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Journal of Integrative Agriculture  2021, Vol. 20 Issue (10): 2758-2771    DOI: 10.1016/S2095-3119(21)63646-8
Special Issue: 昆虫合辑Plant Protection—Entomolgy 农业生态环境-有机碳与农业废弃物还田合辑Agro-ecosystem & Environment—SOC
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Changes in organic C stability within soil aggregates under different fertilization patterns in a greenhouse vegetable field
LUAN Hao-an1, 2*, YUAN Shuo1*, GAO Wei3, TANG Ji-wei1, LI Ruo-nan4, ZHANG Huai-zhi1, HUANG Shao-wen1
1 Institute of Agricultural Resources and Regional Planning/Key Laboratory of Plant Nutrition and Fertilizer of Ministry of Agriculture and Rural Affairs, Chinese Academy of Agricultural Sciences, Beijing 100081, P.R.China
2 College of Forestry, Hebei Agricultural University, Baoding 071000, P.R.China
3 Tianjin Institute of Agricultural Resources and Environment, Tianjin 300192, P.R.China
4 Institute of Agricultural Resources and Environment, Hebei Academy of Agriculture and Forestry Sciences, Shijiazhuang 050051, P.R.China
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理解土壤有机碳(SOC)的稳定性对于农业生态系统中SOC循环及其动态变化至关重要。已有研究观察到施肥对土体土壤中有机碳稳定性的调节作用。然而,在农业生态系统中,施肥如何改变土壤团聚体中有机碳的稳定性尚不清楚。本研究旨在评估中国天津设施蔬菜施肥8年(化肥vs有机措施)后土壤团聚体中有机碳稳定性的变化。为评估土壤团聚体中有机碳的稳定性变化,本研究采用如下四种方法:改良的Walkley-Black方法(化学方法),13C NMR技术(光谱法),胞外酶测定(生物方法)和热重分析法(热力学方法)。通过湿筛方法将土壤分离成四部分:宏团聚体(> 2 mm),大团聚体(0.25–2 mm),微团聚体(0.053–0.25 mm)和粉粘粒(<0.053 mm)。结果表明,与单施化肥模式相比,有机措施可增加土壤团聚体中有机碳含量,并降低有机碳化学、光谱学、热力学和生物学稳定性。在土壤各团聚体中,有机碳含量在微团聚体中最高,其次为宏团聚体和大团聚体,粉粘粒中最低。同时,有机碳光谱学、热力学和生物学稳定性在粉粘粒中最高,其次是宏团聚体和大团聚体,微团聚体内有机碳稳定性最低。此外,由于土壤团聚体内有机碳化学性质与其他稳定性特征之间的相关性较弱,故推断改良的Walkley-Black方法不适用于评价土壤团聚体内有机碳的稳定性。我们的发现可在土壤团聚体水平上,为深入探索中国设施菜田不同施肥模式下有机碳特性的变化提供科学见解。

Knowledge of the stability of soil organic C (SOC) is vital for assessing SOC dynamics and cycling in agroecosystems.  Studies have documented the regulatory effect of fertilization on SOC stability in bulk soils. However, how fertilization alters organic C stability at the aggregate scale in agroecosystems remains largely unclear.  This study aimed to appraise the changes of organic C stability within soil aggregates after eight years of fertilization (chemical vs. organic fertilization) in a greenhouse vegetable field in Tianjin, China.  Changes in the stability of organic C in soil aggregates were evaluated by four methods, i.e., the modified Walkley-Black method (chemical method), 13C NMR spectroscopy (spectroscopic method), extracellular enzyme assay (biological method), and thermogravimetric analysis (thermogravimetric method).  The aggregates were isolated and separated by a wet-sieving method into four fractions: large macroaggregates
(>2 mm), small macroaggregates (0.25–2 mm), microaggregates (0.053–0.25 mm), and silt/clay fractions (<0.053 mm).  The results showed that organic amendments increased the organic C content and reduced the chemical, spectroscopic, thermogravimetric, and biological stability of organic C within soil aggregates relative to chemical fertilization alone.  Within soil aggregates, the content of organic C was the highest in microaggregates and decreased in the order microaggregates>macroaggregates>silt/clay fractions.  Meanwhile, organic C spectroscopic, thermogravimetric, and biological stability were the highest in silt/clay fractions, followed by macroaggregates and microaggregates.  Moreover, the modified Walkley-Black method was not suitable for interpreting organic C stability at the aggregate scale due to the weak correlation between organic C chemical properties and other stability characteristics within the soil aggregates.  These findings provide scientific insights at the aggregate scale into the changes of organic C properties under fertilization in greenhouse vegetable fields in China.
Keywords:   fertilization        organic C stability        soil aggregates       thermogravimetric analysis        13C NMR spectroscopy  
Received: 14 December 2020   Accepted:
Fund: The authors sincerely acknowledge the financial support provided by the China Agriculture Research System of MOF and MARA (CARS-23-B02), the National Key Research and Development Program of China (2016YFD0201001), and the scientific research projects for talents introduce in Hebei Agricultural University (YJ2020054).
Corresponding Authors:  Correspondence TANG Ji-wei, Tel: +86-10-82105027, E-mail:; HUANG Shao-wen, Tel: +86-10-82108662, E-mail:    
About author:  LUAN Hao-an, E-mail:; YUAN Shuo, E-mail:; * These authors contributed equally to this study.

Cite this article: 

LUAN Hao-an, YUAN Shuo, GAO Wei, TANG Ji-wei, LI Ruo-nan, ZHANG Huai-zhi, HUANG Shao-wen. 2021. Changes in organic C stability within soil aggregates under different fertilization patterns in a greenhouse vegetable field. Journal of Integrative Agriculture, 20(10): 2758-2771.

Adhikari D, Yang Y. 2015. Selective stabilization of aliphatic organic carbon by iron oxide. Scientific Reports, 5, 11214.
Angst G, Mueller K E, Eissenstat D M, Trumbore S, Freeman K H, Hobbie S E, Chorover J, Oleksyn J, Reich P B, Mueller C W. 2019. Soil organic carbon stability in forests: Distinct effects of tree species identity and traits. Global Change Biology, 25, 1529–1546.
Ayoubi S, Karchegani P M, Mosaddeghi M R, Honarjoo N. 2012. Soil aggregation and organic carbon as affected by topography and land use change in western Iran. Soil and Tillage Research, 121, 18–26.
Bell C W, Fricks B E, Rocca J D, Steinweg J M, McMahon S K, Wallenstein M D. 2013. High-throughput fluorometric measurement of potential soil extracellular enzyme activities. Journal of Visualized Experiments, 81, e50961.
Boot C M, Hall E K, Denef K, Baron J S. 2016. Long-term reactive nitrogen loading alters soil carbon and microbial community properties in a subalpine forest ecosystem. Soil Biology and Biochemistry, 92, 211–220.
Cambardella C A, Elliott E T. 1993. Carbon and nitrogen distribution in aggregates from cultivated and native grassland soils. Soil Science Society of America Journal, 57, 1071–1076.
Chan K Y, Bowman A, Oates A. 2001. Oxidizible organic carbon fractions and soil quality changes in an Oxic Paleustalf under different pasture leys. Soil Science, 166, 61–67.
Chen X, Han X, You M, Yan J, Lu X, Horwath W R, Zou W. 2019. Soil macroaggregates and organic-matter content regulate microbial communities and enzymatic activity in a Chinese Mollisol. Journal of Integrative Agriculture, 18, 2605–2618.
Cheng X, Luo Y, Xu X, Sherry R, Zhang Q. 2011. Soil organic matter dynamics in a North America tallgrass prairie after
9 yr of experimental warming. Biogeosciences, 8, 1487–1498.
Chung H, Grove J H, Six J. 2008. Indications for soil carbon saturation in a temperate agroecosystem. Soil Science Society of America Journal, 72, 1132–1139.
Covaleda S, Gallardo J F, García-Oliva F, Kirchmann H, Prat C, Bravo M, Etchevers J D. 2011. Land-use effects on the distribution of soil organic carbon within particle-size fractions of volcanic soils in the Transmexican Volcanic Belt (Mexico). Soil Use and Management, 27, 186–194.
Fernández J, Plante A F, Leifeld J, Rasmussen C. 2011. Methodological considerations for using thermal analysis in the characterization of soil organic matter. Journal of Thermal Analysis and Calorimetry, 104, 389–398.
Gao W, Zhou T, Ren T. 2015. Conversion from conventional to no tillage alters thermal stability of organic matter in soil aggregates. Soil Science Society of America Journal, 79, 585–594.
Guan S, Dou S, Chen G, Wang G, Zhuang J. 2015. Isotopic characterization of sequestration and transformation of plant residue carbon in relation to soil aggregation dynamics. Applied Soil Ecology, 96, 18–24.
Guan S, Liu S, Liu R, Zhang J, Ren J, Cai H, Lin X. 2019. Soil organic carbon associated with aggregate-size and density fractions in a Mollisol amended with charred and uncharred maize straw. Journal of Integrative Agriculture, 18, 1496–1507.
Han L, Sun K, Jin J, Xing B. 2016. Some concepts of soil organic carbon characteristics and mineral interaction from a review of literature. Soil Biology and Biochemistry, 94, 107–121.
Hu W, Zhang Y, Huang B, Teng Y. 2017. Soil environmental quality in greenhouse vegetable production systems in eastern China: Current status and management strategies. Chemosphere, 170, 183–195.
Huang X, Jiang H, Li Y, Ma Y, Tang H, Ran W, Shen Q. 2016. The role of poorly crystalline iron oxides in the stability of soil aggregate-associated organic carbon in a rice–wheat cropping system. Geoderma, 279, 1–10.
Karhu K, Auffret M D, Dungait J A J, Hopkins D W, Prosser J I, Singh B K, Subke J A, Wookey P A, Agren G I, Sebastia M T, Gouriveau F, Bergkvist G, Meir P, Nottingham A T, Salinas N, Hartley I P. 2014. Temperature sensitivity of soil respiration rates enhanced by microbial community response. Nature, 513, 81–84.
Kong A Y Y, Scow K M, Córdova-Kreylos A L, Holmes W E, Six J. 2011. Microbial community composition and carbon cycling within soil microenvironments of conventional, low-input, and organic cropping systems. Soil Biology and Biochemistry, 43, 20–30.
Li S, Gu X, Zhuang J, An T, Pei J, Xie H, Li H, Fu S, Wang J. 2016. Distribution and storage of crop residue carbon in aggregates and its contribution to organic carbon of soil with low fertility. Soil and Tillage Research, 155, 199–206.
Liu H, Zhang J, Ai Z, Wu Y, Xu H, Li Q, Xue S, Liu G. 2018. 16-Year fertilization changes the dynamics of soil oxidizable organic carbon fractions and the stability of soil organic carbon in soybean–corn agroecosystem. Agriculture Ecosystems and Environment, 265, 320–330.
Liu K, Huang J, Li D, Yu X, Ye H, Hu H, Hu Z, Huang Q, Zhang H. 2019. Comparison of carbon sequestration efficiency in soil aggregates between upland and paddy soils in a red soil region of China. Journal of Integrative Agriculture, 18, 1348–1359.
Luan H, Gao W, Huang S, Tang J, Li M, Zhang H, Chen X. 2019. Partial substitution of chemical fertilizer with organic amendments affects soil organic carbon composition and stability in a greenhouse vegetable production system. Soil and Tillage Research, 191, 185–196.
Luan H, Gao W, Tang J, Li R, Li M, Zhang H, Chen X, Dainius M, Huang S. 2020. Aggregate-associated changes in nutrient properties, microbial community and functions in a greenhouse vegetable field based on an eight-year fertilization experiment of China. Journal of Integrative Agriculture, 19, 2530–2548.
Luo L, Meng H, Gu J. 2017. Microbial extracellular enzymes in biogeochemical cycling of ecosystems. Journal of Environmental Management, 197, 539–549.
MOA (Ministry of Agriculture, China). 2014. China Agriculture Yearbook 2014. China Agriculture Press, Beijing. (in Chinese)
Mastrolonardo G, Francioso O, Foggia M D, Bonora S, Rumpel C, Certini G. 2014. Application of thermal and spectroscopic techniques to assess fire-induced changes to soil organic matter in a Mediterranean forest. Journal of Geochemical Exploration, 143, 174–182.
Merino A, Ferreiro A, Salgado J, Fontúrbe M T, Barros N, Fernández C, Vega J A. 2014. Use of thermal analysis and solid-state 13C CP-MAS NMR spectroscopy to diagnose organic matter quality in relation to burn severity in Atlantic soils. Geoderma, 226–227, 376–386.
Nandan R, Singh V, Singh S S, Kumar V, Hazra K K, Nath C P, Poonia S, Malik R K, Bhattacharyya R, McDonald A. 2019. Impact of conservation tillage in rice–based cropping systems on soil aggregation, carbon pools and nutrients. Geoderma, 340, 104–114.
Nath A J, Bhattacharyya T, Ray S K, Deka J, Das A K, Devi H. 2016. Assessment of rice farming management practices based on soil organic carbon pool analysis. Tropical Ecology, 57, 607–611.
Nelson D W, Sommers L E. 1982. Total carbon, organic carbon and organic matter. In: Methods of Soil Analysis. Part 2. Chemical and Microbial Properties. Agronomy Society of America Madiso, Wisconsin.
Peltre C, Gregorich E G, Bruun S, Jensen L S, Magid J. 2017. Repeated application of organic waste affects soil organic matter composition: Evidence from thermal analysis, FTIR-PAS, amino sugars and lignin biomarkers. Soil Biology and Biochemistry, 104, 117–127.
Peng X, Zhu Q, Zhang Z, Hallett P D. 2017. Combined turnover of carbon and soil aggregates using rare earth oxides and isotopically labelled carbon as tracers. Soil Biology and Biochemistry, 109, 81–94.
Plante A F, Fernández J M, Leifeld J. 2009. Application of thermal analysis techniques in soil science. Geoderma, 153, 1–10.
Rabbi S M F, Daniel H, Lockwood P V, Macdonald C, Pereg L, Tighe M, Wilson B R, Young I M. 2016. Physical soil architectural traits are functionally linked to carbon decomposition and bacterial diversity. Scientific Reports, 6, 33012.
Schmidt M W, Torn M S, Abiven S, Dittmar T, Guggenberger G, Janssens I A, Kleber M, Kögel-Knabner I, Lehmann J, Manning A C, Nannipieri P, Rasse D P, Weiner S, Trumbore S E. 2011. Persistence of soil organic matter as an ecosystem property. Nature, 478, 49–56.
Shahbaz M, Kuzyakov Y, Heitkamp F. 2016. Decrease of soil organic matter stabilization with increasing inputs: Mechanisms and controls. Geoderma, 304, 76–82.
Sinsabaugh R L, Shah J J F. 2011. Ecoenzymatic stoichiometry of recalcitrant organic matter decomposition: The growth rate hypothesis in reverse. Biogeochemistry, 102, 31–43.
Six J, Bossuyt H, Degryze S, Denef K. 2004. A history of research on the link between (micro) aggregates, soil biota, and soil organic matter dynamics. Soil and Tillage Research, 79, 7–31.
Smith A P, Marín-Spiotta E, de Graaff M A, Balser T C. 2014. Microbial community structure varies across soil organic matter aggregate pools during tropical land cover change. Soil Biology and Biochemistry, 77, 292–303.
Smith P, Ashmore M R, Black H I, Burgess P J, Evans C D, Quine T A, Thomson A M, Hicks K, Orr H G. 2013. Review: The role of ecosystems and their management in regulating climate, and soil, water and air quality. Journal of Applied Ecology, 50, 812–829.
Srivastava P, Singh R, Bhadouria R, Tripathi S, Raghubanshi A S. 2020. Temporal change in soil physicochemical, microbial, aggregate and available C characteristic in dry tropical ecosystem. Catena, 190, 104553.
Ussiri D A, Jacinthe P A, Lal R. 2014. Methods for determination of coal carbon in reclaimed mine soils: a review. Geoderma, 214, 155–167.
Wang H, Nie Y, Butterly C R, Wanz L, Chen Q, Tian W, Song B, Xi Y Y. 2017. Fertilization alters microbial community composition and functional patterns by changing the chemical nature of soil organic carbon: A field study in a Halosol. Geoderma, 292, 17–24.
Wang Y, Hu N, Ge T, Kuzyakov Y, Wang Z, Li Z, Tang Z, Chen Y, Wu C, Lou Y. 2017. Soil aggregation regulates distributions of carbon, microbial community and enzyme activities after 23-year manure amendment. Applied Soil Ecology, 111, 65–72.
Xu P, Zhu J, Wang H, Shi L, Zhuang Y, Fu Q, Chen J, Hu H, Huang Q. 2021. Regulation of soil aggregate size under different fertilizations on dissolved organic matter, cellobiose hydrolyzing microbial community and their roles in organic matter mineralization. Science of the Total Environment, 755, 142595.
Xu X, Schaeffer S, Sun Z, Zhang J, An T, Wang J. 2020. Carbon stabilization in aggregate fractions responds to straw input levels under varied soil fertility levels. Soil and Tillage Research, 199, 104593.
Zhang H, Hu K, Zhang L, Ji Y, Qin W. 2019. Exploring optimal catch crops for reducing nitrate leaching in vegetable greenhouse in North China. Agricultural Water Management, 212, 273–282.
Zhang Q, Zhou W, Liang G, Sun J, Wang X, He P. 2015. Distribution of soil nutrients, extracellular enzyme activities and microbial communities across particle-size fractions in a long-term fertilizer experiment. Applied Soil Ecology, 94, 59–71.
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