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30 November 2022, Volume 42 Issue 6

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ORIGINAL PAPERS

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Characteristics of food plants consumed by Hainan gibbon (Nomascus hainanus) in fragmented habitat

Huaiqing DENG, Baoping REN, Yun LIU, Jiang ZHOU

2022, 42(6):  615-623.  DOI: 10.16829/j.slxb.150658

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Quantity, availability, and diameter structure of feeding plant species of Hainan gibbons (Nomascus hainanus) were investigated in Hainan Tropical Rainforest National Park of Bawangling Bureau from January 2013 to July 2014. Sixty-four food species with 1 484 plant samples of tree diameter at breast height ≥ 5 cm were recorded in the habitat of Group C of Hainan gibbon. The gibbons highly preferred large and tall trees to feed on. Fifteen tagged plant species have a fructiferous rate of more than 50.0%. The maximum is 76.7% by Monoon laui and the minimum is 9.6% by Heptapleurum heptaphyllum. Among 18 main food plants, 15 speciesshowed a growing structure and only Pouteria annamensis showed the recession structure. Food plants consisted of young individuals and only 37 species (71.2%) can fruit every year for the gibbons. Fruit rate of feeding tree species was not affected by altitude and was significantly associated with tree height and diameter at breast height. Hainan gibbons ate tender leaves (15.6%) when fruits were scarce in the dry season. High fluctuations in fruit availability yearly might limit the population growth of Hainan gibbons in a long run.

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Effects of food resources seasonality on home range utilization of wild Tibetan macaque (Macaca thibetana)

Yadong LI, Bowen LI, Xi WANG, Penghui LI, Jinhua LI

2022, 42(6):  624-633.  DOI: 10.16829/j.slxb.150647

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Distribution and availability of food sources dramatically influence home range dynamics. Studies on home range utilization are critical for revealing the ecological adaptations and behavioral complexity in wild animals. From September 2020 to August 2021, we studied one group of Tibetan macaques (Macaca thibetana, Tianhu group, TH) in Huangshan, Anhui province, China. We directly observed and recorded spatial positions of the study group and monitored habitat conditions, vegetation distribution and food availability. 4 307 GPS positions were obtained and the kernel density estimation of GPS sites revealed that the Tibetan macaque’s home range area decreased from spring to winter, with areas of 7.16 km², 5.09 km², 3.85 km², and 0.35 km², respectively. The average daily ranging distance (d= 1735.67 m ± 288.35 m, n = 12) of the monkeys was positively correlated with food availability, with the longest average daily ranging distance in July and the shortest one in January. Monkeys preferred to stay in the mixed coniferous and mixed evergreen deciduous broadleaf forests. The monkeys used bamboo forests more in spring, mixed coniferous and broad forests in summer and winter, and mixed evergreen deciduous broadleaf forests in autumn. Tibetan macaques use their home ranges to adapt to low altitudes based on food resource distribution, food availability, and other factors.

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Use of an artificial water source by wild camels in the Gansu Annanba Wild Camel National Nature Reserve

Yongxiang ZHOU, Jianquan LIU, Duoliang ZHOU, Hao WU, Xiaomei YANG, Tianhui WANG, Yadong XUE

2022, 42(6):  634-640.  DOI: 10.16829/j.slxb.150663

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Artificial water sources are an important conservation tool for endangered species living in desert landscapes because they increase water availability and survival likelihood. To determine the degree to which artificial water sources are used by wild animals, video surveillance data collected from August 2020 to August 2021 of an artificial water source in the Gansu Annanba Wild Camel National Nature Reserve were analyzed. During the monitoring period, a total of 533 video records were obtained, including 299 independent records. Our results showed that a variety of wild animals used the artificial water source, including 7 mammalian species and 7 avian species. Wild camel (Camelus ferus), the main target of species protection in the reserve, had the highest number of records (205), accounting for 67% of total independent records. The average time wild camels spent at the artificial water source was (15.66 ± 15.35) min and the average number of camels present was 6.82 ± 7.01. Time spent at the artificial water source by wild camels was significantly correlated with the number of camels present (P < 0.001), and the number of wild camels was significantly different among seasons (P < 0.005). The use of the artificial water source was the highest in summer and the lowest in spring. Daily activity patterns revealed a unimodal pattern, with the highest peak of activity occurring at 12: 00. This study revealed that artificial water sources are used by animals of conservation concern, such as wild camels. These results provide a useful reference for further revealing the behavior and ecological habits of wild camels and for promoting the conservation and management of imperiled wildlife by artificial measures.

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Temporal and spatial niche differentiation of sympatric black muntjac and Reeves’ muntjac

Juan HU, Peigen XIE, Tingting LI, Rui GUO, Lijuan XU, Xiao SONG, Aichun XU

2022, 42(6):  641-651.  DOI: 10.16829/j.slxb.150638

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Niche differentiation is an important ecological theory in explaining the coexistence of species. Schonenr believes that the spatial dimension has the highest influence on the formation of niche differences, followed by the nutritional dimension, and the time dimension is the last to be activated. To verify this hypothesis, we used the kilometer grid method to place 52 infrared cameras in the Longtangshan area of the Qingliangfeng National Nature Reserve in Zhejiang from December 2018 to November 2019. We monitored the populations of sympatric black muntjac and Reeves’ muntjac that have similar feeding habits. The average capture rate was calculated to analyze the differences in the species’ selection of vegetation type, altitude, slope position, and distance from water sources in different seasons. The nuclear density estimation method was used to analyze the daily activity rhythm and the degree of overlap in the activities of the two species. The results indicate that black muntjac and Reeves’ muntjac have different choices in spatial niche: black muntjac prefers mixed broadleaf-conifer forest, primarily inhabiting areas with high altitude between 1 301 - 1 500 m and avoiding areas with low altitudes and valleys. Activities of the black muntjac are frequent in areas closer to water sources. The Reeves’ muntjac prefers deciduous broadleaved forests, mainly inhabits areas with an elevation of 901 - 1 100 m, prefers mid-slope positions, avoids valleys, and has no obvious tendency towards choosing water sources. The black muntjac and the Reeves’ muntjac are both diurnal animals with morning and twilight activities, and the overlap of their daily activity rhythms throughout the year is relatively high (Δ4 = 0.86), and only lower in winter (Δ1 = 0.65). The above results support the hypothesis of Schonenr. First, spatial dimension has a greater impact on species niche differentiation than the temporal dimension. The black muntjac and Reeves’ muntjac in the Longtang Mountain area mainly choose different habitats to avoid overlapping territories and reduce the competition between both species. Secondly, there are seasonal differences in this model. In winter, due to the reduction of available resources, competition intensifies. Both species adjust their rhythm of daily activities to increase the degree of temporal niche differentiation in order to achieve coexistence in the same region.

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Diet conversions of pre-released giant panda (Ailuropoda melanoleuca) cubs

Shiqiang ZHOU, Shengshan HE, Yuanyuan QU, Yong LUO, Daifu WU, Yan HUANG, Desheng LI, Hemin ZHANG

2022, 42(6):  652-664.  DOI: 10.16829/j.slxb.150655

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This paper takes 15 giant panda cubs undergoing pre-release training, including female animals with cubs, monitored from 2010 to 2020 as the research object. Based on the behavior data observed and interpreted by infrared video monitoring system and audio collar, and the fecal sample data collected by GPS collar tracking and positioning, this paper analyzes the behavior development process and food conversion characteristics of giant pandas undergoing pre-release training. The results show that with the growth and development of giant pandas undergoing pre-release training, the behaviors related to foraging and vigilance are fully developed, and have a strong temporal correlation，including feeding, crawling, walking, playing with objects, climbing trees, biting and playing with bamboo, drinking water and eating bamboo. Generally, at the age of 8 ? 10 months, giant panda cubs begin to eat bamboo organs, and the process of developmental dietary transition is clearly divided into three stages: ready?to?eat milk period (1 ? 7 months old), breast milk bamboo conversion period (8 ? 28 months old) and bamboo eating period (29 ? 39 months old). The conversion period can be divided into critical period (8 ? 18 months old) and transition period (19 ? 28 months old). According to the statistical test, there are significant differences between different feeding stages, and the giant panda in the transition period can leave the mother animal and live independently in the study area. The proportions of food components in the transition period are not significantly different from that in the bamboo feeding stage. The seasonal dietary shift pattern of the wild training giant panda is similar to the mother animal with offspring and the wild giant panda in that is the main food is bamboo shoots in spring, young bamboo stems and leaves in summer and autumn, and bamboo leaves and stems in winter. The results of this study not only verify the scientific basis and feasibility of the pre-release training method of female animals with cubs, but also provide a reference for the pre-release training and reintroduction of captive giant pandas in the future.

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Utilization characteristics of wildlife on earthquake‑damaged sites based on camera-traps

Zhenshan GUO, Jinyan HUANG, Jin HOU, Jiao XIANG, Dian LIU, Jindong ZHANG

2022, 42(6):  665-676.  DOI: 10.16829/j.slxb.150660

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Earthquake and secondary geological disasters significantly affect the diversity and space use of wildlife. To investigate the utilization characteristics of wildlife on earthquake damage sites caused by earthquakes and secondary geological disasters, and provide basic data for biodiversity protection and the ecological recovery in post-earthquake, here we surveyed the mammal and bird species composition and their relative abundance index inside and outside earthquake-damaged sites of the Wolong Nature Reserve using camera-trap data. Based on 2 833 camera-days, we recorded 28 species (15 mammals and 13 birds) in earthquake-damaged sites, of which the animals with the highest frequency were herbivorous (those eating roots, leaves, and fruits) such as Chrysolophus pictus, Hystrix brachyura, and Naemorhedus griseus. 60% of the recorded animals are classified as endangered (EN), vulnerable (VU), and near threatened (NT) by the IUCN Red List. This indicates that rare wildlife used the earthquake-damaged sites in the process of recovery, and those earthquake-damaged sites have potential ecological meaning for rare wildlife. The species composition was apparently varied among weak, moderate, and severe damaged sites, and the relative abundance index (RAI) of animals was the highest in moderate damaged sites, followed by weak and severe damaged sites. The number of species and RAI of wild animals outside the earthquake-damaged sites are higher than inside. This shows the secondary geological disasters caused by the Wenchuan earthquake still influence wild animals’habitat selection and utilization. We suggest carrying out long-term monitoring on the wildlife utilization in those earthquake-damaged areas.

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The variations of nephrons and relevant function factors between hibernating and non-hibernating Daurian ground squirrels

Xiujing ZHANG, Heng WANG, Qiumei ZHONG, Chenxi YANG, Jianli WANG

2022, 42(6):  677-686.  DOI: 10.16829/j.slxb.150587

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Hibernation is an adaptive survival strategy through which the hibernating species copes with months of low ambient temperature and a lack of food. The Daurian ground squirrel (Spermophilus dauricus) is a typical fat-storing hibernator. To further investigate the renal adaptive mechanisms of hibernators, the nephronal morphology changes and the concentrations of serum creatinine, urine and antidiuretic hormone (ADH) were examined during summer active (July), winter hibernating (December), and early spring arousal (March) periods in the Daurian ground squirrel by the means of histology, blood biochemical analysis, and enzyme-linked immunosorbent assay. The gene expression of aquaporins (AQP1, AQP2,and AQP3), ADH receptor (V2R), and endothelial nitric oxide synthase (eNOS) were also examined by the means of real-time PCR. The density of glomerulus, relative diameter of distal tubules and proximal tubules, and ratio of corticomedullary proximal tubules to distal tubules were found to be lower during hibernating and arousal periods compared to active period. The concentration of serum creatinine and urine increased significantly during hibernating period compared to those during active and arousal periods. The serum ADH concentration and V2R gene expression level decreased significantly during hibernating period compared to those during active periods. The gene expression of AQP1 during hibernating period was higher than that during arousal period, and the AQP3 gene expression was lower than that during active period, while the AQP2 gene expression level did not change significantly. The eNOS gene expression during hibernating period was lower than that during arousal period. These results indicate that the Daurian ground squirrel lowered its renal function during hibernation. The aquaporins, eNOS, and ADH show functional adjustments to adapt to different periods. These results might provide a better understanding of the renal adaptation mechanism in hibernating animals.

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Vkorc1 polymorphism of two rodent species in different habitats

Xingen YANG, Yanlong WANG, Bo ZOU, Wenying CHANG, Yu HOU, Youyou ZHAO, Tinglin WANG, Jianxu ZHANG

2022, 42(6):  687-697.  DOI: 10.16829/j.slxb.150692

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To explore the polymorphism of vitamin K epoxide reductase complex subunit 1 gene (Vkorc1), which is closely related to the resistance to anticoagulant rodenticides in the long-tailed hamster (Cricetulus longicaudatus)and the Asian house rat (Rattus tanezumi),the mutation sites of Vkorc1 and their distribution were detected. In present study, samples were collected using the trapping methods from farms at 14 sites and agricultural fields at 13 sites. The exons of Vkorc1 were amplified and sequenced. The sequences were aligned using MEGA X to visually detect the mutation sites in exons and their distribution. The results showed that C. longicaudatus samples werecaptured in all the 13 sampling sites and accounted for 23.29% of wild rodents. R.tanezumi were distributed in 8 sampling sites, accounting for 68.63% of commensal rodents. Six silent mutation sites and 5 missense mutation sites in Vkorc1 were detected in C. longicaudatus samples (n = 105). Among them, silent mutation C438T (His146His) had the highest mutation rate of 67.62%. A total of 17 C. longicaudatus samples existed missense mutation sites. We found 6 silent mutation sites and 1 missense mutation site in R. tanezumi samples (n = 70). The mutation rates of the most common silent mutation sites A321C (Ile107Ile) and T411C (Thr137Thr) was up 18.57%. The missense mutation A416G (Tyr139Cys) associated with drug resistance was found in 8 R. tanezumi samples, of which 7 were captured from Xiaodian, Taiyuan, with a mutation rate of 35.00%. In conclusion, Vkorc1 mutations were detected both in anthropogenic habitats and natural ecosystems. We should strengthen the monitoring of R. tanezumi in Xiaodian, Taiyuan, since the formation of the resistant population.

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An investigation of brodifacoum resistance and Vkorc1 gene polymorphism in the Rattus norvegicus from Macao

Min GUO, Jie LIANG, Xiangyang HE, Weixin OU, Dingxiong PENG, Zhanzhao MAI, Haitao HUANG, Libiao ZHANG

2022, 42(6):  698-704.  DOI: 10.16829/j.slxb.150579

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The 2nd-generation anticoagulant rodenticides (ARs) are widely used for their higher eradicative rate and safety than the 1st-generation ARs. However, long-term use of the 2nd generation ARs could cause AR resistance in rats. Recently, researchers have reported resistance to the 2nd generation ARs bromadiolone and difenacoum in rats. Brodifacoum is a widely used 2nd-generation ARs of high toxicity that causes coagulation dysfunction and cytotoxicity in rats, but at present, the evolution of rat resistance against brodifacoum remains unclear. Macao has continuously used brodifacoum since 1995, allowing us to explore the development of rat resistance against brodifacoum. In this study, a total of 61 rats (Rattus norvegicus) were captured in Macao from October to December 2019. Among them, 44 rats were chosen to perform the LFP test (with 0.005% brodifacoum). The results showed that these rats consumed (15.28 ± 1.40) mg/kg (mean ± SE) brodifacoum on average, resulting in all of them dying within 7 days. Furthermore, we detected the nucleotide polymorphism of vitamin K-epoxide reductase complex 1 (Vkorc1) in all the 61 captured rats, and found none of the previously identified AR-resistant nonsynonymous mutations in Vkorc1 genes, but did detect 2 synonymous mutations [at amino acid locus 68: H (CAC)-H (CAT), mutation rate: 100%; and amino acid locus 82: I (ATA)-I (ATT), mutation rate: 32.72%]. The fact that none of the rats were brodifacoum-resistant suggests that no resistance propagated in R. norvegicus population after 25 years of use of brodifacoum in Macao. Nevertheless, persistent surveillance on the development of rat resistance to brodifacoum in the region is still needed.

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Distinct patterns of microsatellite and functional analysis of forest musk deer and its closely related species

Qi ZHAO, Qi ZHANG, Haoling LI, Yue LAN, Xingan YAN, Guijun ZHAO, Wenhua QI

2022, 42(6):  705-715.  DOI: 10.16829/j.slxb.150645

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Muscidae and Cervidae belong to artiodactyl ruminants and have important economic value. There is still a lack of relevant studies on using simple sequence repeats (SSRs) to reveal the phylogenetic relationship among species at the genomic level and to explore the gene functions of SSRs and their enriched signaling pathways. With the completion of the genome sequence of the forest musk deer (Moschus berezovskii), Siberian musk deer (Moschus moschiferus), the red deer (Cervus elaphus), the Reeves’ muntjac (Muntiacus reevesi), and the red muntjac (Muntiacus vaginalis), we extracted the coding sequences (CDS) of these species by bioinformatics method and analyzed the distribution patterns of coding SSR and their biological functions. The containing-SSR genes were enriched in the signal pathways and their association with disease were explored. The results prove that the proportion of their coding SSRs were 6.96% (1 696), 7.18% (2 359), 7.29% (3 005), 7.36% (1 916), and 7.48% (1 924), respectively. In addition, the distribution pattern of coding SSRs of the five species was similar, triplet repeats SSR (Tri- and Hexa-SSRs) of the five species were the most similar, which were 96.85%, 94.87%, 65.44%, 64.23%, and 88.04%, respectively. The GO functional enrichment showed that the SSR sequences in the CDS of the five species had many same enriched functions in three aspects: molecular function, cellular component, and biological process, including DNA binding, chromatin, growth, and development. The result of the KEGG pathway enrichment analysis showed that there are 7 KEGG pathways that were significantly co?enriched in forest musk deer and other species.These include protein families: genetic information processing, transcription factors, chromosome and associated proteins, spliceosome, transcription machinery, Notch signaling pathway, and maturity?onset diabetes of the young. By analyzing the SSR-containing key immune genes and their associated KEGG pathways in the CDS region of forset musk deer, 10 SSR-containing key immune genes corresponding to the KEGG pathway were found to be closely associated with the disease.

REVIEWS

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An overview of population survey methods of non-human primates

Xier CHEN, Lijie YIN, Dagong QIN, Jinxian YAO, Xiaoyu LI, Wenshi PAN

2022, 42(6):  716-727.  DOI: 10.16829/j.slxb.150656

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Monitoring and estimating wildlife population size is essential to conservation. Affected by global climate change and human activities, wildlife populations could be relatively unstable. Primates are a group of highly evolved taxa in the animal kingdom and are among the most social of animals. As many as 701 species or subspecies of primates are recognized globally, forming a rich diversity. They could be found in various types of habitats, including rain forests, swamp forests, mangroves, secondary forests, deciduous forests, monsoon forests and montane forests, as well as in grasslands (savannah and steppe) including forest outliers, gallery forests, wooded steppes, thorn forests, Mediterranean scrubs and montane meadows, and even in deserts, dry uplands or permanent snow. Most primate species are endangered from different causes, and therefore effective long-term monitoring is of significant value to primate conservation. Species and habitat diversity have contributed to the numerous methods of censusing primate populations. This article offers a summary of widely-used non-human primate population censusing methods, including the classifications, the fundamentals, the various scenarios for application, and their limitations. The methods are analyzed with case studies and research. Furthermore, we introduce the latest applications of drones, thermal imaging and computer deep learning in primate population surveys, hoping to offer some insights into future non-human primate censusing and population monitoring.

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Advances and prospects in germplasm preservation of non-human primates

Mingwen LI

2022, 42(6):  728-740.  DOI: 10.16829/j.slxb.150626

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Non-human primates are an important part of the biodiversity and valuable laboratory animals for biomedical research, however, wild populations of many non-human primate species have declined alarmingly, even on the brink of extinction, due to human activities, habitat destruction, hunting, and genetic isolation. Germplasm preservation is of great significance to the rescue of non-human primates and preservation of genetic materials. This article reviews research progresses in cryopreservation of sperm, oocytes, embryos, and gonadal tissues in the groups of New World monkeys, Old World monkeys, and great apes, and introduces the main methods of germplasm preservation in marmosets, squirrel monkeys, rhesus monkey, cynomolgus monkeys, and chimpanzees. The future research directions of non-human primate germplasm preservation are also discussed.

SCIENTIFIC NOTES

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Analysis of the Père David’s deer population mortality in Dafeng Milu National Nature Reserve

Yijun REN, Daming SUN, Junai ZHEN, Libo WANG, Yumeng ZHAO, Hua SHEN, Bin LIU, Yuqing CHEN

2022, 42(6):  741-748.  DOI: 10.16829/j.slxb.150631

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From 2009 to 2020, we systematically investigated the population, mortality, and death factors of Père David’s deer (Elaphurus davidianus) in the Dafeng Milu National Nature Reserve, Jiangsu, China. The result showed the annual growth rate of the population was 13.09% ± 5.96%, which continuously increased in the 12 years. The annual mortality rate was 3.53% ± 2.27%, with an obvious fluctuation every 2 years. There was no significant difference in mortality of adults and sub-adults in different seasons, but significant in juveniles.Significant differences in mortality among different age groups were observed. The adults died most in summer and autumn, while the juveniles died most in winter and spring. 48.77% of subjects tend to choose the underbrush for dying. The death factors among different age groups were significantly different. The elders and the juveniles mainly died of epidemic diseases, including viral, bacterial, and parasitic. While the sub-adults died in accidents. We suggested that it is necessary to strengthen the daily monitoring and epidemic disease prevention in wildlife management. Our data provided important information for the protection of Père David’s deer in Dafeng Reserve.