Please wait a minute...
Journal of Integrative Agriculture  2024, Vol. 23 Issue (8): 2807-2819    DOI: 10.1016/j.jia.2023.11.019
Special Issue: 农业生态环境-土壤微生物Agro-ecosystem & Environment—Soil microbe
Agro-ecosystem & Environment Advanced Online Publication | Current Issue | Archive | Adv Search |
Effect of land use on soil nematode community composition and co-occurrence network relationship
Xiaotong Liu1, 3, Siwei Liang2, Yijia Tian1, 3, Xiao Wang1, 3, Wenju Liang1, 4, Xiaoke Zhang1, 4#
1 Institute of Applied Ecology, Chinese Academy of Sciences, Shenyang 110016, China 
2 Tillage and Cultivation Research Institute, Liaoning Academy of Agricultural Sciences, Shenyang 110161, China
3 University of Chinese Academy of Sciences, Beijing 100049, China 
4 Key Lab of Conservation Tillage and Ecological Agriculture in Liaoning Province, Shenyang 110016, China
Download:  PDF in ScienceDirect  
Export:  BibTeX | EndNote (RIS)      
摘要  

土地利用方式可以改变土壤生物的群落组成和多样性,从而影响地下生态系统的过程和功能。为了探究不同土地利用方式对土壤生物的影响,本研究对位于中国北方6个区域中3种不同土地利用方式,即农田、林地和撂荒地中的土壤线虫群落开展了调查研究。研究结果表明,农田土壤线虫的丰富度、多样性、丰度和生物量最低,撂荒地土壤线虫丰富度和多样性比农田高28.8%和15.1%。土壤线虫群落在林地中与撂荒地中无显著差异,但共现网络分析结果表明它们的关键属组成不同。林地的杂食-捕食线虫占网络关键属的50%,撂荒地的食细菌线虫占网络关键属的36%。在林地中,食真菌线虫在网络关键属的比例比撂荒地低了20.8%。共现网络的拓扑特性表明与林地和撂荒地相比,农田土壤网络复杂性和稳定性有所降低。土壤pH值、NH4+-N和NO3--N是农田土壤线虫群落的主要影响因素,而土壤有机碳和含水量是林地土壤线虫群落的主要影响因素。经过人为管理的农田土壤线虫群落对土壤环境的依赖性更强。不同土地利用方式引起的土壤环境的变化可以通过改变共现网络中线虫营养类群在关键属中的比例,从而影响土壤生物的网络关系。



Abstract  

Land use influences soil biota community composition and diversity, and then belowground ecosystem processes and functions.  To characterize the effect of land use on soil biota, soil nematode communities in crop land, forest land and fallow land were investigated in six regions of northern China.  Generic richness, diversity, abundance and biomass of soil nematodes was the lowest in crop land.  The richness and diversity of soil nematodes were 28.8 and 15.1% higher in fallow land than in crop land, respectively.  No significant differences in soil nematode indices were found between forest land and fallow land, but their network keystone genera composition was different.  Among the keystone genera, 50% of forest land genera were omnivores-predators and 36% of fallow land genera were bacterivores.  The proportion of fungivores in forest land was 20.8% lower than in fallow land.  The network complexity and the stability were lower in crop land than forest land and fallow land.  Soil pH, NH4+-N and NO3–-N were the major factors influencing the soil nematode community in crop land while soil organic carbon and moisture were the major factors in forest land.  Soil nematode communities in crop land influenced by artificial management practices were more dependent on the soil environment than communities in forest land and fallow land.  Land use induced soil environment variation and altered network relationships by influencing trophic group proportions among keystone nematode genera.  

Keywords:  soil nematode       trophic groups        community composition        co-occurrence network        land use  
Received: 18 August 2023   Accepted: 08 October 2023
Fund: 

This research was supported by the National Natural Science Foundation of China (U22A20501), the National Key Research and Development Plan of China (2022YFD1500601), the National Science and Technology Fundamental Resources Investigation Program of China (2018FY100304), the Strategic Priority Research Program of the Chinese Academy of Sciences (XDA28090200), the Liaoning Province Applied Basic Research Plan Program, China (2022JH2/101300184), the Shenyang Science and Technology Plan Program, China (21-109-3-05) and the Liaoning Outstanding Innovation Team, China (XLYC2008015).

About author:  Xiaotong Liu, E-mail: liuxiaotong18@mails.ucas.ac.cn; #Correspondence Xiaoke Zhang, Tel: +86-24-83970359, E-mail: zxk@iae.ac.cn

Cite this article: 

Xiaotong Liu, Siwei Liang, Yijia Tian, Xiao Wang, Wenju Liang, Xiaoke Zhang. 2024. Effect of land use on soil nematode community composition and co-occurrence network relationship. Journal of Integrative Agriculture, 23(8): 2807-2819.

Banerjee S, Schlaeppi K, van der Heijden M G A. 2018. Keystone taxa as drivers of microbiome structure and functioning. Nature Reviews Microbiology, 16, 567–576.

Barberan A, Bates S T, Casamayor E O, Fierer N. 2012. Using network analysis to explore co-occurrence patterns in soil microbial communities. The International Society for Microbial Ecology Journal, 6, 343–351.

Bastian M, Heymann S, Jacomy M. 2009. Gephi: An open source software for exploring and manipulating networks. Proceedings of the International AAAI Conference on Web and Social Media, 3, 361–362.

Bongers T. 1994. De nematoden van Nederland. Schoorl, Netherlands. (in Dutch)

Bongers T, Ferris H. 1999. Nematode community structure as a bio-indicator in environmental monitoring. Trends in Ecology and Evolution, 14, 224–228.

Bossio D A, Scow K M, Gunapala N, Graham K J. 1998. Determinants of soil microbial communities: Effects of agricultural management, season, and soil type on phospholipid fatty acid profiles. Microbial Ecology, 36, 1–12.

Briones M J I. 2014. Soil fauna and soil functions: A jigsaw puzzle. Frontiers in Environmental Science, 22, 7.

Cade-Menun B J, Bainard L D, LaForge K, Schellenberg M, Houston B, Hamel C. 2017. Long-term agricultural land use affects chemical and physical properties of soils from southwest Saskatchewan. Canadian Journal of Soil Science, 97, 650–666.

Chapin F S, Zavaleta E S, Eviner V T, Naylor R L, Vitousek P M, Reynolds H L, Hooper D U, Lavorel S, Sala O E, Hobbie S E, Mack M C, Díaz S. 2000. Consequences of changing biodiversity. Nature, 405, 234–242.

Creamer R, Hannula S, Van Leeuwen J, Stone D, Rutgers M, Schmelz R, De Ruiter P, Hendriksen N B, Bolger T, Bouffaud M L. 2016. Ecological network analysis reveals the inter-connection between soil biodiversity and ecosystem function as affected by land use across Europe. Applied Soil Ecology, 97, 112–124.

Csardi G, Nepusz T. 2006. The igraph software package for complex network research. International Journal of Complex System, 1695, 1–9.

da Silva J V C D, Ferris H, Cares J E, Esteves A M. 2021. Effect of land use and seasonality on nematode faunal structure and ecosystem functions in the Caatinga dry forest. European Journal of Soil Biology, 103, 103296.

Daskalova G N, Kamp J. 2023. Abandoning land transforms biodiversity land abandonment is critical when assessing global biodiversity and conservation. Science, 380, 581–583.

Delgado-Baquerizo M, Powell J R, Hamonts K, Reith F, Mele P, Brown M V, Dennis P G, Ferrari B C, Fitzgerald A, Young A, Singh B K, Bissett A. 2017. Circular linkages between soil biodiversity, fertility and plant productivity are limited to topsoil at the continental scale. New Phytologist, 215, 1186–1196.

Denef K, Roobroeck D, Wadu M C W M, Lootens P, Boeckx P. 2009. Microbial community composition and rhizodeposit–carbon assimilation in differently managed temperate grassland soils. Soil Biology and Biochemistry, 41, 144–153.

Ferris H, Bongers T, de Goede R G M. 2001. A framework for soil food web diagnostics: Extension of the nematode faunal analysis concept. Applied Soil Ecology, 18, 13–29.

Ferris H, Pocasangre L E, Serrano E, Munoz J, Garcia S, Perichi G, Martinez G. 2012. Diversity and complexity complement apparent competition: Nematode assemblages in banana plantations. Acta Oecologica, 40, 11–18

Gong X, Chen X, Geisen S, Zhang J R, Zhu H M, Hu F, Liu M Q. 2021. Agricultural habitats are dominated by rapidly evolving nematodes revealed through phylogenetic comparative methods. Soil Biology and Biochemistry, 155, 108183.

Háněl L. 2003. Recovery of soil nematode populations from cropping stress by natural secondary succession to meadow land. Applied Soil Ecology, 22, 255–270.

Heijboer A, de Ruiter P C, Bodelier P L E, Kowalchuk G A. 2018. Modulation of litter decomposition by the soil microbial food web under influence of land use change. Frontiers in Microbiology, 9, 2860.

Hill G T, Mitkowski N A, Aldrich-Wolfe L, Emele L R, Jurkonie D D, Ficke A, Maldonado-Ramirez S, Lynch S T, Nelson E B. 2000. Methods for assessing the composition and diversity of soil microbial communities. Applied Soil Ecology, 15, 25–36.

van den Hoogen J, Geisen S, Routh D, Ferris H, Traunspurger W, Wardle D A, de Goede R G M, Adams B J, Ahmad W, Andriuzzi W S, Bardgett R D, Bonkowski M, Campos-Herrera R, Cares J E, Caruso T, de Brito Caixeta L, Chen X Y, Costa S R, Creamer R, da Cunha Castro J M, et al. 2019. Soil nematode abundance and functional group composition at a global scale. Nature, 572, 194–198.

Kandji S T, Ogol C K P O, Albrecht A. 2001. Diversity of plant–parasitic nematodes and their relationships with some soil physico-chemical characteristics in improved fallows in western Kenya. Applied Soil Ecology, 18, 143–157.

Kou X C, Ma N N, Zhang X K, Xie H T, Zhang X D, Wu Z F, Liang W J, Li Q, Ferris H. 2020. Frequency of stover mulching but not amount regulates the decomposition pathways of soil micro-foodwebs in a no-tillage system. Soil Biology and Biochemistry, 144, 107789.

Kou X C, Morriën E, Tian Y J, Zhang X K, Lu C Y, Xie H T, Liang W J, Li Q, Liang C. 2023. Exogenous carbon turnover within the soil food web strengthens soil carbon sequestration through microbial necromass accumulation. Global Change Biology, 29, 4069–4080.

Kuzyakov Y, Xu X. 2013. Competition between roots and microorganisms for nitrogen: mechanisms and ecological relevance. New Phytologist, 198, 656–669.

Landi P, Minoarivelo H O, Brännström Å, Hui C, Dieckmann U. 2018. Complexity and stability of ecological networks: a review of the theory. Population Ecology, 60, 319–345.

Lenz R, Eisenbeis G. 2000. Short-term effects of different tillage in a sustainable farming system on nematode community structure. Biology and Fertility of Soils, 31, 237–244.

Li J N, Zhao J, Liao X H, Yi Q, Zhang W, Lin H F, Liu K P, Peng P Q, Wang K L. 2023. Long-term returning agricultural residues increases soil microbe–nematode network complexity and ecosystem multifunctionality. Geoderma, 430, 116340.

Li X P, Liu T, Li H X, Geisen S, Hu F, Liu M Q. 2022. Management effects on soil nematode abundance differ among functional groups and land-use types at a global scale. Journal of Animal Ecology, 91, 1770–1780.

Li X P, Zhu H M, Geisen S, Bellard C, Hu F, Li H X, Chen X Y, Liu M Q. 2020. Agriculture erases climate constraints on soil nematode communities across large spatial scales. Global Change Biology, 26, 919–930.

Liang W J, Lou Y L, Li Q, Zhong S, Zhang X K, Wang J K. 2009. Nematode faunal response to long-term application of nitrogen fertilizer and organic manure in Northeast China. Soil Biology and Biochemistry, 41, 883–890.

Liu H W, Du X F, Li Y B, Han X, Li B, Zhang X K, Li Q, Liang W J. 2022. Organic substitutions improve soil quality and maize yield through increasing soil microbial diversity. Journal of Cleaner Production, 347, 131323.

Ma Q X, Kuzyakov Y, Pan W K, Tang S, Chadwick D R, Wen Y, Hill P W, Macdonald A, Ge T D, Si L L, Wu L H, Jones D L. 2021. Substrate control of sulphur utilisation and microbial stoichiometry in soil: Results of C13, N15, C14, and S35 quad labelling. The International Society for Microbial Ecology Journal, 15, 3148–3158.

Meng H Q, Xu M G, Lu J L, He X H, Li J W, Shi X J, Peng C, Wang B R, Zhang H M. 2013. Soil pH dynamics and nitrogen transformations under long-term chemical fertilization in four typical Chinese croplands. Journal of Integrative Agriculture, 12, 2092–2102.

Mooney H A, Cooper A, Reid W. 2005. Confronting the human dilemma. Science, 434, 561–562.

Newman M E J. 2006. Modularity and community structure in networks. Proceedings of the National Academy of Sciences of the United States of America, 103, 8577–8582.

Nielsen S, Minchin T, Kimber S, van Zwieten L, Gilbert J, Munroe P, Joseph S, Thomas T. 2014. Comparative analysis of the microbial communities in agricultural soil amended with enhanced biochars or traditional fertilisers. Agriculture, Ecosystems and Environment, 191, 73–82.

Outhwaite C L, Ortiz A M D, Spooner F E B, Dalin C, Newbold T. 2022. Availability and proximity of natural habitat influence cropland biodiversity in forest biomes globally. Global Ecology and Biogeography, 31, 1589–1602.

Rivest M, Whalen J K, Rivest D. 2019. Tree diversity is not always a strong driver of soil microbial diversity: A 7-yr-old diversity experiment with trees. Ecosphere, 10, e02685.

Sánchez-Jardón L, Acosta B, del Pozo A, Casado M A, Ovalle C, Elizalde H F, Hepp C, de Miguel J M. 2010. Grassland productivity and diversity on a tree cover gradient in Nothofagus pumilio in NW Patagonia. Agriculture, Ecosystems and Environment, 137, 213–218.

Schnecker J, Wild B, Fuchslueger L, Richter A. 2012. A field method to store samples from temperate mountain grassland soils for analysis of phospholipid fatty acids. Soil Biology and Biochemistry, 51, 81–83.

Shi S J, Nuccio E E, Shi Z J, He Z L, Zhou J Z, Firestone M K. 2016. The interconnected rhizosphere: High network complexity dominates rhizosphere assemblages. Ecology Letters, 19, 926–936.

Shi Y, Zhang K P, Li Q, Liu X, He J S, Chu H Y. 2020. Interannual climate variability and altered precipitation influence the soil microbial community structure in a Tibetan Plateau grassland. Science of the Total Environment, 714, 136794.

Sieriebriennikov B, Ferris H, de Goede R G M. 2014. NINJA: An automated calculation system for nematode-based biological monitoring. European Journal of Soil Biology, 61, 90–93.

Singh D, Shi L L, Adams J M. 2013. Bacterial diversity in the mountains of southwest China: Climate dominates over soil parameters. Journal of Microbiology, 51, 439–447.

Vandewalle M, de Bello F, Berg M P, Bolger T, Dolédec S, Dubs F, Feld C K, Harrington R, Harrison P A, Lavorel S, da Silva P M, Moretti M, Niemelä J, Santos P, Sattler T, Sousa J P, Sykes M T, Vanbergen A J, Woodcock B A. 2010. Functional traits as indicators of biodiversity response to land use changes across ecosystems and organisms. Biodiversity and Conservation, 19, 2921–2947.

Vazquez C, de Goede R G M, Korthals G W, Rutgers M, Schouten A J, Creamer R. 2019. The effects of increasing land use intensity on soil nematodes: A turn towards specialism. Functional Ecology, 33, 2003–2016.

Walkley A, Black I A. 1934. An examination of the Degtjareff method for determining soil organic matter, and a proposed modification of the chromic acid titration method. Soil Science, 37, 29–38.

Wang Y S, Li C N, Tu B, Kou Y P, Li X Z. 2021. Species pool and local ecological assembly processes shape the beta-diversity of diazotrophs in grassland soils. Soil Biology and Biochemistry, 160, 108338.

Wu J, Barahona M, Tan Y J, Deng H Z. 2010. Natural connectivity of complex networks. Chinese Physics Letters, 27, 078902.

Wu J, Chen H, Zhang Y. 2016. Latitudinal variation in nematode diversity and ecological roles along the Chinese coast. Ecology and Evolution, 6, 8018–8027.

Xiao H F, Tian Y H, Zhou H P, Ai X S, Yang X D, Schaefer D A. 2014. Intensive rubber cultivation degrades soil nematode communities in Xishuangbanna, southwest China. Soil Biology and Biochemistry, 76, 161–169.

Yang Y, Chai Y B, Xie H J, Zhang L, Zhang Z M, Yang X, Hao S L, Gai J P, Chen Y L. 2023. Responses of soil microbial diversity, network complexity and multifunctionality to three land-use changes. Science of the Total Environment, 859, 160255.

Yeates G W. 2003. Nematodes as soil indicators: Functional and biodiversity aspects. Biology and Fertility of Soils, 37, 199–210.

Yeates G W, Bongers T. 1999. Nematode diversity in agroecosystems. Agriculture, Ecosystems and Environment, 74, 113–135.

Yeates G W, Bongers T, Degoede R G M, Freckman D W, Georgieva S S. 1993. Feeding-habits in soil nematode families and genera - an outline for soil ecologists. Journal of Nematology, 25, 315–331.

Yuan M M, Guo X, Wu L W, Zhang Y, Xiao N J, Ning D L, Shi Z, Zhou X S, Wu L Y, Yang Y F, Tiedje J M, Zhou J Z. 2021. Climate warming enhances microbial network complexity and stability. Nature Climate Change, 11, 343–348.

Zeller V, Bardgett R D, Tappeiner U. 2001. Site and management effects on soil microbial properties of subalpine meadows: A study of land abandonment along a north-south gradient in the European Alps. Soil Biology and Biochemistry, 33, 639–649.

Zhang X K, Guan P T, Wang Y L, Li Q, Zhang S X, Zhang Z Y, Bezemer T M, Liang W J. 2015. Community composition, diversity and metabolic footprints of soil nematodes in differently-aged temperate forests. Soil Biology and Biochemistry, 80, 118–126.

[1] Zhechao Dou, Jing Ma, Kunguang Wang, Qiaofang Lu, Zhiguang Chi, Dongming Cui, Chang Pan, Zhuchi He, Yuanmei Zuo. Use of soil nematodes as indicators of soil and plant health in continuous cropping systems: A case study in dragon fruit[J]. >Journal of Integrative Agriculture, 2025, 24(5): 1987-2001.
[2] Hao Xi, Jing Zeng, Jiayao Han, Yali Zhang, Jianbin Pan, Qi Zhang, Huyuan Feng, Yongjun Liu. Host preferences of root-associated fungi and their responses to decadal nitrogen and fungicide applications in an alpine pasture ecosystem[J]. >Journal of Integrative Agriculture, 2025, 24(3): 885-899.
[3] Yu Li, Shikui Dong, Qingzhu Gao, Yong Zhang, Hasbagan Ganjurjav, Guozheng Hu, Xuexia Wang, Yulong Yan, Fengcai He, Fangyan Cheng. Large herbivores increase the proportion of palatable species rather than unpalatable species in the plant community[J]. >Journal of Integrative Agriculture, 2025, 24(3): 859-870.
[4] Shuting Yu, Tianshu Wang, Li Wang, Shuihong Yao, Bin Zhang. Preceding crop rotation systems shape the selection process of wheat root-associated bacterial communities[J]. >Journal of Integrative Agriculture, 2025, 24(2): 739-753.
[5] CHEN Yun-feng, XIA Xian-ge, HU Cheng, LIU Dong-hai, QIAO Yan, LI Shuang-lai, FAN Xian-peng. Effects of long-term straw incorporation on nematode community composition and metabolic footprint in a rice–wheat cropping system[J]. >Journal of Integrative Agriculture, 2021, 20(8): 2265-2276.
[6] SONG Zhen-wei, ZHANG Bin, TIAN Yun-lu, DENG Ai-xing, ZHENG Cheng-yan, Md Nurul Islam, Md Abdul Mannaf , ZHANG Wei-jian.  Impacts of Nighttime Warming on the Soil Nematode Community in a Winter Wheat Field of Yangtze Delta Plain, China[J]. >Journal of Integrative Agriculture, 2014, 13(7): 1477-1485.
No Suggested Reading articles found!