Shennongjia National Nature Reserve Research Articles

Six new species of Chelipoda (Diptera: Empididae) from Shennongjia, China

Only three species of Chelipoda were known to occur in Shennongjia National Nature Reserve. The following six species are described as new to science: C. biancistroides sp. nov., C. conica sp. nov., C. curva sp. nov., C. digitiformis sp. nov., C. dorsispina sp. nov. and C. trifurcata sp. nov. A key to separate these species is presented.

Dicranum shennongjiaense W.Z.Huang & R.L.Zhu (Dicranaceae, Bryophyta), a new species from Central China supported by morphological and molecular evidence

ABSTRACT Introduction Dicranum Hedw. is one of the most taxonomically challenging genera of mosses, having 93 accepted species worldwide. Although recent integrative taxonomic revisions have clarified the delimitation of most species within this genus, the circumscriptions of some Dicranum species remain unsolved. During our recent survey of Dicranum in China, an intriguing species with an unknown combination of morphological traits was discovered in the Shennongjia National Nature Reserve, Central China. We carried out a study to provide morphological and phylogenetic evidence with which to determine the taxonomic status of this Chinese species. Methods The phylogenetic evidence was obtained through the combined analysis of five loci (rps4–trnT, trnL–trnF, trnH–psbA, rps19–rpl2 and rpoB) and one nuclear region (nrITS1–5.8S–ITS2). Morphological characteristics were investigated by microscopic examination of specimens. Key results and conclusions A new moss species, Dicranum shennongjiaense W.Z.Huang & R.L.Zhu, is described and illustrated based on molecular and morphological evidence. This new species is characterised by its falcate leaves, rectangular and elongated laminal cells with strongly protruding upper angles on the dorsal side in the upper leaf portion, irregularly bistratose laminal cells above the midleaf, one layer of guide cells in the costa, and sharp serrations on the dorsal side of the costa in the upper leaf portion. Additionally, D. baicalense Tubanova, previously known only from Russia, is newly reported for China. A key for identification of the Chinese species of Dicranum sect. Dicranum is provided.

Epidemiological Survey and Risk Factor Analysis of 14 Potential Pathogens in Golden Snub-Nosed Monkeys at Shennongjia National Nature Reserve, China

Golden snub-nosed monkeys (Rhinopithecus roxellanae) belong to Class A, the highest level of endangered primate species. Exploring the infection status of potential pathogens in golden snub-nosed monkeys is important for controlling associated diseases and protecting this species. The objective of this study was to investigate the seroprevalence for a number of potential pathogens and the prevalence of fecal adenovirus and rotavirus. A total of 283 fecal samples were collected from 100 golden snub-nosed monkeys in December 2014, June 2015, and January 2016; 26 blood samples were collected from 26 monkeys in June 2014, June 2015, January 2016 and November 2016 at Shennongjia National Reserve in Hubei, China. The infection of 11 potential viral diseases was examined serologically using an Indirect Enzyme-linked Immunosorbent Assay (iELISA) and Dot Immunobinding Assays (DIA), while the whole blood IFN-γ in vitro release assay was used to test tuberculosis (TB). In addition, fecal Adenovirus and Rotavirus were detected using Polymerase Chain Reaction (PCR). As a result, the Macacine herpesvirus-1 (MaHV-1), Golden snub-nosed monkey cytomegalovirus (GsmCMV), Simian foamy virus (SFV) and Hepatitis A virus (HAV) were detected with the seroprevalence of 57.7% (95% CI: 36.9, 76.6), 38.5% (95% CI: 20.2, 59.4), 26.9% (95% CI: 11.6, 47.8), and 7.7% (95% CI: 0.0, 84.2), respectively. Two fecal samples tested positive for Adenovirus (ADV) by PCR, with a prevalence of 0.7% (95% CI: 0.2, 2.5), and further, the amplification products were sequenced. Phylogenetic analysis revealed that they belonged to the HADV-G group. However, other pathogens, such as Coxsackievirus (CV), Measles virus (MeV), Rotavirus (RV), Simian immunodeficiency virus (SIV), Simian type D retroviruses (SRV), Simian-T-cell lymphotropic virus type 1 (STLV-1), Simian varicella virus (SVV), Simian virus 40 (SV40) and Mycobacterium tuberculosis complex (TB) were negative in all samples. In addition, a risk factor analysis indicated that the seroprevalence of MaHV-1 infection was significantly associated with old age (≥4 years). These results have important implications for understanding the health status and conservation of the endangered golden snub-nosed monkey population at Shennongjia Nature Reserve.

Geum sunhangii (Rosaceae), a new species from Hubei Province, China.

Geum sunhangii – first discovered in Shennongjia National Nature Reserve, Hubei Province, China – is described as a new species of Rosaceae. Compared to all known Chinese Geum species, the new species differs by possessing jointed styles, imbricate petals and a reniform radical leaf terminal leaflet. Most significantly, the jointed style is curved at an obtuse or a right angle. In addition, the inclusion of this species within the genus Geum was supported by phylogenetic analysis using the sequence data of a nuclear ribosomal internal transcribed spacer (nrITS) and a chloroplast trnL–trnF intergenic spacer. The new species was found to be closely related to G. rivale and G. aleppicum.

<p><strong>A new species of <em>Craterium</em> (Myxomycetes, Physaraceae) growing on living grass and new records of the genus from China</strong></p>

A new species of Craterium (C. subpurpurea) collected in the Changbai Mountain National Nature Reserve, Jilin Province, northeastern China, is described. The fruiting bodies of C. subpurpurea are long cylindrical with distinct ridges, with large spinulose spores (8–10 μm diam.) as well as a persistent purplish pale peridium at the base of the sporotheca. A newly described species, C. aureonuleatum, has been documented in China for the first time, based on material collected from the Shennongjia National Nature Reserve, Hubei Province and the Gexigou National Nature Reserve, Sichuan Province. Craterium aureonuleatum is characterized by a yellowish pseudocolumella at the apex of the sporocarp and a persistent cup-like peridium when mature. Descriptions and scanning electron micrographs for these members of the genus Craterium are provided.

Three new Coccomyces species from Shennongjia National Nature Reserve in China

Shennongjia National Nature Reserve is an old-growth forest in China with high biodiversity. But only three species in Rhytismataceae had been reported here. Based on morphological and molecular evidence, specimens of Coccomyces collected in Hubei were proposed here as three new species, named Coccomyces fagicola, C. quercicola, and C. shennongjiaensis. Phylogenetic analyses were inferred based on combined nuclear large subunit ribosomal DNA (nrLSU) and mitochondrial small subunit ribosomal DNA (mtSSU) as well as internal transcribed spacer (ITS).

Lichen as a Biomonitor for Vehicular Emission of Metals: A Risk Assessment of Lichen Consumption by the Sichuan Snub-Nosed Monkey (Rhinopithecus roxellana)

Two lichen species, Usnea aciculifera and Usnea luridorufa, were used as biomonitors for the deposition of traffic-related metals in China's Shennongjia National Nature Reserve. The suitability of the two lichen species for use as biomonitors was compared. The health threat to the Sichuan snub-nosed (aka golden) monkey (Rhinopithecus roxellana) from consuming lichen with elevated metal concentrations due to vehicular traffic was then assessed. Lichens, with large surface areas and neither roots nor stomata, efficiently absorb both particulate and gaseous air pollutants. The resulting data was used to assess the effect of heavy metal accumulation on the lichens as well as the health risk imposed on the monkeys as lichen is a primary food source. Lichen samples were collected in the core area of the reserve at three locations of varying traffic intensity. A forth site in the reserve, with no proximate traffic, was used as the control. Results show: (1) lichen from high traffic sites has significantly higher concentrations of Fe, Cd, Pb Zn, and Cr than lichen collected from the control site; (2) vehicular traffic is the primary source of metals in lichen; (3) U. luridorufa collected at high traffic sites displayed decreased photosynthetic efficiency, an indication of stress; (4) intake of Cd and Pb from vehicle emissions in the Shennongjia National Nature Reserve could adversely affect snub-nosed monkey health. This research advances the science of biomonitoring, contributes to environmental protection efforts in China's nature reserves and helps improve food safety for Sichuan snub-nosed monkey, a national treasure of China.

Evaluating the effectiveness of Shennongjia National Nature Reserve based on the dynamics of forest carbon pools

Evaluating the effectiveness of Shennongjia National Nature Reserve based on the dynamics of forest carbon pools

Identification of Atypical Enteropathogenic Escherichia coli O98 from Golden Snub-Nosed Monkeys with Diarrhea in China.

Fecal samples (n = 76) were collected from 38 snub-nosed monkeys (Rhinopithecus roxellana) in Shennongjia National Nature Reserve (China) and examined for the presence of enteropathogenic Escherichia coli (EPEC). The 56 samples originated from 30 free-ranging monkeys on the reserve and 20 samples from 8 captive monkeys that were previously rescued and kept at the research center. Eight diarrhea samples were collected from four of the eight captive monkeys (two samples from each monkey), and two EPEC strains (2.6%) (95% confidence interval 0.3–9.2%) were isolated from two fecal samples from two diarrheic monkeys. Both strains belonged to serotype O98 and phylogenetic group D (TspE4C2+, ChuA+). The virulence gene detection identified these strains as an atypical EPEC (aEPEC) (bfpB–, stx1–, and stx2–) with the subtype eae+, escV+, and intiminβ+. These strains were highly sensitive to all the antibiotics tested. The lethal dose 50% of the two isolates in Kunming mice was 7.40 × 108 CFU/0.2 mL and 2.40 × 108 CFU/0.2 mL, respectively, indicating low virulence. Based on the report that this serotype had been isolated from some other non-human animals and humans with diarrhea, the first identification of aEPEC O98 strains and their drug resistance profile in R. roxellana is of ecological significance for disease control in this endangered species.

A new Stemonitis species and a new record of Elaeomyxa from China

A new species, Stemonitis planusis, was collected in Shennongjia National Nature Reserve, Hubei Province, China; it has larger sporocarps that usually end in a plane at the apex of the sporotheca, and its capillitia are expanded at the axils. Additionally, Elaeomyxa Hagelst. was documented for the first time in China; E. miyazakiensis (Emoto) Hagelst. was identified based on material collected from Dasu Forest, Fushun City, Liaoning Province, China. This newly recorded species is characterised by the wax in its stalk, peridium, and capillitium, and spores (approximately 7–8 μm in diam.) marked with rows of warts. A description and scanning electron micrographs of the collected Elaeomyxa and Stemonitis are provided. All specimens are deposited in the Herbarium of the Mycological Institute of Jilin Agricultural University (HMJAU), Changchun, China.

The effectiveness of Shennongjia National Nature Reserve in conserving forests and habitat of Sichuan snub-nosed monkey

The effectiveness of Shennongjia National Nature Reserve in conserving forests and habitat of Sichuan snub-nosed monkey

Koenigia hedbergii (Polygonaceae: Persicarieae), a distinct new species from Shennongjia National Nature Reserve, Central China

Koenigia hedbergii, a new and distinct species collected from the Shennongjia National Nature Reserve in the Northwest of Hubei Province (central China) is described and illustrated. The new species can be easily distinguished from other Koenigia species by its leaves lanceolate or lanceolate-ovate each showing 6–11 pairs of lateral veins and with distinct undulate margins, by its ocreae glabrous but sparsely puberulent at the bases, and achenes sharply trigonous with three pronouncedly keeled edges. A morphological comparison among the new species and the related ones, K. nepalensis and K. pilosa, is presented. The Koenigia-type pollen grains of the the new species were also observed and described.

Age-sex analysis for the diet of Sichuan snub-nosed monkeys (Rhinopithecus roxellana) in Shennongjia National Nature Reserve, China.

Age-sex differences in diet have been reported in many nonhuman primates, and body size, reproductive costs, and growth are three mutually non-exclusive factors often proposed to explain such differences. Smaller animals tend to feed on high quality foods (high in protein/energy) more often than larger animals due to their higher metabolic requirements per body weight. Animals of different sizes tend to use different substrate levels, leading to dietary differences if food resources are unevenly distributed along substrate levels. Adult females and juveniles experience additional metabolic requirements for reproduction and growth, respectively, and tend to feed on high quality foods more frequently than adult males. We conducted an age-sex analysis for the diet of Sichuan snub-nosed monkeys (Rhinopithecus roxellana) in Shennongjia, China. In spite of general age-sex similarities, we found that adult males ate herbs more frequently than juveniles and adult females, most likely because they were more terrestrial. As predicted, juveniles ate high quality foods (young leaves, fruits, seeds, and buds) more frequently, and meanwhile ate low quality foods (barks and lichens) less frequently than adult males across the study year or in some seasons when these food types were eaten. However, we found high similarities in diet between adult females and adult males. The most likely reason was that the low diversity of food sources and strong phenological synchrony did not allow adult females to select foods based on quality to cope with their higher metabolic constraints compared to adult males. Surprisingly, the only sex difference in diet except herbs was that adult females ate lichens more frequently in autumn. One plausible reason was that lactating females experienced their highest metabolic requirements in the middle period of infant care (autumn), and had to disproportionately increase the intake of lichens due to the limited availability of plant foods.

Somatochlora shennong sp. nov. from Hubei, China (Odonata: Corduliidae).

A new species, Somatochlora shennong sp. nov. (holotype ♂, Dajiuhu National Wetland Park in Shennongjia National Nature Reserve, Hubei Province, China, 9 August 2012) is described, illustrated, and compared with the related species S. dido Needham and S. taiwana Inoue & Yokota.

Impacts of climate change on the distribution of Sichuan snub-nosed monkeys (Rhinopithecus roxellana) in Shennongjia area, China.

Understanding the effects of climate change on primate ranging patterns is crucial for conservation planning. Rhinopithecus roxellana is an endangered primate species distributed in mountainous forests at the elevation of 1500-3500 m a.s.l. in China. Our study site, the Shennongjia National Nature Reserve, represents the eastern-most distribution of this species. This area has experienced significant habitat loss and fragmentation because of human population growth, increased farming and logging, and climate change. To estimate how changes in temperature and rainfall will affect the presumed future distribution of this species, we examined eco-geographic factors including bioclimate, habitat (vegetation type, landcover, etc.), topography, and human impact (human population, gross domestic product, etc.), and provide suggestions for management and conservation. We used a maximum entropy approach to predict the location and distribution of habitats suitable for R. roxellana in the present, 2020, 2050, and 2080 based on 33 environmental parameters, three general circulation models, three emissions scenarios, and two dispersal hypotheses. According to the ensemble modeling, we found range reductions of almost 30% by 2020, 70% by 2050, and over 80% by 2080. Although no obvious differences were found in distribution change based on full and zero dispersal assumptions, our results revealed range reductions in response to elevational, latitudinal, and longitudinal gradients, with the monkeys forced to migrate to higher elevations over time. Bioclimte factors, such as temperature, precipitation, evapo-transpiration, and aridity condition, were dominant contributors to range shifting. As habitat loss due to human influence and climate change is likely to be even more severe in the future, we considered three conservation hot-spots in the Shennongjia area and recommended: (i) securing existing reserves and establishing new reserves, (ii) re-designing management systems to include the Shenongjia reserve and the surrounding reserves and highlighting ecosystem protection at higher elevations, and (iii) using finer-scale research to guide the conservation planning and education in order to enhance protection and awareness in the local community. National and provincial conservation policies should integrate projections of climate change in making effective conservation strategies.

Aeshna shennong sp. nov., a new species from Hubei Province, China (Odonata: Anisoptera: Aeshnidae).

Aeshna shennnong sp. nov. (holotype male: Dajiuhu national wetland park in Shennongjia National Nature Reserve, Shennongjia City, Hubei Province, China, 28. VIII. 2013) is described, illustrated and compared with its most similar congener, A. petalura Martin, 1908. The holotype will be deposited in the Collection of Aquatic Animals, Institute of Hydrobiology, Chinese Academy of Sciences, Wuhan City, Hubei Province, China. New distribution records of A. petalura from mainland China are also provided.

Foods Eaten by the Sichuan Snub‐Nosed Monkey (Rhinopithecus roxellana) in Shennongjia National Nature Reserve, China, in Relation to Nutritional Chemistry

The diet of Rhinopithecus roxellana is characterized by lichens, which are available year-round and an uncommon food source for nonhuman primates, supplemented by seasonal plant foods. We present the first study of foods eaten by R. roxellana in relation to nutritional chemistry in Shennongjia National Nature Reserve, Hubei Province, China. We analyzed the nutrients (crude protein, crude fat, and water soluble carbohydrate [WSC]) and feeding deterrents (crude fiber, condensed tannin [CT], and total phenolic [TP]) of 111 parts from 53 plant species and of 6 lichen species. Results showed that lichens were a good choice for R. roxellana living in habitats with limited and seasonally available plant foods. They contained higher concentrations of WSC than foliage, fat concentrations equivalent to those in plant parts (except fruits/seeds), and lower concentrations of fiber than mature leaves, flowers, and fruits. Although lichens were lower in protein than plant parts (except fruits), the monkeys could likely meet their protein requirement by eating seasonal plant foods rich in protein, including foliage, flowers, buds, and seeds. The monkeys were not observed to select foliage higher in protein, but appeared to select mature leaves higher in WSC and lower in fiber. Fruits were a good source of WSC and fat, and seeds were a good source of fat. Neither CT nor TP content showed negative effects on the selection of mature leaves or lichens.

Three newCephalaeschnaspecies from central China with descriptions of the hitherto unknown sex of related species (Odonata: Aeshnidae)

Three new Cephalaeschna species, C. discolor sp. nov. (holotype male; Shennongjia National Nature Reserve, Shennongjia City, Hubei province, China, 16 August 2012), C. mattii sp. nov. (holotype male; Lujiahe River, Zigui County, Hubei province, China, 18 September 2012) and C. solitaria sp. nov. (holotype male; Dalongtan in Shennongjia National Nature Reserve, Shennongjia City, Hubei province, China, 19 July 2012) are described, illustrated in color and compared with the known Chinese Cephalaeschna. All the holotypes are deposited in the Collection of Aquatic Animals, Institute of Hydrobiology, Chinese Academy of Sciences, Wuhan City, Hubei Province, China. The hitherto unknown male of C. obversa and female of C. patrorum are also described and illustrated. Brief notes on biology of each species are also provided.

Effect of Group Size on Time Budgets of Sichuan Snub-Nosed Monkeys (Rhinopithecus roxellana) in Shennongjia National Nature Reserve, China

Group size influences intragroup scramble competition, which in turn influences time budgets in some primates, and may impact age–sex classes differently. There is a great deal of debate about whether folivorous primates, e.g., colobines, experience significant feeding competition. Unlike most colobines, Sichuan snub-nosed monkeys (Rhinopithecus roxellana) live in extraordinarily large groups and eat mainly lichens supplemented by seasonal plant food. We examined the effect of group size on time budgets in this species by studying two groups of different sizes in the same habitat in Shennongjia National Nature Reserve, China (study periods: August 2006–July 2008 for the larger group, November 2008–July 2009 for the smaller group). Results showed that the distribution of activities throughout the day did not differ between groups, but that time budgets did differ. Specifically, the monkeys spent more time moving and less time resting in the larger group than in the smaller group. Intergroup comparisons for each age–sex class indicated that adult females (but not adult males or juveniles) in the larger group spent more time moving and less time resting, and tended to spend more time feeding compared to those in the smaller group. The results suggested that increased scramble competition was occurring for adult females in the larger group. We provided preliminary evidence for the existence of intragroup scramble competition in Rhinopithecus roxellana.

Parasitoids of the Sawfly,Arge pullata, in the Shennongjia National Nature Reserve

Larvae of the argid sawfly, Arge pullata (Zaddach) (Hymenoptera: Argidae), feeds on leaves of birch (Betula spp.) in China, Europe, Siberia, and Japan. Parasitoids of A. pullata were studied in Shennongjia National Nature Reserve, Hubei Province, China, in 2009 and 2010. Five parasitoid species were found: Pleolophus suigensis (Uchida), Mastrus nigrus Sheng, Endasys parviventris nipponicus (Uchida) (Hymenoptera: Ichneumonidae), Vibrissina turrita (Meigen) (Diptera: Tachinidae) and Conura xanthostigma (Dalman) (Hymenoptera: Chalcididae). The average parasitism rate of A. pullata by parasitoids was as high as 11.0%. V. turrita was the dominant species, attacking 10.0% of the A. pullata cocoons. The emergence peak of V. turrita was from late May to early June. Three hyperparasitoids of V. turrita emerged from cocoons of A. pullata: Mesochorus ichneutese Uchida (Hymenoptera: Ichneumonidae), Pediobius sp. (Hymenoptera: Eulophidae), and Taeniogonalos maga (Teranishi) (Hymenoptera: Trigonalidae). Hyperparasitism rates were about 1.0% to 3.0%, with an average rate of 1.7%.