Chin J Plant Ecol ›› 2019, Vol. 43 ›› Issue (3): 258-272.doi: 10.17521/cjpe.2018.0299

• Research Articles • Previous Articles    

Characteristics of soil enzymes stoichiometry in rhizosphere of understory vegetation in subtropical forest plantations

GAO Yu-Qiu1,2,DAI Xiao-Qin1,2,3,*(),WANG Jian-Lei1,FU Xiao-Li1,2,3,KOU Liang1,2,3,WANG Hui-Min1,2,3,4   

  1. 1 Qianyanzhou Ecological Research Station, Key Laboratory of Ecosystem Network Observation and Modeling, Institute of Geographic Science and Natural Resources Research, Chinese Academy of Sciences, Beijing 100101, China
    2 College of Resource and Environment, University of Chinese Academy of Sciences, Beijing 100190, China
    3 Zhongke-Ji’an Institute of Eco-Environmental Sciences, Ji’an, Jiangxi 343000, China;
    4 Jiangxi Province Key Laboratory of Regional Ecological Processes and Information, Taihe, Jiangxi 343725, China
  • Received:2018-11-30 Revised:2019-03-07 Online:2019-04-23 Published:2019-03-20
  • Contact: DAI Xiao-Qin
  • Supported by:
    Supported by the National Natural Science Foundation of China(31730014);The National Key R&D Program of China(2016YFD0600202)


Aims The objective was to explore the stoichiometry of rhizosphere soil enzymes under major understory vegetation and their responses to plantation types and seasons.

Methods Rhizosphere soils of understory shrubs (Loropetalum chinense, Adinandra millettii and Eurya muricata) and herbs (Woodwardia japonica and Dryopteris atrata) were sampled in the early growth stage (April) and the vigorous growth stage (July) in Cunninghamia lanceolata, Pinus massoniana and Pinus elliottii plantations at Qianyanzhou Ecological Research Station, Taihe, Jiangxi. Potential activities of β-1,4-glucosidase (BG, carbon (C) acquiring enzyme), β-1,4-N-acetylglucosaminidase (NAG, nitrogen (N) acquiring enzyme) and leucine aminopeptidase (LAP, N-acquiring enzyme), acid phosphatase (AP, phosphorus (P) acquiring enzyme) and their stoichiometric ratios were measured. Soil physical and chemical properties were also analyzed.

Important findings The results found that (1) rhizosphere soil extracellular enzyme activities associated with C and N acquisition and BG:AP (enzyme C:P) were significantly different among understory species, but P acquisition were not. Both forest stand types and sampling seasons influenced BG:(NAG+LAP) (enzyme C:N). Interactions of understory species, forest stand types and seasons observably affected enzyme C:P. Principal component analysis showed that rhizosphere soil enzyme activities and ecoenzymatic stoichiometry differed significantly among different understory species (Loropetalum chinense was obviously different from Eurya muricata, and both of them were evidently different from other understory species), forest stand types (Cunninghamia lanceolata was different from Pinus massoniana and Pinus elliottii plantations) and sampling seasons. Soil NO3 --N, NH4 +-N, DOC content and C:N were the main edaphic abiotic factors influencing the rhizosphere soil enzyme activities and ecoenzymatic stoichiometry. (2) Standardized major axis analysis showed that there were significantly linear relationship among lg(BG), lg(NAG+LAP) and lg(AP) of rhizosphere soils of understory species. lgBG:lg(NAG+LAP):lgAP(enzyme C:N:P) was approximately 1:1:1.3. Rhizosphere soil enzyme C:P and (NAG+LAP):AP (enzyme N:P) of understory species were 0.14 and 0.15, respectively. The regression slopes of lg(BG), lg(NAG+LAP) and lg(AP) deviated significantly from 1 because AP activities were much higher than BG activities and NAG+LAP activities. This study found that rhizosphere soil enzyme activities and ecoenzymatic stoichiometry were affected by understory species, forest stand types and sampling seasons in which substrate availability played an important role. Compared with C- and N-acquiring enzymes, microorganisms allocated more resources to the production of P-acquiring enzymes, which implied that the growth and activity of soil microorganisms were much more limited by P in rhizosphere soil of understory vegetation in subtropical plantations.

Key words: plantation, soil extracellular enzyme, ecological stoichiometry, red soils

Table 1

Characteristics of understory shrub and herb species in three subtropical plantations"

Forest stand type
Understory species
diameter (mm)
width (cm)
value (%)
檵木 Loropetalum chinense 11.9 ± 2.7 126 ± 31 81 ± 15 - 19.72
杨桐 Adinandra millettii 13.1 ± 1.0 152 ± 13 94 ± 7 - 30.44
格药柃 Eurya muricata 13.2 ± 1.5 142 ± 16 86 ± 9 - 32.71
狗脊蕨 Woodwardia japonica - 94 ± 12 - 71 ± 7 3.09
暗鳞鳞毛蕨 Dryopteris atrata - 60 ± 5 - 43 ± 8 1.89
Pinus massoniana forest
檵木 Loropetalum chinense 18.9 ± 2.0 413 ± 41 144 ± 16 - 33.68
杨桐 Adinandra millettii 26.7 ± 2.3 376 ± 64 160 ± 12 - 39.88
格药柃 Eurya muricata 13.2 ± 1.1 302 ± 50 81 ± 6 - 31.43
狗脊蕨 Woodwardia japonica - 99 ± 6 - 60 ± 7 3.85
暗鳞鳞毛蕨 Dryopteris atrata - 64 ± 6 - 53 ± 7 3.41
Pinus elliottii forest
檵木 Loropetalum chinense 25.7 ± 1.7 244 ± 34 180 ± 11 - 36.39
杨桐 Adinandra millettii 20.3 ± 3.1 206 ± 21 118 ± 16 - 33.11
格药柃 Eurya muricata 19.6 ± 3.8 112 ± 25 106 ± 18 - 19.22
狗脊蕨 Woodwardia japonica - 86 ± 10 - 73 ± 8 4.15
暗鳞鳞毛蕨 Dryopteris atrata - 70 ± 4 - 38 ± 5 2.07


变异来源 Source of variation 酶相关参数 Parameter of soil enzyme
林分类型 Forest stand types (F) 0.061 0.881 0.156 0.013* 0.092 0.938
林下植被类型 Understory species (U) 0.009** 0.010* 0.173 0.165 0.027* 0.286
取样季节 Sampling seasons (S) 0.066 0.575 0.148 0.032* 0.082 0.113
F × U 0.556 0.920 0.423 0.845 0.580 0.821
F × S 0.070 0.054 0.089 0.294 0.057 0.122
U × S 0.112 0.792 0.957 0.331 0.167 0.573
F × U × S 0.260 0.396 0.823 0.495 0.036* 0.221

Fig. 1

Rhizosphere soil enzyme activities of understory vegetation under different forest stand types in subtropical plantations (mean + SE, n = 5). CL, Cunninghamia lanceolata forest; PM, Pinus massoniana forest; PE, Pinus elliottii forest. LC, Loropetalum chinense; AM, Adinandra millettii; EM, Eurya muricata; WJ, Woodwardia japonica; DA, Dryopteris atrata. Different lowercase letters were significantly different among different understory vegetation species of the same forest stand types at the same sampling season (p < 0.05), Different uppercase letters were significantly different among different stand types at the same sampling season (p < 0.05). BG, β-1,4-glucosidase; NAG+LAP, the sum of β-1,4-N-acetylglucosaminidase and leucine aminopeptidase; AP, acid phosphatase."

Fig. 2

Rhizosphere soil ecoenzymatic stoichiometry of understory vegetation under different forest stand types in subtropical plantations (mean + SE, n = 5). CL, Cunninghamia lanceolata forest; PM, Pinus massoniana forest; PE, Pinus elliottii forest. LC, Loropetalum chinense; AM, Adinandra millettii; EM, Eurya muricata; WJ, Woodwardia japonica; DA, Dryopteris atrata. Different lowercase letters were significantly different among different understory vegetation species of the same forest stand types at the same sampling season (p < 0.05), Different uppercase letters were significantly different among different stand types at the same sampling season (p < 0.05). BG, β-1,4-glucosidase; NAG+LAP, the sum of β-1,4-N-acetylglucosaminidase and leucine aminopeptidase; AP, acid phosphatase."

Fig. 3

Standardized major axis regressions of the log-transformed soil C-, N-, and P-acquiring enzyme activities in subtropical plantations (n = 150). The colors represent the forest stand types: red symbols, Cunninghamia lanceolata forest; green symbols, Pinus massoniana forest; blue symbols, Pinus elliottii forest. Filled symbols and open symbols respectively represent the sampling seasons at April and July.CL, Cunninghamia lanceolata forest; PM, Pinus massoniana forest; PE, Pinus elliottii forest. LC, Loropetalum chinense; AM, Adinandra millettii; EM, Eurya muricata; WJ, Woodwardia japonica; DA, Dryopteris atrata. BG, β-1,4-glucosidase; NAG+LAP, the sum of β-1,4-N-acetylglucosaminidase and leucine aminopeptidase; AP, acid phosphatase."

Fig. 4

Principal component analysis (PCA) of soil enzyme activities and ecoenzymatic stoichiometry in subtropical plantations. The effect of sampling seasons is from the average of PCA scores of soil enzyme activities and ecoenzymatic stoichiometry of understory vegetation within the same season. The effect of forest stand types is from the average of PCA scores of soil enzyme activities and ecoenzymatic stoichiometry of understory vegetation within the same forest stand type. The effect of understory species is from the average of PCA site scores of soil enzyme activities and ecoenzymatic stoichiometry of the same understory species. The colors represent the forest stand types: red symbols, Cunninghamia lanceolata forest; green symbols, Pinus massoniana forest; blue symbols, Pinus elliottii forest. CL, Cunninghamia lanceolata forest; PM, Pinus massoniana forest; PE, Pinus elliottii forest; LC, Loropetalum chinense; AM, Adinandra millettii; EM, Eurya muricata; WJ, Woodwardia japonica; DA, Dryopteris atrata."

Fig. 5

Redundancy analysis (RDA) of soil enzyme activities, ecoenzymatic stoichiometry and physical and chemical properties in subtropical plantations. NO3--N, nitrate nitrogen; NH4+-N, ammonium nitrogen; DOC, dissolved organic carbon; C:N, the ratio of total carbon to total nitrogen. BG, β-1,4-glucosidase; NAG+LAP, the sum of β-1,4-N-acetylglucosaminidase and leucine aminopeptidase; AP, acid phosphatase."

Table 3

Results (p-value) of multi-way repeated measures ANOVAs on the effects of forest stand types, understory species, sampling seasons and their interactions on four major soil nutrient factors in subtropical plantations"

变异来源 Source of variation DOC NH4+-N NO3--N C:N
林分类型 Forest stand types (F) 0.200 0.021* 0.221 0.112
林下植被类型 Understory species (U) 0.000** 0.002** 0.002** 0.000**
取样季节 Sampling seasons (S) 0.226 0.003** 0.178 0.296
F × U 0.735 0.658 0.506 0.058
F × S 0.407 0.384 0.009** 0.623
U × S 0.311 0.095 0.084 0.267
F × U × S 0.129 0.511 0.270 0.800
[1] Allison SD, Weintraub MN, Gartner TB, Waldrop MP ( 2011). Evolutionary-economic principles as regulators of soil enzyme production and ecosystem function. Soil Enzymology, 22, 229-243.
[2] Bell C, Carrillo Y, Boot CM, Rocca JD, Pendall E, Wallenstein MD ( 2014). Rhizosphere stoichiometry: Are C:N:P ratios of plants, soils, and enzymes conserved at the plant species-level? New Phytologist, 201, 505-517.
[3] Bengtson P, Barker J, Grayston SJ ( 2012). Evidence of a strong coupling between root exudation, C and N availability, and stimulated SOM decomposition caused by rhizosphere priming effects. Ecology and Evolution, 2, 1843-1852.
[4] Bird JA, Herman DJ, Firestone MK ( 2011). Rhizosphere priming of soil organic matter by bacterial groups in a grassland soil. Soil Biology & Biochemistry, 43, 718-725.
[5] Borcard D, Gillet F, Legendre P ( 2011). Numerical Ecology with R. Springer, New York.
[6] Burns RG ( 1978). Soil Enzymes. Academic Press, New York.
[7] Chapin III FS, Matson PA, Mooney HA ( 2002). Principles of Terrestrial Ecosystem Ecology. Springer, New York.
[8] 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.
[9] Cheng W, Johnson DW, Fu S ( 2003). Rhizosphere effects on decomposition: Controls of plant species, phenology, and fertilization. Soil Science Society of America Journal, 67, 1418-1427.
[10] Cleveland CC, Liptzin D ( 2007). C:N:P stoichiometry in soil: Is there a “Redfield ratio” for the microbial biomass? Biogeochemistry, 85, 235-252.
[11] Cui YX, Fang LC, Guo XB, Wang X, Zhang YJ, Li PF, Zhang XC ( 2018). Ecoenzymatic stoichiometry and microbial nutrient limitation in rhizosphere soil in the arid area of the northern Loess Plateau, China. Soil Biology & Biochemistry, 116, 11-21.
[12] Dai XQ, Fu XL, Kou L, Wang HM, Shock CC ( 2018). C:N:P stoichiometry of rhizosphere soils differed significantly among overstory trees and understory shrubs in plantations in subtropical China. Canadian Journal of Forest Research, 48, 1398-1405.
[13] DeForest JL, Zak DR, Pregitzer KS, Burton AJ ( 2004). Atmospheric nitrate deposition, microbial community composition, and enzyme activity in northern hardwood forests. Soil Science Society of America Journal, 68, 132-138.
[14] Du Z, Cai XH, Bao WK, Chen H, Pan HL ( 2016). Understory effects on overstory trees: A review. Chinese Journal of Applied Ecology, 27, 963-972.
[ 杜忠, 蔡小虎, 包维楷, 陈槐, 潘红丽 ( 2016). 林下层植被对上层乔木的影响研究综述. 应用生态学报, 27, 963-972.]
[15] Duan L, Huang YM, Hao JM, Zhou ZP ( 2002). Vegetation uptake of nitrogen and base cation in China and its role in soil acidification. Environmental Science, 23(3), 69-74.
[ 段雷, 黄永梅, 郝吉明, 周中平 ( 2002). 中国植被对氮和盐基阳离子吸收速率及其在土壤酸化中的作用. 环境科学, 23(3), 69-74.]
[16] Fu XL, Yang FT, Wang JL, Di YB, Dai XQ, Zhang XY, Wang HM ( 2015). Understory vegetation leads to changes in soil acidity and in microbial communities 27 years after reforestation. Science of the Total Environment, 502, 280-286.
[17] Gianfreda L ( 2015). Enzymes of importance to rhizosphere processes. Journal of Soil Science and Plant Nutrition, 15, 283-306.
[18] Guo DL, Xia MX, Wei X, Chang WJ, Liu Y, Wang ZQ ( 2008). Anatomical traits associated with absorption and mycorrhizal colonization are linked to root branch order in twenty-three Chinese temperate tree species. New Phytologist, 180, 673-683.
[19] Guo ZM, Zhang XY, Li DD, Dong WT, Li ML ( 2017). Characteristics of soil organic carbon and related exo-enzyme activities at different altitudes in temperate forests. Chinese Journal of Applied Ecology, 28, 2888-2896.
[ 郭志明, 张心昱, 李丹丹, 董文亭, 李美玲 ( 2017). 温带森林不同海拔土壤有机碳及相关胞外酶活性特征. 应用生态学报, 28, 2888-2896.]
[20] He TX, Li YP, Zhang FY, Wang QK ( 2015). Effects of understory removal on soil respiration and microbial community composition structure in a Chinese fir plantation. Chinese Journal of Plant Ecology, 39, 797-806.
[ 贺同鑫, 李艳鹏, 张方月, 王清奎 ( 2015). 林下植被剔除对杉木林土壤呼吸和微生物群落结构的影响. 植物生态学报, 39, 797-806.]
[21] Hill BH, Elonen CM, Jicha TM, Bolgrien DW, Moffett MF ( 2010). Sediment microbial enzyme activity as an indicator of nutrient limitation in great lakes coastal wetlands. Freshwater Biology, 51, 1670-1683.
[22] Hill BH, Elonen CM, Jicha TM, Kolka RK, Lehto LLP, Sebestyen SD, Seifert-Monson LR ( 2014). Ecoenzymatic stoichiometry and microbial processing of organic matter in northern bogs and fens reveals a common P-limitation between peatland types. Biogeochemistry, 120, 203-224.
[23] Hu YL, Wang SL, Huang Y, Yu XJ ( 2005). Effects of litter chemistry on soil biological property and enzymatic activity. Acta Ecoligica Sinica, 25, 2662-2668.
[ 胡亚林, 汪思龙, 黄宇, 于小军 ( 2005). 凋落物化学组成对土壤微生物学性状及土壤酶活性的影响. 生态学报, 25, 2662-2668.]
[24] Huang YM, Yang WQ, Zhang J, Lu CT, Liu X, Wang W, Guo W, Zhang DJ ( 2014). Response of soil microorganism and soil enzyme activity to understory plant removal in the subalpine coniferous plantation of western Sichuan. Acta Ecologica Sinica, 34, 4183-4192.
[ 黄玉梅, 杨万勤, 张健, 卢昌泰, 刘旭, 王伟, 郭伟, 张丹桔 ( 2014). 川西亚高山针叶林土壤微生物及酶对林下植物去除的响应. 生态学报, 34, 4183-4192.]
[25] Kivlin SN, Treseder KK ( 2014). Soil extracellular enzyme activities correspond with abiotic factors more than fungal community composition. Biogeochemistry, 117, 23-37.
[26] Kuzyakov Y ( 2002). Review: Factors affecting rhizosphere priming effects. Journal of Plant Nutrition and Soil Science, 165, 66-70.
[27] Kuzyakov Y, Xu XL ( 2013). Competition between roots and microorganisms for nitrogen: Mechanisms and ecological relevance. New Phytologist, 198, 656-669.
[28] Li B ( 2000). Ecology. High Educational Press, Beijing.
[ 李博 ( 2000). 生态学. 高等教育出版社, 北京.]
[29] Li CC, Li QR, Xu XL, Ouyang H ( 2016). Nitrogen acquisition strategies of Cunninghamia lanceolata at different ages. Acta Ecologica Sinica, 36, 2620-2625.
[ 李常诚, 李倩茹, 徐兴良, 欧阳华 ( 2016). 不同林龄杉木氮素的获取策略. 生态学报, 36, 2620-2625.]
[30] Lin GG, McCormack ML, Ma CE, Guo DL ( 2017). Similar belowground carbon cycling dynamics but contrasting modes of nitrogen cycling between arbuscular mycorrhizal and ectomycorrhizal forests. New Phytologist, 213, 1440-1451.
[31] Lin GG, Zhao Q, Zhao L, Li HC, Zeng DH ( 2012). Effects of understory removal and nitrogen addition on the soil chemical and biological properties of Pinus sylvestris var. mongolica plantation in Keerqin Sandy Land. Chinese Journal of Applied Ecology, 23, 1188-1194.
[ 林贵刚, 赵琼, 赵蕾, 李慧超, 曾德慧 ( 2012). 林下植被去除与氮添加对樟子松人工林土壤化学和生物学性质的影响. 应用生态学报, 23, 1188-1194.]
[32] Lin N, Liu Y, Li GL, Yu HQ ( 2010). Research progress on forest soil enzyme. World Forestry Research, 23(4), 21-25.
[ 林娜, 刘勇, 李国雷, 于海群 ( 2010). 森林土壤酶研究进展. 世界林业研究, 23(4), 21-25.]
[33] Liu BT, Li HB, Zhu B, Koide RT, Eissenstat DM, Guo DL ( 2015). Complementarity in nutrient foraging strategies of absorptive fine roots and arbuscular mycorrhizal fungi across 14 coexisting subtropical tree species. New Phytologist, 208, 125-136.
[34] Liu JB, Chen GS, Guo JF, Yang ZJ, Li YQ, Lin CF, Yang YS ( 2017). Advances in research on the responses of forest soil enzymes to environmental change. Acta Ecologica Sinica, 37, 110-117.
[ 刘捷豹, 陈光水, 郭剑芬, 杨智杰, 李一清, 林成芳, 杨玉盛 ( 2017). 森林土壤酶对环境变化的响应研究进展. 生态学报, 37, 110-117.]
[35] Liu SJ, Xia X, Chen GM, Mao D, Che SG, Li YX ( 2011). Study progress on functions and affecting factors of soil enzymes. Chinese Agricultural Science Bulletin, 27(21), 1-7.
[ 刘善江, 夏雪, 陈桂梅, 卯丹, 车升国, 李亚星 ( 2011). 土壤酶的研究进展. 中国农学通报, 27(21), 1-7.]
[36] Lu SB, Zhou XQ, Rui YC, Chen CR, Xu ZH, Guo XM ( 2011). Effects of forest type on soil organic matter, microbial biomass, and enzyme activities. Chinese Journal of Applied Ecology, 22, 2567-2573.
[ 鲁顺保, 周小奇, 芮亦超, 陈成榕, 徐志红, 郭晓敏 ( 2011). 森林类型对土壤有机质、微生物生物量及酶活性的影响. 应用生态学报, 22, 2567-2573.]
[37] Mccormack ML, Guo DL, Iversen CM, Chen WL, Eissenstat DM, Fernandez CW, Li L, Ma CE, Ma ZQ, Poorter H, Reich PB, Zadworny M, Zanne A ( 2017). Building a better foundation: Improving root-trait measurements to understand and model plant and ecosystem processes. New Phytologist, 215, 27-37.
[38] McDaniel MD, Kaye JP, Kaye MW ( 2013). Increased temperature and precipitation had limited effects on soil extracellular enzyme activities in a post-harvest forest. Soil Biology & Biochemistry, 56, 90-98.
[39] McKane RB, Johnson LC, Shaver GR, Nadelhoffer KJ, Rastetter EB, Fry B, Giblin AE, Kielland K, Kwiatkowski BL, Laundre JA, Murray G ( 2002). Resource-based niches provide a basis for plant species diversity and dominance in arctic tundra. Nature, 415, 68-71.
[40] Mo XL, Dai XQ, Wang HM, Kou L, Fu XL ( 2018). Rhizosphere effect of overstory tree and understory shrub species in central subtropical plantations—A case study at Qianyanzhou, Taihe, Jiangxi. Chinese Journal of Plant Ecology, 42, 723-733.
[ 莫雪丽, 戴晓琴, 王辉民, 寇亮, 付晓莉 ( 2018). 中亚热带常见乔木灌木根际效应研究——以江西泰和千烟洲为例. 植物生态学报, 42, 723-733.]
[41] Nannipieri P, Trasar-Cepeda C, Dick RP ( 2018). Soil enzyme activity: A brief history and biochemistry as a basis for appropriate interpretations and meta-analysis. Biology and Fertility of Soils, 54, 11-19.
[42] National Forestry Administration of China ( 2014). National Forest Resources Statistics:The Eighth National Inventory of Forest Resources. China Forestry Publishing House, Beijing.
[ 国家林业局 ( 2014). 全国森林资源统计:第八次全国森林资源清查. 中国林业出版社, 北京.]
[43] Peng X, Wang W ( 2016). Stoichiometry of soil extracellular enzyme activity along a climatic transect in temperate grasslands of northern china. Soil Biology & Biochemistry, 98, 74-84.
[44] Phillips RP, Erlitz Y, Bier R, Bernhardt ES ( 2008). New approach for capturing soluble root exudates in forest soils. Functional Ecology, 22, 990-999.
[45] Phillips RP, Fahey TJ ( 2006). Tree species and mycorrhizal associations influence the magnitude of rhizosphere effects. Ecology, 87, 1302-1313.
[46] 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.
[47] Riley D, Barber SA ( 1970). Salt accumulation at the soybean (Glycine max (L.) Merr.) root-soil interface. Soil Science Society of America Journal, 34, 154-155.
[48] Saiya-Cork KR, Sinsabaugh RL, Zak DR ( 2002). The effects of long term nitrogen deposition on extracellular enzyme activity in an Acer saccharum forest soil. Soil Biology & Biochemistry, 34, 1309-1315.
[49] Santiago L, Wright S ( 2007). Leaf functional traits of tropical forest plants in relation to growth form. Functional Ecology, 21, 19-27.
[50] Scientific Investigation Team of Chinese Academy of Sciences for Southern Mountainous Areas ( 1989). Management and Development of Red Hilly Area-Experimental Study in Qianyanzhou. Science Press, Beijing.
[ 中国科学院南方山区综合科学考察队 ( 1989). 红壤丘陵综合开发治理——千烟洲综合开发治理试验研究. 科学出版社, 北京.]
[51] Shukla G, Varma A ( 2011). Soil Enzymology. Springer, Berlin.
[52] Sinsabaugh RL, Follstad Shah JJ ( 2012). Ecoenzymatic stoichiometry and ecological theory. Annual Review of Ecology Evolution and Systematics, 43, 313-343.
[53] Sinsabaugh RL, Hill BH, Shah JJF ( 2009). Ecoenzymatic stoichiometry of microbial organic nutrient acquisition in soil and sediment. Nature, 462, 795-798.
[54] Sinsabaugh RL, Lauber CL, Weintraub MN, Ahmed B, Allison SD, Crenshaw C, Contosta AR, Cusack D, Frey S, Gallo ME, Gartner TB, Hobbie SE, Holland K, Keeler BL, Powers JS, Stursova M, Takacs-Vesbach C, Waldrop MP, Wallenstein MD, Zak DR, Zeglin LH ( 2008). Stoichiometry of soil enzyme activity at global scale. Ecology Letters, 11, 1252-1264.
[55] Sinsabaugh RL, Moorhead DL ( 1994). Resource allocation to extracellular enzyme production: A model for nitrogen and phosphorus control of litter decomposition. Soil Biology & Biochemistry, 26, 1305-1311.
[56] Smalla K, Sessitsch A, Hartmann A ( 2006). The rhizosphere: “Soil compartment influenced by the root”. FEMS Microbiology Ecology, 56, 165-165.
[57] Steinaker DF, Wilson SD, Peltzer DA ( 2010). Asynchronicity in root and shoot phenology in grasses and woody plants. Global Change Biology, 16, 2241-2251.
[58] Sterner RW, Elser JJ ( 2002). Ecological Stoichiometry:The Biology of Elements from Molecules to the Biosphere. Princeton University Press, Princeton.
[59] Su LY, Cheng AX, Yu AL, Fu WQ, Zhen PY ( 1992). Investigation on mycorrhizae of forest trees in natural reserve of Mount Tianmu. Journal of Zhejiang Forestry College, 3, 263-276.
[ 苏琍英, 程爱兴, 喻爱林, 傅卫庆, 郑平谣 ( 1992). 天目山自然保护区林木菌根调查. 浙江林学院学报, 3, 263-276.]
[60] Sun LJ, Kominami Y, Yoshimura K, Kitayama K ( 2017). Root-exudate flux variations among four co-existing canopy species in a temperate forest, Japan. Ecological Research, 32, 331-339.
[61] 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.]
[62] Tao BX, Zhang JC, Yu YC, Cong RL ( 2010). Season variations of forest soil enzyme activities in the hilly region of southern Jiangsu Province. Ecology and Environmental Sciences, 19, 2349-2354.
[ 陶宝先, 张金池, 愈元春, 丛日亮 ( 2010). 苏南丘陵地区森林土壤酶活性季节变化. 生态环境学报, 19, 2349-2354.]
[63] Tapia-Torres Y, Elser JJ, Souza V, García-Oliva F ( 2015). Ecoenzymatic stoichiometry at the extremes: How microbes cope in an ultra-oligotrophic desert soil. Soil Biology & Biochemistry, 87, 34-42.
[64] Toberman H, Evans CD, Freeman C, Fenner N, White M, Emmett BA, Artz RRE ( 2008). Summer drought effects upon soil and litter extracellular phenol oxidase activity and soluble carbon release in an upland Calluna heathland. Soil Biology & Biochemistry, 40, 1519-1532.
[65] Wang RL, Wang QF, Zhao N, Yu GR, He NP ( 2017). Complex trait relationships between leaves and absorptive roots: Coordination in tissue N concentration but divergence in morphology. Ecology and Evolution, 7, 2697-2705.
[66] Wang T, Yang YH, Ma WH ( 2008). Storage, patterns and environmental controls of soil phosphorus in China. Acta Scientiarum Naturalium Universitatis Pekinensis, 44, 945-951.
[ 汪涛, 杨元合, 马文红 ( 2008). 中国土壤磷库的大小、分布及其影响因素. 北京大学学报(自然科学版), 44, 945-951.]
[67] Waring BG, Weintraub SR, Sinsabaugh RL ( 2014). Ecoenzymatic stoichiometry of microbial nutrient acquisition in tropical soils. Biogeochemistry, 117, 101-113.
[68] Warton DI, Duursma RA, Falster DS, Taskinen S ( 2012). Smatr 3—An R package for estimation and inference about allometric lines. Methods in Ecology and Evolution, 3, 257-259.
[69] Wei Y, Wang ZQ, Zhang XY, Yang H, Liu XY, Liu WJ ( 2017). Enzyme activities and microbial communities in subtropical forest soil aggregates to ammonium and nitrate-‌nitrogen additions. Journal of Resources and Ecology, 8, 258-267.
[70] Wu WD, Liao CH, Liu KS, Wang JM ( 1994). A study on the soil deterioration of the first generation of artificial fir plantation in Jiangxi Province. Research of Soil and Water Conservation, 1(Suppl.1), 64-74.
[ 吴蔚东, 廖彩恢, 刘开树, 王景明 ( 1994). 江西省第一代人工杉木林土壤退化的研究. 水土保持研究, 1(Suppl.1), 64-74.]
[71] Wu XQ, Sun MQ ( 2006). Mycorrhizal formation between seven ectomycorrhizal fungi and seedlings of three pines species. Acta Ecologica Sinica, 26, 4186-4191.
[ 吴小芹, 孙民琴 ( 2006). 七株外生菌根真菌与三种松苗菌根的形成能力. 生态学报, 26, 4186-4191.]
[72] Yang WQ, Wang KY ( 2004). Advances in forest soil enzymology. Scientia Silvae Sinicae, 40(2), 152-159.
doi: 10.11707/j.1001-7488.20040227
[ 杨万勤, 王开运 ( 2004). 森林土壤酶的研究进展. 林业科学, 40(2), 152-159.]
doi: 10.11707/j.1001-7488.20040227
[73] Yang Y, Wang JF, Zhang XY, Li DD, Wang HM, Chen FS, Sun XM, Wen XF ( 2016). Mechanism of litter and understory vegetation effects on soil carbon and nitrogen hydrolase activities in Chinese fir forests. Acta Ecologica Sinica, 36, 8102-8110.
[ 杨洋, 王继富, 张心昱, 李丹丹, 王辉民, 陈伏生, 孙晓敏, 温学发 ( 2016). 凋落物和林下植被对杉木林土壤碳氮水解酶活性的影响机制. 生态学报, 36, 8102-8110.]
[74] Yang Y, Zhang XY, Zhang C, Wang HM, Fu XL, Chen FS, Wan SZ, Sun XM, Wen XF, Wang JF ( 2018). Understory vegetation plays the key role in sustaining soil microbial biomass and extracellular enzyme activities. Biogeosciences, 15, 4481-4494.
[75] Yin HJ, Wheeler E, Phillips RP ( 2014). Root-induced changes in nutrient cycling in forests depend on exudation rates. Soil Biology & Biochemistry, 78, 213-221.
[76] Zhang XX, Yang LM, Chen Z, Li YQ, Lin YY, Zheng XZ, Chu HY, Yang YS ( 2018). Patterns of ecoenzymatic stoichiometry on types of forest soils form different parent materials in subtropical areas. Acta Ecoligica Sinica, 38, 5828-5836.
[ 张星星, 杨柳明, 陈忠, 李一清, 林燕语, 郑宪志, 楚海燕, 杨玉盛 ( 2018). 中亚热带不同母质和森林类型土壤生态酶化学计量特征. 生态学报, 38, 5828-5836.]
[77] Zhang YL, Chen LJ, Liu GF, Wu ZJ ( 2003). Research advance in catalytic kinetics of soil hydrolas. Chinese Journal of Applied Ecology, 14, 2326-2332.
[ 张玉兰, 陈利军, 刘桂芬, 武志杰 ( 2003). 土壤水解酶类催化动力学研究进展. 应用生态学报, 14, 2326-2332.]
[78] Zhao J, Wan SZ, Fu SL, Wang XL, Wang M, Liang CF, Chen YQ, Zhu XL ( 2013). Effects of understory removal and nitrogen fertilization on soil microbial communities in Eucalyptus plantations. Forest Ecology and Management, 310, 80-86.
[79] Zhao ZW ( 1998 a). VA mycorrhizal fungi in the rhizosphere soil of tropical and subtropical pteridophytes in Yunnan. Acta Botanica Yunnanica, 20, 183-192.
[ 赵之伟 ( 1998 a). 云南热带、亚热带蕨类植物根际土壤中的VA菌根真菌. 云南植物研究, 20, 183-192.]
[80] Zhao ZW ( 1998 b). Vesicular Arbuscular mycorrhizae of Pteridophytes. Journal of Yunnan University, 20(2), 97-100.
[ 赵之伟 ( 1998 b). 蕨类植物的VA菌根. 云南大学学报(自然科学版), 20(2), 97-100.]
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[1] Yang Li-rui and Cheng Mu-chu. Relationship between Plant Stress Resistance and Photorespiration[J]. Chin Bull Bot, 1991, 8(01): 43 -47 .
[2] . [J]. Chin Bull Bot, 1996, 13(专辑): 74 -75 .
[3] Cui Kai-rong;Chen Ke-ming;Wang Xiao-zhe and Wang Ya-fu. Current Reseach on Plant Somatic Embryogenesis[J]. Chin Bull Bot, 1993, 10(03): 14 -20 .
[4] Huang Yao Li Chao-luan Ma Cheng Wu Nai-hu. Chloroplast DNA and Its Application to Plant Systematic Studies[J]. Chin Bull Bot, 1994, 11(02): 11 -25 .
[5] WANG Pu ZHAO Xiu-Qin. The Effect of Extracting Condition on the Analysis Result of Allelochemicals in Wheat Straw[J]. Chin Bull Bot, 2001, 18(06): 735 -738 .
[6] Yun Zihou;Liang Mingxia;Zhang Cunjie and Tan Zhiyi. The Determination of Trace Cytokinin in a Small Plant Sample by Gas Chromatography[J]. Chin Bull Bot, 1988, 5(01): 60 -63 .
[7] Yanxia He;Zicheng Wang*. Variation of DNA Methylation in Arabidopsis thaliana Seedlings After the Cryopreservation[J]. Chin Bull Bot, 2009, 44(03): 317 -322 .
[8] Yiting Shi, ShuhuaYang. Chinese Scientists Made Breakthrough in Study on Ethylene Signaling Transduction in Plants[J]. Chin Bull Bot, 2016, 51(3): 287 -289 .
[10] LONG Wen-Xing, DING Yi, ZANG Run-Guo, YANG Min, CHEN Shao-Wei. Environmental characteristics of tropical cloud forests in the rainy season in Bawangling National Nature Reserve on Hainan Island, South China[J]. Chin J Plan Ecolo, 2011, 35(2): 137 -146 .