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

doi:10.17520/biods.2019006

Abstract

Abstract:

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

Baijing Zhu, Jingrong Xue, Rong Xia, Miaomiao Jin, You Wu, Shanyi Tian, Xiaoyun Chen, Manqiang Liu, Feng Hu. Effect of soil nematode functional guilds on plant growth and aboveground herbivores[J]. Biodiv Sci, 2019, 27(4): 409-418.

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URL: https://www.biodiversity-science.net/EN/10.17520/biods.2019006

https://www.biodiversity-science.net/EN/Y2019/V27/I4/409

Figures/Tables 6

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

变异来源 Source of variation	茎叶 Shoot				根系 Root				褐飞虱数量 Brown planthoppers abundance
变异来源 Source of variation	生物量 Biomass	可溶性糖 Sugars	游离氨基酸 Amino acids	总酚 Phenolics	生物量 Biomass	可溶性糖 Sugars	游离氨基酸 Amino acids	总酚 Phenolics	褐飞虱数量 Brown planthoppers abundance
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.

References 51

[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
[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 URL
[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 URL
[4]	Bardgett RD, van der Putten WH (2014) Belowground biodiversity and ecosystem functioning. Nature, 515, 505-511. DOI URL
[5]	Barrios E (2007) Soil biota, ecosystem services and land productivity. Ecological Economics, 64, 269-285. DOI URL
[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 URL
[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 URL
[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 URL
[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 URL
[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 URL
[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 URL
[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 URL
[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 URL
[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
[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 URL
[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 URL
[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
[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 URL
[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 URL
[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 URL
[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 URL
[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 URL
[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 URL
[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 URL
[35]	Pineda A, Kaplan I, Bezemer TM (2017) Steering soil microbiomes to suppress aboveground insect pests. Trends in Plant Science, 22, 770-778. DOI URL
[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 URL
[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 URL
[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 URL
[41]	Wardle DA (2006) The influence of biotic interactions on soil biodiversity. Ecology Letters, 9, 870-886. DOI URL
[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 URL
[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 URL
[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 URL
[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 URL
[48]	Yemm EW, Cocking EC, Ricketts RE (1955) The determination of amino-acids with ninhydrin. Analyst, 80, 209-214. DOI URL
[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 URL
[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.