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30 November 2021, Volume 41 Issue 6

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ORIGINAL PAPERS

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Seasonality of abundant and rare taxa in gut microbiota of plateau pikas

FAN Chao, ZHANG Liangzhi, FU Haibo, LIU Chuanfa, LI Wenjing, ZHANG He, TANG Xianjiang, CHENG Qi, SHEN Wenjuan, ZHANG Yanming

2021, 41(6):  617-630.  DOI: 10.16829/j.slxb.150540

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Climate and diet are important factors driving seasonal changes in gut microbiota of small herbivorous mammals. However, most previous studies rarely addressed abundant and rare taxa in gut microbiota. Here, we used plateau pika (Ochotona curzoniae) as a model and conducted 16S rRNA gene-based large-scale structural profiling to explore the seasonal differences (spring, summer, autumn, and winter) in microbial composition, diversity, and function in abundant and rare taxa. The results showed that the Shannon index of abundant and rare taxa was significantly higher in winter than in other seasons. However, the ACE index of abundant taxa was significantly lower in autumn than in other seasons while that of rare taxa was significantly higher in winter than in spring and summer. For the abundant taxa, the relative abundance of Bacteroidetes in winter and autumn was significantly higher than that in spring and summer, while for the rare taxa, the relative abundance of Bacteroidetes in summer and autumn was significantly higher than that in winter and spring. The relative abundance of the amino acid metabolism pathway in abundant taxa was significantly higher in winter than that in spring and summer, while the relative abundance of this pathway in rare taxa was significantly higher in spring than that in summer and autumn. Air temperature, precipitation, and vegetative nutrition were significantly associated with variations in the microbial composition of both abundant and rare taxa. The total explanation proportions of environmental variables to the changes of abundant and rare taxa were 18% (air temperature:3%; precipitation:4%; vegetative nutrition:10%; combined:1%) and 9% (air temperature:1%; precipitation:2%; vegetative nutrition:5%; combined:1%), respectively. The results indicate that abundant and rare taxa of gut microorganisms have different distribution patterns, seasonal characteristics, and contributions to the entire microbial variation. The abundant taxa were more strongly influenced by environmental variables, reflecting the inconsistency in responses of different gut microbial taxa to seasonal changes. This study promotes our understanding of seasonal processes and environmental adaptability of animal's gut microbiota.

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Discussion on the taxonomy and distribution of the Micromys Dehne, 1841 in China

PEI Xiaoxin, QU Weiying, ZHANG Min, SHAO Jiangshan, FANG Lei, CHEN Zhongzheng

2021, 41(6):  631-640.  DOI: 10.16829/j.slxb.150554

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Micromys Dehne, 1841 is part of the Muridae family and is one of the smallest rodents. Previous studies have shown that the genus consists of two species, M. minutus and M. erythrotis. However, due to the lack of data, the species status of M. erythrotis is still controversial, and the geographical distribution of the two species in China is uncertain. In this study, a number of specimens of the genus Micromys were recently collected from Qingliangfeng National Nature Reserve in Anhui Province. They were identified as M. minutus and M. erythrotis based on morphology and molecular analyses. Both species occur in sympatry at altitude 1 600 m in Qingliangfeng. Our findings therefore support the species status of M. erythrotis. Based on the morphological characteristics of the M. minutus and M. erythrotis individuals collected in Qingliangfeng, we analyzed the photos of Micromys specimens housed in the National Animal Collection Resource Center and, combined with the data available in the literature, reorganized the geographical distribution of the genus Micromys in China and provided updated distribution maps. The results showed that M. minutus is mainly distributed in Heilongjiang, Jilin, Liaoning, Inner Mongolia, Hebei, Shaanxi, Gansu, Xinjiang, Jiangsu, Anhui, Zhejiang, Hunan, Jiangxi, Guangdong, Fujian and Taiwan. M. erythrotis is mainly distributed in Yunnan, Sichuan, Shaanxi, Hubei, Tibet, Guizhou, Chongqing, Anhui, Fujian and Guangxi. Qingliangfeng in Anhui Province and Zhenba and Chenggu counties in Shaanxi Province are the overlapping distribution areas of the two species. In addition, the results of the molecular phylogenetic analysis show that the diversity of the genus is still underestimated in China and it is very likely that there are undescribed taxa in the genus.

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Habitat utilization and spatial patterns of pre-released giant panda (Ailuropoda melanoleuca)

ZHOU Yanshan, HOU Rong, LIU Jiabin, BI Wenlei, Jacob R. Owens, ZHANG Zhihe, HUANG Feng, LUO Wei, QI Dunwu

2021, 41(6):  641-648.  DOI: 10.16829/j.slxb.150457

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Understanding the habitat and space utilization patterns of wildlife provides a foundation for designing effective strategies for successful conservation translocations. To clarify these patterns in captive born giant pandas (Ailuropoda melanoleuca) being prepared for the wild, the movement data of two pre-released individuals with GPS collars were studied in the Liziping National Nature Reserve. The GPS data were extracted and calculated using animal movement module in the geographic information system (GIS) through a digital elevation model (DEM). We found the following results:the two giant pandas gradually migrated from the broad-leaved forest on the southwest slopes of low altitude areas to the mixed coniferous and broad-leaved forests on the high altitude southern slopes. There were significant differences in the slope selection of the two giant pandas, but both of them tended to choose the gentle areas with a slope of 17°-20°. The average daily movement distance of the two giant pandas gradually decreased through the study, then stabilized with time spent in the wild habitat. Their home ranges were also significantly different both within any given month and throughout the study duration. Both individuals had several primary use patches of varied areas and distances between each site, which indicated that the pre-released giant pandas had an unstable random selection mode in the initial stage of acclimation to the wild habitat.

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Food composition and nutrients of wild Tibetan macaques (Macaca thibetana) in winter

LIU Chao, LI Wenbo, LI Bowen, YANG Peipei, XIA Dongpo, LI Jinhua

2021, 41(6):  649-657.  DOI: 10.16829/j.slxb.150551

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Foraging is an important way to obtain nutrients and energy. Low temperature and relatively scarce food resources in winter are the bottleneck period for primates survival and growth. In order to explore food composition and the influence of chemical components on feeding of wild Tibetan macaques (Macaca thibetana) at Mt. Huangshan in winter. We collected from November 2019 to January 2020 foraging data of monkeys using instantaneous scan sampling method and analyzed the chemical constituents of plant samples. The results showed that the wild Tibetan macaques fed on 34 plant species of 23 families during the winter. Fagaceae (21. 62%), Lauraceae (17. 57%) and Rosaceae (8. 11%) were the main consumed families, Feeding parts were dominated by leaves (66. 22%) and fruits/seeds (24. 32%). There were significant differences in water, total sugar, starch, fat and tannin content among different feeding parts. The water content in leaves was higher than in fruits/seeds, stems and buds. Stems and fruits/seeds contained higher total sugar. The starch and fat content in fruits/seeds and the tannin content in buds were the highest. We also found that the wild Tibetan macaques tended to feed on plants with higher total sugar content in winter. Our research indicated that the foraging strategy of wild Tibetan macaques adapted to cold winter and food scarcity is a comprehensive result of plant species, plant parts and their main nutrients.

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The cooperative food hoarding behaviors of Brandt's voles and their influencing factors

SONG Yiran, LI Guoliang, ZHANG Zhibin

2021, 41(6):  658-666.  DOI: 10.16829/j.slxb.150546

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Food hoarding is a crucial strategy to cope with the seasonal shortage of food resources in many social animals, but the underlying ecological mechanisms remain unclear. In this study, Brandt's voles were divided into kin group (from the same family) and non-kin group (from different families). We used video camera to record the cooperative food hoarding patterns of different groups and individuals in experimental boxes, and calculated the time of different behaviors. We used correlation analysis to study the association between cost and benefit for cooperative food hoarding individuals, and its influencing factors. We found, as compared to the non-kin group, Brandt's voles in the kin group spent more time on cooperative food hoarding behavior. However, cooperative food hoarding behavior differed greatly among individuals in the same kin group. There was a significant negative correlation between time of hoarding food and time of eating food by voles. Voles with more time of hoarding food showed a significant decrease in testicle index and testosterone content. Our study suggests that kinship is essential for maintaining cooperative food hoarding in voles, but the reproduction of cooperators who largely contributed to food hoarding was inhibited.

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Effects of seed coat thickness on rodents' seed dispersal behavior and seed fate

ZHU Yunlong, YANG Xifu, GU Haifeng, TENG Yuwei, ZHANG Zhibin

2021, 41(6):  667-675.  DOI: 10.16829/j.slxb.150555

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Seed dispersal is an important strategy for seed regeneration and distribution expansion of plants. Rodents adopt different seed dispersal and hoarding strategies in response to food shortages, which also promote seed dispersal. Seeds have evolved a series of traits, such as physical and chemical defenses in response to overfeeding by rodents. Seed coat thickness, as a physical defense strategy, is a key factor affecting the hoarding behavior of rodents and seed fates. However, there is still a lack of effective methods to artificially simulate seed coat thickness. In this study, by removing the coat of natural Quercus variabilis seeds, and then wrapping the seed kernels with different layers of polyethylene plastic, we aimed to accurately control the artificial seed coat thickness of the seed coats. The effects of seed coat thickness on seed dispersal and seed fate of artificially simulated seeds were investigated in the forests of the Dujiangyan region, Sichuan Province of China, from October 2020 to January 2021. We found that:(1) rodents preferred to disperse artificial seeds with the thinner coat (covered with 1 layer of polyethylene film); with the increase of seed coat thickness, the seed removal rate gradually decreased; the seeds with the thickest coat (covered with 6 layers of polyethylene film) had the slowest removal rate (P < 0. 001); (2) Rodents preferred to scatter-hoard seeds with 1 and 2 layers of polyethylene film. When the coat thickness increases to 4 and 6 layers of polyethylene film, the proportion of scatter-hoarded was significantly reduced (P < 0. 05); (3) Rodents preferred to larder-hoard seeds with 4 layers of film, compared to seeds covered with the other layers of polyethylene film (P < 0. 05); (4) There was no significant difference in seed dispersal distance among seeds with different seed coat thickness (P > 0. 05); (5) Seeds with thinner coat thickness (1 layer of film) had a higher proportion of scatter-hoarding within 3 m. The use of polyethylene film wrapping is a feasible method for simulating the seed coat, and could be used to evaluate the impact of the thickness of the seed coat on the hoarded behavior of rodent seeds and the fate of seeds.

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The effects of coccidian infection and predators on reproductive performance of root vole (Alexandromys oeconomus)

YANG Yuangang, SHANG Guozhen, BIAN Jianghui

2021, 41(6):  676-684.  DOI: 10.16829/j.slxb.150547

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In nature, predators and parasites are two major extrinsic population regulators, their interaction can play important roles on the prey/host population dynamics. However, some studies found that coccidia with lower infection intensity and predators have no significant interactive effects on the reproduction of root voles (Alexandromys oeconomus). In the wild, coccidian infection in root voles has seasonal variation, and their infection peak of prevalence and intensity occur in autumn. Whether the primary effect of coccidian infection or the interactive effects of coccidian infection and predators can affect the reproduction of root voles are obscure. To test the main and interactive effects of coccidian infection with higher intensity and predators on reproduction of root voles, the two-level factorial design was conducted. Then, the prevalence and intensity of intestinal parasites, testicular index, testosterone levels, sperm density, sperm motility and ovary index were evaluated. Our results showed that coccidian infection with higher intensity significantly suppressed the reproductive performance of voles, but had no significant difference in the interaction between coccidian infection and predators, which may correlate with the time mismatch. We suggested that coccidian infection had a slightly limited effect on the reproduction of small mammal populations, but they could affect the fluctuation of host populations via reducing the overwinter survival of the host when interacted with predators.

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Histological structure of the vomeronasal organ and accessory olfactory bulb and the seasonal changes of olfactory bulb c-Fos expression in Spermophilus dauricus

WANG Heng, WANG Jianli, YANG Chenxi, HE Yating

2021, 41(6):  685-694.  DOI: 10.16829/j.slxb.150483

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The vomeronasal organ (VNO) and the accessory olfactory bulb (AOB) in rodents are related to social communication and reproductive behavior, while the main olfactory bulb (MOB) influences foraging behavior. The Daurian ground squirrel (Spermophilus dauricus) is a typical fat-storing hibernator that exhibits low levels of social behaviors. Using histological and immunohistochemical methods, this study has investigated the detailed histological features of the VNO and AOB in the Daurian ground squirrels and how the neuronal activation of the MOB responds to the seasonal variations. There is a large vomeronasal blood vessel in the VNO of the Daurian ground squirrel. The lumen of the VNO is lined laterally by a non-sensory respiratory epithelium (RE) and medially by the sensory epithelium (SE). The RE is thinner than that of the SE, and it consists of pseudostratified columnar epithelium near the lumen. At the middle region of the VNO, no sex differences are observed in either the height or length of the SE, nor in the density of the receptor cells. The AOB is located caudal and dorso-medially relative to the position of the MOB. The AOB strata consist of six layers of cells. The lateral olfactory tract (LOT) passes through the AOB and is positioned above the granule cell layer (GCL). The mitral cell layer (MCL) and GCL in males are longer than that in females. The densities of c-Fos-ir neurons of the glomerular layer (GL), MCL, and GCL in spring (March) and winter (January) are less than that in summer (July) and autumn (October). Furthermore, the external plexiform layer (EPL) displays fewer c-Fos-ir neurons in winter than that in summer and autumn. These results indicate that the olfactory bulb of the Daurian ground squirrel exhibits much weaker neuronal activation in winter and spring, showing a physiological adaptation to hibernation. The present study adds to the body of morphological knowledge on the VNO and AOB and furthers our understanding of the specific acclimatization of the olfactory system to seasonal variation and hibernation in hibernating rodents.

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Analysis of volatile constituents from preputial gland of Chinese mole shrew (Anourosorex squamipes)

ZONG Hao, FAN Hailing, FU Changkun, LEI Ziyong, WANG Qian, ZHAO Tianmeng, CHEN Deng, HU Tao

2021, 41(6):  695-705.  DOI: 10.16829/j.slxb.150440

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The preputial gland is an exocrine gland in mammals. It is generally believed that its secretion plays an important role in information exchange between individuals and population regulation; however, there have been no previous studies on insectivorous animals. In this study, headspace solid-phase microextraction-gas chromatography-mass spectrometry (HS-SPME-GC/MS) was used to analyze the chemical composition of volatile substances in the preputial glands of male Chinese mole shrews. The results showed that the volatile chemical composition of the preputial glands of male Chinese mole-shrews (Anourosorex squamipes) mainly contained 45 compounds, including alkanes, alcohols, ketones, aldehydes, ethers, esters, acids, and aromatic hydrocarbons. The preputial gland secretions of adult males contained 4 unique volatile chemical components, whereas only one unique component was detected in young males. In addition, there were 39 volatile components in the preputial glands of adult male and 28 in young male Chinese mole shrews. These results reveal age differences in the volatile chemical components in the preputial glands of mole-shrews, in which adult males have more volatile components than juvenile males. Moreover, the relative contents of different chemical components in the preputial gland secretion of the mole-shrews were different, and the relative contents of the same chemical components varied between individuals. This study shows that the preputial glands of male mole-shrews are rich in volatile compounds, with obvious differences across individuals and ages. We speculated that Butanoic acid, Ethyl acetate and Phenol are among the volatile compounds which make up the pheromones of the Chinese mole shrews. This study provides basic data for further verification of the pheromone components of the animal's preputial gland and its transmission mechanism.

METHOD AND TECHNOLOGY

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Preliminary survey on mammal and bird species diversity using infrared camera traps in the Matoushan National Nature Reserve, Jiangxi Province

SHAO Ruiqing, LI Yankuo, ZHONG Yifeng, WU Heping, LUO Xiaomin, XIONG Yu, CAO Kaiqiang

2021, 41(6):  706-713.  DOI: 10.16829/j.slxb.150508

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Although designated as a protected area, our current knowledge of the diversity of wildlife species in the Matoushan National Nature Reserve, located in the central region of the Wuyi Mountain, remains relatively limited. With a view to gaining further insights on the species inhabiting the reserve, between January 2016 and December 2018, we randomly established four line transects perpendicular to the reserve's contour lines. Each of these transects spanned the distance from the base of the mountain to its summit, traversing the major habitat types characterizing the reserve. Along each transect, we installed infrared cameras (n=50, separated by distances of up to 100 m) at sites showing clear evidence of animal activity. Over a period of 34 551 camera-days, we obtained 810 and 1 724 independent images of birds and mammals, respectively, from which 13 mammal and 30 bird species were identified. Among the state key protected wild animals, ten are classed as category II species:rhesus macaque (Macaca mulatta), Chinese serow (Capricornis milneedwardsii), Asiatic black bear (Ursus thibetanus), silver pheasant (Lophura nycthemera), crested serpent-eagle (Spilornis cheela), besra sparrowhawk (Accipiter virgatus), Chinese sparrowhawk (A. soloensis), collared owlet (Glaucidium brodiei), white-necklaced partridge (Arborophila gingica), and red-headed trogon (Harpactes erythrocephalus). The white-necklaced partridge, bay woodpecker (Blythipicus pyrrhotis), and eyebrowed thrush (Turdus obscurus) were observed for the first time in the reserve. The reeves' muntjac (Muntiacus reevesi), silver pheasant, and wild boar (Sus scrofa) were identified as being the most abundant species. For more effective monitoring of wildlife within the reserve, a larger number of infrared cameras should be installed throughout the area.

SCIENTIFIC NOTES

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A preliminary study of spatial distribution of Chinese goral carcasses in mid-Qinling Mountains

ZHU Qifeng, ZHAO Qingxia, JIN Xuelin, SHI Dong, WU Qiaoxing, YANG Minghai

2021, 41(6):  714-720.  DOI: 10.16829/j.slxb.150461

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In recent years, Chinese goral (Nemorhaedus griseus) carcasses were frequently found in the mid-Qinling Mountains. In order to assess the spatial distribution pattern of goral carcasses, data of the individuals from Shaanxi's Fourth Giant Panda Survey was used in this study to analyse how the gorals/goral carcasses sites were related to altitude, slope, aspect, river, and road through quantitative analyses. The results showed:(1) the correlation between the sites of goral carcasses and topographic factors was relatively significant. Goral carcasses tend to be found at relatively low altitude (1 200-2 400 m) and mild slope (6°-25°). The chi-square test also showed that the aspect of the goral carcasses sites was significantly different from the goral sites. Most of the goral carcasses were found at south-facing/half southfacing slopes. (2) The correlation between the sites of goral carcasses and the distance to river was significant. The kernel density analysis and Z-test further showed that there were significant differences between the gorals/goral carcasses sites and the distance to river. Most of the goral carcasses sites were close to river (< 100 m). (3) The correlation between the sites of goral carcasses and the distance to road was not significant. Kernel density analysis and Z-test showed that there was no significant difference between the sites of gorals/goral carcasses and the distance to road. This study proposed several suggestions about how to strengthen the protection of gorals in the future.

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A study on the relationship between oxytocin level and maternal behavior in captive giant pandas

WANG Ziye, BI Wenlei, WU Wei, YU Jiaojiao, ZHOU Yanshan, HOU Rong, XIANG Zuofu, QI Dunwu

2021, 41(6):  721-730.  DOI: 10.16829/j.slxb.150477

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Maintaining a good cub-rearing relationship is of great significance for the healthy development of newborn giant panda cubs. Oxytocin plays a key role in this cub-rearing relationship development during the breeding period. To investigate the relationship between oxytocin levels and maternal behavior, we sampled the maternal behavior of 6 adult female giant pandas (3 in lactation group, 3 in non-lactation group) at Chengdu Research Base of Giant Panda Breeding from June to September 2019 by using the focal sampling method, and tested the urine oxytocin level of each individuals by using enzyme-linked immunosorbent assay. The results showed that the oxytocin levels were significantly higher in the lactation group (278. 86 pg/mg ±44. 42 pg/mg) than in the non-lactation group. For the two types of breastfeeding groups, the level of oxytocin in the multiparous female pandas (185. 64 pg/mg ±44. 61 pg/mg) was significantly lower than that in the primiparous female pandas (465. 30 pg/mg ±82. 39 pg/mg). Compared with the primiparous female pandas, the multiparous female pandas had more embracing cub behavior (77. 45% ±1. 24%) and feeding behavior (15. 22% ±1. 62%), but less licking cub (14. 26% ±0. 91%) and position adjustment behavior (1. 69% ±0. 29%). Finally, we found the licking cub behavior was significantly positively correlated with the oxytocin level in the lactation group, and the embracing cub behavior was significantly negatively correlated with the oxytocin level in the lactation group. The results indicate that primiparous female pandas show more maternal behavior, less individual behavior and higher oxytocin levels. The results of this study suggest that the different reactions of oxytocin in the two types of giant panda females may help to improve the refined and differentiated breeding techniques for captive giant pandas in the future.

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Characteristics of vaginal cells and dynamics of serum gonadotropin content in estrus cycle of plateau zokor (Eospalax baileyi)

WANG Yanli, YAO Baohui, ZHANG Caijun, TAN Yuchen, KANG Yukun, ZHANG De-gang, SU Junhu

2021, 41(6):  731-740.  DOI: 10.16829/j.slxb.150505

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In order to determine the change characteristics of vaginal cells in the estrus cycle and the duration of the estrus cycle, vaginal smears and HE staining methods were used to observe and count the types, morphological changes, and proportions of vaginal cells in plateau zokor (Eospalax baileyi). The hormone secretion dynamics of follicle-stimulating hormone (FSH) and luteinizing hormone (LH) in the serum of plateau zokor in the estrus cycle were determined by ELISA. The results showed that the main vaginal cells of plateau zokor were leukocytes, nuclear epithelial cells, incompletely cornified epithelial cells, and complete cornified epithelial cells. The proportion of nuclear epithelial cells in the proestrus was significantly higher than that during the other three periods (48. 4 ±3. 09)% (n=12, P < 0. 05). The proportion of complete cornified epithelial cells in the oestrus was the highest and significantly higher than that in the other three periods (59. 73 ±7. 59)% (n=15, P < 0. 05). The proportion of leukocytes in the metestrus and dioestrum was significantly higher than that in the proestrus and oestrus (P < 0. 05). The expression level of LH was the highest in the metestrus (4. 709 5 ±1. 094 0) ng/mL (n=6, P < 0. 05), which showed an increasing trend in proestrus and oestrus, and a decreasing trend in the metestrus and dioestrum. There was no significant difference in the expression level of FSH among the four periods (P > 0. 05); the estrus cycle duration of plateau zokor was 16 to 19 d, the characteristics of vaginal cell types in different stages of the estrus cycle were obvious, and the relative number was statistically significant. The study provided a basis for vaginal smear identification in the estrous cycle and reproductive physiology study of plateau zokor.