Effects of nitrogen addition amount and frequency on soil respiration and its components in a temperate semiarid grassland

doi:10.17521/cjpe.2020.0171

Abstract

Abstract:

Aims Increasing global nitrogen (N) deposition has exerted significant influences on productivity and carbon cycle of terrestrial ecosystems. More than 90% of the carbon in grasslands is stored in the soil, therefore any changes in soil total respiration (R_s) might have a vital impact on the carbon balance and the stability of soil carbon pool of grassland ecosystems. Most of our understanding about the responses of R_s to N deposition was based on N deposition manipulative experiments with short-term (<5 years) and low frequency (1-2 times per year) N addition treatments. It is still unclear how the long term N addition and different N addition frequency will affect R_s and its components in semiarid grasslands.
Methods Our study is based on a long term N addition manipulative experiment platform conducted in a typical temperate semiarid steppe, Nei Mongol. The experimental treatment consisted of six N addition amounts and two N addition frequencies. N addition treatments began at 2008. Soil respiration and its components were measured every two weeks during the growing season in 2018 and 2019.
Important findings 1) R_s significantly decreased with increasing N addition amount. The negative impact of N addition on R_s was mainly resulted from the inhibition of heterotrophic respiration (R_h). 2) No significant differences were observed in responses of R_s and its components to low and high frequency N addition treatments. 3) Soil acidification caused by long term N addition inhibited soil microbial activity and changed soil microbial community composition, consequently decreased R_s and R_h. Our results suggested that the negative effect of N addition on soil carbon release still lasted after a decade of N addition treatment. In particular, the decrease of R_h would enhance the stability of soil carbon pool. No significant differences in the two N addition frequency treatments indicated that the potential impacts caused by simulated N addition with different frequencies would be diminished with prolonged treatment period. Therefore, the results of long-term (>10 years) simulated N addition experiments can provide reliable references for evaluating the responses of natural ecosystems to atmospheric N deposition.

Key words: long-term nitrogen addition, nitrogen addition frequency, soil respiration, autotrophic respiration, heterotrophic respiration

YANG Ze, null null, TAN Xing-Ru, YOU Cui-Hai, WANG Yan-Bing, YANG Jun-Jie, HAN Xing-Guo, CHEN Shi-Ping. Effects of nitrogen addition amount and frequency on soil respiration and its components in a temperate semiarid grassland[J]. Chin J Plant Ecol, 2020, 44(10): 1059-1072.

Add to citation manager EndNote|Ris|BibTeX

URL: https://www.plant-ecology.com/EN/10.17521/cjpe.2020.0171

https://www.plant-ecology.com/EN/Y2020/V44/I10/1059

Figures/Tables 7

Table 1 Results of the effects of year (Y), nitrogen addition amount (N), nitrogen addition frequency (NF) and their interactions on soil temperature (ST), soil water content (SWC), soil total respiration rate (Rs) and its components (Rh and Ra) and Rh/Rs ratio

处理 Treatment		土壤温度 ST (℃)		土壤水分含量 SWC (%)		土壤总呼吸速率 R_s (mol·m^-2·s^-1)		异养呼吸速率 R_h (mol·m^-2·s^-1)		自养呼吸速率 R_a (mol·m^-2·s^-1)		异养呼吸比值 R_h/R_s
处理 Treatment	df	F	p	F	p	F	p	F	p	F	p	F	p
Y	1	49.08	<0.001	6.11	<0.05	21.81	<0.001	67.29	<0.001	0.53	0.46	71.57	<0.001
N	5	16.65	<0.001	5.56	<0.001	16.15	<0.001	113.73	<0.001	1.68	0.16	1.60	0.19
NF	1	0.87	0.36	1.08	0.30	2.52	0.12	0.02	0.90	3.03	0.09	1.84	0.18
N × NF	4	1.75	0.15	1.33	0.27	2.53	0.05	9.23	<0.001	2.30	0.07	2.14	0.09
Y × N	5	0.31	0.91	0.09	0.99	0.62	0.69	1.23	0.29	0.58	0.71	1.20	0.32
Y × NF	1	0.00	0.96	0.11	0.74	0.04	0.84	0.19	0.67	0.01	0.91	0.30	0.59
Y × N × NF	4	0.06	0.99	0.01	1.00	0.33	0.86	0.03	1.00	1.12	0.34	2.13	0.09

Fig. 1 Changes in soil temperature (ST)(A, C) and soil water content (SWC)(B, D) in 0-10 cm surface soil layer under different N addition amount and frequency treatments in 2018 and 2019. Data are mean ± SE. The different color icons in the figure represent N addition treatments with 0, 2, 5, 10, 20, 50 g·m-2·a-1, respectively. The ANOVA results were shown in the figure to address the significance of effects of N addition amount (N), frequency (NF) and their interactions (N × NF) on the parameters (***, p < 0.001; *, p < 0.05; ns, p > 0.05). The lowercase letters in the figure represent the significance among different nitrogen addition treatments. The same letter means no significance (p > 0.05), while different letters mean significant differences (p < 0.05). HF, N addition with high frequency; LF, N addition with low frequency.

Fig. 2 Inter- and intra-annual variations in soil respiration rate (Rs) and its heterotrophic (Rh) and autotrophic (Ra) components under different N addition amount and frequency treatments in 2018 and 2019 (mean ± SE). The different color icons in the figure represent N addition treatments with 0, 2, 5, 10, 20, 50 g·m-2·a-1, respectively. The ANOVA results were shown in the figure to address the significance of effects of N addition amount (N), frequency (NF) and their interactions (N × NF) on the parameters (***, p < 0.001; ns, p > 0.05). HF, N addition with high frequency; LF, N addition with low frequency.

Fig. 3 Seasonal mean values of soil respiration rate (Rs) and its heterotrophic (Rh) and autotrophic (Ra) components under different N addition amount and frequency treatments in 2018 and 2019. Data are mean ± SE. The different color icons in the figure represent N addition treatments with 0, 2, 5, 10, 20, 50 g·m-2·a-1, respectively. The ANOVA results were shown in the figure to address the significance of effects of N addition amount (N), frequency (NF) and their interactions (N × NF) on the parameters (***, p < 0.001; **, p < 0.01; *, p < 0.05; ns, p > 0.05). The lowercase letters in the figure represent the significance among different nitrogen addition treatments. The same letter means no significance (p > 0.05), while different letters mean significant differences (p < 0.05). HF, N addition with high frequency; LF, N addition with low frequency.

Fig. 4 Relationships between soil respiration rate (Rs) and its heterotrophic (Rh) and autotrophic (Ra) component with soil temperature (ST), soil water content (SWC) and soil pH value. Different color icons in the figure represent N addition treatments with 0, 2, 5, 10, 20, 50 g·m-2·a-1, respectively. The circle sign and black line represent the low frequency N addition (LF) treatment, and the triangle sign and red line indicate the high frequency N addition (HF) treatment. The solid line represents marginally significant relation (p < 0.1) and the dash line represents insignificant relation (p > 0.1).

Fig. 5 Changes in temperature (Q10, A, B) and water (C, D) sensitivities of soil respiration (Rs) and its heterotrophic component (Rh) under different nitrogen addition amount and frequency treatments. Data are mean ± SE. The different color icons in the figure represent N addition treatments with 0, 2, 5, 10, 20, 50 g·m-2·a-1, respectively. The ANOVA results were shown in the figure to address the significance of effects of N addition amount (N), frequency (NF) and their interactions (N × NF) on the parameters (***, p < 0.001; **, p < 0.01; *, p < 0.05; ns, p > 0.05). The lowercase letters in the figure represent the significance among different nitrogen addition treatments. The same letter means no significance (p > 0.05), while different letters mean significant differences (p < 0.05). HF, N addition with high frequency; LF, N addition with low frequency.

Fig. 6 Relationships between soil total respiration and its components with aboveground net primary productivity (ANPP), soil microbial biomass (MB) and fungal biomass/bacterial biomass ratio (F/B). The different color icons in the figure represent N addition treatments with 0, 2, 5, 10, 20, 50 g·m-2·a-1, respectively. The circle sign and black line represent the low frequency N addition (LF) treatment, and the triangle sign and red line indicate the high frequency N addition (HF) treatment. The solid line represents marginally significant relation (p < 0.1) and the dash line represents insignificant relation (p > 0.1).

References 78

[1]	Allison SD, Czimczik CI, Treseder KK (2008). Microbial activity and soil respiration under nitrogen addition in Alaskan boreal forest. Global Change Biology, 14, 1156-1168.
[2]	ArchMiller A, Samuelson L (2016). Partitioning longleaf pine soil respiration into its heterotrophic and autotrophic components through root exclusion. Forests, 7, 1-13.
[3]	Bai TS, Wang P, Hall SJ, Wang FW, Ye CL, Li Z, Li SJ, Zhou LY, Qiu YP, Guo JX, Guo H, Wang Y, Hu SJ (2020). Interactive global change factors mitigate soil aggregation and carbon change in a semi-arid grassland. Global Change Biology, 26, 5320-5332.
[4]	Bai WM, Guo DL, Tian QY, Liu NN, Cheng WX, Li LH, Zhang WH (2015). Differential responses of grasses and forbs led to marked reduction in below-ground productivity in temperate steppe following chronic N deposition. Journal of Ecology, 103, 1570-1579.
[5]	Bai YF, Wu JG, Clark CM, Naeem S, Pan QM, Huang JH, Zhang LX, Han XG (2010). Tradeoffs and thresholds in the effects of nitrogen addition on biodiversity and ecosystem functioning: evidence from Inner Mongolia grasslands. Global Change Biology, 16, 358-372.
[6]	Bond-Lamberty B, Bailey VL, Chen M, Gough CM, Vargas R (2018). Globally rising soil heterotrophic respiration over recent decades. Nature, 560, 80-83.
[7]	Bond-Lamberty B, Thomson A (2010). A global database of soil respiration data. Biogeosciences, 7, 1915-1926.
[8]	Bond-Lamberty B, Wang C, Gower ST (2004). A global relationship between the heterotrophic and autotrophic components of soil respiration? Global Change Biology, 10, 1756-1766.
[9]	Bowden RD, Davidson E, Savage K, Arabia C, Steudler P (2004). Chronic nitrogen additions reduce total soil respiration and microbial respiration in temperate forest soils at the Harvard Forest. Forest Ecology and Management, 196, 43-56.
[10]	Bowden RD, Wurzbacher SJ, Washko SE, Wind L, Rice AM, Coble AE, Baldauf N, Johnson B, Wang JJ, Simpson M, Lajtha K (2019). Long-term nitrogen addition decreases organic matter decomposition and increases forest soil carbon. Soil Science Society of America Journal, 83, 82-95.
[11]	Cao JR, Pang S, Wang QB, Williams MA, Jia X, Dun SS, Yang JJ, Zhang YH, Wang J, Lü XT, Hu YC, Li LH, Li YC, Han XG (2020). Plant-bacteria-soil response to frequency of simulated nitrogen deposition has implications for global ecosystem change. Functional Ecology, 34, 723-734.
[12]	Chen DM, Lan ZC, Hu SJ, Bai YF (2015a). Effects of nitrogen enrichment on belowground communities in grassland: relative role of soil nitrogen availability vs. soil acidification. Soil Biology & Biochemistry, 89, 99-108.
[13]	Chen DM, Li JJ, Lan ZC, Hu SJ, Bai YF (2016). Soil acidification exerts a greater control on soil respiration than soil nitrogen availability in grasslands subjected to long-term nitrogen enrichment. Functional Ecology, 30, 658-669.
[14]	Chen DM, Xing W, Lan ZC, Saleem M, Wu YQQG, Hu SJ, Bai YF (2019). Direct and indirect effects of nitrogen enrichment on soil organisms and carbon and nitrogen mineralization in a semi-arid grassland. Functional Ecology, 33, 175-187.
[15]	Chen H, Li DJ, Gurmesa GA, Yu GR, Li LH, Zhang W, Fang HJ, Mo JM (2015b). Effects of nitrogen deposition on carbon cycle in terrestrial ecosystems of China: a meta- analysis. Environmental Pollution, 206, 352-360.
[16]	Chen J, Groenigen KJ, Hungate BA, Terrer C, Groenigen JW, Maestre FT, Ying S, Luo YQ, Jorgensen U, Sinsabaugh RL, Olesen JE, Elsgaard L (2020). Long-term nitrogen loading alleviates phosphorus limitation in terrestrial ecosystems. Global Change Biology, 9, 5077-5086.
[17]	Chen ZM, Xu YH, He YJ, Zhou XH, Fan JL, Yu HY, Ding WX (2018). Nitrogen fertilization stimulated soil heterotrophic but not autotrophic respiration in cropland soils: a greater role of organic over inorganic fertilizer. Soil Biology & Biochemistry, 116, 253-264.
[18]	Chen ZZ, Wang SP (2000). Typical Steppe Ecosystems of China. Science Press, Beijing.
	[ 陈佐忠, 汪诗平 (2000). 中国典型草原生态系统. 科学出版社, 北京.]
[19]	Clark CM, Tilman D (2008). Loss of plant species after chronic low-level nitrogen deposition to prairie grasslands. Nature, 451, 712-715.
[20]	Cox PM, Betts RA, Jones CD, Spall SA, Totterdell IJ (2000). Acceleration of global warming due to carbon-cycle feedbacks in a coupled climate model. Nature, 408, 184-187.
[21]	Craine JM, Wedin DA, Reich PB (2001). The response of soil CO₂ flux to changes in atmospheric CO₂, nitrogen supply and plant diversity. Global Change Biology, 7, 945-953.
[22]	Fang C, Li FM, Pei JY, Rena J, Gong YH, Yuan ZG, Ke WB, Zheng Y, Bai XK, Ye JS (2018). Impacts of warming and nitrogen addition on soil autotrophic and heterotrophic respiration in a semi-arid environment. Agricultural and Forest Meteorology, 248, 449-457.
[23]	Fang C, Ye JS, Gong YH, Pei JY, Yuan ZQ, Xie C, Zhu YS, Yu YY (2017). Seasonal responses of soil respiration to warming and nitrogen addition in a semi-arid alfalfa- pasture of the Loess Plateau, China. Science of the Total Environment, 590, 729-738.
[24]	Fornara DA, Tilman D (2012). Soil carbon sequestration in prairie grasslands increased by chronic nitrogen addition. Ecology, 93, 2030-2036.
[25]	Frostegård Å, Tunlid A, Bååth E (2011). Use the misuse of PLFA measurements in soils. Soil Biology & Biochemistry, 43, 1621-1625.
[26]	Fu Z, Niu SL, Dukes JS (2015). What have we learned from global change manipulative experiments in China? A meta-analysis. Scientific reports, 5, 12344. DOI: 10.1038/srep12344.
[27]	Galloway JN, Dentener FJ, Capone DG, Boyer EW, Howarth RW, Seitzinger SP, Asner GP, Cleveland CC, Green PA, Holland EA, Karl DM, Michaels AF, Porter JH, Townsend AR, Vörösmarty CJ (2004). Nitrogen cycles: past, present, and future. Biogeochemistry, 70, 153-226.
[28]	Galloway JN, Townsend AR, Jan Willem E, Mateete B, Zucong C, Freney JR, Martinelli LA, Seitzinger SP, Sutton MA (2008). Transformation of the nitrogen cycle: recent trends, questions, and potential solutions. Science, 320, 889-892.
[29]	Giese M, Brueck H, Gao Y, Lin S, Steffens M, Kögelknabner I, Glindemann T, Susenbeth A, Taube F, Butterbachbahl K (2013). Data from: N balance and cycling of Inner Mongolia typical steppe—A comprehensive case study of grazing effects. Ecological Monographs, 83, 195-219.
[30]	Hanson PJ, Edwards NT, Garten CT, Andrews JA (2000). Separating root and soil microbial contributions to soil respiration—A review of methods and observations. Biogeochemistry, 48, 115-146.
[31]	Hasselquist NJ, Metcalfe DB, Högberg P (2012). Contrasting effects of low and high nitrogen additions on soil CO₂ flux components and ectomycorrhizal fungal sporocarp production in a boreal forest. Global Change Biology, 18, 3596-3605.
[32]	Janssens IA, Dieleman W, Luyssaert S, Subke JA, Reichstein M, Ceulemans R, Ciais P, Dolman AJ, Grace J, Matteucci G (2010). Reduction of forest soil respiration in response to nitrogen deposition. Nature Geoscience, 3, 315-322.
[33]	Jia XX, Shao MA, Wei XR (2012). Responses of soil respiration to N addition, burning and clipping in temperate semiarid grassland in northern China. Agricultural and Forest Meteorology, 166, 32-40.
[34]	Lee KH, Jose S (2003). Soil respiration, fine root production, and microbial biomass in cottonwood and loblolly pine plantations along a nitrogen fertilization gradient. Forest Ecology and Management, 185, 263-273.
[35]	Li YL, Hong M, Bai WM, Han GD, Wang HM, Zhou M (2015). The responses of soil respiration to water and nitrogen in Stipa breviflora steppe. Acta Ecologica Sinica, 35, 1727-1733.
	[ 李寅龙, 红梅, 白文明, 韩国栋, 王海明, 周萌 (2015). 水、氮控制对短花针茅草原土壤呼吸的影响. 生态学报, 35, 1727-1733.]
[36]	Liang LZ, Chen F, Han HR, Zhang YR, Zhu J, Niu SK (2019). Pathways regulating decreased soil respiration with nitrogen addition in a subtropical forest in China. Water Air and Soil Pollution, 230, 91-100.
[37]	Liu W, Lu XT, Xu WF, Shi HQ, Hou LY, Li LH, Yuan WP (2018). Effects of water and nitrogen addition on ecosystem respiration across three types of steppe: the role of plant and microbial biomass. Science of the Total Environment, 619, 103-111.
[38]	Liu XJ, Zhang Y, Han WX, Tang AH, Shen JL, Cui ZL, Vitousek P, Erisman JW, Goulding K, Christie P, Fangmeier A, Zhang FS (2013). Enhanced nitrogen deposition over China. Nature, 494, 459-462.
[39]	Lovett GM, Cole JJ, Pace ML (2006). Is net ecosystem production equal to ecosystem carbon accumulation? Ecosystems, 9, 152-155.
[40]	Luca B, Chris F, Timothy J, HaKan R, Juul L, Nathalie F, Tim E, Renato G, Michal H, Tomás H (2006). Atmospheric nitrogen deposition promotes carbon loss from peat bogs. Proceedings of the National Academy of Sciences of the United States of America, 103, 19386-19389.
[41]	Luo QP, Gong JR, Zhai ZW, Pan Y, Liu M, Xu S, Wang YH, Yang LL, Baoyin TT (2016). The responses of soil respiration to nitrogen addition in a temperate grassland in northern China. Science of the Total Environment, 569, 1466-1477.
[42]	Ma SY, Verheyen K, Props R, Wasof S, Vanhellemont M, Boeckx P, Boon N, de Frenne P (2018). Plant and soil microbe responses to light, warming and nitrogen addition in a temperate forest. Functional Ecology, 32, 1293-1303.
[43]	Masciandaro G, Macci C, Peruzzi E, Doni S (2018). Soil carbon in the world: ecosystem services linked to soil carbon in forest and agricultural soilsGarcia C, Nannipieri P, Hernandez T. Future of Soil Carbon: Its Conservation and Formation. Academic Press, London. 1-38.
[44]	Mo JM, Zhang W, Zhu WX, Gundersen P, Fang Y, Li D, Wang H (2008). Nitrogen addition reduces soil respiration in a mature tropical forest in southern China. Global Change Biology, 14, 403-412.
[45]	Niu SL, Wu MY, Han Y, Xia JY, Li LH, Wan SQ (2008). Water-mediated responses of ecosystem carbon fluxes to climatic change in a temperate steppe. New Phytologist, 177, 209-219.
[46]	Niu SL, Wu MY, Han Y, Xia JY, Zhang Z, Yang HJ, Wan SQ (2010). Nitrogen effects on net ecosystem carbon exchange in a temperate steppe. Global Change Biology, 16, 144-155.
[47]	Peng YF, Guo DL, Yang YH (2017). Global patterns of root dynamics under nitrogen enrichment. Global Ecology and Biogeography, 26, 102-114.
[48]	Raich JW, Schlesinger WH (1992). The global carbon dioxide flux in soil respiration and its relationship to vegetation and climate. Tellus B: Chemical and Physical Meteorology, 44, 81-99.
[49]	Scharlemann JPW, Tanner EVJ, Hiederer R, Kapos V (2014). Global soil carbon: understanding and managing the largest terrestrial carbon pool. Carbon Management, 5, 81-91.
[50]	Shan D, Han GD, Zhao ML, Wang Z, Han X, Gao FG (2009). The effects of experimental warming and nitrogen addition on soil respiration in desert steppe. Journal of Arid Land Resources and Environment, 23, 106-112.
	[ 珊丹, 韩国栋, 赵萌莉, 王珍, 韩雄, 高福光 (2009). 控制性增温和施氮对荒漠草原土壤呼吸的影响. 干旱区资源与环境, 23, 106-112.]
[51]	Shi BK, Xu WL, Zhu Y, Wang CL, Loik ME, Sun W (2019). Heterogeneity of grassland soil respiration: antagonistic effects of grazing and nitrogen addition. Agricultural and Forest Meteorology, 268, 215-223.
[52]	Smith MD, Knapp AK, Collins SL (2009). A framework for assessing ecosystem dynamics in response to chronic resource alterations induced by global change. Ecology, 90, 3279-3289.
[53]	Song J, Wan SQ, Piao SL, Knapp AK, Classen AT, Vicca S, Ciais P, Hovenden MJ, Leuzinger S, Beier C, Kardol P, Xia JY, Liu Q, Ru JY, Zhou ZX, et al. (2019). A meta-analysis of 1,119 manipulative experiments on terrestrial carbon-cycling responses to global change. Nature Ecology & Evolution, 3, 1309-1320.
[54]	Tian DS, Niu SL (2015). A global analysis of soil acidification caused by nitrogen addition. Environmental Research Letters, 10, 1-10.
[55]	Tian DS, Wang H, Sun J, Niu SL (2016). Global evidence on nitrogen saturation of terrestrial ecosystem net primary productivity. Environmental Research Letters, 11, 024012. DOI: 10.1088/1748-9326/11/2/024012.
[56]	Treseder KK (2008). Nitrogen additions and microbial biomass: a meta-analysis of ecosystem studies. Ecology Letters, 11, 1111-1120.
[57]	Tu LH, Hu TX, Zhang J, Li XW, Hu HL, Liu L, Xiao YL (2013). Nitrogen addition stimulates different components of soil respiration in a subtropical bamboo ecosystem. Soil Biology & Biochemistry, 58, 255-264.
[58]	Wang J, Gao YZ, Zhang YH, Yang JJ, Smith MD, Knapp AK, Eissenstat DM, Han XG (2019a). Asymmetry in above- and belowground productivity responses to N addition in a semi-arid temperate steppe. Global Change Biology, 25, 2958-2969.
[59]	Wang JB, Fu XL, Zhang Z, Li MH, Cao HJ, Zhou XL, Ni HW (2019b). Responses of soil respiration to nitrogen addition in the Sanjiang Plain wetland, northeastern China. PLOS ONE, 14, e0211456. DOI: 10.1371/journal.pone.0211456.
[60]	Wang JS, Song B, Ma FF, Tian DS, Li Y, Yan T, Quan Q, Zhang FY, Li ZL, Wang BX, Gao Q, Chen WN, Niu SL (2019c). Nitrogen addition reduces soil respiration but increases the relative contribution of heterotrophic component in an alpine meadow. Functional Ecology, 33, 2239-2253.
[61]	Wei L, Liu J, Su JH, Jing GH, Zhao J, Cheng JM, Jin JW (2016). Effect of clipping on soil respiration components in temperate grassland of Loess Plateau. European Journal of Soil Biology, 75, 157-167.
[62]	Wei L, Su JS, Jing GH, Zhao J, Liu J, Cheng JM, Jin JW (2018). Nitrogen addition decreased soil respiration and its components in a longterm fenced grassland on the Loess Plateau. Journal of Arid Environments, 152, 37-44.
[63]	Xiao H, Wang B, Lu SB, Chen DM, Wu Y, Zhu YH, Hu SJ, Bai YF (2020). Soil acidification reduces the effects of short-term nutrient enrichment on plant and soil biota and their interactions in grasslands. Global Change Biology, 26, 4626-4637.
[64]	Yan LM, Chen SP, Huang JH, Lin GH (2010). Differential responses of auto- and heterotrophic soil respiration to water and nitrogen addition in a semiarid temperate steppe. Global Change Biology, 16, 2345-2357.
[65]	Yan WD, Chen XY, Peng YY, Zhu F, Zhen W, Zhang XY (2020). Response of soil respiration to nitrogen addition in two subtropical forest types. Pedosphere, 30, 478-486.
[66]	Yang Q, Wang W, Zeng H (2018). Effects of nitrogen addition on the plant diversity and biomass of degraded grasslands of Nei Mongol, China. Chinese Journal of Plant Ecology, 42, 430-441.
	[ 杨倩, 王娓, 曾辉 (2018). 氮添加对内蒙古退化草地植物群落多样性和生物量的影响. 植物生态学报, 42, 430-441.]
[67]	Zeng WJ, Chen JB, Liu HY, Wang W (2018). Soil respiration and its autotrophic and heterotrophic components in response to nitrogen addition among different degraded temperate grasslands. Soil Biology & Biochemistry, 124, 255-265.
[68]	Zhang BW, Li S, Chen SP, Ren TT, Yang ZQ, Zhao HL, Liang Y, Han XG (2016a). Arbuscular mycorrhizal fungi regulate soil respiration and its response to precipitation change in a semiarid steppe. Scientific Reports, 6, 19990. DOI: 10.1038/srep19990.
[69]	Zhang BY, Li WJ, Chen SP, Tan XR, Wang SS, Chen ML, Ren TT, Xia JY, Huang JH, Han XG (2019). Changing precipitation exerts greater influence on soil heterotrophic than autotrophic respiration in a semiarid steppe. Agricultural and Forest Meteorology, 271, 413-421.
[70]	Zhang YH, Lü XT, Isbell F, Stevens C, Han X, He NP, Zhang GM, Yu Q, Huang JH, Han XG (2014). Rapid plant species loss at high rates and at low frequency of N addition in temperate steppe. Global Change Biology, 20, 3520-3529.
[71]	Zhang YH, Stevens CJ, Lu XT, He NP, Huang JH, Han XG (2016b). Fewer new species colonize at low frequency N addition in a temperate grassland. Functional Ecology, 30, 1247-1256.
[72]	Zhou JD, Shi RJ, Zhao F, Han SQ, Zhang Y (2016). Effects of the frequency and intensity of nitrogen addition on soil pH, the contents of carbon, nitrogen and phosphorus in temperate steppe in Inner Mongolia, China. Chinese Journal of Applied Ecology, 27, 2467-2476.
	[ 周纪东, 史荣久, 赵峰, 韩斯琴, 张颖 (2016). 施氮频率和强度对内蒙古温带草原土壤pH及碳、氮、磷含量的影响. 应用生态学报, 27, 2467-2476.]
[73]	Zhou LY, Zhou XH, Shao JJ, Nie YY, He YH, Jiang LL, Wu ZT, Bai SH (2016). Interactive effects of global change factors on soil respiration and its components: a meta-analysis. Global Change Biology, 22, 3157-3169.
[74]	Zhou LY, Zhou XH, Zhang BC, Lu M, Luo YQ, Liu LL, Bo L (2014). Different responses of soil respiration and its components to nitrogen addition among biomes: a meta-analysis. Global Change Biology, 20, 2332-2343.
[75]	Zhou XH, Wan SQ, Luo YQ (2007). Source components and interannual variability of soil CO₂ efflux under experimental warming and clipping in a grassland ecosystem. Global Change Biology, 13, 761-775.
[76]	Zhou ZH, Wang CK, Luo YQ (2020). Meta-analysis of the impacts of global change factors on soil microbial diversity and functionality. Nature Communications, 11, 3072-3081. DOI URL
[77]	Zhou ZH, Wang CK, Zheng MH, Jiang LF, Luo YQ (2017). Patterns and mechanisms of responses by soil microbial communities to nitrogen addition. Soil Biology & Biochemistry, 115, 433-441. DOI URL
[78]	Zhu C, Ma YP, Wu HH, Sun T, La Pierre KJ, Sun ZW, Yu Q (2016). Divergent effects of nitrogen addition on soil respiration in a semiarid grassland. Scientific Reports, 6, 33541. DOI: 10.1038/srep33541. DOI URL