土壤磷有效性调控亚热带森林土壤酶活性和酶化学计量对凋落叶输入的响应

doi:10.17521/cjpe.2022.0430

植物生态学报 ›› 2024, Vol. 48 ›› Issue (2): 242-253.DOI: 10.17521/cjpe.2022.0430

土壤磷有效性调控亚热带森林土壤酶活性和酶化学计量对凋落叶输入的响应

吴君梅¹, 曾泉鑫¹, 梅孔灿¹, 林惠瑛¹, 谢欢¹, 刘苑苑¹, 徐建国², 陈岳民¹^,^*()

¹福建师范大学地理科学学院, 湿润亚热带山地生态国家重点实验室培育基地, 福州 350007
²福建戴云山国家级自然保护区管理局, 福建泉州 362500

收稿日期:2022-10-31 接受日期:2023-04-06 出版日期:2024-02-28 发布日期:2023-04-20
通讯作者: 陈岳民
基金资助:
福建省自然科学基金(2020J01142);福建省自然科学基金(2020J01397)

Soil phosphorus availability regulates the response of soil enzyme activity and enzymatic stoichiometry to litter addition in a subtropical forest

WU Jun-Mei¹, ZENG Quan-Xin¹, MEI Kong-Can¹, LIN Hui-Ying¹, XIE Huan¹, LIU Yuan-Yuan¹, XU Jian-Guo², CHEN Yue-Min¹^,^*()

¹School of Geographical Science, Fujian Normal University, Cultivation Base of State Key Laboratory of Humid Subtropical Mountain Ecology, Fuzhou 350007, China
²Daiyun Mountain National Nature Reserve Administration Bureau, Quanzhou, Fujian 362500, China

Received:2022-10-31 Accepted:2023-04-06 Online:2024-02-28 Published:2023-04-20
Contact: CHEN Yue-Min
Supported by:
Natural Science Foundation of Fujian Province(2020J01142);Natural Science Foundation of Fujian Province(2020J01397)

摘要/Abstract

摘要：

探究土壤胞外酶活性及其化学计量对了解土壤微生物的养分限制情况和土壤养分的循环过程具有重要意义。尽管亚热带森林土壤风化严重, 土壤磷有效性低, 但是亚热带森林生态系统具有较高水平的植被生产力。在气候变化(如变暖和CO₂浓度增加)背景下, 预测植被生产力将会提高, 这将增加凋落叶的输入。然而, 未来不同质量凋落叶输入增加对土壤酶活性及其化学计量的影响是否受土壤磷有效性的调控仍不清楚。该研究以马尾松(Pinus massoniana)林土壤为研究对象, 探究了3种不同质量(如叶碳氮比或碳磷比存在差异)的凋落叶(马尾松、醉香含笑(俗名: 火力楠, Michelia macclurei)和枫香树(Liquidambar formosana))和磷添加对土壤理化性质、胞外酶活性的影响。同时, 结合土壤酶化学计量、矢量长度(VL)和矢量角度(VA)分析, 解析了土壤微生物的养分限制状况及其关键调控因素。结果表明: 与对照相比, 凋落叶添加增加了土壤β-N-乙酰氨基葡糖苷酶和酸性磷酸酶(ACP)活性。通过酶化学计量分析发现, 凋落叶添加显著提高VL和VA, 且影响强度表现为醉香含笑>枫香>马尾松, 表明凋落叶添加会改变土壤微生物的养分限制状况, 且影响程度与凋落叶的质量有关。与凋落叶单独添加相比, 凋落叶与磷共同添加显著增加土壤有效磷含量, 降低ACP活性和VA, 表明磷添加有助于缓解凋落叶输入下土壤微生物的磷限制。冗余分析表明, 土壤碳氮比、可溶性有机碳和有效磷含量是影响土壤酶活性和酶化学计量的主要因素。综上所述, 该研究发现亚热带森林土壤微生物养分限制对凋落叶输入的响应不仅受凋落叶质量的影响, 同时还受土壤磷有效性的调控。这一结果可以为未来气候变化下亚热带森林土壤微生物养分获取策略对不同凋落叶输入和磷添加的响应提供理论参考, 同时也将有助于提高对亚热带低磷森林生态系统土壤生物地球化学循环过程的理解。

关键词: 凋落叶, 磷添加, 土壤酶活性, 酶化学计量, 磷限制

Abstract:

Aims It is of great significance to explore soil extracellular enzyme activity and its stoichiometry to understand soil nutrient availability and changes in the nutrient requirements of microorganisms. Subtropical forest ecosystems have high net primary productivity, but the availability of phosphorus (P) in soil is low due to severe soil weathering. Under climate change (i.e., warming, elevated CO₂ concentration), plant productivity is predicted to increase, which would increase the input of leaf litter. However, it is still unclear whether the effect of increasing litter input on soil enzyme activity and its stoichiometry is affected by soil P availability in the future.

Methods This study investigated the effects of the addition of three kinds of litters (Pinus massoniana, Michelia macclurei and Liquidambar formosa) with different quality (characterized by different leaf C:N or C:P) and P on soil properties and enzyme activities in subtropical low-P soils. By analyzing the stoichiometric ratio of soil enzymes, vector length (VL), and vector angle (VA), the relative nutrient limitation to soil microorganisms and the key regulatory factors were explored.

Important findings The results showed that litter addition increased β-N-acetyl-glucosaminidase and acid phosphatase (ACP) activities. The addition of litter significantly increased VL and VA in the order of M. macclurei > L. formosana > P. massoniana. Litter addition could change the status of nutrient limitation to soil microorganisms, with the degree of changes being related to the quality of litter. Compared with the addition of litter alone, the addition of both litter and P significantly increased the content of available P, and reduced ACP activity and VA, suggesting that P addition could help alleviate P limitation to soil microorganisms under the input of litter. Redundancy analysis results showed that the soil carbon/nitrogen ratio, dissolved organic carbon content, and available P content were the main factors affecting enzyme activities and their stoichiometry. In conclusion, our study found that the response of soil microbial nutrient limitation to litter input in subtropical forest was not only affected by litter quality, but also regulated by soil P availability. This study provides a theoretical reference for the response of microbial nutrient acquisition strategies to different litter inputs and P additions in subtropical forests under future climate change, and is conducive to improving our understanding of the soil biogeochemical cycling in subtropical low P forest ecosystems.

Key words: litter, phosphorus addition, soil enzyme activity, enzymatic stoichiometry, phosphorus limitation

吴君梅, 曾泉鑫, 梅孔灿, 林惠瑛, 谢欢, 刘苑苑, 徐建国, 陈岳民. 土壤磷有效性调控亚热带森林土壤酶活性和酶化学计量对凋落叶输入的响应. 植物生态学报, 2024, 48(2): 242-253. DOI: 10.17521/cjpe.2022.0430

WU Jun-Mei, ZENG Quan-Xin, MEI Kong-Can, LIN Hui-Ying, XIE Huan, LIU Yuan-Yuan, XU Jian-Guo, CHEN Yue-Min. Soil phosphorus availability regulates the response of soil enzyme activity and enzymatic stoichiometry to litter addition in a subtropical forest. Chinese Journal of Plant Ecology, 2024, 48(2): 242-253. DOI: 10.17521/cjpe.2022.0430

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链接本文: https://www.plant-ecology.com/CN/10.17521/cjpe.2022.0430

https://www.plant-ecology.com/CN/Y2024/V48/I2/242

图/表 8

表1 供试凋落叶的基本性质(平均值±标准差, n = 3)

Table 1 Basic properties of three kinds of litters (mean ± SD, n = 3)

	全碳(C)含量 Total carbon (C) content (g·kg^-1)	全氮(N)含量 Total nitrogen (N) content (g·kg^-1)	C:N	全磷(P)含量 Total phosphorus (P) content (g·kg^-1)	C:P
马尾松 Pinus massoniana	458.37 ± 9.84^ab	12.07 ± 0.41^a	37.98 ± 0.53^c	2.03 ± 0.01^a	225.58 ± 5.24^c
醉香含笑 Michelia macclurei	475.18 ± 1.89^a	10.38 ± 0.25^b	45.81 ± 1.23^b	0.96 ± 0.02^c	496.57 ± 13.45^a
枫香树 Liquidambar formosana	454.87 ± 1.01^b	9.44 ± 0.14^c	48.17 ± 0.78^a	1.41 ± 0.01^b	323.38 ± 2.36^b
p	0.011	<0.001	<0.001	<0.001	<0.001

图1 亚热带森林凋落叶和磷添加对土壤理化性质的影响(平均值±标准差, n = 3)。CK, 对照; LF, 枫香凋落叶添加; LF+PA, 枫香凋落叶和磷共同添加; MM, 醉香含笑凋落叶添加; MM+PA, 醉香含笑凋落叶和磷共同添加; PA, 磷添加; PM, 马尾松凋落叶添加; PM+PA, 马尾松凋落叶和磷共同添加。L、PA和L×PA分别表示在双因素方差分析下凋落叶添加和磷添加的主效应以及两者的交互作用。不同小写字母表示处理间差异显著(p < 0.05)。

Fig. 1 Effects of litter and phosphorus (P) addition on soil physical and chemical properties in a subtropical forest (mean ± SD, n = 3). CK, control; LF, Liquidambar formosana litter addition; LF+PA, L. formosana litter and P addition; MM, Michelia macclurei litter addition; MM+PA, M. macclurei litter and P addition; PA, P addition; PM, Pinus massoniana litter addition; PM+PA, P. massoniana litter and P addition. L, PA and L×PA respectively represent the main effects of litter addition and P addition and their interactions respectively following a two-way ANOVA. AP, available P; DOC, dissolved organic carbon; DON, dissolved organic nitrogen; TC, total carbon; TN, total nitrogen; TP, total P. Different lowercase letters meant significant difference at 0.05 level among treatments.

图2 亚热带森林凋落叶和磷添加对土壤微生物生物量养分含量的影响(平均值±标准差, n = 3)。CK, 对照; LF, 枫香凋落叶添加; LF+PA, 枫香凋落叶和磷共同添加; MM, 醉香含笑凋落叶添加; MM+PA, 醉香含笑凋落叶和磷共同添加; PA, 磷添加; PM, 马尾松凋落叶添加; PM+PA, 马尾松凋落叶和磷共同添加。L、PA和L×PA分别表示在双因素方差分析下凋落叶添加和磷添加的主效应以及两者的交互作用。不同小写字母表示处理间差异显著(p < 0.05)。

Fig. 2 Effects of litter and phosphorus (P) addition on soil microbial biomass nutrient content in a subtropical forest (mean ± SD, n = 3). CK, control; LF, Liquidambar formosana litter addition; LF+PA, L. formosana litter and P addition; MM, Michelia macclurei litter addition; MM+PA, M. macclurei litter and P addition; PA, P addition; PM, Pinus massoniana litter addition; PM+PA, P. massoniana litter and P addition. L, PA and L×PA represent the main effects of litter addition and P addition, and their interactions, respectively following a two-way ANOVA. MBC, microbial biomass carbon; MBN, microbial biomass nitrogen; MBP, microbial biomass P. Different lowercase letters meant significant difference at 0.05 level among treatments.

图3 亚热带森林凋落叶和磷添加对土壤酶活性的影响(平均值±标准差, n = 3)。CK, 对照; LF, 枫香凋落叶添加; LF+PA, 枫香凋落叶和磷共同添加; MM, 醉香含笑凋落叶添加; MM+PA, 醉香含笑凋落叶和磷共同添加; PA, 磷添加; PM, 马尾松凋落叶添加; PM+PA, 马尾松凋落叶和磷共同添加。L、PA和L×PA分别表示在双因素方差分析下凋落叶添加和磷添加的主效应以及两者的交互作用。不同小写字母表示处理间差异显著(p < 0.05)。

Fig. 3 Effects of litter and phosphorus (P) addition on soil enzymes activities in a subtropical forest (mean ± SD, n = 3). CK, control; LF, Liquidambar formosana litter addition; LF+PA, L. formosana litter and P addition; MM, Michelia macclurei litter addition; MM+PA, M. macclurei litter and P addition; PA, P addition; PM, Pinus massoniana litter addition; PM+PA, P. massoniana litter and P addition. L, PA and L×PA represent the main effects of litters addition and P addition, and their interactions, respectively following a two-way ANOVA. ACP, acid phosphatase; βG, β-glucosidase; NAG, β-N-acetyl-glucosaminidase. Different lowercase letters meant significant difference at 0.05 level among treatments.

表2 亚热带森林凋落叶和磷添加对土壤酶化学计量的影响(平均值±标准差, n = 3)

Table 2 Effects of litter and phosphorus (P) addition on soil enzymatic stoichiometry in a subtropical forest (mean ± SD, n = 3)

处理 Treatment	E_C:N	E_C:P	E_N:P	VL	VA (°)
CT	0.98 ± 0.03^bcd	0.49 ± 0.01^ab	0.507 ± 0.02^ab	1.09 ± 0.03^bcd	63.11 ± 0.73^bc
PA	0.90 ± 0.04^d	0.48 ± 0.01^b	0.533 ± 0.02^a	1.02 ± 0.04^d	61.81 ± 0.99^c
PM	0.95 ± 0.05^cd	0.50 ± 0.02^ab	0.527 ± 0.02^ab	1.07 ± 0.05^cd	62.22 ± 0.73^bc
MM	1.15 ± 0.11^a	0.52 ± 0.02^ab	0.457 ± 0.03^c	1.26 ± 0.10^a	65.49 ± 1.50^a
LF	1.03 ± 0.08^bc	0.51 ± 0.04^ab	0.500 ± 0.01^ab	1.15 ± 0.09^abcd	63.46 ± 0.45^b
PM+PA	0.97 ± 0.05^bcd	0.52 ± 0.04^ab	0.533 ± 0.01^a	1.10 ± 0.06^bcd	61.99 ± 0.65^bc
MM+PA	1.07 ± 0.04^ab	0.54 ± 0.03^a	0.503 ± 0.01^ab	1.20 ± 0.05^ab	63.20 ± 0.43^bc
LF+PA	1.05 ± 0.07^abc	0.52 ± 0.03^ab	0.497 ± 0.01^b	1.17 ± 0.08^abc	63.46 ± 0.58^b
Two-way ANOVA
L	<0.001	0.063	<0.001	<0.001	<0.001
PA	0.323	0.421	0.310	0.422	0.446
L×PA	0.350	0.689	0.104	0.101	0.468

图4 亚热带森林土壤酶矢量长度(A)和矢量角度(B)对凋落叶和磷添加的响应比(平均值±标准差, n = 3)。LF, 枫香凋落叶添加; LF+PA, 枫香凋落叶和磷共同添加; MM, 醉香含笑凋落叶添加; MM+PA, 醉香含笑凋落叶和磷共同添加; PA, 磷添加; PM, 马尾松凋落叶添加; PM+PA, 马尾松凋落叶和磷共同添加。L、PA和L×PA分别表示在双因素方差分析下凋落叶添加和磷添加的主效应以及两者的交互作用。不同小写字母表示处理间差异显著(p < 0.05)。

Fig. 4 Response ratio of soil enzyme vector length (A) and vector angle (B) to litter and phosphorus (P) addition in a subtropical forest (mean ± SD, n = 3). LF, Liquidambar formosana litter addition; LF+PA, L. formosana litter and P addition; MM, Michelia macclurei litter addition; MM+PA, M. macclurei litter and P addition; PA, P addition; PM, Pinus massoniana litter addition; PM+PA, P. massoniana litter and P addition. L, PA and L×PA represent the main effects of litter addition and P addition, and their interactions, respectively following a two-way ANOVA. VA, vector angle; VL, vector length. Different lowercase letters mean significant difference at 0.05 level among treatments.

图5 凋落叶单独添加(A)和凋落叶与磷共同添加(B)下土壤酶活性和酶化学计量的冗余分析。ACP, 酸性磷酸酶活性; AP, 有效磷含量; βG, β-葡糖苷酶活性; CK, 对照; DOC, 可溶性有机碳含量; EC:N, 碳获取酶活性:氮获取酶活性; EC:P, 碳获取酶活性:磷获取酶活性; EN:P, 氮获取酶活性:磷获取酶活性; LF, 枫香凋落叶添加; LF+PA, 枫香凋落叶和磷共同添加; MM, 醉香含笑凋落叶添加; MM+PA, 醉香含笑凋落叶和磷共同添加; NAG, β-N-乙酰氨基葡糖苷酶活性; PM, 马尾松凋落叶添加; PM+PA, 马尾松凋落叶和磷共同添加; TC:TN, 总碳与总氮含量比值; TN, 总氮含量; TP, 总磷含量; VA, 矢量角度; VL, 矢量长度。

Fig. 5 Redundancy analysis of soil enzyme activity and enzymatic stoichiometry under litter (A) and phosphorus (P) addition (B). ACP, acid phosphatase activity; AP, available P content; βG, β-glucosaminidase activity; CK, control; DOC, dissolved organic carton content; EC:N, the ratio of carbon-acquiring enzyme activity to nitrogen-acquiring enzyme activity; EC:P, the ratio of carbon-acquiring enzyme activity to phosphorus-acquiring enzyme activity; EN:P, the ratio of nitrogen-acquiring enzyme activity to phosphorus-acquiring enzyme activity; LF, Liquidambar formosana litter addition; LF+PA, L. formosana litter and P addition; MM, Michelia macclurei litter addition; MM+PA, M. macclurei litter and P addition; NAG, β-N-acetyl-glucosaminidase activity; PM, Pinus massoniana litter addition; PM+PA, P. massoniana litter and P addition. TC:TN, the ratio of total carbon content to total nitrogen content; TN, total nitrogen content; TP, total P content; VA, vector angle; VL, vector length.

图6 亚热带森林土壤酶活性及其化学计量对凋落叶和磷(P)添加响应的概念图。CK, 对照; LF, 枫香; MM, 火力楠; PM, 马尾松。ACP, 酸性磷酸酶活性; AP, 有效磷含量; βG, β-葡糖苷酶活性; DOC, 可溶性有机碳含量; EC:N, 碳获取酶活性:氮获取酶活性; EC:P, 碳获取酶活性:磷获取酶活性; EN:P, 氮获取酶活性:磷获取酶活性; NAG, β-N-乙酰氨基葡糖苷酶活性; TC:TN, 总碳与总氮含量比值; VA, 矢量角度; VL, 矢量长度。梯形和CK的宽度表示相应指标数值的大小。

Fig. 6 A conceptual framework of soil enzyme activity and its stoichiometry in response to litter and phosphorus (P) addition in a subtropical forest. CK, control; LF, Liquidambar formosana; MM, Michelia macclurei; PM, Pinus massoniana. ACP, acid phosphatase activity; AP, available P content; βG, β-glucosaminidase activity; DOC, dissolved organic carton content; EC:N, the ratio of carbon-acquiring enzyme activity to nitrogen-acquiring enzyme activity; EC:P, the ratio of carbon-acquiring enzyme activity to phosphorus-acquiring enzyme activity; EN:P, the ratio of nitrogen-acquiring enzyme activity to phosphorus-acquiring enzyme activity; NAG, β-N-acetyl-glucosaminidase activity; TC:TN, the ratio of total carbon content to total nitrogen content; VA, vector angle; VL, vector length. The width of the trapezoid and CK represent the size of the corresponding index value.

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土壤磷有效性调控亚热带森林土壤酶活性和酶化学计量对凋落叶输入的响应

Soil phosphorus availability regulates the response of soil enzyme activity and enzymatic stoichiometry to litter addition in a subtropical forest

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