Rhizosphere effects of Betula platyphylla and Quercus mongolica and their seasonal dynamics in Dongling Mountain, Beijing

doi:10.17521/cjpe.2022.0485

Abstract

Abstract:

Aims The objective of this study was to explore the seasonal variations of the rhizosphere effects of woody plants and their driving factors, and to assess the importance of plant functional traits in the control of rhizosphere processes.
Methods We collected paired rhizosphere and bulk soils of the dominant tree species of two main types of vegetation in Dongling Mountain, Beijing, Betula platyphylla forest and Quercus mongolica forest. Soil physiochemical properties, microbial biomass, carbon and net nitrogen mineralization rates, extracellular enzyme activities and vector characteristics of rhizosphere and bulk soils, as well as plant root and leaf functional traits, in spring (May), summer (July), autumn (September), and winter (December) of 2017 were measured to analyze the seasonal dynamics of rhizosphere effects and their driving factors.
Important findings (1) There were significant differences in soil pH, NH₄⁺-N, microbial biomass, carbon and net nitrogen mineralization rates, extracellular enzyme activities and vector characteristics between rhizosphere soil and bulk soil, and these rhizosphere effects were mainly positive. (2) The rhizosphere effects had significant seasonal dynamics, usually being strongest in autumn. (3) There were often significant correlations between rhizosphere effects and plant root and leaf functional traits. Among them, fine root biomass was significantly and positively correlated with the rhizosphere effect on contents of extractable organic carbon, soil total carbon and total nitrogen. Leaf dry matter content and leaf carbon and nitrogen ratio were significantly and positively correlated with the rhizosphere effect on microbial biomass carbon content, microbial biomass nitrogen content, carbon mineralization rate, and acid phosphatase activity. These results showed that the functional traits of plants were of great significance in rhizosphere processes. In the temperate deciduous broadleaf forest in Dongling Mountain, the highest belowground carbon allocation of plants leads to an increase in the biomass and activity of rhizosphere microorganisms in autumn, which makes the rhizosphere effect of microbial biomass and activity in autumn higher than that in other seasons.

Key words: rhizosphere effect, seasonal dynamic, plant functional traits, soil extracellular enzymes, forest

FU Liang-Chen, DING Zong-Ju, TANG Mao, ZENG Hui, ZHU Biao. Rhizosphere effects of Betula platyphylla and Quercus mongolica and their seasonal dynamics in Dongling Mountain, Beijing[J]. Chin J Plant Ecol, 2024, 48(4): 508-522.

Add to citation manager EndNote|Ris|BibTeX

URL: https://www.plant-ecology.com/EN/10.17521/cjpe.2022.0485

https://www.plant-ecology.com/EN/Y2024/V48/I4/508

Figures/Tables 7

References 49

[1]	Bardgett RD, Bowman WD, Kaufmann R, Schmidt SK (2005). A temporal approach to linking aboveground and belowground ecology. Trends in Ecology & Evolution, 20, 634-641.
[2]	Bardgett RD, Mommer L, de Vries FT (2014). Going underground: root traits as drivers of ecosystem processes. Trends in Ecology & Evolution, 29, 692-699.
[3]	Calvaruso C, N’Dira V, Turpault MP (2011). Impact of common European tree species and Douglas-fir (Pseudotsuga menziesii [Mirb.] Franco) on the physicochemical properties of the rhizosphere. Plant and Soil, 342, 469-480.
[4]	Chen J, Elsgaard L, van Groenigen KJ, Olesen JE, Liang Z, Jiang Y, Lærke PE, Zhang YF, Luo YQ, Hungate BA, Sinsabaugh RL, Jørgensen U (2020). Soil carbon loss with warming: new evidence from carbon-degrading enzymes. Global Change Biology, 26, 1944-1952.
[5]	Chen X, Ding ZJ, Tang M, Zhu B (2018). Greater variations of rhizosphere effects within mycorrhizal group than between mycorrhizal group in a temperate forest. Soil Biology & Biochemistry, 126, 237-246.
[6]	Cheng W, Parton WJ, Gonzalez-Meler MA, Phillips R, Asao S, McNickle GG, Brzostek E, Jastrow JD (2014). Synthesis and modeling perspectives of rhizosphere priming. New Phytologist, 201, 31-44. DOI PMID
[7]	Cui XT, Yuan FH, Wang AZ, Guan DX, Wu JB, Jin CJ (2017). Leaf age-related changes in photosynthesis of Quercus mongolica leaves in relation to leaf functional traits. Chinese Journal of Ecology, 36, 3160-3167.
	[崔西甜, 袁凤辉, 王安志, 关德新, 吴家兵, 金昌杰 (2017). 蒙古栎叶片光合作用随叶龄的变化及其与叶片功能性状的关系. 生态学杂志, 36, 3160-3167.]
[8]	Dijkstra FA, Cheng WX (2007). Interactions between soil and tree roots accelerate long-term soil carbon decomposition. Ecology Letters, 10, 1046-1053. PMID
[9]	Ding ZJ, Tang M, Chen X, Yin LM, Gui HC, Zhu B (2019). Measuring rhizosphere effects of two tree species in a temperate forest: a comprehensive method comparison. Rhizosphere, 10, 100153. DOI: 10.1016/j.rhisph.2019.100153.
[10]	Eviner V, Chapin III FS (2003). Functional matrix: a conceptual framework for predicting multiple plant effects on ecosystem processes. Annual Review of Ecology, Evolution, and Systematics, 34, 455-485.
[11]	Fang JY, Liu GH, Zhu B, Wang XK, Liu SH (2006). Carbon cycle of three temperate forest ecosystems in Dongling Mountain, Beijing. Science in China: Earth Science, 36, 533-543.
	[方精云, 刘国华, 朱彪, 王效科, 刘绍辉 (2006). 北京东灵山三种温带森林生态系统的碳循环. 中国科学: 地球科学, 36, 533-543.]
[12]	Gan DY, Feng JG, Han MG, Zeng H, Zhu B (2021). Rhizosphere effects of woody plants on soil biogeochemical processes: a meta-analysis. Soil Biology & Biochemistry, 160, 108310. DOI: 10.1016/j.soilbio.2021.108310.
[13]	Gan DY, Zeng H, Zhu B (2022). The rhizosphere effect on soil gross nitrogen mineralization: a meta-analysis. Soil Ecology Letters, 4, 144-154. DOI
[14]	Han MG, Sun LJ, Gan DY, Fu LC, Zhu B (2020). Root functional traits are key determinants of the rhizosphere effect on soil organic matter decomposition across 14 temperate hardwood species. Soil Biology & Biochemistry, 151, 108019. DOI: 10.1016/j.soilbio.2020.108019.
[15]	Jenkinson DS, Brookes PC, Powlson DS (2004). Measuring soil microbial biomass. Soil Biology & Biochemistry, 36, 5-7.
[16]	Jin BB, Guo QX (2013). Root decomposition and nutrient dynamics of Quercus mongolica and Betula Platyphylla. Acta Ecologica Sinica, 33, 2416-2424.
	[靳贝贝, 国庆喜 (2013). 蒙古栎、白桦根系分解及养分动态. 生态学报, 33, 2416-2424.]
[17]	Jing X, Chen X, Fang JY, Ji CJ, Shen HH, Zheng CY, Zhu B (2020). Soil microbial carbon and nutrient constraints are driven more by climate and soil physicochemical properties than by nutrient addition in forest ecosystems. Soil Biology & Biochemistry, 141, 107657. DOI: 10.1016/j.soilbio.2019.107657.
[18]	Kaiser C, Fuchslueger L, Koranda M, Gorfer M, Stange CF, Kitzler B, Rasche F, Strauss J, Sessitsch A, Zechmeister- Boltenstern S, Richter A (2011). Plants control the seasonal dynamics of microbial N cycling in a beech forest soil by belowground allocation. Ecology, 92, 1036-1051.
[19]	Kaiser C, Koranda M, Kitzler B, Fuchslueger L, Schnecker J, Schweiger P, Rasche F, Zechmeister-Boltenstern S, Sessitsch A, Richter A (2010). Belowground carbon allocation by trees drives seasonal patterns of extracellular enzyme activities by altering microbial community composition in a beech forest soil. New Phytologist, 187, 843-858. DOI PMID
[20]	Kuzyakov Y (2010). Priming effects: interactions between living and dead organic matter. Soil Biology & Biochemistry, 42, 1363-1371.
[21]	Kuzyakov Y (2002). Review: factors affecting rhizosphere priming effects. Journal of Plant Nutrition and Soil Science, 165, 382-396.
[22]	Kuzyakov Y, Cheng W (2004). Photosynthesis controls of CO₂ efflux from maize rhizosphere. Plant and Soil, 263, 85-99.
[23]	Kuzyakov Y, Xu XL (2013). Competition between roots and microorganisms for nitrogen: mechanisms and ecological relevance. New Phytologist, 198, 656-669. DOI PMID
[24]	Lai JS (2019). An explanation about the negative value in the common explanation part of environmental factors in redundancy analysis (RDA).[2023-05-29]. https://blog.sciencenet.cn/blog-267448-1187530.html.
	[赖江山 (2019). 关于冗余分析(RDA)中环境因子共同解释部分出现负值的说明.[2023-05-29]. https://blog.sciencenet.cn/blog-267448-1187530.html.
[25]	Li YL, Cui JY, Su YZ (2005). Specific leaf area and leaf dry matter content of some plants in different dune habitats. Acta Ecologica Sincia, 25, 304-311.
	[李玉霖, 崔建垣, 苏永中 (2005). 不同沙丘生境主要植物比叶面积和叶干物质含量的比较. 生态学报, 25, 304-311.]
[26]	Liu S, Sheng KY, Liu XS, Wu ZH, Guo XM, Xiao FM, Zhang WY (2017). Contents of soil organic carbon and nitrogen forms in rhizosphere soil of Cunninghamia lanceolata and the rhizosphere effect. Chinese Journal of Ecology, 36, 1957-1964.
	[刘顺, 盛可银, 刘喜帅, 吴珍花, 郭晓敏, 肖复明, 张文元 (2017). 陈山红心山根际土壤有机碳、氮含量及根际效应. 生态学杂志, 36, 1957-1964.]
[27]	Liu XJ, Ma KP (2015). Plant functional traits—Concepts, applications and future directions. Scientia Sinica (Vitae), 45, 325-339.
	[刘晓娟, 马克平 (2015). 植物功能性状研究进展. 中国科学: 生命科学, 45, 325-339.]
[28]	Mo XL, Dai XQ, Wang HM, Fu XL, Kou L (2018). Rhizosphere effects of overstory tree and understory shrub species in central subtropical plantations—A case study at Qianyanzhou, Taihe, Jiangxi, China. Chinese Journal of Plant Ecology, 42, 723-733.
	[莫雪丽, 戴晓琴, 王辉民, 付晓莉, 寇亮 (2018). 中亚热带典型人工林常见乔灌木根际效应——以江西泰和千烟洲为例. 植物生态学报, 42, 723-733.] DOI
[29]	Moorhead DL, Rinkes ZL, Sinsabaugh RL, Weintraub MN (2013). Dynamic relationships between microbial biomass, respiration, inorganic nutrients and enzyme activities: informing enzyme-based decomposition models. Frontiers in Microbiology, 4, 223. DOI: 10.3389/fmicb.2013.00223.
[30]	Moorhead DL, Sinsabaugh RL, Hill BH, Weintraub MN (2016). Vector analysis of ecoenzyme activities reveal constraints on coupled C, N and P dynamics. Soil Biology & Biochemistry, 93, 1-7.
[31]	Paterson E, Gebbing T, Abel C, Sim A, Telfer G (2007). Rhizodeposition shapes rhizosphere microbial community structure in organic soil. New Phytologist, 173, 600-610. DOI PMID
[32]	Pausch J, Zhu B, Kuzyakov Y, Cheng WX (2013). Plant inter-species effects on rhizosphere priming of soil organic matter decomposition. Soil Biology & Biochemistry, 57, 91-99.
[33]	Pérez-Harguindeguy N, Díaz S, Garnier E, Lavorel S, Poorter H, Jaureguiberry P, Bret-Harte MS, Cornwell WK, Craine JM, Gurvich DE, Urcelay C, Veneklaas EJ, Reich PB, Poorter L, Wright IJ, et al. (2013). New handbook for standardised measurement of plant functional traits worldwide. Australian Journal of Botany, 61, 167. DOI: 10.1071/BT12225.
[34]	Philippot L, Raaijmakers JM, Lemanceau P, van der Putten WH (2013). Going back to the roots: the microbial ecology of the rhizosphere. Nature Reviews Microbiology, 11, 789-799. DOI PMID
[35]	Phillips RP, Fahey TJ (2006). Tree species and mycorrhizal associations influence the magnitude of rhizosphere effects. Ecology, 87, 1302-1313. PMID
[36]	Phillips RP, Fahey TJ (2008). The influence of soil fertility on rhizosphere effects in northern hardwood forest soils. Soil Science Society of America Journal, 72, 453-461.
[37]	Stone EL, Gibson EJ (1975). Effects of species on nutrient cycles and soil change. Philosophical Transactions of the Royal Society of London B, Biological Sciences, 271, 149-162.
[38]	Strickland MS, Rousk J (2010). Considering fungal:bacterial dominance in soils—Methods, controls, and ecosystem implications. Soil Biology & Biochemistry, 42, 1385-1395.
[39]	Su HX, Li GQ (2012). Simulating the response of the Quercus mongolica forest ecosystem carbon budget to asymmetric warming. Chinese Science Bulletin, 57, 1544-1552.
	[苏宏新, 李广起 (2012). 模拟蒙古栎林生态系统碳收支对非对称性升温的响应. 科学通报, 57, 1544-1552.]
[40]	Sun L, Ataka M, Han M, Han Y, Gan D, Xu T, Guo Y, Zhu B (2021). Root exudation as a major competitive fine-root functional trait of 18 coexisting species in a subtropical forest. New Phytologist, 229, 259-271.
[41]	Sun LJ, Ataka M, Kominami Y, Yoshimura K (2017). Relationship between fine-root exudation and respiration of two Quercus species in a Japanese temperate forest. Tree Physiology, 37, 1011-1020.
[42]	Sun Y, Xu XL, Kuzyakov Y (2014). Mechanisms of rhizosphere priming effects and their ecological significance. Chinese Journal of Plant Ecology, 38, 62-75.
	[孙悦, 徐兴良, Kuzyakov Y, (2014). 根际激发效应的发生机制及其生态重要性. 植物生态学报, 38, 62-75.] DOI
[43]	Wang XP, Xiao X, Tang TW, Li YX, Xiao J (2018). Seasonal changes of the input of root exudates and its driving characteristics of rhizosphere microbe in a Cercidiphyllum japonicum Sieb. plantation. Bulletin of Botanical Research, 38(1), 47-55. DOI
	[王小平, 肖肖, 唐天文, 黎云祥, 肖娟 (2018). 连香树人工林根系分泌物输入季节性变化及其驱动的根际微生物特性研究. 植物研究, 38(1), 47-55.] DOI
[44]	Xiao W, Chen X, Jing X, Zhu B (2018). A meta-analysis of soil extracellular enzyme activities in response to global change. Soil Biology & Biochemistry, 123, 21-32.
[45]	Yao H, Hu XY, Zhu JL, Zhu JX, Ji CJ, Fang JY (2015). Soil respiration and the 20-year change in three temperate forests in Mt. Dongling, Beijing. Chinese Journal of Plant Ecology, 39, 849-856. DOI
	[姚辉, 胡雪洋, 朱江玲, 朱剑霄, 吉成均, 方精云 (2015). 北京东灵山3种温带森林土壤呼吸及其20年的变化. 植物生态学报, 39, 849-856.] DOI
[46]	Zhu B, Cheng WX (2012). Nodulated soybean enhances rhizosphere priming effects on soil organic matter decomposition more than non-nodulated soybean. Soil Biology & Biochemistry, 51, 56-65.
[47]	Zhu B, Gutknecht JLM, Herman DJ, Keck DC, Firestone MK, Cheng WX (2014). Rhizosphere priming effects on soil carbon and nitrogen mineralization. Soil Biology & Biochemistry, 76, 183-192.
[48]	Zhu B, Panke-Buisse K, Kao-Kniffin J (2015). Nitrogen fertilization has minimal influence on rhizosphere effects of smooth crabgrass (Digitaria ischaemum) and bermudagrass (Cynodon dactylon). Journal of Plant Ecology, 8, 390-400.
[49]	Zhu XM, Liu DY, Yin HJ (2021). Roots regulate microbial N processes to achieve an efficient NH₄⁺ supply in the rhizosphere of alpine coniferous forests. Biogeochemistry, 155, 39-57.

		白桦林 Betula platyphylla forest					蒙古栎林 Quercus mongolica forest
		春 Spring	夏 Summer	秋 Autumn		冬 Winter	春 Spring		夏 Summer	秋 Autumn	冬 Winter
SWC (%)	r	42.11 ± 2.97^a	45.71 ± 1.39^a	18.77 ± 1.04^b		45.74 ± 5.75^a	17.11 ± 0.39^c		30.75 ± 1.18^a	13.32 ± 0.80^d	26.13 ± 1.46^b
SWC (%)	b	43.62 ± 2.20^a	44.85 ± 1.21^a	16.84 ± 0.76^b		46.25 ± 7.61^a	20.96 ± 3.26^b		29.76 ± 1.62^a	12.60 ± 0.84^c	24.33 ± 1.85a^b
pH	r	5.48 ± 0.08^c	5.97 ± 0.19^b	6.45 ± 0.16^a		5.89 ± 0.07^bc	5.64 ± 0.07^b		5.55 ± 0.13^b	6.20 ± 0.17^a	5.57 ± 0.19^b
pH	b	6.41 ± 0.06^a	6.39 ± 0.24^a	6.65 ± 0.14^a		6.46 ± 0.13^a	6.34 ± 0.08^a		5.82 ± 0.06^b	6.44 ± 0.13^a	5.55 ± 0.21^b
EOC content (mg·kg^-1)	r	1 420.02 ± 212.81^a	1 552.22 ± 143.35^a	741.49 ± 125.89^b		491.32 ± 110.09^b	955.42 ± 77.67^a		1 092.27 ± 81.65^a	494.17 ± 43.51^b	263.94 ± 20.23^c
EOC content (mg·kg^-1)	b	1 175.09 ± 138.55^a	1 289.81 ± 96.76^a	485.55 ± 69.81^b		437.68 ± 74.89^b	922.87 ± 113.96^a		1 092.05 ± 102.71^a	404.52 ± 45.92^b	242.67 ± 13.41^b
TC content (mg·g^-1)	r	65.97 ± 6.84^a	63.22 ± 3.51^a	58.08 ± 5.95^a		88.08 ± 20.58^a	37.54 ± 1.03^a		35.58 ± 1.36^a	39.83 ± 3.33^a	35.97 ± 2.61^a
TC content (mg·g^-1)	b	58.99 ± 5.69^ab	55.09 ± 2.39^b	46.01 ± 4.06^b		86.64 ± 18.54^a	35.73 ± 1.74^a		33.94 ± 2.37^a	38.47 ± 3.58^a	34.64 ± 2.60^a
TN content (mg·g^-1)	r	5.16 ± 0.43^a	5.19 ± 0.32^a	4.54 ± 0.43^a		6.65 ± 1.49^a	3.18 ± 0.06^a		2.95 ± 0.14^a	3.27 ± 0.24^a	3.01 ± 0.23^a
TN content (mg·g^-1)	b	4.73 ± 0.42^ab	4.55 ± 0.23^ab	3.79 ± 0.27^b		6.65 ± 1.38^a	3.12 ± 0.19^a		2.85 ± 0.23^a	3.15 ± 0.27^a	2.91 ± 0.22^a
Soil C:N	r	12.74 ± 0.35^ab	12.19 ± 0.15^b	12.76 ± 0.13^ab		13.10 ± 0.35^a	11.81 ± 0.32^a		12.07 ± 0.30^a	12.16 ± 0.23^a	11.96 ± 0.13^a
Soil C:N	b	12.45 ± 0.13^b	12.11 ± 0.10^b	12.10 ± 0.21^b		12.96 ± 0.13^a	11.48 ± 0.30^a		11.97 ± 0.31^a	12.19 ± 0.16^a	11.91 ± 0.08^a
ETN content (mg·kg^-1)	r	138.18 ± 16.83^a	135.56 ± 10.73^a	50.48 ± 11.13^b		67.00 ± 15.17^b	86.18 ± 5.38^b		100.25 ± 2.12^a	31.80 ± 2.50^c	31.89 ± 1.82^c
ETN content (mg·kg^-1)	b	100.97 ± 11.66^a	110.43 ± 5.31^a	39.88 ± 5.38^b		59.03 ± 8.36^b	82.00 ± 8.12^a		93.73 ± 4.49^a	28.51 ± 1.57^b	33.99 ± 0.88^b
NH₄⁺-N content (μg·g^-1)	r	15.14 ± 1.34^ab	11.63 ± 1.15^ab	9.55 ± 1.24^b		19.79 ± 4.99^a	11.43 ± 0.54^ab		15.41 ± 2.54^a	8.53 ± 0.58^b	7.52 ± 0.42^b
NH₄⁺-N content (μg·g^-1)	b	5.08 ± 0.36^b	7.75 ± 0.68^a	6.86 ± 1.01^ab		7.18 ± 0.72^ab	6.10 ± 0.97^b		10.12 ± 1.34^a	5.02 ± 0.12^b	6.29 ± 0.71^b
NO₃^--N content (μg·g^-1)	r	2.94 ± 0.32^bc	5.82 ± 1.46^b	0.12 ± 0.02^c		12.43 ± 2.72^a	1.31 ± 0.28^b		4.57 ± 0.74^a	0.07 ± 0.00^b	3.98 ± 0.31^a
NO₃^--N content (μg·g^-1)	b	5.99 ± 0.76^b	7.31 ± 0.87^b	0.00 ± 0.00^c		16.42 ± 3.43^a	2.60 ± 0.67^b		5.99 ± 0.85^a	0.00 ± 0.00^c	5.14 ± 1.15^a
MBC content (mg·kg^-1)	r	1 224.41 ± 71.60^a	1 456.06 ± 115.29^a	1 202.39 ± 118.77^a		1 362.10 ± 290.82^a	509.07 ± 60.41^c		732.73 ± 39.53^b	920.16 ± 73.95^a	447.73 ± 40.34^c
MBC content (mg·kg^-1)	b	1 222.59 ± 140.84^a	1 160.56 ± 72.54^ab	692.14 ± 66.88^b		1 048.46 ± 295.22^ab	648.17 ± 104.11^a		608.29 ± 54.09^ab	405.67 ± 46.44^b	487.32 ± 71.78^ab
MBN content (mg·kg^-1)	r	210.49 ± 5.73^a	225.58 ± 19.78^a	86.91 ± 11.09^b		137.24 ± 29.16^b	66.34 ± 5.34^b		105.61 ± 7.91^a	62.91 ± 9.23^b	40.69 ± 4.47^c
MBN content (mg·kg^-1)	b	187.31 ± 26.82^a	187.49 ± 19.21^a	67.81 ± 7.86^b		140.38 ± 41.66^ab	93.36 ± 14.70^a		100.08 ± 6.35^a	36.12 ± 0.86^b	51.42 ± 9.80^b
MBC:MBN	r	5.82 ± 0.31^c	6.48 ± 0.24^c	14.03 ± 0.90^a		9.90 ± 0.07^b	7.77 ± 0.91^c		7.00 ± 0.35^c	15.12 ± 1.16^a	11.10 ± 0.62^b
MBC:MBN	b	6.66 ± 0.41^b	6.27 ± 0.29^b	10.38 ± 0.87^a		7.95 ± 0.72^b	7.03 ± 0.74^b		6.07 ± 0.38^b	11.18 ± 1.12^a	9.80 ± 0.68^a
C_min(mg·g^-1·d^-1)	r	0.21 ± 0.02^a	0.17 ± 0.01^a	0.04 ± 0.01^c		0.10 ± 0.01^b	0.14 ± 0.01^a		0.12 ± 0.02^a	0.02 ± 0.00^b	0.04 ± 0.00^b
C_min(mg·g^-1·d^-1)	b	0.21 ± 0.02^a	0.16 ± 0.02^b	0.02 ± 0.00^c		0.05 ± 0.01^c	0.18 ± 0.01^a		0.11 ± 0.01^b	0.02 ± 0.00^c	0.03 ± 0.00^c
N_min(μg·g^-1·d^-1)	r	5.01 ± 0.72^a	1.89 ± 0.29^b	0.98 ± 0.21^b		1.62 ± 0.35^b	1.02 ± 0.30^a		0.85 ± 0.23^ab	0.33 ± 0.08^b	0.90 ± 0.12^ab
N_min(μg·g^-1·d^-1)	b	3.23 ± 0.42^a	1.85 ± 0.26^b	0.81 ± 0.11^c		1.68 ± 0.23^b	1.38 ± 0.26^a		1.02 ± 0.37^ab	0.33 ± 0.06^b	1.07 ± 0.08^ab
	r	6.80 ± 1.58^b	21.89 ± 5.09^a	14.84 ± 1.97^ab		8.17 ± 1.61^b	2.68 ± 0.73^b		8.42 ± 0.59^a	6.48 ± 0.81^a	2.07 ± 0.43^b
BG activity (nmol·g^-1·h^-1)	b	13.34 ± 2.19^b	26.06 ± 4.15^a	16.24 ± 2.72^b		12.19 ± 1.84^b	4.95 ± 0.80^c		12.94 ± 1.27^a	8.07 ± 0.93^b	3.26 ± 0.53^c
NAG activity (nmol·g^-1·h^-1)	r	5.28 ± 0.60^c	24.51 ± 3.21^a	17.09 ± 1.63^b		6.65 ± 1.63^c	4.49 ± 0.68^b		11.79 ± 0.57^a	10.17 ± 2.57^a	2.74 ± 0.25^b
NAG activity (nmol·g^-1·h^-1)	b	6.62 ± 0.73^c	22.55 ± 1.14^a	14.37 ± 2.54^b		6.02 ± 1.07^c	4.73 ± 0.70^b		10.59 ± 1.03^a	8.68 ± 1.76^a	2.95 ± 0.40^b
AP activity (nmol·g^-1·h^-1)	r	26.79 ± 0.60^b	56.05 ± 5.74^a	36.61 ± 3.30^b		26.93 ± 3.61^b	19.43 ± 1.11^c		48.05 ± 1.25^a	32.79 ± 3.03^b	20.54 ± 1.60^c
AP activity (nmol·g^-1·h^-1)	b	29.90 ± 1.20^b	57.40 ± 11.50^a	32.49 ± 2.06^b		25.01 ± 1.76^b	22.56 ± 1.91^b		43.32 ± 4.59^a	25.08 ± 1.78^b	25.63 ± 1.42^b
POX+PER activity (μmol·g^-1·h^-1)	r	22.87 ± 1.69^a	10.10 ± 2.03^b	8.55 ± 1.06^b	11.23 ± 1.26^b		21.98 ± 3.58^a	14.08 ± 0.74^b		12.22 ± 1.58^b	13.07 ± 1.05^b
POX+PER activity (μmol·g^-1·h^-1)	b	24.52 ± 0.67^a	10.50 ± 1.54^b	8.23 ± 1.66^b	11.79 ± 1.08^b		21.06 ± 4.10^a	12.97 ± 0.76^bc		6.14 ± 0.92^c	15.83 ± 2.96^ab
Vector length	r	0.58 ± 0.05^a	0.54 ± 0.06^a	0.55 ± 0.03^a	0.61 ± 0.01^a		0.38 ± 0.06^a	0.44 ± 0.03^a		0.44 ± 0.05^a	0.43 ± 0.04^a
Vector length	b	0.73 ± 0.03^a	0.63 ± 0.06^a	0.62 ± 0.05^a	0.75 ± 0.01^a		0.54 ± 0.03^a	0.60 ± 0.01^a		0.55 ± 0.01^a	0.53 ± 0.06^a
Vector angle	r	70.62 ± 2.37^a	59.84 ± 3.90^bc	58.25 ± 2.46^c	67.96 ± 1.82^ab		72.20 ± 2.91^ab	70.31 ± 0.30^b		67.60 ± 1.87^b	77.84 ± 1.83^a
Vector angle	b	65.54 ± 1.54^a	59.08 ± 4.07^a	58.22 ± 1.98^a	64.48 ± 1.98^a		70.67 ± 2.47^b	67.21 ± 1.37^bc		63.50 ± 2.85^c	77.77 ± 1.45^a

		白桦林 Betula platyphylla forest					蒙古栎林 Quercus mongolica forest
		春 Spring	夏 Summer	秋 Autumn		冬 Winter	春 Spring		夏 Summer	秋 Autumn	冬 Winter
SWC (%)	r	42.11 ± 2.97^a	45.71 ± 1.39^a	18.77 ± 1.04^b		45.74 ± 5.75^a	17.11 ± 0.39^c		30.75 ± 1.18^a	13.32 ± 0.80^d	26.13 ± 1.46^b
SWC (%)	b	43.62 ± 2.20^a	44.85 ± 1.21^a	16.84 ± 0.76^b		46.25 ± 7.61^a	20.96 ± 3.26^b		29.76 ± 1.62^a	12.60 ± 0.84^c	24.33 ± 1.85a^b
pH	r	5.48 ± 0.08^c	5.97 ± 0.19^b	6.45 ± 0.16^a		5.89 ± 0.07^bc	5.64 ± 0.07^b		5.55 ± 0.13^b	6.20 ± 0.17^a	5.57 ± 0.19^b
pH	b	6.41 ± 0.06^a	6.39 ± 0.24^a	6.65 ± 0.14^a		6.46 ± 0.13^a	6.34 ± 0.08^a		5.82 ± 0.06^b	6.44 ± 0.13^a	5.55 ± 0.21^b
EOC content (mg·kg^-1)	r	1 420.02 ± 212.81^a	1 552.22 ± 143.35^a	741.49 ± 125.89^b		491.32 ± 110.09^b	955.42 ± 77.67^a		1 092.27 ± 81.65^a	494.17 ± 43.51^b	263.94 ± 20.23^c
EOC content (mg·kg^-1)	b	1 175.09 ± 138.55^a	1 289.81 ± 96.76^a	485.55 ± 69.81^b		437.68 ± 74.89^b	922.87 ± 113.96^a		1 092.05 ± 102.71^a	404.52 ± 45.92^b	242.67 ± 13.41^b
TC content (mg·g^-1)	r	65.97 ± 6.84^a	63.22 ± 3.51^a	58.08 ± 5.95^a		88.08 ± 20.58^a	37.54 ± 1.03^a		35.58 ± 1.36^a	39.83 ± 3.33^a	35.97 ± 2.61^a
TC content (mg·g^-1)	b	58.99 ± 5.69^ab	55.09 ± 2.39^b	46.01 ± 4.06^b		86.64 ± 18.54^a	35.73 ± 1.74^a		33.94 ± 2.37^a	38.47 ± 3.58^a	34.64 ± 2.60^a
TN content (mg·g^-1)	r	5.16 ± 0.43^a	5.19 ± 0.32^a	4.54 ± 0.43^a		6.65 ± 1.49^a	3.18 ± 0.06^a		2.95 ± 0.14^a	3.27 ± 0.24^a	3.01 ± 0.23^a
TN content (mg·g^-1)	b	4.73 ± 0.42^ab	4.55 ± 0.23^ab	3.79 ± 0.27^b		6.65 ± 1.38^a	3.12 ± 0.19^a		2.85 ± 0.23^a	3.15 ± 0.27^a	2.91 ± 0.22^a
Soil C:N	r	12.74 ± 0.35^ab	12.19 ± 0.15^b	12.76 ± 0.13^ab		13.10 ± 0.35^a	11.81 ± 0.32^a		12.07 ± 0.30^a	12.16 ± 0.23^a	11.96 ± 0.13^a
Soil C:N	b	12.45 ± 0.13^b	12.11 ± 0.10^b	12.10 ± 0.21^b		12.96 ± 0.13^a	11.48 ± 0.30^a		11.97 ± 0.31^a	12.19 ± 0.16^a	11.91 ± 0.08^a
ETN content (mg·kg^-1)	r	138.18 ± 16.83^a	135.56 ± 10.73^a	50.48 ± 11.13^b		67.00 ± 15.17^b	86.18 ± 5.38^b		100.25 ± 2.12^a	31.80 ± 2.50^c	31.89 ± 1.82^c
ETN content (mg·kg^-1)	b	100.97 ± 11.66^a	110.43 ± 5.31^a	39.88 ± 5.38^b		59.03 ± 8.36^b	82.00 ± 8.12^a		93.73 ± 4.49^a	28.51 ± 1.57^b	33.99 ± 0.88^b
NH₄⁺-N content (μg·g^-1)	r	15.14 ± 1.34^ab	11.63 ± 1.15^ab	9.55 ± 1.24^b		19.79 ± 4.99^a	11.43 ± 0.54^ab		15.41 ± 2.54^a	8.53 ± 0.58^b	7.52 ± 0.42^b
NH₄⁺-N content (μg·g^-1)	b	5.08 ± 0.36^b	7.75 ± 0.68^a	6.86 ± 1.01^ab		7.18 ± 0.72^ab	6.10 ± 0.97^b		10.12 ± 1.34^a	5.02 ± 0.12^b	6.29 ± 0.71^b
NO₃^--N content (μg·g^-1)	r	2.94 ± 0.32^bc	5.82 ± 1.46^b	0.12 ± 0.02^c		12.43 ± 2.72^a	1.31 ± 0.28^b		4.57 ± 0.74^a	0.07 ± 0.00^b	3.98 ± 0.31^a
NO₃^--N content (μg·g^-1)	b	5.99 ± 0.76^b	7.31 ± 0.87^b	0.00 ± 0.00^c		16.42 ± 3.43^a	2.60 ± 0.67^b		5.99 ± 0.85^a	0.00 ± 0.00^c	5.14 ± 1.15^a
MBC content (mg·kg^-1)	r	1 224.41 ± 71.60^a	1 456.06 ± 115.29^a	1 202.39 ± 118.77^a		1 362.10 ± 290.82^a	509.07 ± 60.41^c		732.73 ± 39.53^b	920.16 ± 73.95^a	447.73 ± 40.34^c
MBC content (mg·kg^-1)	b	1 222.59 ± 140.84^a	1 160.56 ± 72.54^ab	692.14 ± 66.88^b		1 048.46 ± 295.22^ab	648.17 ± 104.11^a		608.29 ± 54.09^ab	405.67 ± 46.44^b	487.32 ± 71.78^ab
MBN content (mg·kg^-1)	r	210.49 ± 5.73^a	225.58 ± 19.78^a	86.91 ± 11.09^b		137.24 ± 29.16^b	66.34 ± 5.34^b		105.61 ± 7.91^a	62.91 ± 9.23^b	40.69 ± 4.47^c
MBN content (mg·kg^-1)	b	187.31 ± 26.82^a	187.49 ± 19.21^a	67.81 ± 7.86^b		140.38 ± 41.66^ab	93.36 ± 14.70^a		100.08 ± 6.35^a	36.12 ± 0.86^b	51.42 ± 9.80^b
MBC:MBN	r	5.82 ± 0.31^c	6.48 ± 0.24^c	14.03 ± 0.90^a		9.90 ± 0.07^b	7.77 ± 0.91^c		7.00 ± 0.35^c	15.12 ± 1.16^a	11.10 ± 0.62^b
MBC:MBN	b	6.66 ± 0.41^b	6.27 ± 0.29^b	10.38 ± 0.87^a		7.95 ± 0.72^b	7.03 ± 0.74^b		6.07 ± 0.38^b	11.18 ± 1.12^a	9.80 ± 0.68^a
C_min(mg·g^-1·d^-1)	r	0.21 ± 0.02^a	0.17 ± 0.01^a	0.04 ± 0.01^c		0.10 ± 0.01^b	0.14 ± 0.01^a		0.12 ± 0.02^a	0.02 ± 0.00^b	0.04 ± 0.00^b
C_min(mg·g^-1·d^-1)	b	0.21 ± 0.02^a	0.16 ± 0.02^b	0.02 ± 0.00^c		0.05 ± 0.01^c	0.18 ± 0.01^a		0.11 ± 0.01^b	0.02 ± 0.00^c	0.03 ± 0.00^c
N_min(μg·g^-1·d^-1)	r	5.01 ± 0.72^a	1.89 ± 0.29^b	0.98 ± 0.21^b		1.62 ± 0.35^b	1.02 ± 0.30^a		0.85 ± 0.23^ab	0.33 ± 0.08^b	0.90 ± 0.12^ab
N_min(μg·g^-1·d^-1)	b	3.23 ± 0.42^a	1.85 ± 0.26^b	0.81 ± 0.11^c		1.68 ± 0.23^b	1.38 ± 0.26^a		1.02 ± 0.37^ab	0.33 ± 0.06^b	1.07 ± 0.08^ab
	r	6.80 ± 1.58^b	21.89 ± 5.09^a	14.84 ± 1.97^ab		8.17 ± 1.61^b	2.68 ± 0.73^b		8.42 ± 0.59^a	6.48 ± 0.81^a	2.07 ± 0.43^b
BG activity (nmol·g^-1·h^-1)	b	13.34 ± 2.19^b	26.06 ± 4.15^a	16.24 ± 2.72^b		12.19 ± 1.84^b	4.95 ± 0.80^c		12.94 ± 1.27^a	8.07 ± 0.93^b	3.26 ± 0.53^c
NAG activity (nmol·g^-1·h^-1)	r	5.28 ± 0.60^c	24.51 ± 3.21^a	17.09 ± 1.63^b		6.65 ± 1.63^c	4.49 ± 0.68^b		11.79 ± 0.57^a	10.17 ± 2.57^a	2.74 ± 0.25^b
NAG activity (nmol·g^-1·h^-1)	b	6.62 ± 0.73^c	22.55 ± 1.14^a	14.37 ± 2.54^b		6.02 ± 1.07^c	4.73 ± 0.70^b		10.59 ± 1.03^a	8.68 ± 1.76^a	2.95 ± 0.40^b
AP activity (nmol·g^-1·h^-1)	r	26.79 ± 0.60^b	56.05 ± 5.74^a	36.61 ± 3.30^b		26.93 ± 3.61^b	19.43 ± 1.11^c		48.05 ± 1.25^a	32.79 ± 3.03^b	20.54 ± 1.60^c
AP activity (nmol·g^-1·h^-1)	b	29.90 ± 1.20^b	57.40 ± 11.50^a	32.49 ± 2.06^b		25.01 ± 1.76^b	22.56 ± 1.91^b		43.32 ± 4.59^a	25.08 ± 1.78^b	25.63 ± 1.42^b
POX+PER activity (μmol·g^-1·h^-1)	r	22.87 ± 1.69^a	10.10 ± 2.03^b	8.55 ± 1.06^b	11.23 ± 1.26^b		21.98 ± 3.58^a	14.08 ± 0.74^b		12.22 ± 1.58^b	13.07 ± 1.05^b
POX+PER activity (μmol·g^-1·h^-1)	b	24.52 ± 0.67^a	10.50 ± 1.54^b	8.23 ± 1.66^b	11.79 ± 1.08^b		21.06 ± 4.10^a	12.97 ± 0.76^bc		6.14 ± 0.92^c	15.83 ± 2.96^ab
Vector length	r	0.58 ± 0.05^a	0.54 ± 0.06^a	0.55 ± 0.03^a	0.61 ± 0.01^a		0.38 ± 0.06^a	0.44 ± 0.03^a		0.44 ± 0.05^a	0.43 ± 0.04^a
Vector length	b	0.73 ± 0.03^a	0.63 ± 0.06^a	0.62 ± 0.05^a	0.75 ± 0.01^a		0.54 ± 0.03^a	0.60 ± 0.01^a		0.55 ± 0.01^a	0.53 ± 0.06^a
Vector angle	r	70.62 ± 2.37^a	59.84 ± 3.90^bc	58.25 ± 2.46^c	67.96 ± 1.82^ab		72.20 ± 2.91^ab	70.31 ± 0.30^b		67.60 ± 1.87^b	77.84 ± 1.83^a
Vector angle	b	65.54 ± 1.54^a	59.08 ± 4.07^a	58.22 ± 1.98^a	64.48 ± 1.98^a		70.67 ± 2.47^b	67.21 ± 1.37^bc		63.50 ± 2.85^c	77.77 ± 1.45^a

	白桦 Betula platyphylla				蒙古栎 Quercus mongolica
	春 Spring	夏 Summer	秋 Autumn	冬 Winter	春 Spring	夏 Summer	秋 Autumn	冬 Winter
SLA (m²·kg^-1)	33.1 ± 1.6^a	29.1 ± 2.1^a	22.5 ± 0.8^b	NA	20.4 ± 1.3^a	16.4 ± 0.8^b	16.1 ± 0.3^b	NA
LDMC (g·g^-1)	0.189 ± 0.005^b	0.173 ± 0.008^b	0.261 ± 0.010^a	NA	0.217 ± 0.010^b	0.214 ± 0.004^b	0.348 ± 0.004^a	NA
Leaf C content (mg·g^-1)	NA	481 ± 7^a	491 ± 2^a	NA	458 ± 1^c	480 ± 3^a	467 ± 2^b	NA
Leaf N content (mg·g^-1)	NA	27.4 ± 1.0^a	21.2 ± 0.7^b	NA	56.1 ± 0.7^a	27.5 ± 0.6^b	21.2 ± 0.6^c	NA
Leaf C:N	NA	17.7 ± 0.8^b	23.2 ± 0.8^a	NA	8.2 ± 0.1^c	17.5 ± 0.3^b	22.1 ± 0.5^a	NA
Fine root biomass (g)	21.2 ± 1.8^b	25.6 ± 2.9^b	37.6 ± 2.7^a	6.4 ± 0.3^c	15.9 ± 1.3^b	25.9 ± 1.3^a	28.7 ± 2.8^a	6.7 ± 0.9^c
Root C content (mg·g^-1)	489 ± 8^b	463 ± 7^c	484 ± 6^b	518 ± 3^a	500 ± 4^a	494 ± 8^a	497 ± 9^a	507 ± 1^a
Root N content (mg·g^-1)	12.28 ± 0.47^a	9.98 ± 0.66^ab	9.34 ± 0.32^b	11.19 ± 1.10^ab	9.65 ± 0.61^a	9.13 ± 0.34^a	9.70 ± 0.97^a	8.38 ± 0.69^a
Root C:N	40.1 ± 2.2^b	47.2 ± 3.1^ab	52.1 ± 2.2^a	48.2 ± 4.8^ab	52.7 ± 3.5^a	54.5 ± 2.7^a	53.7 ± 6.2^a	61.9 ± 4.5^a
Fine root density (kg·m^-3)	1 077 ± 127^b	1 285 ± 161^b	2 091 ± 150^a	NA	580 ± 78^b	1437 ± 71^a	1 593 ± 153^a	NA

	白桦 Betula platyphylla				蒙古栎 Quercus mongolica
	春 Spring	夏 Summer	秋 Autumn	冬 Winter	春 Spring	夏 Summer	秋 Autumn	冬 Winter
SLA (m²·kg^-1)	33.1 ± 1.6^a	29.1 ± 2.1^a	22.5 ± 0.8^b	NA	20.4 ± 1.3^a	16.4 ± 0.8^b	16.1 ± 0.3^b	NA
LDMC (g·g^-1)	0.189 ± 0.005^b	0.173 ± 0.008^b	0.261 ± 0.010^a	NA	0.217 ± 0.010^b	0.214 ± 0.004^b	0.348 ± 0.004^a	NA
Leaf C content (mg·g^-1)	NA	481 ± 7^a	491 ± 2^a	NA	458 ± 1^c	480 ± 3^a	467 ± 2^b	NA
Leaf N content (mg·g^-1)	NA	27.4 ± 1.0^a	21.2 ± 0.7^b	NA	56.1 ± 0.7^a	27.5 ± 0.6^b	21.2 ± 0.6^c	NA
Leaf C:N	NA	17.7 ± 0.8^b	23.2 ± 0.8^a	NA	8.2 ± 0.1^c	17.5 ± 0.3^b	22.1 ± 0.5^a	NA
Fine root biomass (g)	21.2 ± 1.8^b	25.6 ± 2.9^b	37.6 ± 2.7^a	6.4 ± 0.3^c	15.9 ± 1.3^b	25.9 ± 1.3^a	28.7 ± 2.8^a	6.7 ± 0.9^c
Root C content (mg·g^-1)	489 ± 8^b	463 ± 7^c	484 ± 6^b	518 ± 3^a	500 ± 4^a	494 ± 8^a	497 ± 9^a	507 ± 1^a
Root N content (mg·g^-1)	12.28 ± 0.47^a	9.98 ± 0.66^ab	9.34 ± 0.32^b	11.19 ± 1.10^ab	9.65 ± 0.61^a	9.13 ± 0.34^a	9.70 ± 0.97^a	8.38 ± 0.69^a
Root C:N	40.1 ± 2.2^b	47.2 ± 3.1^ab	52.1 ± 2.2^a	48.2 ± 4.8^ab	52.7 ± 3.5^a	54.5 ± 2.7^a	53.7 ± 6.2^a	61.9 ± 4.5^a
Fine root density (kg·m^-3)	1 077 ± 127^b	1 285 ± 161^b	2 091 ± 150^a	NA	580 ± 78^b	1437 ± 71^a	1 593 ± 153^a	NA