigation for mammal and bird resources using infrared camera traps in Maolan National Nature Reserve, Guizhou

LIU Jia, LIN Jianzhong, LI Shengqiang, LI Youbang, YAO Zhengming, WEI Luming, TAN Chengjiang, ZHOU Qihai, HUANG Chengming

2018, 38(3):  323-330.  DOI: 10.16829/j.slxb.150158

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From August to December in 2016, we placed 69 infrared cameras  (1 camera was lost and 3 suffered breakdowns during the study period), to monitor large and medium-sized mammals and forest birds in Maolan National Nature Reserve, Guizhou. We identified 11 mammal species and 16 bird species, including 1 Class I state key protected animal Syrmaticus ellioti and 4 Class II state key protected animals - Prionodon pardicolor, Macaca mulatta, Lophura nycthemera, and Pitta nympha. Based on the relative abundance index (RAI), Leopoldamys edwardsi (RAI=15.22), Dremomys pyrrhomerus (RAI=9.58), Atherurus macrourus (RAI=1.46), Melogale moschata (RAI=1.04) and Callosciurus erythraeus (RAI=0.57) were ranked as the top five most abundant mammal specices. Myophoneus caeruleus (RAI=3.79), Lophura nycthemera (RAI=3.25), Zoothera citrine (RAI=0.45) and Zoothera dauma (RAI=0.45)

were ranked as the top four most common bird species. In addition, Prionailurus bengalensis, Pitta nympha, Turdus rubrocanus, Turdus boulboul, Alcippe morrisonia, Chalcophaps indica and Blythipicus pyrrhotis were new species, recorded in the reserve for the first time. Lophura nycthemera and Myophonus caeruleus were diurnal animals, Atherurus macrourus and Melogale moschata were nocturnal animals; this result was expected. Our results offer valuable data for monitoring the resources of large and medium-sized mammals and forest birds in Maolan reserve, and can offer guidelines for future research and management of China’s important protected areas.