亚热带人工林下植被根际土壤酶化学计量特征

doi:10.17521/cjpe.2018.0299

植物生态学报 ›› 2019, Vol. 43 ›› Issue (3): 258-272.DOI: 10.17521/cjpe.2018.0299

所属专题：生态化学计量；微生物生态学

• 研究论文 • 上一篇

亚热带人工林下植被根际土壤酶化学计量特征

高雨秋^1,²,戴晓琴^1,^2,^3,^*(),王建雷¹,付晓莉^1,^2,³,寇亮^1,^2,³,王辉民^1,^2,^3,⁴

¹ 中国科学院地理科学与资源研究所生态系统网络观测与模拟重点实验室千烟洲试验站, 北京 100101
² 中国科学院大学资源与环境学院, 北京 100190
³ 中科吉安生态环境研究院, 江西吉安 343000
⁴ 江西省区域生态过程与信息重点实验室, 江西泰和 343725

收稿日期:2018-11-30 修回日期:2019-03-07 出版日期:2019-03-20 发布日期:2019-04-23
通讯作者: 戴晓琴
基金资助:
国家自然科学基金(31730014);国家重点研发计划(2016YFD0600202)

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

GAO Yu-Qiu^1,²,DAI Xiao-Qin^1,^2,^3,^*(),WANG Jian-Lei¹,FU Xiao-Li^1,^2,³,KOU Liang^1,^2,³,WANG Hui-Min^1,^2,^3,⁴

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:2019-03-20 Published:2019-04-23
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)

摘要/Abstract

摘要：

为探讨林下植被根际土壤酶化学计量特征及其对林分类型和季节的响应, 该研究以江西省泰和县千烟洲试验站典型人工杉木(Cunninghamia lanceolata)、马尾松(Pinus massoniana)和湿地松(Pinus elliottii)林林下优势灌草檵木(Loropetalum chinense)、杨桐(Adinandra millettii)、格药柃(Eurya muricata)、狗脊蕨(Woodwardia japonica)和暗鳞鳞毛蕨(Dryopteris atrata)为对象, 在植被生长初期(4月)和旺盛期(7月)测定优势灌草根际土壤与碳(C)循环相关的β-1,4-葡萄糖苷酶(BG)、与氮(N)循环相关的β-1,4-N-乙酰葡糖氨糖苷酶(NAG)和亮氨酸氨基肽酶(LAP)、与磷(P)循环相关的酸性磷酸酶(AP)活性、酶化学计量比及土壤理化性质。结果发现: (1)根际土壤与C和N循环相关的酶活性以及BG:AP (酶C:P)在不同林下植被之间存在显著差异, 而与P循环相关的酶活性差异不显著。林分类型和取样季节显著影响BG:(NAG+LAP)(酶C:N), 且林下植被类型、林分类型和取样季节交互影响酶C:P。主成分分析表明, 根际土壤酶的活性及计量比在不同林下植被(檵木不同于格药柃, 且二者显著区别于其他物种)、林分类型(杉木林区别于马尾松、湿地松林)和取样季节之间均存在显著差异。土壤硝态氮(NO₃ ^--N)、铵态氮(NH₄ ⁺-N)、可溶性有机碳(DOC)含量和碳氮比(C:N)是影响林下植被根际土壤酶的活性及化学计量比的主要因素。(2)标准主轴回归分析表明, 林下植被根际土壤lg(BG)、lg(NAG+LAP)和lg(AP)之间存在显著线性关系, lgBG:lg(NAG+LAP):lgAP (酶C:N:P)约为1:1:1.3, 酶C:P及(NAG+LAP):AP (酶N:P)分别为0.14和0.15。AP远大于BG和NAG+LAP的活性, 导致lg(BG)和lg(NAG+LAP)与lg(AP)的回归斜率极显著偏离1。说明林下植被根际土壤酶的活性及计量比受植被种类、林分类型及取样季节影响, 且基质有效性在其中发挥重要作用。相较于C循环和N循环, 微生物会分配更多资源用于P循环相关酶的生产, 暗示亚热带人工林林下植被根际土壤微生物生长和活性更易受P限制。

关键词: 人工林, 胞外酶, 生态化学计量比, 红壤丘陵区

Abstract:

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

高雨秋, 戴晓琴, 王建雷, 付晓莉, 寇亮, 王辉民. 亚热带人工林下植被根际土壤酶化学计量特征. 植物生态学报, 2019, 43(3): 258-272. DOI: 10.17521/cjpe.2018.0299

GAO Yu-Qiu, DAI Xiao-Qin, WANG Jian-Lei, FU Xiao-Li, KOU Liang, WANG Hui-Min. Characteristics of soil enzymes stoichiometry in rhizosphere of understory vegetation in subtropical forest plantations. Chinese Journal of Plant Ecology, 2019, 43(3): 258-272. DOI: 10.17521/cjpe.2018.0299

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链接本文: https://www.plant-ecology.com/CN/10.17521/cjpe.2018.0299

https://www.plant-ecology.com/CN/Y2019/V43/I3/258

图/表 8

表1 亚热带人工林生态系统林下植被基本信息

Table 1 Characteristics of understory shrub and herb species in three subtropical plantations

林分类型 Forest stand type	林下植被类型 Understory species	基径 Basal diameter (mm)	高度 Height (cm)	冠幅 Crown width (cm)	盖度 Coverage (%)	重要值 Importance value (%)
杉木林 Cunninghamia lanceolata forest	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
马尾松林 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
湿地松林 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

Table 2 Results (p-value) of multi-way repeated measures ANOVAs on the effects of forest stand types, understory species, sampling seasons and their interactions on soil enzyme activities and ecoenzymatic stoichiometry in rhizosphere of subtropical forest plantations

变异来源 Source of variation	酶相关参数 Parameter of soil enzyme
	BG	NAG+LAP	AP	BG:(NAG+LAP)	BG:AP	(NAG+LAP):AP
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

图1 不同林分类型亚热带人工林林下植被根际土壤酶活性(平均值+标准误差, n = 5)。CL, 杉木林; PM, 马尾松林; PE, 湿地松林。LC, 檵木; AM, 杨桐; EM, 格药柃; WJ, 狗脊蕨; DA, 暗鳞鳞毛蕨。不同小写字母代表根际土壤C、N或P循环相关的酶活性在同一取样季节相同林分类型下不同林下植被之间差异显著(p ＜ 0.05), 不同大写字母代表根际土壤C、N或P循环相关的酶活性在同一取样季节不同林分类型下差异显著(p ＜ 0.05)。BG, β-1,4-葡萄糖苷酶; NAG+LAP, β-1,4-N-乙酰葡糖氨糖苷酶和亮氨酸氨基肽酶之和; AP, 酸性磷酸酶。

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.

图2 不同林分类型亚热带人工林林下植被根际土壤酶的生态化学计量比(平均值+标准误差, n = 5)。CL, 杉木林; PM, 马尾松林; PE, 湿地松林。 LC, 檵木; AM, 杨桐; EM, 格药柃; WJ, 狗脊蕨; DA, 暗鳞鳞毛蕨。不同小写字母代表根际土壤C、N或P循环相关的酶活性在同一取样季节相同林分类型下不同林下植被之间差异显著(p ＜ 0.05), 不同大写字母代表根际土壤C、N或P循环相关的酶活性计量比在同一取样季节不同林分类型下差异显著(p ＜ 0.05)。BG, β-1,4-葡萄糖苷酶; NAG+LAP, β-1,4-N-乙酰葡糖氨糖苷酶和亮氨酸氨基肽酶之和; AP, 酸性磷酸酶。

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.

图3 亚热带人工林土壤C、N、P获得酶活性关系的标准主轴回归分析(n = 150)。颜色代表林分: 红色, 杉木林; 绿色, 马尾松林; 蓝色, 湿地松林。空心和实心符号分别表示取样时间为4月或7月。CL, 杉木林; PM, 马尾松林; PE, 湿地松林。 LC, 檵木; AM, 杨桐; EM, 格药柃; WJ, 狗脊蕨; DA, 暗鳞鳞毛蕨。BG, β-1,4-葡萄糖苷酶; NAG+LAP, β-1,4-N-乙酰葡糖氨糖苷酶和亮氨酸氨基肽酶之和; AP, 酸性磷酸酶。

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.

图4 亚热带人工林土壤酶活性及计量比的主成分分析(PCA)。相同取样季节, 林下植被土壤的酶活性及计量比PCA坐标平均值表征取样季节效应。同一林分类型下, 林下植被土壤酶的活性及计量比PCA坐标平均值表征林分类型的效应。同一林下植被类型土壤酶活性及计量比PCA坐标平均值为林下植被类型的效应。颜色代表林分: 红色, 杉木林; 绿色, 马尾松林; 蓝色, 湿地松林。CL, 杉木林; PM, 马尾松林; PE, 湿地松林; LC, 檵木; AM, 杨桐; EM, 格药柃; WJ, 狗脊蕨; DA, 暗鳞鳞毛蕨。

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.

图5 亚热带人工林土壤酶活性及计量比与土壤理化性质关系的冗余分析(RDA)。NO3--N, 硝态氮; NH4+-N, 铵态氮; DOC, 可溶性有机碳; C:N, 全碳和全氮的比值。BG, β-1,4-葡萄糖苷酶; NAG+LAP, β-1,4-N-乙酰葡糖氨糖苷酶和亮氨酸氨基肽酶之和; AP, 酸性磷酸酶。

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.

表3 林分类型、林下植被类型和取样季节对亚热带人工林4种主要土壤养分影响的重复测量多因素方差分析结果(p值)

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

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亚热带人工林下植被根际土壤酶化学计量特征

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

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