Biodiversity Science ›› 2019, Vol. 27 ›› Issue (4): 409-418.doi: 10.17520/biods.2019006

• Original Papers • Previous Article     Next Article

Effect of soil nematode functional guilds on plant growth and aboveground herbivores

Zhu Baijing, Xue Jingrong, Xia Rong, Jin Miaomiao, Wu You, Tian Shanyi, Chen Xiaoyun(), Liu Manqiang, Hu Feng   

  1. Soil Ecology Laboratory, College of Resources and Environmental Sciences, Nanjing Agricultural University, Nanjing 210095
  • Received:2019-01-08 Accepted:2019-03-14 Online:2019-06-05
  • Chen Xiaoyun

Soil multitrophic interactions are the keystone of understanding mechanisms of ecological function. In order to test the effect of nematode functional guilds on rice growth and Nilaparvata lugens abundance, a pot experiment was conducted by growing rice with a complete factorial design manipulating microbivores (microbivorous nematodes), herbivores (herbivorous nematodes) and omnivore-carnivores (omnivore-carnivorous nematodes). Results showed that compared with no nematodes, herbivores significantly increased rice root biomass (P < 0.05) and total shoot phenolic content (P < 0.05). The microbivores significantly increased N. lugens abundance and significantly reduced root biomass (P < 0.05). Omnivore-carnivores promoted rice shoot growth (P < 0.05), decreased the number of N. lugens (P < 0.05). Higher total phenolic content occurred in treatment receiving all three nematode functional guilds, suggesting stronger potential for insect resistance. In conclusion, organisms at higher trophic levels, such as omnivore-carnivores, could promote plant defense and suppress aboveground herbivory via regulating the herbivores and microbivores. Soil biota managements play central roles in control of trophic level diversity.

Key words: soil biodiversity, biotic interactions, plant chemistry, aboveground-belowground, plant defense

Fig. 1

Conceptual framework showing the main pathways of how nematode functional guilds affect brown planthopper via nutrient and defense effects. Solid arrows represent positive impact and dotted arrows represent negative impact."

Table 1

Multivariate linear regression results showing the effects of herbivores, microbivores and omnivore-carnivores abundance on the biomass and chemical composition contents of rice shoots and roots and the abundance of brown planthoppers"

of variation
茎叶 Shoot 根系 Root 褐飞虱数量
Brown planthoppers abundance
Amino acids
Amino acids
植食线虫 H 0.06 0.15 -0.03 0.36** 0.29** -1.15 -0.23 0.21* -0.22
食微线虫 M -0.13 -0.28 0.06 -0.23 -0.19 0.33 -0.34 -0.41* -0.93**
捕杂食线虫 O 0.23** -0.10 -0.04 -0.02 -0.03 0.81 -0.55 0.40** -1.07**
H × M 0.14 -0.23 0.15 0.26 -0.51 2.39 0.41 -0.13 1.48
H × O 0.69 -0.62 0.23 0.57 -0.56* 7.32** 0.89 -0.21 1.46
M × O 0.00 -0.17 0.02 0.56 -0.94 -1.75 1.25 -0.09 2.43**
M × H × O -0.72 0.96 -2.78 -1.20 5.88* -8.33 -1.48 1.31 -3.97
R2 0.5 0.24 0.24 0.53 0.59 0.63 0.11 0.42 0.47

Fig. 2

Effects of soil nematode functional guilds on the biomass, concentrations of soluble sugars, amino acids in rice shoot (A, C, E) and root (B, D, F). Means with different letters indicate significant difference among treatments (Fisher’s LSD test, P < 0.05). Error bars are standard errors."

Fig. 3

Effects of soil nematode functional guilds on the concentrations of phenolics in rice shoot (A) and root (B). Means with different letters indicate significant difference among treatments (Fisher’s LSD test, P < 0.05). Error bars are standard errors."

Fig. 4

Abundance of microbivores (A), herbivores (B), omnivore-carnivores (C) and brown planthoppers (D) affected by the manipulations of different nematode functional guilds. Means with different letters indicate significant difference among treatments (Fisher’s LSD test, P < 0.05). Error bars are standard errors."

Fig. 5

Scatter plots between the abundance of nematode functional guilds and rice biomass, phenolics concentrations, the abundance of brown planthoppers."

[1] Ainsworth EA, Gillespie KM ( 2007) Estimation of total phenolic content and other oxidation substrates in plant tissues using Folin-Ciocalteu reagent. Nature Protocols, 2, 875-877.
doi: 10.1038/nprot.2007.102
[2] Altieri MA, Nicholls CI ( 2003) Soil fertility management and insect pests: Harmonizing soil and plant health in agroecosystems. Soil and Tillage Research, 72, 203-211.
doi: 10.1016/S0167-1987(03)00089-8
[3] Bakker MG, Manter DK, Sheflin AM, Weir TL, Vivanco JM ( 2012) Harnessing the rhizosphere microbiome through plant breeding and agricultural management. Plant and Soil, 360, 1-13.
doi: 10.1007/s11104-012-1361-x
[4] Bardgett RD, van der Putten WH ( 2014) Belowground biodiversity and ecosystem functioning. Nature, 515, 505-511.
doi: 10.1038/nature13855
[5] Barrios E ( 2007) Soil biota, ecosystem services and land productivity. Ecological Economics, 64, 269-285.
doi: 10.1016/j.ecolecon.2007.03.004
[6] Bender SF, van der Heijden MGA ( 2015) Soil biota enhance agricultural sustainability by improving crop yield, nutrient uptake and reducing nitrogen leaching losses. Journal of Applied Ecology, 52, 228-239.
doi: 10.1111/1365-2664.12351
[7] Bernaola L, Cosme M, Schneider RW, Stout M ( 2018) Belowground inoculation with arbuscular mycorrhizal fungi increases local and systemic susceptibility of rice plants to different pest organisms. Frontiers in Plant Science, 9, 747.
doi: 10.3389/fpls.2018.00747
[8] Bezemer TM, de Deyn GB, Bossinga TM, van Dam NM, Harvey JA, van der Putten WH ( 2005) Soil community composition drives aboveground plant-herbivore-parasitoid interactions. Ecology Letters, 8, 652-661.
doi: 10.1111/ele.2008.8.issue-6
[9] Bjørnlund L, Liu MQ, Rønn R, Christensen S, Ekelunda F ( 2012) Nematodes and protozoa affect plants differently, depending on soil nutrient status. European Journal of Soil Biology, 50, 28-31.
doi: 10.1016/j.ejsobi.2011.11.012
[10] Bongers T ( 1988) De Nematoden Van Nederland.(in Dutch) Stichting Uitgeverij Koninklijke Nederlandse Natuurhistorische Vereniging, Utrecht.
[11] Bonkowski M, Villenave C, Griffiths B ( 2009) Rhizosphere fauna: The functional and structural diversity of intimate interactions of soil fauna with plant roots. Plant and Soil, 321, 213-233.
doi: 10.1007/s11104-009-0013-2
[12] Buchan D, Moeskops B, Ameloot N, De Neve S, Sleutel S ( 2012) Selective sterilisation of undisturbed soil cores by gamma irradiation: Effects on free-living nematodes, microbial community and nitrogen dynamics. Soil Biology and Biochemistry, 47, 10-13.
doi: 10.1016/j.soilbio.2011.12.014
[13] Chakraborty S, Pangga IB, Roper MM ( 2012) Climate change and multitrophic interactions in soil: The primacy of plants and functional domains. Global Change Biology, 18, 2111-2125.
doi: 10.1111/j.1365-2486.2012.02667.x
[14] Chen XY, Liu MQ, Hu F, Mao XF, Li HX ( 2007) Contributions of soil micro-fauna (protozoa and nematodes) to rhizospere ecological functions. Acta Ecologica Sinica, 27, 3132-3143. (in Chinese with English abstract)
[ 陈小云, 刘满强, 胡锋, 毛小芳, 李辉信 ( 2007) 根际微型土壤动物——原生动物和线虫的生态功能. 生态学报, 27, 3132-3143.]
[15] Dubois M, Gilles KA, Hamilton JK, Rebers PA, Smith F ( 1956) Colorimetric method for determination of sugars and related substances. Analytical Chemistry, 28, 350-356.
doi: 10.1021/ac60111a017
[16] Eisenhauer N, Vogel A, Jensen B, Scheu S ( 2018) Decomposer diversity increases biomass production and shifts aboveground-belowground biomass allocation of common wheat. Scientific Reports, 8, 17894.
doi: 10.1038/s41598-018-36294-3
[17] Faucon MP, Houben D, Lambers H ( 2017) Plant functional traits: Soil and ecosystem services. Trends in Plant Science, 22, 385-394.
[18] Ferris H, Griffiths BS, Porazinska DL, Powers TO, Wang KH, Tenuta M ( 2012 a) Reflections on plant and soil nematode ecology: Past, present and future. Journal of Nematology, 44, 115-126.
[19] Ferris H, Sánchez-Moreno S, Brennan EB ( 2012 b) Structure, functions and interguild relationships of the soil nematode assemblage in organic vegetable production. Applied Soil Ecology, 61, 16-25.
doi: 10.1016/j.apsoil.2012.04.006
[20] Gebremikael MT, Buchan D, De Neve S ( 2014) Quantifying the influences of free-living nematodes on soil nitrogen and microbial biomass dynamics in bare and planted microcosms. Soil Biology and Biochemistry, 70, 131-141.
doi: 10.1016/j.soilbio.2013.12.006
[21] Gebremikael M T, Steel H, Buchan D, Bert W, de Neve S ( 2016) Nematodes enhance plant growth and nutrient uptake under C and N-rich conditions. Scientific Reports, 6, 32862.
doi: 10.1038/srep32862
[22] Guo RH, Luo L, Zhang TH, Liu MQ, Chen XY, Hu F ( 2017) Effects of interactions of above- and below-ground herbivores on nitrogen distribution in rice plant and labile nitrogen in soil. Acta Pedolocica Sinica, 493-502. (in Chinese with English abstract)
[ 郭瑞华, 罗琌, 张腾昊, 刘满强, 陈小云, 胡锋 ( 2017) 地上和地下植食线虫互作对水稻氮分配及土壤活性氮的影响. 土壤学报, 493-502.]
[23] Huang JH, Liu MQ, Chen XY, Chen J, Chen FJ, Li HX, Hu F ( 2013) Intermediate herbivory intensity of an aboveground pest promotes soil labile resources and microbial biomass via modifying rice growth. Plant and Soil, 367, 437-447.
doi: 10.1007/s11104-012-1480-4
[24] Jiang LH, Luo L, Xiao ZG, Li DM, Chen XY, Liu MQ, Hu F ( 2016) Effects of soil biota influenced by long-term organic and chemical fertilizers on rice growth and resistance to insects. Biodiversity Science, 24, 907-915. (in Chinese with English abstract)
[ 蒋林惠, 罗琌, 肖正高, 李大明, 陈小云, 刘满强, 胡锋 ( 2016) 长期施肥对水稻生长和抗虫性的影响: 解析土壤生物的贡献. 生物多样性, 24, 907-915.]
[25] Johnson SN, Clark KE, Hartley SE, Jones TH, Mckenzie SW, Koricheva J ( 2012) Aboveground-belowground herbivore interactions: A meta-analysis. Ecology, 93, 2208-2215.
doi: 10.1890/11-2272.1
[26] Kulmatiski A, Anderson-Smith A, Beard KH, Doucette-Riise S, Mazzacavallo M, Nolan NE, Ramirez RA, Stevens JR ( 2015) Most soil trophic guilds increase plant growth: A meta-analytical review. Oikos, 123, 1409-1419.
[27] Li Q, Liang WJ, Jiang Y ( 2007) Present situation and prospect of soil nematode diversity in farmland Ecosystems. Biodiversity Science, 15, 134-141. (in Chinese with English abstract)
[ 李琪, 梁文举, 姜勇 ( 2007) 农田土壤线虫多样性研究现状及展望. 生物多样性, 15, 134-141.]
[28] Liu MQ, Chen XY, Qin JT, Wang D, Griffiths B, Hu F ( 2008) A sequential extraction procedure reveals that water management affects soil nematode communities in paddy fields. Applied Soil Ecology, 40, 250-259.
doi: 10.1016/j.apsoil.2008.05.001
[29] Liu T, Ye CL, Li Y, Chen XY, Ran W, Shen QR, Hu F, Li HX ( 2015) Effects of different organic fertilizers on soil nematodes in the rhizosphere of rice and wheat cropland. Acta Ecologica Sinica, 35, 6259-6268. (in Chinese with English abstract)
[ 刘婷, 叶成龙, 李勇, 陈小云, 冉炜, 沈其荣, 胡锋, 李辉信 ( 2015) 不同有机类肥料对小麦和水稻根际土壤线虫的影响. 生态学报, 35, 6259-6268.]
[30] Liu YD, Chen XY, Liu MQ, Qin JT, Li HX, Hu F ( 2013) Changes in soil microbial properties and nematode assemblage over time during rice cultivation. Biodiversity Science, 21, 334-342. (in Chinese with English abstract)
[ 刘雨迪, 陈小云, 刘满强, 秦江涛, 李辉信, 胡锋 ( 2013) 不同稻作年限下土壤微生物学性质和线虫群落特征的变化. 生物多样性, 21, 334-342.]
[31] Milcu A, Allan E, Roscher C, Jenkins T, Meyer S T, Flynn D, Bessler H, Buscot F, Engels C, Gubsch M, König S, Lipowsky A, Loranger J, Renker C, Scherber C, Schmid B, Thébault E, Wubet T, Weisser WW, Scheu S, Eisenhauer N ( 2013) Functionally and phylogenetically diverse plant communities key to soil biota. Ecology, 94, 1878-1885.
doi: 10.1890/12-1936.1
[32] Moretti M, Dias ATC, De Bello F, Altermatt F, Chown SL, Azcárate FM, Bell JR, Fournier B, Hedde M, Hortal J, Ibanez S, Öckinger E, Sousa JP, Ellers J, Berg MP ( 2017) Handbook of protocols for standardized measurement of terrestrial invertebrate functional traits. Functional Ecology, 31, 558-567.
doi: 10.1111/1365-2435.12776
[33] Phillips RP, Finzi AC, Bernhardt ES ( 2011) Enhanced root exudation induces microbial feedbacks to N cycling in a pine forest under long-term CO2 fumigation. Ecology Letters, 14, 187-194.
doi: 10.1111/j.1461-0248.2010.01570.x
[34] Pineda A, Zheng SJ, van Loon JJA, Pieterse CMJ, Dicke M ( 2010) Helping plants to deal with insects: The role of beneficial soil-borne microbes. Trends in Plant Science, 15, 507-514.
doi: 10.1016/j.tplants.2010.05.007
[35] Pineda A, Kaplan I, Bezemer TM ( 2017) Steering soil microbiomes to suppress aboveground insect pests. Trends in Plant Science, 22, 770-778.
doi: 10.1016/j.tplants.2017.07.002
[36] Ren YW, Xiao ML, Yuan HC, Zhu ZK, Li QY, Ge TD, Su YR, Wu JS ( 2018) Allocation of rice photosynthates in plant-soil system in response to elevated CO2 and nitrogen fertilization. Chinese Journal of Applied Ecology, 29, 1397-1404. (in Chinese with English abstract)
[ 任逸文, 肖谋良, 袁红朝, 祝贞科, 李巧云, 葛体达, 苏以荣, 吴金水 ( 2018) 水稻光合碳在植物-土壤系统中的分配及其对CO2升高和施氮的响应. 应用生态学报, 29, 1397-1404.]
[37] Sackett TE, Classen AT, Sanders NJ ( 2010) Linking soil food web structure to above- and belowground ecosystem processes: A meta-analysis. Oikos, 119, 1984-1992.
doi: 10.1111/more.2010.119.issue-12
[38] Sun Y, Xu XL, Kuzyakov Y ( 2014) Mechanisms of rhizosphere priming effects and their ecological significanc. Chinese Journal of Plant Ecology, 38, 62-75. (in Chinese with English abstract)
[ 孙悦, 徐兴良 , Kuzyakov Y ( 2014) 根际激发效应的发生机制及其生态重要性. 植物生态学报, 38, 62-75.]
[39] Tao L, Ahmad A, de Roode JC, Hunter MD ( 2016) Arbuscular mycorrhizal fungi affect plant tolerance and chemical defenses to herbivory through different mechanisms. Journal of Ecology, 104, 561-571.
doi: 10.1111/1365-2745.12535
[40] Thakur MP, Herrmann M, Steinauer K, Rennoch S, Cesarz S, Eisenhauer N ( 2015) Cascading effects of belowground predators on plant communities are density-dependent. Ecology and Evolution, 5, 4300-4314.
doi: 10.1002/ece3.2015.5.issue-19
[41] Wardle DA ( 2006) The influence of biotic interactions on soil biodiversity. Ecology Letters, 9, 870-886.
doi: 10.1111/ele.2006.9.issue-7
[42] Wardle DA, Bardgett RD, Klironomos JN, Setälä H, van der Putten WH, Wall DH ( 2004) Ecological linkages between aboveground and belowground biota. Science, 304, 1629-1633.
doi: 10.1126/science.1094875
[43] Wagg C, Bender SF, Widmer F, van der Heijden MGA ( 2014) Soil biodiversity and soil community composition determine ecosystem multifunctionality. Proceedings of the National Academy of Sciences,USA, 111, 5266-5270.
doi: 10.1073/pnas.1320054111
[44] Wang SJ, Ruan HH ( 2008) Feedback mechanisms of soil biota to aboveground biology in terrestrial ecosystems. Biodiversity Science, 16, 407-416. (in Chinese with English abstract)
[ 王邵军, 阮宏华 ( 2008) 土壤生物对地上生物的反馈作用及其机制. 生物多样性, 16, 407-416.]
[45] Wurst S, Wagenaar R, Biere A, van der Putten WH ( 2010) Microorganisms and nematodes increase levels of secondary metabolites in roots and root exudates of Plantago lanceolata. Plant and Soil, 329, 117-126.
doi: 10.1007/s11104-009-0139-2
[46] Wu JH, Song CY, Chen JK ( 2007) Effect of microbivorous nematodes on plant growth and soil nutrient cycling: A review. Biodiversity Science, 15, 124-133. (in Chinese with English abstract)
[ 吴纪华, 宋慈玉, 陈家宽 ( 2007) 食微线虫对植物生长及土壤养分循环的影响. 生物多样性, 15, 124-133.]
[47] Yang XD, Chen J ( 2009) Plant litter quality influences the contribution of soil fauna to litter decomposition in humid tropical forests, southwestern China. Soil Biology and Biochemistry, 41, 910-918.
doi: 10.1016/j.soilbio.2008.12.028
[48] Yemm EW, Cocking EC, Ricketts RE ( 1955) The determination of amino-acids with ninhydrin. Analyst, 80, 209-214.
doi: 10.1039/an9558000209
[49] Yin WY ( 1998) Illustrated Handbook of Chinese Soil Fauna. Science Press, Beijing. (in Chinese)
[ 尹文英 ( 1998) 中国土壤动物检索图鉴. 科学出版社, 北京.]
[50] Zhang XK, Ferris H, Mitchell J, Liang WJ ( 2017) Ecosystem services of the soil food web after long-term application of agricultural management practices. Soil Biology and Biochemistry, 111, 36-43.
doi: 10.1016/j.soilbio.2017.03.017
[51] Zhu TB, Yang C, Wang J, Zeng S, Liu MQ, Yang JL, Bai B, Cao JH, Chen XY, Müller C ( 2017) Bacterivore nematodes stimulate soil gross N transformation rates depending on their species. Biology and Fertility of Soils, 54, 107-118.
[1] Yu Zhang, Zhenggao Xiao, Linhui Jiang, Lei Qian, Xiaoyun Chen, Fajun Chen, Feng Hu, Manqiang Liu. Nitrogen levels modify earthworm-mediated tomato growth and resistance to pests [J]. Biodiv Sci, 2018, 26(12): 1296-1307.
[2] Linhui Jiang,Ling Luo,Zhenggao Xiao,Daming Li,Xiaoyun Chen,Manqiang Liu,Feng Hu. Effects of soil biota influenced by long-term organic and chemical fertilizers on rice growth and resistance to insects [J]. Biodiv Sci, 2016, 24(8): 907-915.
[3] ZHANG Su-Fang, ZHANG Zhen, WANG Hong-Bin, and KONG Xiang-Bo. New discovery about plant defense: plant-plant communication [J]. Chin J Plan Ecolo, 2012, 36(10): 1120-1124.
[5] Min Zhang*. Advances in Vegetative Storage Proteins and Their Biological Functions [J]. Chin Bull Bot, 2008, 25(05): 624-630.
[6] GAO Guo-Qing CHU Cheng-Cai LIU Xiao-Qiang LI Yang-Rui. Current Progress on WRKY Superfamily of Plant Transcription Factors [J]. Chin Bull Bot, 2005, 22(01): 11-18.
[7] HAN Xing-Guo, WANG Zhi-Ping. Soil biodiversity and trace gases (CO2, CH4, N2O) metabolism: a review [J]. Biodiv Sci, 2003, 11(4): 322-332.
[8] ZHANG Jia-En. The scope and content of study on soil biodiversity and its sustainable exploitation [J]. Biodiv Sci, 1999, 07(2): 140-144.
Full text



[1] Gui Ji-xun, Zhu Ting-cheng. Study of Energy Flow Between Litter and Decomposers in Aneurolepidium chinese Grassland[J]. Chin J Plan Ecolo, 1992, 16(2): 143 -148 .
[2] Meixia Zhang, Yan Luo, Zhengbing Yan, Jiao Chen, Anwar Eziz, Kaihui Li and Wenxuan Han. Resorptions of 10 mineral elements in leaves of desert shrubs and their contrasting responses to aridity[J]. J Plant Ecol, 2019, 12(2): 358 -366 .
[3] MENG Ying-, YANG Yong-Ping. Chromosome Atlas of Eight Asteraceae Species from the Qinghai-Tibet Plateau[J]. Plant Diversity, 2013, 35(3): 361 -366 .
[4] Trevor Wang, Cristobal Uauy, Brad Till, and Chun-Ming Liu. TILLING and Associated Technologies[J]. J Integr Plant Biol, 2010, 52(11): 1027 -1030 .
[5] Hai-Lin Qin, An-Jun Deng, Guan-Hua Du, Peng Wang, Jin-Lan Zhang and Zhi-Hong Li. Fingerprinting Analysis of Rhizoma Chuanxiong of Commercial Types using 1H Nuclear Magnetic Resonance Spectroscopy and High Performance Liquid Chromatography Method[J]. J Integr Plant Biol, 2009, 51(6): 537 -544 .
[6] Scott A. Heckathorn and Jiquan Chen. Plants and Global Environmental Change: A Special Issue Highlighting Younger Scientists[J]. J Integr Plant Biol, 2008, 50(11): 1337 -1338 .
[7] MENG Meng, NI Jian, ZHANG Zhi-Guo. ARIDITY INDEX AND ITS APPLICATIONS IN GEO-ECOLOGICAL STUDY[J]. Chin J Plan Ecolo, 2004, 28(6): 853 -861 .
[8] YANG Qin-Er. Cytology of eleven species in the genus Ranunculus L. and five in its four related genera from China[J]. J Syst Evol, 2001, 39(5): 405 -422 .
[9] HE Feng WU Zhen-Bin. Application of Aquatic Plants in Sewage Treatment and Water Quality Improvement[J]. Chin Bull Bot, 2003, 20(06): 641 -647 .
[10] CHENG Han-Ting,LI Qin-Fen,LIU Jing-Kun,YAN Ting-Liang,ZHANG Qiao-Yan,WANG Jin-Chuang. Seasonal changes of photosynthetic characteristics of Alpinia oxyphylla growing under Hevea brasiliensis[J]. Chin J Plan Ecolo, 2018, 42(5): 585 -594 .