Effects of habitat type and seasonal changes on the gut microbiota of Brandt’s voles

doi:10.16829/j.slxb.2015-1207

Abstract

Abstract:

The gut microbiota plays a crucial role in host physiological function and ecological adaptation. Investigating the impact of different habitat types and seasonal changes on its structure is of significant scientific importance for revealing the host-microbe interaction mechanism. This study collected fecal samples from Brandt’s voles (Lasiopodomys brandtii) under summer field, winter field, and summer indoor conditions, and analyzed the composition, co-occurrence network, assembly mechanism, and predicted metabolic function of the gut microbiota based on 16S rRNA gene amplicon sequencing. The results showed that both seasonal changes and habitat type significantly shaped the gut microbiota of Brandt’s voles, with seasonal factors having a more pronounced effect. In terms of habitat comparison, wild summer individuals, due to highly heterogeneous food intake and complex environmental stimuli, exhibited significantly higher alpha diversity and co-occurrence network complexity of gut microbiota than indoor summer individuals. Their community assembly was primarily driven by deterministic processes (homogeneous selection accounted for 77.8%), while indoor individuals, living in a constant environment for extended periods, showed a looser network structure, with assembly patterns shifting towards stochastic processes (71.1%). In terms of seasonal comparison, winter wild individuals showed the lowest microbial diversity, with a dramatic restructuring of the core microbial community.The relative abundance of Bacillota and other phyla decreased significantly, while Bacteroidota (mainly the family Muribaculaceae) experienced an explosive increase, leading to a significant decrease in the Bacillota/Bacteroidota ratio. Although the microbial network shrank in winter, its local aggregation (clustering coefficient) and the importance of key nodes increased significantly, intensifying antagonistic competition. Furthermore, community assembly mechanism analysis revealed that environmental directional selection pressure weakened from summer to winter, while the relative contribution of stochastic processes such as ecological drift increased. Functional predictions indicate that extreme winter cold and food scarcity broadly inhibited the basal metabolism and tricarboxylic acid cycle of the gut microbiota, while activating specific degradation pathways, such as D-arabinose and glycolic acid metabolism, to maintain host energy homeostasis. Furthermore, the outdoor environment, compared to indoor conditions, induced metabolic potential in the gut microbiota for cellular defense and multinutrient utilization, including cell membrane or wall synthesis and specific amino acid degradation. This study systematically reveals the structural reorganization and simultaneous functional remodeling of the gut microbiota of Brandt’s voles under extreme resource and environmental stress, providing important evidence for a deeper understanding of the ecological adaptation strategies of wild animals and host-microbe interactions.

Key words: Brandt’s vole (Lasiopodomys brandtii), Gut microbiota, Habitat type, Seasonal change

摘要：

肠道微生物在宿主生理功能及生态适应中发挥了关键作用，探究不同生境类型及季节变化对其结构的影响，对于揭示宿主‑微生物互作机制具有重要科学意义。本研究采集了夏季野外、冬季野外以及夏季室内条件下布氏田鼠（Lasiopodomys brandtii）的粪便样品，并基于16S rRNA基因的扩增子测序分析其肠道微生物的组成、共现网络、组装机制及预测代谢功能。结果表明，季节变化与生境类型均能显著塑造布氏田鼠的肠道微生物，且季节因素的影响更为显著。在生境对比方面，野外夏季个体由于高异质性的食物摄入及复杂的环境刺激，其肠道微生物的α多样性和共现网络复杂度显著高于室内夏季个体，其群落组装主要受确定性过程驱动（同质选择占比77.8%），而长期处于恒定环境下的室内个体其网络结构趋于松散，组装模式向随机性过程（占71.1%）转变。在季节对比方面，冬季野外个体的菌群多样性降至最低，且核心菌群结构发生剧烈重构：芽孢杆菌门（Bacillota）等菌群相对丰度大幅降低，而拟杆菌门（Bacteroidota，主要为鼠杆菌科Muribaculaceae）暴发式升高，导致芽孢杆菌门/拟杆菌门比值大幅下降。尽管冬季菌群网络规模收缩，但其局部聚集度（聚类系数）和关键节点的重要度显著增加，拮抗竞争加剧。此外，群落组装机制分析显示，从夏季到冬季环境定向选择压力减弱，生态漂变等随机过程的相对贡献有所增加。功能预测表明，冬季极寒和食物匮乏对菌群的基础代谢和三羧酸循环产生了广泛的抑制作用，但靶向激活了D‑阿拉伯糖和乙醇酸代谢等特殊降解通路以维持宿主能量稳态；而野外环境相比室内则诱导了菌群在细胞膜/细胞壁合成及特定氨基酸降解等细胞防御与多元营养利用上的代谢潜能。本研究系统揭示了布氏田鼠肠道微生物在极端资源及环境压力下的结构重组与功能同步谱系重塑，为深入理解野生动物的生态适应策略和宿主‑微生物互作关系提供了重要依据。

关键词: 布氏田鼠, 肠道微生物, 生境类型, 季节变化

CLC Number:

Q958.1

Zewei ZHANG, Siyu WANG, Guoliang LI. Effects of habitat type and seasonal changes on the gut microbiota of Brandt’s voles[J]. ACTA THERIOLOGICA SINICA, 2026, 46(5): 688-704.

张泽伟, 王思雨, 李国梁. 不同生境类型和季节变化对布氏田鼠肠道菌群组成和群落组装的影响[J]. 兽类学报, 2026, 46(5): 688-704.

Add to citation manager EndNote|Ris|BibTeX

URL: https://www.mammal.cn/EN/10.16829/j.slxb.2015-1207

https://www.mammal.cn/EN/Y2026/V46/I5/688

Figures/Tables 6

Fig. 1 Shannon index (a), observed ASVs number (b), Simpson index (c), and β-diversity analysis (d) of Brandt’s vole gut microbiota in different habitats and seasons.β-diversity analysis of gut microbiota between summer indoor group (FIS) and summer field group (FWS) (e), and β-diversity analysis of gut microbiota between summer field group (FWS) and winter field group (FWW) (f). Different letters represent statistical significance (P < 0.05)

Fig. 2 Analysis of gut microbial community structure and differences in Brandt’s vole under different habitats and seasons. a: Phylum level relative abundance composition; b: Genus level relative abundance distribution; c: Analysis of significant differences between groups of low-abundance phyla; d: Analysis of significant differences between groups of high-abundance genera; e: LEfSe analysis of LDA discriminant plot of significantly different species. Different lowercase letters represent statistically significant differences between groups (P < 0.05)

Fig. 3 Co-occurrence network analysis of gut microbiota at the ASV level in Brandt’s voles under different habitats and seasons. a ‑ c: represent the microbial co-occurrence networks of the summer indoor group (FIS), summer field group (FWS), and winter field group (FWW), respectively. Node size is proportional to the relative abundance of nodes, and node color represents different bacterial phyla

Table 1 Comparison of topological characteristics of co-occurrence networks of gut microbiota in different groups of Brandt’s voles

特征参数 Parameters	组别 Group
特征参数 Parameters	夏季室内饲养组 FIS	夏季野外组FWS	冬季野外组 FWW
节点数 Nodes	134	395	52
边数 Edges	243	2 158	80
正相关边数 Positive edges	129	1 107	35
负相关边数 Negative edges	114	1 051	45
平均度 Average degree	3.626 9	10.926 6	3.076 9
平均路径长度 Average path length	3.094 8	2.260 9	2.497 0
网络直径 Network diameter	6.827 3	4.637 7	5.771 0
网络密度 Network density	0.027 3	0.027 7	0.060 3
聚类系数 Clustering coefficient	0.301 4	0.379 3	0.597 7
模块化系数 Modularity	0.666 4	0.609 6	0.750 0
平均接近中心性 Average closeness centrality	0.154 7	0.218 0	0.202 3
平均介数中心性 Average betweenness centrality	0.029 7	0.006 0	0.091 9
平均离心率 Average eccentricity	5.319 5	3.732 9	4.715 2

Fig. 4 Distribution of βNTI values for sample pairs in different groups (a), and assembly process of Brandt’s vole fecal microbial community under different survival conditions (b - d). b: Summer indoor group (FIS); c: Summer field group (FWS); d: Winter field group (FWW). Different letters represent statistical significance (P < 0.05). Different colors in the figure b - d represent different ecological processes: homogeneous selection and heterogeneous selection are deterministic processes, while dispersal limitation, homogenizing dispersal, and drift or undominated are stochastic processes

Fig. 5 Differential analysis of MetaCyc metabolic pathway of intestinal microbiota in Brandt’s voles based on PICRUSt2 prediction.a: Volcano plot of MetaCyc metabolic pathway differences between FWW and FWS, pathways significantly enriched in FWW on the red dot (P < 0.05, log2 Fold change > 1), blue dots indicate pathways significantly reduced in the FWW group (P < 0.05, log2 Fold change < -1), gray dots indicate pathways with insignificant differences, dashed lines indicate significance thresholds (P = 0.05) and fold change (|log2 Fold change| = 1), respectively; b: Cluster heat map of the top 30 most significantly different MetaCyc pathways, rows representing metabolic pathways, columns representing samples, colors representing normalized relative abundance (Z-score) after variance stabilization transformation (VST), blue representing lower relative abundance, and red representing higher relative abundance

References

	Bai D F， Wan X R， Li G L， Wan X R， Guo Y W， Shi D Z， Zhang Z B，2022. Factors influencing range contraction of a rodent herbivore in a steppe grassland over the past decades［J］. Ecology and Evolution，12（2）：e8546. DOI：10.1002/ece3.8546 .
	Bastian M， Heymann S， Jacomy M，2009. Gephi：An open source software for exploring and manipulating networks［C］. Proceedings of the international AAAI conference on web and social media，3（1）：361‑362. DOI：10.1609/icwsm.v3i1.13937 .
	Bauwe H， Hagemann M， Fernie A R，2010. Photorespiration： players，partners and origin［J］. Trends in Plant Science，15（6）：330‑336. DOI：10.1016/j.tplants.2010.03.006 .
	Berry D， Widder S，2014. Deciphering microbial interactions and detecting keystone species with co‑occurrence networks［J］. Frontiers in Microbiology，5：219. DOI：10.3389/fmicb.2014.00219
	Bo T B， Zhang X Y， Wen J， Deng K， Qin X W， Wang D H，2019. The microbiota‑gut‑brain interaction in regulating host metabolic adaptation to cold in male Brandt’s voles（Lasiopodomys brandtii）［J］. The ISME Journal，13（12）：3037‑3053. DOI：10.1038/s41396-019-0492-y .
	Bolyen E， Rideout J R， Dillon M R， Bokulich N A， Abnet C C， Al‑Ghalith G A， Alexander H， Alm E J， Arumugam M， Asnicar F， Bai Y， Bisanz J E， Bittinger K， Brejnrod A， Brislawn C J， Brown C T， Callahan B J， Caraballo‑Rodríguez A M， Chase J， Cope E K， Da Silva R， Diener C， Dorrestein P C， Douglas G M， Durall D M， Duvallet C， Edwardson C F， Ernst M， Estaki M， Fouquier J， Gauglitz J M， Gibbons S M， Gibson D L， Gonzalez A， Gorlick K， Guo J， Hillmann B， Holmes S， Holste H， Huttenhower C， Huttley G A， Janssen S， Jarmusch A K， Jiang L， Kaehler B D， Kang K B， Keefe C R， Keim P， Kelley S T， Knights D， Koester I， Kosciolek T， Kreps J， Langille M G I， Lee J， Ley R， Liu Y X， Loftfield E， Lozupone C， Maher M， Marotz C， Martin B D， McDonald D， McIver L J， Melnik A V， Metcalf J L， Morgan S C， Morton J T， Naimey A T， Navas-Molina J A， Nothias L F， Orchanian S B， Pearson T， Peoples S L， Petras D， Preuss M L， Pruesse E， Rasmussen L B， Rivers A， Robeson M S， Rosenthal P， Segata N， Shaffer M， Shiffer A， Sinha R， Song S J， Spear J R， Swafford A D， Thompson L R， Torres P J， Trinh P， Tripathi A， Turnbaugh P J， Ul‑Hasan S， Van Der Hooft J J J， Vargas F， Vázquez‑Baeza Y， Vogtmann E， Von Hippel M， Walters W， Wan Y， Wang M， Warren J， Weber K C， Williamson C H D， Willis A D， Xu Z Z， Zaneveld J R， Zhang Y， Zhu Q， Knight R， Caporaso J G，2019. Reproducible，interactive，scalable and extensible microbiome data science using QIIME 2［J］. Nature Biotechnology，37（8）：852‑857. DOI：10.1038/s41587-019-0209-9 .
	Cao K L， Tao M F， Pu X S， Hou Y， Ren Y， Liu W， Yang X G，2024. Effects of dietary nutrients of the gut microbiota in the long‑tailed dwarf hamster（Cricetulus longicaudatus）［J］. Ecology and Evolution，14（6）：e11507. DOI：10.1002/ece3. 11507 .
	Callahan B J， McMurdie P J， Rosen M J， Han A W， Johnson A J A， Holmes S P，2016. DADA2：High‑resolution sample inference from Illumina amplicon data［J］. Nature Methods，13 （7）：581‑583. DOI：10.1038/nmeth.3869 .
	Chen C Y， Chen P C， Weng F C H， Shaw G T W， Wang D，2017. Habitat and indigenous gut microbes contribute to the plasticity of gut microbiome in oriental river prawn during rapid environmental change［J］. PLoS ONE，12（7）：e0181427. DOI：10.1371/journal.pone.0181427 .
	Chiang E， Deblois C L， Carey H V， Suen G，2022. Characterization of captive and wild 13‑lined ground squirrel cecal microbiotas using Illumina‑based sequencing［J］. Animal Microbiome，4（1）：1. DOI：10.1186/s42523-021-00154-9 .
	Chidwick H S， Flack E K P， Keenan T， Walton J， Thomas G H， Fascione M A，2021. Reconstitution and optimisation of the biosynthesis of bacterial sugar pseudaminic acid（Pse5Ac7Ac） enables preparative enzymatic synthesis of CMP‑Pse5Ac7Ac［J］. Scientific Reports，11（1）：4756. DOI：10.1038/s41598-021-83707-x .
	Culp E J， Goodman A L，2023. Cross‑feeding in the gut microbiome： ecology and mechanisms［J］. Cell Host & Microbe，31（4）：485‑499. DOI：10.1016/j.chom.2023.03.016 .
	Dai Z L，2011. Amino acid metabolism in intestinal bacteria：links between gut ecology and host health［J］. Front Biosci，16（1）：1768. DOI：10.2741/3820 .
	Deng Y， Jiang Y H， Yang Y F， He Z L， Luo F， Zhou J Z，2012. Molecular ecological network analyses［J］. BMC Bioinformatics，13（1）：113. DOI：10.1186/1471-2105-13-113 .
	Douglas G M， Maffei V J， Zaneveld J R， Yurgel S N， Brown J R， Taylor C M， Huttenhower C， Langille M G I，2020. PICRUSt2 for prediction of metagenome functions［J］. Nat Biotechnol，38（6）：685‑688. DOI：10.1038/s41587-020-0548-6 .
	Fan C， Zhang L Z， Jia S G， Tang X J， Fu H B， Li W J， Liu C F， Zhang H， Cheng Q， Zhang Y M，2022. Seasonal variations in the composition and functional profiles of gut microbiota reflect dietary changes in plateau pikas［J］. Integrative Zoology，17（3）：379‑395. DOI：10.1111/1749-4877.12630 .
	Faust K， Raes J，2012. Microbial interactions：from networks to models［J］. Nature Reviews Microbiology，10（8）：538‑550. DOI：10.1038/nrmicro2832 .
	Flint H J， Scott K P， Duncan S H， Louis P， Forano E，2012. Microbial degradation of complex carbohydrates in the gut［J］. Gut Microbes，3（4）：289‑306. DOI：10.4161/gmic.19897 .
	Gromov V S，2023. Ecology and social behavior of the Brandt’s vole： a generalized review［J］. Journal of Arid Environments，214：104994. DOI：10.1016/j.jaridenv.2023.104994 .
	Guimerà R， Nunes Amaral L A，2005. Functional cartography of complex metabolic networks［J］. Nature，433（7028）：895‑900. DOI：10.1038/nature03288 .
	Hanski E， Raulo A， Knowles S C L，2024. Early‑life gut microbiota assembly patterns are conserved between laboratory and wild mice［J］. Communications Biology，7（1）：1456. DOI：10.1038/s42003-024-07039-y .
	Heiman M L， Greenway F L，2016. A healthy gastrointestinal microbiome is dependent on dietary diversity［J］. Molecular Metabolism，5（5）：317‑320. DOI：10.1016/j.molmet. 2016.02.005 .
	Hibbing M E， Fuqua C， Parsek M R， Peterson S B，2010. Bacterial competition：surviving and thriving in the microbial jungle［J］. Nature Reviews Microbiology，8（1）：15‑25. DOI：10.1038/nrmicro2259 .
	Hossain K S， Amarasena S， Mayengbam S，2022. B vitamins and their roles in gut health［J］. Microorganisms，10（6）：1168. DOI：10.3390/microorganisms10061168 .
	Hou J L， Xiang J G， Li D L， Liu X H， Pan W C，2022. Gut microbial response to host metabolic phenotypes［J］. Frontiers in Nutrition，9：1019430. DOI：10.3389/fnut.2022.1019430 .
	Jiang Z P， Mei L， Li Y Q， Guo Y G， Yang B， Huang Z Y， Li Y Y，2024. Enzymatic regulation of the gut microbiota：mechanisms and implications for host health［J］. Biomolecules，14（12）：1638. DOI：10.3390/biom14121638 .
	Khakisahneh S， Zhang X Y， Nouri Z， Wang D H，2020. Gut microbiota and host thermoregulation in response to ambient temperature fluctuations［J］. mSystems，5（5）：e00514‑20. DOI：10.1128/mSystems.00514-20 .
	Kim M， Sung J， Chia N，2022. Resource‑allocation constraint governs structure and function of microbial communities in metabolic modeling［J］. Metabolic Engineering，70：12‑22. DOI：10.1016/j.ymben.2021.12.011 .
	Kraft N J B， Adler P B， Godoy O， James E C， Fuller S， Levine J M，2015. Community assembly，coexistence and the environmental filtering metaphor［J］. Functional Ecology，29（5）：592‑599. DOI：10.1111/1365-2435.12345 .
	Lebrija‑Trejos E， Pérez‑García E A， Meave J A， Bongers F， Poorter L，2010. Functional traits and environmental filtering drive community assembly in a species‑rich tropical system［J］. Ecology，91（2）：386‑398. DOI：10.1890/08-1449.1 .
	Li G L， Li J， Kohl K D， Yin B F， Wei W H， Wan X R， Zhu B L， Zhang Z B，2019. Dietary shifts influenced by livestock grazing shape the gut microbiota composition and co‐occurrence networks in a local rodent species［J］. Journal of Animal Ecology，88（2）：302‑314. DOI：10.1111/1365-2656.12920 .
	Li G L， Shi C， Song Y R， Chu H Y， Zhang Z B，2021. The role transition of dietary species richness in modulating the gut microbial assembly and postweaning performance of a generalist herbivore［J］. mSystems，6（6）：e00979‑21. DOI：10.1128/mSystems.00979-21 .
	Li G L， Yin B F， Wan X R， Wei W H， Wang G M， Krebs C J， Zhang Z B，2016. Successive sheep grazing reduces population density of Brandt’s voles in steppe grassland by altering food resources：a large manipulative experiment［J］. Oecologia，180（1）：149‑159. DOI：10.1007/s00442-015-3455-7 .
	Li H， Zhou R， Zhu J X， Huang X D， Qu J P，2019. Environmental filtering increases with elevation for the assembly of gut microbiota in wild pikas［J］. Microbial Biotechnology，12（5）：976‑992. DOI：10.1111/1751-7915.13450 .
	Lindsay E C， Metcalfe N B， Llewellyn M S，2020. The potential role of the gut microbiota in shaping host energetics and metabolic rate［J］. Journal of Animal Ecology，89（11）：2415‑2426. DOI：10.1111/1365-2656.13327 .
	Liu J， Huang S L， Li G L， Zhao J D， Lu W， Zhang Z B，2020. High housing density increases stress hormone‑ or disease‑associated fecal microbiota in male Brandt’s voles（Lasiopodomys brandtii）［J］. Hormones and Behavior，126：104838. DOI：10.1016/j.yhbeh.2020.104838 .
	Liu M， Zou D S， Zhang X Y， Wang D H，2025. Huddling behavior regulate adaptive thermogenesis in Brandt’s voles（Lasiopodomys brandtii）［J］. Cell & Bioscience，15（1）：51. DOI：10.1186/s13578-025-01391-0 .
	Magoč T， Salzberg S L，2011. FLASH：Fast length adjustment of short reads to improve genome assemblies［J］. Bioinformatics，27（21）：2957‑2963. DOI：10.1093/bioinformatics/btr507 .
	Martínez‑Mota R， Kohl K D， Orr T J， Denise Dearing M，2020. Natural diets promote retention of the native gut microbiota in captive rodents［J］. The ISME Journal，14（1）：67‑78. DOI：10.1038/s41396-019-0497-6 .
	Memmott J， Waser N M， Price M V，2004. Tolerance of pollination networks to species extinctions［J］. Proceedings of the Royal Society of London，Series B：Biological Sciences，271（1557）：2605‑2611. DOI：10.1098/rspb.2004.2909 .
	Milici M， Deng Z L， Tomasch J， Decelle J， Wos‑Oxley M L， Wang H， Jáuregui R， Plumeier I， Giebel H A， Badewien T H， Wurst M， Pieper D H， Simon M， Wagner‑Döbler I，2016. Co‑occurrence analysis of microbial taxa in the atlantic ocean reveals high connectivity in the free‑living bacterioplankton［J］. Frontiers in Microbiology，7：649. DOI：10.3389/fmicb. 2016.00649 .
	Neha S A， Salazar‑Bravo J，2023. Fine‑scale spatial variation shape fecal microbiome diversity and composition in black‑tailed prairie dogs（Cynomys ludovicianus）［J］. BMC Microbiology，23（1）：51. DOI：10.1186/s12866-023-02778-0 .
	Neumann‑Schaal M， Jahn D， Schmidt‑Hohagen K，2019. Metabolism the difficile way：the key to the success of the pathogen Clostridioides difficile ［J］. Frontiers Microbiology，10：219. DOI：10.3389/fmicb.2019.00219 .
	Olesen J M， Bascompte J， Dupont Y L， Jordano P，2007. The modularity of pollination networks［J］. Proceedings of the National Academy of Sciences of the United States of America，104（50）：19891‑19896. DOI：10.1073/pnas.0706375104 .
	Ottman N， Ruokolainen L， Suomalainen A， Sinkko H， Karisola P， Lehtimäki J， Lehto M， Hanski I， Alenius H， Fyhrquist N，2019. Soil exposure modifies the gut microbiota and supports immune tolerance in a mouse model［J］. Journal of Allergy and Clinical Immunology，143（3）：1198‑1206.e12. DOI：10.1016/j.jaci.2018.06.024 .
	Raulo A， Bürkner P C， Finerty G E， Dale J， Hanski E， English H M， Lamberth C， Firth J A， Coulson T， Knowles S C L，2024. Social and environmental transmission spread different sets of gut microbes in wild mice［J］. Nature Ecology＆Evolution，8（5）：972‑985. DOI：10.1038/s41559-024-02381-0 .
	Rosshart S P， Vassallo B G， Angeletti D， Hutchinson D S， Morgan A P， Takeda K， Hickman H D， McCulloch J A， Badger J H， Ajami N J， Trinchieri G， Pardo‑Manuel De Villena F， Yewdell J W， Rehermann B，2017. Wild mouse gut microbiota promotes host fitness and improves disease resistance［J］. Cell，171（5）：1015‑1028.e13. DOI：10.1016/j.cell.2017.09.016 .
	Schmidt E， Mykytczuk N， Schulte‑Hostedde A I，2019. Effects of the captive and wild environment on diversity of the gut microbiome of deer mice（Peromyscus maniculatus）［J］. The ISME Journal，13（5）：1293‑1305. DOI：10.1038/s41396-019-0345-8 .
	Shen W J， Gao P， Zhou K Y， Li J， Bo T B， Xu D L，2024. The impact of high‑temperature stress on gut microbiota and reproduction in Siberian hamsters（Phodopus sungorus）［J］. Microorganisms，12（7）：1426. DOI：10.3390/microorganisms12071426 .
	Stegen J C， Lin X J， Konopka A E， Fredrickson J K，2012. Stochastic and deterministic assembly processes in subsurface microbial communities［J］. The ISME Journal，6（9）：1653‑1664. DOI：10.1038/ismej.2012.22 .
	Teng Y W， Yang X F， Li G L， Zhu Y L， Zhang Z B，2022. Habitats show more impacts than host species in shaping gut microbiota of sympatric rodent species in a fragmented forest［J］. Frontiers in Microbiology，13：811990. DOI：10.3389/fmicb. 2022.811990 .
	Terrapon N， Lombard V， Drula É， Lapébie P， Al‑Masaudi S， Gilbert H J， Henrissat B，2018. PULDB： the expanded database of polysaccharide utilization loci［J］. Nucleic Acids Research，46（D1）：D677‑D683. DOI：10.1093/nar/gkx1022 .
	Tylianakis J M， Laliberté E， Nielsen A， Bascompte J，2010. Conservation of species interaction networks［J］. Biological Conservation，143（10）：2270‑2279. DOI：10.1016/j.biocon. 2009.12.004 .
	Vellend M，2010. Conceptual synthesis in community ecology［J］. The Quarterly Review of Biology，85（2）：183‑206. DOI：10.1086/652373 .
	Wang J J， Shen J， Wu Y C， Tu C， Soininen J， Stegen J C， He J Z， Liu X Q， Zhang L， Zhang E L，2013. Phylogenetic beta diversity in bacterial assemblages across ecosystems：deterministic versus stochastic processes［J］. The ISME Journal，7（7）：1310‑1321. DOI：10.1038/ismej.2013.30 .
	Wefers D， Tyl C E， Bunzel M，2014. Novel arabinan and galactan oligosaccharides from dicotyledonous plants［J］. Frontiers in Chemistry，2：100. DOI：10.3389/fchem.2014.00100 .
	Willdigg J R， Helmann J D，2021. Mini Review：bacterial membrane composition and its modulation in response to stress［J］. Frontiers in Molecular Biosciences，8：634438. DOI：10.3389/fmolb.2021.634438 .
	Williams C E， Williams C L， Logan M L，2023. Climate change is not just global warming：multidimensional impacts on animal gut microbiota［J］. Microbial Biotechnology，16（9）：1736‑1744. DOI：10.1111/1751-7915.14276 .
	Willmann M R， Endres M W， Cook R T， Gregory B D，2011. The functions of RNA‑dependent RNA polymerases in arabidopsis［J］. The Arabidopsis Book，9：e0146. DOI：10.1199/tab.0146 .
	Yun Y， Duan C， He X C， Tang R X， Lan Y， Lu M Y， Liu T J， Fan X， Fan Z X， Ran J H，2026. Gut microbiome plasticity explains the altitudinal distribution pattern and adaptability in a small mammal species（Apodemus draco）［J］. Microbiology Spectrum，14（1）：e02388‑25. DOI：10.1128/spectrum. 02388-25 .
	Zeng H， Rohani R， Huang W E， Yang A，2021. Understanding and mathematical modelling of cellular resource allocation in microorganisms：a comparative synthesis［J］. BMC Bioinformatics，22（1）：467. DOI：10.1186/s12859-021-04382-3 .
	Zhang X Y， Khakisahneh S， Liu W， Zhang X Y， Zhai W W， Cheng J L， Speakman J R， Wang D H，2023. Phylogenetic signal in gut microbial community rather than in rodent metabolic traits［J］. National Science Review，10（10）：nwad209. DOI：10.1093/nsr/nwad209 .
	Zhang X Y， Sukhchuluun G， Bo T B， Chi Q S， Yang J J， Chen B， Zhang L， Wang D H，2018. Huddling remodels gut microbiota to reduce energy requirements in a small mammal species during cold exposure［J］. Microbiome，6（1）：103. DOI：10.1186/s40168-018-0473-9 .
	Zhang Y M， Rock C O，2008. Membrane lipid homeostasis in bacteria［J］. Nature Reviews Microbiology，6（3）：222‑233. DOI：10.1038/nrmicro1839 .
	Zhang Z B， Pech R， Davis S， Shi D Z， Wan X R， Zhong W Q，2003. Extrinsic and intrinsic factors determine the eruptive dynamics of Brandt’s voles Microtus brandti in Inner Mongolia，China［J］. Oikos，100（2）：299‑310. DOI：10.1034/j. 1600-0706.2003.11810.x .
	Zhou J Z， Ning D L，2017. Stochastic community assembly： Does it matter in microbial ecology？［J］. Microbiology and Molecular Biology Reviews，81（4）：e00002‑17. DOI：10.1128/MMBR. 00002-17 .
	张知彬，王祖望， 1998. 农业重要害鼠的生态学及控制对策［M］. 北京：海洋出版社.

[1]	Xiaolong GAO, Wanxiang ZHANG, Hongjuan ZHAI, Hanyi ZHU, Zhibin ZHANG. The role of gut microbiota differences in the coexistence of norway rats (Rattus norvegicus) and Asian house rats (Rattus tanezumi) in Hainan [J]. ACTA THERIOLOGICA SINICA, 2026, 46(5): 705-719.
[2]	Xinlei HUANG, wei LANG, Jiang FENG, Boyu LIU. Advances in bat gut microbiota research [J]. ACTA THERIOLOGICA SINICA, 2026, 46(5): 638-649.
[3]	Qiyuan XUE, He CAI, Yifei ZHANG, Yi GAO, Qiuying GUO, Zhihui ZHANG, Zhimin JIN, Junsheng ZHANG, Zhu LIU. Gut microbiota structure and function in Sorex caecutiens across different seasons within the same region [J]. ACTA THERIOLOGICA SINICA, 2026, 46(5): 734-743.
[4]	Tianxin ZHANG, Wanlong ZHU. Cross-scale physiological and ecological effects of gut microbiota in small mammals under food restriction [J]. ACTA THERIOLOGICA SINICA, 2026, 46(5): 650-669.
[5]	Binpeng WANG, Danhui ZHANG, Zhimei YANG, Yueting PAN, Xiaobin LUO, Ran MO, Linsen ZAN, Xiaoyu WANG, Chugang MEI. Analysis of structural and functional differences in the gut microbiota between juvenile and adult captive giant pandas in the Qinling region [J]. ACTA THERIOLOGICA SINICA, 2026, 46(5): 744-758.
[6]	Yuting SUN, Dongdong YANG, Yinhu LI, Congran GONG, Han HU, Lina SU, Peiwei LI, Yan LIU, Hongfeng ZHANG, Xiaomin WU. Effect of sex on the gut microbiota of Tibetan antelopes [J]. ACTA THERIOLOGICA SINICA, 2026, 46(2): 278-286.
[7]	Yuxiang LI, Xi TIAN, Chunbing LIU, Li YU. The effects of captivity on gut microbiota of wild mammals [J]. ACTA THERIOLOGICA SINICA, 2026, 46(1): 1-19.
[8]	NIE Yonggang, ZHANG Chao, GAO Huayao, LIU Hanqing, XIE Bing. Advances in conservation research of large- and medium-sized terrestrial mammals in China [J]. ACTA THERIOLOGICA SINICA, 2025, 45(5): 559-576.
[9]	SUN Kai, ZHU Zhaoling, Naheya, HAO Shuxiang, LIANG Yongliang, XU Hao, Alima, LIU Zhen-sheng, TENG Liwei. Gender difference in gut microbiota composition of blue sheep (Pseudois nayaur) on the eastern slope of the Helan Mountains between summer and winter [J]. ACTA THERIOLOGICA SINICA, 2025, 45(4): 492-502.
[10]	ZHAO Xing, MA Rui, WU Wei, LI Mingxi, CHEN Chao, ZHOU Yanshan, HONG Mingsheng, QI Dunwu. Changing patterns of cortisol and gut microbiota in Ailurus fulgens under different living environments [J]. ACTA THERIOLOGICA SINICA, 2024, 44(4): 427-435.
[11]	LI Hongjuan, WANG Dehua, WANG Zhenshan, ZHANG Xueying. High temperature during lactation shortens the thermoneutral zone in the F1 generation of Brandt’s voles (Lasiopodomys brandtii) [J]. ACTA THERIOLOGICA SINICA, 2023, 43(4): 412-421.
[12]	Feng JIANG, Pengfei SONG, Jingjie ZHANG, Hongmei GAO, Haijing WANG, Zhenyuan CAI, Daoxin LIU, Tongzuo ZHANG. Comparative analysis of gut microbial composition and functions of forest musk deer in different breeding centres [J]. ACTA THERIOLOGICA SINICA, 2023, 43(2): 129-140.
[13]	Min MAO, Ming YANG, Xinyu LIU. Effects of hibernation on cecal microbiota in Daurian ground squirrel [J]. ACTA THERIOLOGICA SINICA, 2022, 42(4): 420-431.
[14]	FAN Chao, ZHANG Liangzhi, FU Haibo, LIU Chuanfa, LI Wenjing, ZHANG He, TANG Xianjiang, CHENG Qi, SHEN Wenjuan, ZHANG Yanming. Seasonality of abundant and rare taxa in gut microbiota of plateau pikas [J]. ACTA THERIOLOGICA SINICA, 2021, 41(6): 617-630.
[15]	WANG Dehua, ZHAO Zhijun, ZHANG Xueying, ZHANG Zhiqiang, XU Deli, XING Xin, YANG Shengmei, WANG Zhengkun, GAO Yunfang, YANG Ming. Research advances and prespectives in mammal physiological ecology in China [J]. ACTA THERIOLOGICA SINICA, 2021, 41(5): 537-555.