氮添加促进丛枝菌根真菌和根系协作维持土壤磷有效性

doi:10.17521/cjpe.2021.0280

摘要/Abstract

摘要：

磷是亚热带地区植物生长的主要限制营养元素, 而氮沉降量的增加会降低土壤磷的有效性。该研究以微生物和植物细根为重点探究土壤磷转化, 揭示氮沉降背景下低磷有效性土壤的磷供应及生产力维持。通过在福州长安山模拟氮沉降实验, 设置对照(0 kg·hm^-2·a^-1)、低氮(40 kg·hm^-2·a^-1)和高氮(80 kg·hm^-2·a^-1) 3个处理, 收集杉木(Cunninghamia lanceolata)幼苗的土壤和根系样本, 综合分析土壤磷组分和养分含量、土壤微生物特征和植物根系特征。结果显示, 与对照处理相比, 低氮处理显著增加土壤易分解态有机磷、中等易分解态无机磷和闭蓄态磷含量, 但是显著降低原生矿物态磷和中等易分解态有机磷含量; 而高氮处理对土壤磷组分无显著影响。冗余分析表明, 土壤酸性磷酸酶活性、丛枝菌根真菌的相对丰度、土壤微生物生物量磷含量和根系生物量是解释土壤磷组分变化的重要微生物和植物因子。方差分解分析发现植物根系特征-土壤微生物特征共同解释了土壤磷组分变化的57%, 并且通过相关分析发现丛枝菌根真菌的相对丰度和根系生物量呈显著正相关关系。综上所述, 低水平的氮输入促进土壤丛枝菌根真菌的定殖, 丛枝菌根真菌和杉木根系通过协作促进中等易分解态有机磷和原生矿物态磷向易分解态磷的转换, 维持了杉木幼苗的生长。

关键词: 氮添加, 磷, 微生物特征, 根系特征, 杉木, 幼苗

Abstract:

Aims Phosphorus is one of the major limiting nutrients for plant growth in subtropical areas, whereas increasing nitrogen deposition may be a limiting factor in determining the availability of soil phosphorus. Here, focusing on soil microorganisms and plant fine roots, we explored the transformation of soil phosphorus to unravel the maintenance of soil phosphorus supply and plant productivity with low availability under nitrogen deposition.

Methods At the Fuzhou Changʼan Mountain in Fujian Province, China, control (0 kg·hm^-2·a^-1), low nitrogen (40 kg·hm^-2·a^-1), and high nitrogen (80 kg·hm^-2·a^-1) treatments were set up to simulate nitrogen addition. Soil and root samples of Cunninghamia lanceolata seedlings were then collected to comprehensively analyze soil phosphorus and nutrient contents as well as microbiological-plant root characteristics.

Important findings The results showed that the contents of soil labile organic phosphorus, moderately labile inorganic phosphorus and occluded phosphorus were significantly increased, whereas those of primary mineral phosphorus and moderately labile organic phosphorus decreased under the low nitrogen treatment as compared to the control treatment. However, there were no significant changes under the high nitrogen treatment. Redundancy analysis indicated that soil acid phosphatase activity, relative abundance of mycorrhizal fungi, soil microbial biomass phosphorus content, and root biomass were important soil microbiological-plant root characteristics factors that could explain the changes in soil phosphorus components. Variance partitioning analysis revealed that the soil microbiological-plant root characteristics synergy explained 57% of the alternations in soil phosphorus components, whereas correlation analysis showed a significant positive correlation between the relative abundance of mycorrhizal fungi and root biomass. Overall, these results suggest that mycorrhizal colonization is promoted under a low level of nitrogen input and the synergistic action of mycorrhizal fungi and C. lanceolata fine roots promotes the conversion of moderately labile organic and primary mineral phosphorus to labile phosphorus, thus maintaining the growth of C. lanceolata seedlings.

Key words: nitrogen addition, phosphorus, microbiologic characteristic, root characteristic, Cunninghamia lanceolata, seedling

谢欢, 张秋芳, 陈廷廷, 曾泉鑫, 周嘉聪, 吴玥, 林惠瑛, 刘苑苑, 尹云锋, 陈岳民. 氮添加促进丛枝菌根真菌和根系协作维持土壤磷有效性. 植物生态学报, 2022, 46(7): 811-822. DOI: 10.17521/cjpe.2021.0280

XIE Huan, ZHANG Qiu-Fang, CHEN Ting-Ting, ZENG Quan-Xin, ZHOU Jia-Cong, WU Yue, LIN Hui-Ying, LIU Yuan-Yuan, YIN Yun-Feng, CHEN Yue-Min. Interaction of soil arbuscular mycorrhizal fungi and plant roots acts on maintaining soil phosphorus availability under nitrogen addition. Chinese Journal of Plant Ecology, 2022, 46(7): 811-822. DOI: 10.17521/cjpe.2021.0280

导出引用管理器 EndNote|Ris|BibTeX

链接本文: https://www.plant-ecology.com/CN/10.17521/cjpe.2021.0280

https://www.plant-ecology.com/CN/Y2022/V46/I7/811

图/表 11

图1 土壤磷(P)组分的提取流程和分类(图片内容参考自Hedley等(1982), Tiessen和Moir (2007))。

Fig. 1 Extraction procedure and classification of soil phosphorus (P) fractions (Picture content referenced from Hedley et al. (1982), Tiessen & Moir (2007)). Pi, inorganic phosphorus; Po, organic phosphorus.

表1 施氮对福州长安山土壤理化性质的影响

Table 1 Effects of nitrogen (N) addition on soil physical and chemical properties at the Fuzhou Changʼan Mountain in Fujian Province

处理 Treatment	pH	总碳含量 Total carbon (C) content (g·kg^-1)	总氮含量 Total N content (g·kg^-1)	有效氮含量 Available N content (mg·kg^-1)	可溶性有机碳含量 Dissolved organic C content (mg·kg^-1)	可溶性有机氮含量 Dissolved organic N content (mg·kg^-1)
CK	4.55 ± 0.06^a	16.30 ± 0.23^a	1.47 ± 0.03^a	7.97 ± 0.22^b	7.67 ± 0.60^a	4.61 ± 0.40^b
LN	4.51 ± 0.06^a	16.20 ± 0.04^a	1.48 ± 0.05^a	8.58 ± 0.49^a	6.78 ± 0.44^b	6.68 ± 0.36^a
HN	4.40 ± 0.09^b	16.61 ± 0.24^a	1.50 ± 0.02^a	8.83 ± 0.25^a	3.99 ± 0.71^c	7.24 ± 0.71^a
p	0.03	0.06	0.57	0.01	<0.01	<0.01

图2 施氮(N)对福州长安山土壤磷(P)组分含量的影响(平均值±标准差)。不同小写字母表示处理间差异显著(p < 0.05)。CK, 对照; HN, 高氮; LN, 低氮。

Fig. 2 Effects of nitrogen (N) addition on soil phosphorus (P) components contents at the Fuzhou Changʼan Mountain in Fujian Province (mean ± SD). Different lowercase letters mean significant difference among different treatments (p < 0.05). CK, control; HN, high nitrogen; LN, low nitrogen. Pi, inorganic phosphorus; Po, organic phosphorus.

表2 施氮(N)对福州长安山土壤真菌群落的影响(%)(平均值±标准差)

Table 2 Effects of nitrogen addition on soil fungi community (%) at the Fuzhou Changʼan Mountain in Fujian Province (mean ± SD)

处理 Treatment	子囊菌门 Ascomycota	担子菌门 Basidiomycotaota	被孢菌门 Mortierellomycota	未定义 Unclassified	罗兹菌门 Rozellomycota	球囊菌门 Glomeromycota	其他 Other
CK	38.73 ± 9.28^a	26.04 ± 7.02^a	11.94 ± 3.16^a	11.18 ± 1.03^a	9.87 ± 6.22^a	0.27 ± 0.01^b	1.97 ± 0.56^a
LN	39.02 ± 6.00^a	26.16 ± 3.33^a	16.86 ± 3.52^a	10.83 ± 4.13^a	4.61 ± 0.97^a	1.09 ± 0.11^a	1.43 ± 0.48^a
HN	35.05 ± 12.21^a	37.24 ± 13.12^a	14.43 ± 2.39^a	8.11 ± 3.91^a	3.77 ± 1.27^a	0.62 ± 0.01^a	0.90 ± 0.63^a
p	0.809	0.175	0.129	0.400	0.091	<0.001	0.072

表3 施氮对福州长安山土壤酶活性和微生物生物量养分含量的影响(平均值±标准差)

Table 3 Effects of nitrogen (N) addition on soil enzymes activity and microbial biomass nutrient content at the Fuzhou Changʼan Mountain in Fujian Province (mean ± SD)

处理 Treatment	酸性磷酸单酯酶 Acid phosphomonoesterase (nmol·g^-1·h^-1)	酸性磷酸双酯酶 Acid phosphodiesterase (nmol·g^-1·h^-1)	微生物生物量碳含量 Microbial biomass carbon content (mg·kg^-1)	微生物生物量氮含量 Microbial biomass N content (mg·kg^-1)	微生物生物量磷含量 Microbial biomass phosphorus content (mg·kg^-1)
CK	24.68 ± 2.44^b	1.67 ± 0.08^a	215.42 ± 21.87^c	29.59 ± 1.40^a	41.07 ± 3.31^a
LN	48.89 ± 4.08^a	1.72 ± 0.05^a	273.59 ± 18.53^b	26.45 ± 0.98^b	21.75 ± 2.09^b
HN	19.59 ± 2.90^c	1.19 ± 0.03^b	358.27 ± 20.05^a	27.62 ± 0.95^b	20.78 ± 6.45^b
p	<0.001	<0.001	<0.001	0.003	<0.001

表4 施氮对福州长安山植物根系特征的影响(平均值±标准差)

Table 4 Effects of nitrogen (N) addition on plant roots traits at the Fuzhou Changʼan Mountain in Fujian Province (mean ± SD)

处理 Treatment	根系生物量 Root biomass (g·plant^-1)	根系总碳含量 Root total carbon content (g·kg^-1)	根系总氮含量 Root total N content (g·kg^-1)	根系总磷含量 Root total phosphorous content (g·kg^-1)	侵染率 Root colonization rate (%)	直径 root diameter (mm)	比根长 Specific root length (m·g^-1)	比表面积 Specific root surface area (cm·g^-1)	组织密度 Root tissue density (g·cm^-3)
CK	2.79 ± 0.46^b	459.61 ± 4.62^b	9.61 ± 1.20^a	1.66 ± 0.23^a	58.23 ± 8.71^c	0.82 ± 0.13^a	36.13 ± 6.39^a	554.02 ± 25.53^a	0.20 ± 0.10^a
LN	4.01 ± 0.39^a	467.72 ± 8.98^a	10.01 ± 0.98^a	1.37 ± 0.19^ab	80.09 ± 4.13^b	0.69 ± 0.44^a	35.36 ± 9.58^a	265.01 ± 62.72^b	0.62 ± 0.37^a
HN	3.06 ± 0.49^b	470.08 ± 5.63^a	8.63 ± 1.18^a	1.31 ± 0.11^b	89.67 ± 4.69^a	0.39 ± 0.12^a	36.68 ± 12.59^a	342.53 ± 63.65^b	0.44 ± 0.21^a
p	0.003	<0.001	0.180	0.023	<0.001	0.079	0.978	<0.001	0.062

图3 生物因子和非生物因子解释土壤磷组分变化的百分比。

Fig. 3 Percentages of the variance in soil phosphorus components explained by biotic factors and abiotic factors.

图4 土壤微生物特征(A)和植物根系特征(B)对福州长安山土壤磷(P)组分影响的冗余分析(RDA)。

Fig. 4 Redundancy analysis (RDA) of soil microbial (A) and plant roots characteristics (B) on soil phosphorus (P) components at the Fuzhou Changʼan Mountain in Fujian Province. AcP, acid phosphomonolase; AMF, arbuscular mycorrhizal fungi; FRD, fine root diameter; MBC, microbial biomass carbon; MBN, microbial biomass nitrogen; MBP, microbial biomass phosphorus; PD, acid phosphodiesterase; Pi, inorganic phosphorus; Po, organic phosphorus; RC, root colonization; RM, root biomass; RTC, root total carbon; RTD, special root density; RTN, root total nitrogen; RTP, root total phosphorous; SRA, special root area; SRL, special root length.

图5 方差分解分析显示由植物变量和微生物变量解释土壤磷组分变异百分比。

Fig. 5 Variation-partitioning analysis showing the percentages of the variance in soil phosphorus components explained by plant and microorganism variables.

表5 福州长安山土壤微生物特征和植物根系特征的相关系数

Table 5 Correlation coefficients between soil microbial and plant roots characteristics at the Fuzhou Changʼan Mountain in Fujian Province

	根系生物量 Root biomass	直径 Root diameter	比根长 Specific root length	比表面积 Specific root surface area	组织密度 Root tissue density	侵染率 Root colonization rate	根系总碳含量 Root total carbon content
酸性磷酸单酯酶活性 Acid phosphomonoesterase activity	0.713^**	0.264	-0.009	-0.287	-0.434	0.064	0.267
酸性磷酸双酯酶活性 Acid phosphodiesterase activity	0.306	0.541^*	0.001	0.400	-0.585^*	-0.590^*	-0.417
丛枝菌根真菌相对丰度 Mycorrhizal Fungi relative abundance	0.789^**	0.013	0.032	-0.668^**	-0.112	0.485	0.625^*
微生物生物量碳含量 Microbial biomass carbon content	0.007	-0.639^*	-0.042	-0.713^**	0.537^*	0.740^**	0.796^**
微生物生物量氮含量 Microbial biomass nitrogen content	-0.566^*	0.061	-0.068	0.687^**	0.041	-0.589^*	-0.642^**
微生物生物量磷含量 Microbial biomass phosphorus content	-0.439	0.362	0.119	0.829^**	-0.177	0.855^**	-0.894^**

图6 土壤磷(P)组分对施氮(N)的响应概念图。“ ”、“ ”、“ ”分别表示土壤微生物、植物根系指标含量显著增加、降低和无显著变化。“ ”和“ ”分别表示土壤各P组分显著增加和降低。Pi, 无机P; Po, 有机P。

Fig. 6 A conceptual diagram of the responses of soil phosphorus (P) components to nitrogen (N) addition and the regulation effect of soil microbes and plant root systems. “ ”、“ ”、“ ” represent that the contents of soil microbial and plant root index show significant increase, decrease, and no significant change, respectively. “ ” and “ ” represent that soil phosphorus components show significant increase and decrease, respectively. Pi, inorganic phosphorus; Po, organic phosphorus.

参考文献 44

[1]	Ackerman D, Millet DB, Chen X (2019). Global estimates of inorganic nitrogen deposition across four decades. Global Biogeochemical Cycles, 33, 100-107.
[2]	Aoki M, Fujii K, Kitayama K (2012). Environmental control of root exudation of low-molecular weight organic acids in tropical rainforests. Ecosystems, 15, 1194-1203. DOI URL
[3]	Bing HJ, Wu YH, Zhou J, Sun HY, Luo J, Wang JP, Yu D (2016). Stoichiometric variation of carbon, nitrogen, and phosphorus in soils and its implication for nutrient limitation in alpine ecosystem of eastern Tibetan Plateau. Journal of Soils & Sediments, 16, 405-416.
[4]	Braun S, Thomas VFD, Quiring R, Flückiger W (2010). Does nitrogen deposition increase forest production? The role of phosphorus. Environmental Pollution, 158, 2043-2052. DOI URL
[5]	Brookes PC, Powlson DS, Jenkinson DS (1982). Measurement of microbial biomass phosphorus in soil. Soil Biology & Biochemistry, 14, 319-329. DOI URL
[6]	Cao JL, Lin TC, Yang ZJ, Zheng Y, Xie L, Xiong DC, Yang YS (2020). Warming exerts a stronger effect than nitrogen addition on the soil arbuscular mycorrhizal fungal community in a young subtropical Cunninghamia lanceolata plantation. Geoderma, 367, DOI: 10.1016/j.geoderma.2020.114273. DOI
[7]	Fan YX, Zhong XJ, Lin F, Liu CC, Yang LM, Wang MH, Chen GS, Chen YM, Yang YS (2019). Responses of soil phosphorus fractions after nitrogen addition in a subtropical forest ecosystem: insights from decreased Fe and Al oxides and increased plant roots. Geoderma, 337, 246-255. DOI URL
[8]	Fujii K, Aoki M, Kitayama K (2013). Reprint of “Biodegradation of low molecular weight organic acids in rhizosphere soils from a tropical montane rain forest”. Soil Biology & Biochemistry, 56, 3-9. DOI URL
[9]	George TS, Turner BL, Gregory PJ, Cade-Menun BJ, Richardson AE (2006). Depletion of organic phosphorus from Oxisols in relation to phosphatase activities in the rhizosphere. European Journal of Soil Science, 57, 47-57. DOI URL
[10]	Goswami S, Fisk MC, Vadeboncoeur MA, Garrison-Johnston M, Yanai RD, Fahey TJ (2018). Phosphorus limitation of aboveground production in northern hardwood forests. Ecology, 99, 438-449. DOI URL
[11]	Guo W, Geng ZZ, Chen Z, Li Q, Yang YX, Shen S, Jin DM, Wang CG (2018). Effects of nitrogen addition on mycorrhizal fungi community structure and diversity of Pinus koraiensis and Fraxinus mandshurica in Changbai Mountain. Ecology and Environmental Sciences, 27, 10-17.
	[郭伟, 耿珍珍, 陈朝, 李晴, 杨颜熙, 申思, 金大明, 王存国 (2018). 模拟氮沉降增加对长白山红松和水曲柳菌根真菌群落结构及多样性的影响. 生态环境学报, 27, 10-17.]
[12]	Hedley MJ, Stewart JWB, Chauhan BS (1982). Changes in inorganic and organic soil phosphorus fractions induced by cultivation practices and by laboratory incubations. Soil Science Society of America Journal, 46, 970-976. DOI URL
[13]	Helfenstein J, Tamburini F, von Sperber C, Massey MS, Pistocchi C, Chadwick OA, Vitousek PM, Kretzschmar R, Frossard E (2018). Combining spectroscopic and isotopic techniques gives a dynamic view of phosphorus cycling in soil. Nature Communications, 9, 3226. DOI: 10.1038/s41467-018-05731-2. DOI PMID
[14]	Heuck C, Smolka G, Whalen ED, Frey S, Gundersen P, Moldan F, Fernandez IJ, Spohn M (2018). Effects of long-term nitrogen addition on phosphorus cycling in organic soil horizons of temperate forests. Biogeochemistry, 141, 167-181. DOI URL
[15]	Hou E, Chen C, Kuang Y, Zhang Y, Heenan M, Wen D (2016). A structural equation model analysis of phosphorus transformations in global unfertilized and uncultivated soils. Global Biogeochemical Cycles, 30, 1300-1309. DOI URL
[16]	Huang WJ, Zhou GY, Liu JX, Duan HL, Liu XZ, Fang X, Zhang DQ (2014). Shifts in soil phosphorus fractions under elevated CO₂and N addition in model forest ecosystems in subtropical China. Plant Ecology, 215, 1373-1384. DOI URL
[17]	James M, Bernard M (1997). Reviews: working with mycorrhizas in forestry and agriculture. New Phytologist, 135, 788.
[18]	Jia LQ, Chen GS, Zhang LH, Chen TT, Jiang Q, Chen YH, Fan AL, Wang X (2019). Plastic responses of fine root morphological traits of Castanopsis fabri and Castanopsis carlesii to short-term nitrogen addition. Chinese Journal of Applied Ecology, 30, 4003-4011.
	[贾林巧, 陈光水, 张礼宏, 陈廷廷, 姜琦, 陈宇辉, 范爱连, 王雪 (2019). 罗浮栲和米槠细根形态功能性状对短期氮添加的可塑性响应. 应用生态学报, 30, 4003-4011.] DOI
[19]	Kramer-Walter KR, Laughlin DC (2017). Root nutrient concentration and biomass allocation are more plastic than morphological traits in response to nutrient limitation. Plant and Soil, 416, 539-550. DOI URL
[20]	Lambers H, Raven JA, Shaver GR, Smith SE (2008). Plant nutrient-acquisition strategies change with soil age. Trends in Ecology & Evolution, 23, 95-103. DOI URL
[21]	Li L, McCormack ML, Chen FS, Wang HM, Ma ZQ, Guo DL (2019). Different responses of absorptive roots and arbuscular mycorrhizal fungi to fertilization provide diverse nutrient acquisition strategies in Chinese fir. Forest Ecology and Management, 433, 64-72. DOI URL
[22]	Lin GG, Gao MX, Zeng DH, Fang YT (2020). Aboveground conservation acts in synergy with belowground uptake to alleviate phosphorus deficiency caused by nitrogen addition in a larch plantation. Forest Ecology and Management, 473, 118309. DOI: 10.1016/j.foreco.2020.118309. DOI URL
[23]	Marklein AR, Houlton BZ (2012). Nitrogen inputs accelerate phosphorus cycling rates across a wide variety of terrestrial ecosystems. New Phytologist, 193, 696-704. DOI PMID
[24]	Oehl F, Oberson A, Probst M, Fliessbach A, Roth HR, Frossard E (2001). Kinetics of microbial phosphorus uptake in cultivated soils. Biology and Fertility of Soils, 34, 31-41. DOI URL
[25]	Ostonen I, Truu M, Helmisaari HS, Lukac M, Borken W, Vanguelova E, Godbold DL, Lõhmus K, Zang U, Tedersoo L, Preem JK, Rosenvald K, Aosaar J, Armolaitis K, Frey J, et al. (2017). Adaptive root foraging strategies along a boreal-temperate forest gradient. New Phytologist, 215, 977-991. DOI PMID
[26]	Peñuelas J, Poulter B, Sardans J, Ciais P, van der Velde M, Bopp L, Boucher O, Godderis Y, Hinsinger P, Llusia J, Nardin E, Vicca S, Obersteiner M, Janssens IA (2013). Human-induced nitrogen-phosphorus imbalances alter natural and managed ecosystems across the globe. Nature Communications, 4, 2934. DOI: 1038/ncomms3934. DOI PMID
[27]	Rennenberg H, Herschbach C (2013). Phosphorus nutrition of woody plants: many questions-few answers. Plant Biology, 15, 785-788. DOI PMID
[28]	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. DOI URL
[29]	Shipley B, Meziane D (2002). The balanced-growth hypothesis and the allometry of leaf and root biomass allocation. Functional Ecology, 16, 326-331. DOI URL
[30]	Smith SE, Read DJ (2008). Mycorrhizal Symbiosis. 3rd ed. Academic Press, Salt Lake City, USA.
[31]	Solaiman MZ, Ezawa T, Kojima T, Saito M (1999). Polyphosphates in intraradical and extraradical hyphae of an arbuscular mycorrhizal fungus, Gigaspora margarita. Applied and Environmental Microbiology, 65, 5604-5606.
[32]	Tian J, Wei K, Condron LM, Chen Z, Xu Z, Chen L (2016). Impact of land use and nutrient addition on phosphatase activities and their relationships with organic phosphorus turnover in semi-arid grassland soils. Biology and Fertility of Soils, 52, 675-683. DOI URL
[33]	Tiessen H, Moir JO (2007). Characterization of available P by sequential extraction//Carter MR, Gregorich EG. Soil Sampling and Methods of Analysis. 2nd ed. CRC Press, Boca Raton, USA. 293-306.
[34]	Toljander JF, Lindahl BD, Paul LR, Elfstrand M, Finlay RD (2007). Influence of arbuscular mycorrhizal mycelial exudates on soil bacterial growth and community structure. FEMS Microbiology Ecology, 61, 295-304. PMID
[35]	Ushio M, Fujiki Y, Hidaka A, Kitayama K (2015). Linkage of root physiology and morphology as an adaptation to soil phosphorus impoverishment in tropical montane forests. Functional Ecology, 29, 1235-1245. DOI URL
[36]	Vance ED, Brookes PC, Jenkinson DS (1987). An extraction method for measuring soil microbial biomass C. Soil Biology & Biochemistry, 19, 703-707. DOI URL
[37]	Vitousek PM, Porder S, Houlton BZ, Chadwick OA (2010). Terrestrial phosphorus limitation: mechanisms, implications, and nitrogen-phosphorus interactions. Ecological Applications, 20, 5-15. DOI URL
[38]	Wardle DA, Walker LR, Bardgett RD (2005). Response to comment on “Ecosystem properties and forest decline in contrasting long-term chronosequences”. Science, 308, 633.
[39]	Wright SJ, Turner BJ, Yavitt JB, Harms KE, Kaspari M, Tanner EVJ, Bujan J, Griffin EA, Mayor JR, Pasquini SC, Sheldrake M, Garcia MN (2018). Plant responses to fertilization experiments in lowland, species-rich, tropical forests. Ecology, 99, 1129-1138. DOI URL
[40]	Xiang W, Li L, Ouyang S, Xiao W, Zeng L, Chen L, Lei P, Deng X, Zeng Y, Fang J, Forrester DI (2021). Effects of stand age on tree biomass partitioning and allometric equations in Chinese fir (Cunninghamia lanceolata) plantations. European Journal of Forest Research, 140, 317-332. DOI URL
[41]	Xie H, Zhang QF, Zeng QX, Li YX, Ma YP, Lin HY, Liu YY, Yin YF, Chen YM (2020). Nitrogen application drives the transformation of phosphorus fractions in Cunninghamia lanceolata plantation by changing microbial biomass phosphorus. Chinese Journal of Ecology, 39, 3934-3942.
	[谢欢, 张秋芳, 曾泉鑫, 李宇轩, 马亚培, 林惠瑛, 刘苑苑, 尹云锋, 陈岳民 (2020). 施氮通过改变微生物生物量磷驱动杉木人工林土壤磷组分转化. 生态学杂志, 39, 3934-3942.]
[42]	Zeng QX, Zeng XM, Lin KM, Zhang QF, Cheng L, Zhou JC, Lin QY, Chen YM, Xu JG (2020). Responses of soil phosphorus fractions and microorganisms to nitrogen application in a subtropical Phyllostachys pubescen forest. Chinese Journal of Applied Ecology, 31, 753-760.
	[曾泉鑫, 曾晓敏, 林开淼, 张秋芳, 程蕾, 周嘉聪, 林巧玉, 陈岳民, 徐建国 (2020). 亚热带毛竹林土壤磷组分和微生物对施氮的响应. 应用生态学报, 31, 753-760.] DOI
[43]	Zhang HZ, Shi LL, Wen D, Yu KL (2016). Soil potential labile but not occluded phosphorus forms increase with forest succession. Biology & Fertility of Soils, 52, 41-51.
[44]	Zhang W (2013). Observation of N/S Deposition Fluxes and Investigation of Simulated S Deposition Effect on Soil N₂O Production of Castanopsis carlesii Forests. Master degree dissertation, Fujian Normal University, Fuzhou. 15-19.
	[章伟 (2013). N/S沉降通量观测及模拟氮沉降对米槠林土壤N₂O产生影响研究. 硕士学位论文, 福建师范大学, 福州. 15-19.]