贡嘎山树线过渡带土壤胞外酶活性及其化学计量比特征

doi:10.17521/cjpe.2021.0215

植物生态学报 ›› 2022, Vol. 46 ›› Issue (2): 232-242.DOI: 10.17521/cjpe.2021.0215

所属专题：生态化学计量；青藏高原植物生态学：植物-土壤-微生物；生物地球化学

贡嘎山树线过渡带土壤胞外酶活性及其化学计量比特征

李东¹^,², 田秋香², 赵小祥²^,³, 林巧玲²^,³, 岳朋芸²^,³, 姜庆虎², 刘峰²^,^*()

¹西藏大学青藏高原生态与环境研究中心, 西藏大学理学院, 拉萨 850000
²中国科学院武汉植物园水生植物与流域生态重点实验室, 武汉 430074
³中国科学院大学, 北京 100049

收稿日期:2021-06-07 接受日期:2021-09-15 出版日期:2022-02-20 发布日期:2021-10-15
通讯作者: 刘峰
作者简介:*(liufeng@wbgcas.cn)
ORCID:刘峰: 0000-0003-3383-7598
基金资助:
国家自然科学基金(31870465);国家自然科学基金(31700462)

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

LI Dong¹^,², TIAN Qiu-Xiang², ZHAO Xiao-Xiang²^,³, LIN Qiao-Ling²^,³, YUE Peng-Yun²^,³, JIANG Qing-Hu², LIU Feng²^,^*()

¹Research Center for Ecology and Environment of Qinghai-Tibetan Plateau, College of Science, Tibet University, Lhasa 850000, China
²Key Laboratory of Aquatic Botany and Watershed Ecology, Wuhan Botanical Garden, Chinese Academic of Sciences, Wuhan 430074, China
³University of Chinese Academic of Sciences, Beijing 100049, China

Received:2021-06-07 Accepted:2021-09-15 Online:2022-02-20 Published:2021-10-15
Contact: LIU Feng
Supported by:
National Natural Science Foundation of China(31870465);National Natural Science Foundation of China(31700462)

摘要/Abstract

摘要：

土壤胞外酶及其化学计量比是反映土壤养分可用性和微生物底物限制的敏感指标。然而, 对全球变化敏感的高山树线过渡带土壤酶活性和化学计量比的变化特征及其关键驱动因素仍不清楚。该研究在青藏高原东南部的川西贡嘎山高山树线过渡带(森林、树线、灌丛)进行土壤采样, 测定了树线过渡带土壤中5种水解酶(β-葡萄糖苷酶(BG)、纤维素二糖水解酶(CBH)、木聚糖水解酶(XYL)、N-乙酰氨基葡萄糖苷酶(NAG)、亮氨酸氨基肽酶(LAP))和2种氧化酶(多酚氧化酶(POX)、过氧化氢酶(CAT))的活性, 并计算土壤胞外酶活性化学计量比(碳、氮(N)酶活性比和碳质量指数)。结果表明: 灌丛土壤LAP、POX、CAT活性显著低于树线和森林土壤, XYL活性在树线最低, 其他胞外酶活性在树线过渡带不同位置差异不显著。灌丛土壤lnBG/lnLAP显著高于森林和树线处土壤, lnBG/ln(NAG + LAP)在树线过渡带没有显著变化, 碳质量指数在树线处最高。非度量多维尺度分析表明, 土壤有机碳、全氮、硝态氮含量和植物叶片木质素:N是影响树线过渡带土壤酶活性差异的主要因素, 植物叶片碳氮比、木质素:N和土壤可溶性氮含量是影响树线过渡带土壤胞外酶活性化学计量比差异的主要因素。综上所述, 贡嘎山地区的部分土壤酶活性及其化学计量比沿树线过渡带会发生明显的变化, 这种变化可能是由不同植物类型下微生物群落差异导致。这表明, 未来气候变化引起的树线迁移可能会改变胞外酶活性进而影响土壤养分循环。

关键词: 胞外酶活性, 树线过渡带, 酶化学计量比, 植被类型

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

李东, 田秋香, 赵小祥, 林巧玲, 岳朋芸, 姜庆虎, 刘峰. 贡嘎山树线过渡带土壤胞外酶活性及其化学计量比特征. 植物生态学报, 2022, 46(2): 232-242. DOI: 10.17521/cjpe.2021.0215

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. Chinese Journal of Plant Ecology, 2022, 46(2): 232-242. DOI: 10.17521/cjpe.2021.0215

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链接本文: https://www.plant-ecology.com/CN/10.17521/cjpe.2021.0215

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

图/表 8

图1 贡嘎山树线过渡带样地示意图。F1、F2、F3为树线下方的森林样方; S1、S2、S3为灌丛样方; Treeline为树线处样方。从F3到S3海拔依次升高。

Fig. 1 Schematic diagram of the sample sites in the alpine treeline ecotones in Gongga Mountain. F1, F2, F3 are the forest samples; S1, S2, S3 are the shrub samples; Treeline is the sample at the treeline. Altitude rises from F3 to S3 in ascending order.

表1 贡嘎山树线过渡带不同位置优势树种植被属性及叶片养分特征(平均值±标准误)

Table 1 Vegetation properties and leaf nutrient characteristics of dominant tree species at different locations in the treeline ecotone in Gongga Mountain (mean ± SE)

	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	***

表2 贡嘎山树线过渡带不同位置土壤基本理化性质(平均值±标准误)

Table 2 Soil physic-chemical properties at different locations in the treeline ecotone in Gongga Mountain (mean ± SE)

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

表2 贡嘎山树线过渡带不同位置土壤基本理化性质(平均值±标准误)

Table 2 Soil physic-chemical properties at different locations in the treeline ecotone in Gongga Mountain (mean ± SE)

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

图2 贡嘎山树线过渡带不同位置土壤水解酶活性的变化(平均值±标准误)。BG, β-葡萄糖苷酶; CBH, 纤维素二糖水解酶; LAP, 亮氨酸氨基肽酶; NAG, N-乙酰氨基葡萄糖苷酶; XYL, 木聚糖水解酶。F1、F2、F3为树线下方的森林样方; S1、S2、S3为灌丛样方; Treeline为树线处样方。不同小写字母表示过渡带不同位置(植被类型)差异显著(p < 0.05)。

Fig. 2 Soil hydrolytic enzyme activities at different locations in the treeline ecotone in Gongga Mountain (mean ± SE). BG, β-1,4-glucosidase; CBH, cellobiohydrolase; LAP, leucine aminopeptidase; NAG, β-N-acetyl glucosaminidase; XYL, xylosidase. F1, F2, F3 are forest samples; S1, S2, S3 are shrub samples; Treeline is the sample at the tree line. Different lowercase letters indicate significant differences (p < 0.05) among different locations or vegetation types in the treeline ecotone.

图3 贡嘎山树线过渡带不同位置土壤氧化酶活性的变化(平均值±标准误)。CAT, 过氧化氢酶; POX, 多酚氧化酶。F1、F2、F3为树线下方的森林样方; S1、S2、S3为灌丛样方; Treeline为树线处样方。不同小写字母表示过渡带不同位置(植被类型)差异显著(p < 0.05)。

Fig. 3 Soil oxidative enzyme activities at different locations in the treeline ecotone in Gongga Mountain (mean ± SE). CAT, Catalase; POX, phenol oxidase. F1, F2, F3 are forest samples; S1, S2, S3 are shrub samples; Treeline is the sample at the tree line. Different lowercase letters indicate significant differences (p < 0.05) among different locations or vegetation types in the treeline ecotone.

图4 贡嘎山树线过渡带土壤胞外酶化学计量比的变化(平均值±标准误)。CQI1、CQI2表示碳质量指数; Ecn1、Ecn2表示微生物碳、氮酶活性计量比。F1、F2、F3为树线下方的森林样方; S1、S2、S3为灌丛样方; Treeline为树线处样方。不同小写字母表示过渡带不同位置(植被类型)差异显著(p < 0.05)。

Fig. 4 Soil extracellular enzyme stoichiometry at different locations in the treeline ecotone in Gongga Mountain (mean ± SE). CQI1, CQI2 indicate carbon quality index; Ecn1, Ecn2 indicate microbial carbon and nitrogen enzyme activity stoichiometry ratios. F1, F2, F3 are the forest samples; S1, S2, S3 are the shrub samples; Treeline is the sample at the tree line. Different lowercase letters indicate significant differences (p < 0.05) between different locations or vegetation types in the treeline ecotone.

表3 贡嘎山树线过渡带土壤酶活性及其化学计量比与环境变量之间的相关关系

Table 3 Spearman’s correlation coefficients between environmental variables and enzyme activities and enzyme stoichiometry in the treeline ecotone in Gongga Mountain

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

图5 贡嘎山树线过渡带土壤胞外酶活性(A)及其化学计量比(B)的非度量多维尺度(NMDS)分析。应力函数可以检验NMDS分析结果的优劣, 通常认为stress < 0.2时可用NMDS的二维点图表示, 其图形有一定的解释意义; 当stress < 0.1时, 可认为是一个好的排序。图中仅显示有显著影响的因素。BG, β-葡萄糖苷酶; CAT, 过氧化氢酶; CBH, 纤维素二糖水解酶; DN, 土壤可溶性氮含量; DOC, 土壤可溶性有机碳含量; LAP, 亮氨酸氨基肽酶; Leaf C:N, 优势树种叶片碳氮比; Lignin:N, 叶片木质素比氮; MBC, 微生物生物量碳含量; NAG, N-乙酰氨基葡萄糖苷酶; NO3--N, 硝态氮含量; POX, 多酚氧化酶; SOC, 土壤有机碳含量; TN, 全氮含量; XYL, 木聚糖水解酶。Ecn1、Ecn2表示微生物碳、氮酶活性计量比; CQI1、CQI2表示碳质量指数。

Fig. 5 Bray-Curtis-based non-metric multidimensional scaling (NMDS) of the soil enzyme activities (A) and enzyme stoichiometry (B) in the treeline ecotone in Gongga Mountain. The stress function can test the merit of NMDS analysis results. It is generally considered that stress < 0.2 can be represented by a two-dimensional point diagram of NMDS, and its graph has some interpretative significance; when stress < 0.1, it can be considered a good ranking. Only significant factors (p < 0.05) were showed in the figure. BG, β-1,4-glucosidase; CAT, catalase; CBH, cellobiohydrolase; DN, soil dissolved nitrogen content; DOC, soil dissolved organic carbon content; LAP, leucine aminopeptidase; Leaf C:N, carbon to nitrogen ratio of leaves of dominant species; Lignin:N, leaf lignin to nitrogen ratio; MBC, microbial biomass carbon content; NAG, β-N-acetyl glucosaminidase; NO3--N, nitrate nitrogen content; POX, phenol oxidase; SOC, soil organic carbon content; TN, total nitrogen content; XYL, xylosidase. Ecn1, Ecn2 indicate microbial carbon and nitrogen enzyme activity stoichiometry ratios; CQI1, CQI2 indicate carbon quality index.

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贡嘎山树线过渡带土壤胞外酶活性及其化学计量比特征

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

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