Soil extracellular enzyme activities and their stoichiometric ratio in the alpine treeline ecotones in Gongga Mountain, China

doi:10.17521/cjpe.2021.0215

Abstract

Abstract:

Aims Soil extracellular enzymes and enzyme stoichiometry are indicators of soil nutrient availability and microbial substrate limitation. Subalpine treeline ecotones are special areas which are sensitive to global change. However, the patterns in soil enzyme activities and stoichiometry, and their key drivers remain unclear in the subalpine treeline ecotones.

Methods In this study, soils from a subalpine treeline ecotone in Gongga Mountain in Southeast of Qingzang Plateau were collected. The activities of five hydrolases (β-1,4-glucosidase (BG), cellobiohydrolase (CBH), xylosidase (XYL), β-N-acetyl glucosaminidase (NAG), leucine aminopeptidase (LAP)) and two oxidases (polyphenol oxidase (POX), catalase (CAT)) were detected. The stoichiometric ratios of soil extracellular enzyme activities (carbon and nitrogen enzyme activity ratio and carbon quality index) were calculated.

Important findings Our results showed that LAP, POX and CAT activities of the shrub soils were significantly lower than those of the treeline and forest soils, XYL activity was the lowest at the treeline, and the activities of other extracellular enzymes did not differ significantly among locations in the treeline ecotone. The lnBG/lnLAP of the shrub soil was significantly higher than those of the forest and treeline soils, lnBG/ln(NAG + LAP) did not vary significantly at the treeline ecotone, and the carbon quality index was highest at the treeline. Soil extracellular enzyme activity stoichiometric ratios were not significantly related to microbial nutrient status. Non-metric multidimensional scaling analysis showed that total carbon, total nitrogen, nitrate nitrogen content and lignin to nitrogen ratio of plant leaves were the main factors influencing soil extracellular enzyme activities in the treeline ecotone. The main drivers of the stoichiometric ratios of extracellular enzyme activities were soil dissolved nitrogen, carbon to nitrogen ratio, and lignin to nitrogen ratio of plant leaves. In summary, some soil enzyme activities and their stoichiometric ratios varied significantly along the treeline ecotone, which was mainly influenced by the changes in vegetation type, possibly via its influences on plant-associated microbial communities. Treeline migration induced by future climate change may change extracellular enzyme activities and thus affect soil nutrient cycling.

Key words: soil extracellular enzyme activities, treeline ecotones, enzyme stoichiometric ratio, vegetation type

LI Dong, TIAN Qiu-Xiang, ZHAO Xiao-Xiang, LIN Qiao-Ling, YUE Peng-Yun, JIANG Qing-Hu, LIU Feng. Soil extracellular enzyme activities and their stoichiometric ratio in the alpine treeline ecotones in Gongga Mountain, China[J]. Chin J Plant Ecol, 2022, 46(2): 232-242.

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https://www.plant-ecology.com/EN/Y2022/V46/I2/232

Figures/Tables 8

References 42

[1]	Adair EC, Parton WJ, del Grosso SJ, Silver WL, Harmon ME, Hall SA, Burke IC, Hart SC (2008). Simple three-pool model accurately describes patterns of long-term litter decomposition in diverse climates. Global Change Biology, 14, 2636-2660. DOI URL
[2]	Allison SD, Gartner TB, Holland K, Weintraub M, Sinsabaugh RL (2007). Soil enzymes: linking proteomics and ecological processes//Hurst CJ, Crawford RL, Garland JL, Lispon DA, Mills AL, Stetzenbach LD. Manual of Environmental Microbiology. 3rd ed. American Society of Microbiology Press, Washington D.C. 704-711.
[3]	Banerjee S, Bora S, Thrall PH, Richardson AE (2016). Soil C and N as causal factors of spatial variation in extracellular enzyme activity across grassland-woodland ecotones. Applied Soil Ecology, 105, 1-8. DOI URL
[4]	Bhardwaj N, Kumar B, Verma P (2019). A detailed overview of xylanases: an emerging biomolecule for current and future prospective. Bioresources and Bioprocessing, 6, 40. DOI: 10.1186/s40643-019-0276-2. DOI URL
[5]	Bloom AJ, Chapin III FS, Mooney HA (1985). Resource limitation in plants-An economic analogy. Annual Review of Ecology and Systematics, 16, 363-392. DOI URL
[6]	Bowles TM, Acosta-Martínez V, Calderón F, Jackson LE (2014). Soil enzyme activities, microbial communities, and carbon and nitrogen availability in organic agroecosystems across an intensively-managed agricultural landscape. Soil Biology & Biochemistry, 68, 252-262.
[7]	Caldwell BA (2005). Enzyme activities as a component of soil biodiversity: a review. Pedobiologia, 49, 637-644. DOI URL
[8]	Carreiro MM, Sinsabaugh RL, Repert DA, Parkhurst DF (2000). Microbial enzyme shifts explain litter decay responses to simulated nitrogen deposition. Ecology, 81, 2359-2365.
[9]	Crim PM, Cumming JR (2020). Extracellular soil enzyme activities in high-elevation mixed red spruce forests in central Appalachia, USA. Forests, 11, 468. DOI: 10.3390/ f11040468. DOI URL
[10]	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. DOI URL
[11]	German DP, Weintraub MN, Grandy AS, Lauber CL, Rinkes ZL, Allison SD (2011). Optimization of hydrolytic and oxidative enzyme methods for ecosystem studies. Soil Biology & Biochemistry, 43, 1387-1397. DOI URL
[12]	Hall SJ, Huang W, Timokhin VI, Hammel KE (2020). Lignin lags, leads, or limits the decomposition of litter and soil organic carbon. Ecology, 101, e03113. DOI: 10.1002/ecy. 3113. DOI
[13]	He QQ, Wu YH, Bing HJ, Zhou J, Wang JP (2020). Vegetation type rather than climate modulates the variation in soil enzyme activities and stoichiometry in subalpine forests in the eastern Tibetan Plateau. Geoderma, 374, 114424. DOI: 10.1016/j.geoderma.2020.114424. DOI URL
[14]	Hernández DL, Hobbie SE (2010). The effects of substrate composition, quantity, and diversity on microbial activity. Plant and Soil, 335, 397-411. DOI URL
[15]	Hill BH, Elonen CM, Herlihy AT, Jicha TM, Serenbetz G (2018). Microbial ecoenzyme stoichiometry, nutrient limitation, and organic matter decomposition in wetlands of the conterminous United States. Wetlands Ecology and Management, 26, 425-439. DOI URL
[16]	Jiang J, Song MH (2010). Review of the roles of plants and soil microorganisms in regulating ecosystem nutrient cycling. Chinese Journal of Plant Ecology, 34, 979-988.
	[ 蒋婧, 宋明华 (2010). 植物与土壤微生物在调控生态系统养分循环中的作用. 植物生态学报, 34, 979-988.] DOI
[17]	Kivlin SN, Treseder KK (2014). Soil extracellular enzyme activities correspond with abiotic factors more than fungal community composition. Biogeochemistry, 117, 23-37. DOI URL
[18]	LeBauer DS, Treseder KK (2008). Nitrogen limitation of net primary productivity in terrestrial ecosystems is globally distributed. Ecology, 89, 371-379. PMID
[19]	Liu JB, Chen J, Chen GS, Guo JF, Li YQ (2020). Enzyme stoichiometry indicates the variation of microbial nutrient requirements at different soil depths in subtropical forests. PLOS ONE, 15, e0220599. DOI: 10.1371/journal.pone.0220599. DOI URL
[20]	Min K, Freeman C, Kang H, Choi SU (2015). The regulation by phenolic compounds of soil organic matter dynamics under a changing environment. BioMed Research International, 2015, 825098. DOI: 10.1155/2015/825098. DOI
[21]	Müller M, Oelmann Y, Schickhoff U, Böhner J, Scholten T (2017). Himalayan treeline soil and foliar C:N:P stoichiometry indicate nutrient shortage with elevation. Geoderma, 291, 21-32. DOI URL
[22]	Okubo A, Matsusaka M, Sugiyama S (2016). Impacts of root symbiotic associations on interspecific variation in sugar exudation rates and rhizosphere microbial communities: a comparison among four plant families. Plant and Soil, 399, 345-356. DOI URL
[23]	Peng XQ, 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. DOI URL
[24]	Ran F, Liang YM, Yang Y, Yang Y, Wang GX (2014). Spatial-temporal dynamics of an Abies fabri population near the alpine treeline in the Yajiageng area of Gongga Mountain, China. Acta Ecologica Sinica, 34, 6872-6878.
	[ 冉飞, 梁一鸣, 杨燕, 杨阳, 王根绪 (2014). 贡嘎山雅家埂峨眉冷杉林线种群的时空动态. 生态学报, 34, 6872-6878.]
[25]	Rumpel C, Kögel-Knabner I (2011). Deep soil organic matter -A key but poorly understood component of terrestrial C cycle. Plant and Soil, 338, 143-158. DOI URL
[26]	Sagar R, Singh JS (2006). Tree density, basal area and species diversity in a disturbed dry tropical forest of northern India: implications for conservation. Environmental Conservation, 33, 256-262. DOI URL
[27]	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
[28]	Shi XJ, Pan JJ, Chen JY, Yang ZQ, Zhang LM, Sun B, Li ZP (2009). Effects of different types of litters on soil organic carbon mineralization. Environmental Science, 30, 1832-1837.
	[ 史学军, 潘剑君, 陈锦盈, 杨志强, 张黎明, 孙波, 李忠佩 (2009). 不同类型凋落物对土壤有机碳矿化的影响. 环境科学, 30, 1832-1837.]
[29]	Sigdel SR, Liang E, Wang Y, Dawadi B, Camarero JJ (2020). Tree-to-tree interactions slow down Himalayan treeline shifts as inferred from tree spatial patterns. Journal of Biogeography, 47, 1816-1826. DOI URL
[30]	Sinsabaugh RL, Follstad Shah JJ (2012). Ecoenzymatic stoichiometry and ecological theory. Annual Review of Ecology, Evolution, and Systematics, 43, 313-343. DOI URL
[31]	Sinsabaugh RL, Hill BH, Follstad Shah JJ (2009). Ecoenzymatic stoichiometry of microbial organic nutrient acquisition in soil and sediment. Nature, 462, 795-798. DOI URL
[32]	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, et al. (2008). Stoichiometry of soil enzyme activity at global scale. Ecology Letters, 11, 1252-1264. DOI PMID
[33]	Tedersoo L, Bahram M (2019). Mycorrhizal types differ in ecophysiology and alter plant nutrition and soil processes. Biological Reviews of the Cambridge Philosophical Society, 94, 1857-1880. DOI PMID
[34]	Thevenot M, Dignac MF, Rumpel C (2010). Fate of lignins in soils: a review. Soil Biology & Biochemistry, 42, 1200-1211. DOI URL
[35]	Wang B, Xue S, Liu GB, Zhang GH, Li G, Ren ZP (2012). Changes in soil nutrient and enzyme activities under different vegetations in the Loess Plateau area, Northwest China. Catena, 92, 186-195.
[36]	Xu ZW, Yu GR, Zhang XY, He NP, Wang QF, Wang SZ, Wang RL, Zhao N, Jia YL, Wang CY (2017). Soil enzyme activity and stoichiometry in forest ecosystems along the North-South Transect in eastern China (NSTEC). Soil Biology & Biochemistry, 104, 152-163. DOI URL
[37]	Yin R, Deng H, Wang HL, Zhang B (2014). Vegetation type affects soil enzyme activities and microbial functional diversity following re-vegetation of a severely eroded red soil in sub-tropical China. Catena, 115, 96-103. DOI URL
[38]	Zeglin LH, Kluber LA, Myrold DD (2013). The importance of amino sugar turnover to C and N cycling in organic horizons of old-growth Douglas-fir forest soils colonized by ectomycorrhizal mats. Biogeochemistry, 112, 679-693. DOI URL
[39]	Zhang Y, Li C, Wang ML (2019). Linkages of C:N:P stoichiometry between soil and leaf and their response to climatic factors along altitudinal gradients. Journal of Soils and Sediments, 19, 1820-1829. DOI
[40]	Zheng HF, Liu Y, Zhang J, Chen YM, Yang L, Li HJ, Wang LF (2018). Factors influencing soil enzyme activity in China’s forest ecosystems. Plant Ecology, 219, 31-44. DOI URL
[41]	Zhou LH, Liu SS, Shen HH, Zhao MY, Xu LC, Xing AJ, Fang JY (2020). Soil extracellular enzyme activity and stoichiometry in Chinaʼs forests. Functional Ecology, 34, 1461-1471. DOI URL
[42]	Zuo YP, Li JP, Zeng H, Wang W (2018). Vertical pattern and its driving factors in soil extracellular enzyme activity and stoichiometry along mountain grassland belts. Biogeochemistry, 141, 23-39. DOI URL

	森林(峨眉冷杉) Forest (Abies fabri)					树线(峨眉冷杉) Treeline (Abies fabri)	灌丛(毡毛栎叶杜鹃) Shrub (Rhododendron phaeochrysum var. levistratum)			位置 Location
	F3	F2		F1		树线(峨眉冷杉) Treeline (Abies fabri)	S1	S2	S3	位置 Location
单位面积胸高断面积 BA (m²·hm^-2)	291.0 ± 49.0^a		235.7 ± 42.2^ab		171.1 ± 47.9^abc	110.1 ± 22.9^c	135.6 ± 17.3^bc	149.9 ± 14.7^bc	124.8 ± 19.2^bc	**
叶片碳含量 Leaf carbon (C) content (mg·g^-1)	429.4 ± 35.5^ab		457.9 ± 41.1^a		431.0 ± 28.8^a	397.2 ± 25.0^abc	361.8 ± 34.3^bc	369.0 ± 26.1^bc	354.8 ± 20.2^c	***
叶片氮含量 Leaf nitrogen (N) content (mg·g^-1)	13.2 ± 0.3^a		12.7 ± 0.8^a		13.1 ± 0.8^a	12.2 ± 0.5^a	8.6 ± 0.8^b	8.3 ± 0.5^b	7.9 ± 0.7^b	***
叶片碳氮比 Leaf C:N	32.5 ± 2.2^c		36.0 ± 1.4^bc		33.2 ± 2.2^bc	32.7 ± 2.4^bc	42.3 ± 2.6^ab	44.8 ± 3.4^a	45.8 ± 3.3^a	***
叶片木质素:氮 Leaf lignin:N	1.7 ± 0.1^b		1.9 ± 0.1^ab		2.0 ± 0.1^ab	2.1 ± 0.1^a	0.8 ± 0.1^c	0.7 ± 0.0^c	0.7 ± 0.1^c	***

	森林(峨眉冷杉) Forest (Abies fabri)					树线(峨眉冷杉) Treeline (Abies fabri)	灌丛(毡毛栎叶杜鹃) Shrub (Rhododendron phaeochrysum var. levistratum)			位置 Location
	F3	F2		F1		树线(峨眉冷杉) Treeline (Abies fabri)	S1	S2	S3	位置 Location
单位面积胸高断面积 BA (m²·hm^-2)	291.0 ± 49.0^a		235.7 ± 42.2^ab		171.1 ± 47.9^abc	110.1 ± 22.9^c	135.6 ± 17.3^bc	149.9 ± 14.7^bc	124.8 ± 19.2^bc	**
叶片碳含量 Leaf carbon (C) content (mg·g^-1)	429.4 ± 35.5^ab		457.9 ± 41.1^a		431.0 ± 28.8^a	397.2 ± 25.0^abc	361.8 ± 34.3^bc	369.0 ± 26.1^bc	354.8 ± 20.2^c	***
叶片氮含量 Leaf nitrogen (N) content (mg·g^-1)	13.2 ± 0.3^a		12.7 ± 0.8^a		13.1 ± 0.8^a	12.2 ± 0.5^a	8.6 ± 0.8^b	8.3 ± 0.5^b	7.9 ± 0.7^b	***
叶片碳氮比 Leaf C:N	32.5 ± 2.2^c		36.0 ± 1.4^bc		33.2 ± 2.2^bc	32.7 ± 2.4^bc	42.3 ± 2.6^ab	44.8 ± 3.4^a	45.8 ± 3.3^a	***
叶片木质素:氮 Leaf lignin:N	1.7 ± 0.1^b		1.9 ± 0.1^ab		2.0 ± 0.1^ab	2.1 ± 0.1^a	0.8 ± 0.1^c	0.7 ± 0.0^c	0.7 ± 0.1^c	***

土壤指标 Soil index	森林 Forest			树线 Treeline	灌丛 Shrub			位置 Location
土壤指标 Soil index	F3	F2	F1	树线 Treeline	S1	S2	S3	位置 Location
有机碳含量 SOC content (mg·g^-1)	218.8 ± 34.0^a	185.8 ± 23.7^ab	171.1 ± 24.6^ab	173.9 ± 16.2^ab	139.9 ± 27.1^b	160.3 ± 7.0^ab	118.3 ± 12.3^b	*
全氮含量 TN content (mg·g^-1)	11.0 ± 1.9^a	8.7 ± 1.2^ab	9.1 ± 1.4^ab	8.5 ± 0.7^ab	7.4 ± 1.3^ab	7.9 ± 0.5^ab	6.0 ± 0.8^b	*
碳氮比 C:N	20.2 ± 0.6^a	21.5 ± 1.5^a	18.9 ± 0.8^a	20.5 ± 0.5^a	19.0 ± 0.7^a	20.4 ± 0.7^a	19.9 ± 0.7^a	NS
可溶性有机碳含量 DOC content (μg·g^-1)	317.7 ± 53.3^a	3 109.8 ± 84.1^a	241.3 ± 29.8^ab	265.2 ± 42.5^ab	199.9 ± 56.6^ab	227.9 ± 18.8^ab	142.3 ± 23.4^b	**
可溶性氮含量 DN content (μg·g^-1)	30.5 ± 2.3^a	34.1 ± 13.1^a	21.9 ± 3.7^ab	22.2 ± 4.1^ab	16.8 ± 3.0^ab	28.7 ± 7.7^a	11.6 ± 0.7^b	**
可溶性碳氮比 DOC:DN	10.4 ± 1.6^a	10.2 ± 0.8^a	11.3 ± 0.6^a	12.8 ± 2.0^a	11.4 ± 1.7^a	10.1 ± 2.4^a	12.2 ± 1.9^a	NS
铵态氮含量 NH₄⁺-N content (μg·g^-1)	41.2 ± 11.4^a	40.5 ± 9.2^a	36.2 ± 6.9^a	36.8 ± 3.4^a	42.3 ± 15.0^a	48.1 ± 15.0^a	26.5 ± 6.3^a	NS
硝态氮含量 NO₃^--N content (μg·g^-1)	5.8 ± 0.5^a	5.6 ± 0.5^a	5.0 ± 0.4^ab	5.0 ± 0.5^ab	4.3 ± 0.5^b	4.5 ± 0.4^ab	3.8 ± 0.4^b	***
pH	4.0 ± 0.1^b	3.9 ± 0.1^b	4.3 ± 0.1^a	4.1 ± 0.1^ab	4.2 ± 0.1^ab	4.1 ± 0.1^ab	4.1 ± 0.1^ab	*
黏粒含量 Clay content (%)	5.1 ± 0.8^a	4.9 ± 0.5^a	4.7 ± 0.9^a	3.9 ± 0.6^a	4.8 ± 0.8^a	4.3 ± 0.4^a	5.1 ± 0.6^a	NS
砂粒含量 Sand content (%)	27.6 ± 6.2^a	28.1 ± 3.5^a	33.8 ± 7.6^a	37.3 ± 5.5^a	38.9 ± 3.8^a	33.8 ± 2.2^a	29.0 ± 4.1^a	NS
微生物生物量碳含量 MBC content (μg·g^-1)	2 905 ± 611^a	2 672 ± 203^a	2 141 ± 386^a	2 696 ± 323^a	2 242 ± 605^a	2 717 ± 142^a	1 859 ± 239^a	NS

土壤指标 Soil index	森林 Forest			树线 Treeline	灌丛 Shrub			位置 Location
土壤指标 Soil index	F3	F2	F1	树线 Treeline	S1	S2	S3	位置 Location
有机碳含量 SOC content (mg·g^-1)	218.8 ± 34.0^a	185.8 ± 23.7^ab	171.1 ± 24.6^ab	173.9 ± 16.2^ab	139.9 ± 27.1^b	160.3 ± 7.0^ab	118.3 ± 12.3^b	*
全氮含量 TN content (mg·g^-1)	11.0 ± 1.9^a	8.7 ± 1.2^ab	9.1 ± 1.4^ab	8.5 ± 0.7^ab	7.4 ± 1.3^ab	7.9 ± 0.5^ab	6.0 ± 0.8^b	*
碳氮比 C:N	20.2 ± 0.6^a	21.5 ± 1.5^a	18.9 ± 0.8^a	20.5 ± 0.5^a	19.0 ± 0.7^a	20.4 ± 0.7^a	19.9 ± 0.7^a	NS
可溶性有机碳含量 DOC content (μg·g^-1)	317.7 ± 53.3^a	3 109.8 ± 84.1^a	241.3 ± 29.8^ab	265.2 ± 42.5^ab	199.9 ± 56.6^ab	227.9 ± 18.8^ab	142.3 ± 23.4^b	**
可溶性氮含量 DN content (μg·g^-1)	30.5 ± 2.3^a	34.1 ± 13.1^a	21.9 ± 3.7^ab	22.2 ± 4.1^ab	16.8 ± 3.0^ab	28.7 ± 7.7^a	11.6 ± 0.7^b	**
可溶性碳氮比 DOC:DN	10.4 ± 1.6^a	10.2 ± 0.8^a	11.3 ± 0.6^a	12.8 ± 2.0^a	11.4 ± 1.7^a	10.1 ± 2.4^a	12.2 ± 1.9^a	NS
铵态氮含量 NH₄⁺-N content (μg·g^-1)	41.2 ± 11.4^a	40.5 ± 9.2^a	36.2 ± 6.9^a	36.8 ± 3.4^a	42.3 ± 15.0^a	48.1 ± 15.0^a	26.5 ± 6.3^a	NS
硝态氮含量 NO₃^--N content (μg·g^-1)	5.8 ± 0.5^a	5.6 ± 0.5^a	5.0 ± 0.4^ab	5.0 ± 0.5^ab	4.3 ± 0.5^b	4.5 ± 0.4^ab	3.8 ± 0.4^b	***
pH	4.0 ± 0.1^b	3.9 ± 0.1^b	4.3 ± 0.1^a	4.1 ± 0.1^ab	4.2 ± 0.1^ab	4.1 ± 0.1^ab	4.1 ± 0.1^ab	*
黏粒含量 Clay content (%)	5.1 ± 0.8^a	4.9 ± 0.5^a	4.7 ± 0.9^a	3.9 ± 0.6^a	4.8 ± 0.8^a	4.3 ± 0.4^a	5.1 ± 0.6^a	NS
砂粒含量 Sand content (%)	27.6 ± 6.2^a	28.1 ± 3.5^a	33.8 ± 7.6^a	37.3 ± 5.5^a	38.9 ± 3.8^a	33.8 ± 2.2^a	29.0 ± 4.1^a	NS
微生物生物量碳含量 MBC content (μg·g^-1)	2 905 ± 611^a	2 672 ± 203^a	2 141 ± 386^a	2 696 ± 323^a	2 242 ± 605^a	2 717 ± 142^a	1 859 ± 239^a	NS

变量 Variable	BG	CBH	XYL	LAP	NAG	POX	CAT	E_cn1	E_cn2	CQI₁	CQI₂
SOC	0.62^***	0.52^**	0.55^***	0.37^*	0.51^**	0.38^*	0.49^**	-0.15	-0.15	-0.31	-0.51^**
TN	0.63^***	0.52^**	0.62^***	0.32	0.44^**	0.45^**	0.57^***	-0.05	-0.13	-0.26	-0.49^**
C:N	-0.09	-0.09	-0.21	-0.23	-0.07	-0.24	-0.25	0.11	0.31	-0.17	0.01
DOC	0.43^**	0.32	0.34	0.18	0.36^*	0.37^*	0.50^**	-0.11	-0.08	-0.07	-0.25
DN	0.16	0.04	0.25	0.14	0.12	0.02	0.18	-0.14	-0.12	-0.21	-0.08
DOC:DN	0.43^*	0.46^**	0.15	0.23	0.24	0.51^**	0.56^***	0.12	-0.08	0.07	-0.24
MBC	0.52^**	0.34^*	0.48^**	0.25	0.55^***	0.23	0.29	-0.29	-0.04	-0.30	-0.50^**
NO₃^--N	0.59^***	0.47^**	0.42^*	0.48^**	0.27	0.34	0.51^**	-0.06	-0.29	-0.21	-0.43^**
NH₄⁺-N	0.04	-0.21	-0.07	-0.02	-0.04	-0.15	-0.19	-0.01	-0.06	-0.19	-0.12
pH	0.09	0.27	0.07	0.03	0.18	0.29	0.41^*	-0.04	0.01	0.19	0.05
Clay	0.08	0.01	0.10	0.02	-0.23	-0.01	0.09	0.22	-0.11	-0.03	-0.01
Leaf C:N	-0.04	-0.05	0.23	-0.38^*	0.07	-0.25	-0.20	0.03	0.45^**	-0.13	-0.02
Leaf lignin:N	0.10	0.20	-0.32	0.48^**	-0.09	0.43^**	0.07	0.06	-0.50^**	0.35^*	-0.06
CQI₁	-0.52^**	-0.38^*	-0.53^***	-0.15	-0.36^*	0.39^*	0.00	0.04	-0.14
CQI₂	-0.90^***	-0.76^***	-0.58^***	-0.38^*	-0.63^***	-0.29	-0.22	0.00	-0.04