不同土壤线虫功能团对水稻生长及地上部植食者的影响
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摘要
探明土壤生物多营养级相互作用是了解生态功能调控机制的核心。本研究通过调控土壤线虫的典型功能团的完全交互设计(食微线虫有无、植食线虫有无、捕杂食线虫有无)探索了线虫功能团对水稻(Oryzasativa)生长及褐飞虱(Nilaparvata lugens)数量的影响。结果表明,与不接种线虫相比,植食线虫显著增加水稻根系生物量(P<0.05),显著增加其茎叶总酚含量(P <0.05);单独的食微线虫增加了褐飞虱数量(P <0.05),但显著降低水稻根系生物量(P <0.05);捕杂食线虫促进水稻茎叶生长,降低了褐飞虱数量;当食微、植食和捕杂食线虫同时存在时,植物茎叶及根系总酚含量均处于较高水平,暗示其抗虫潜力更强。总之,处于较高营养级的捕杂食线虫能够通过调控植食和食微线虫的数量,提高植物的防御能力,暗示土壤生物调控措施在植物地上部病原物防控方面有重要的前景。
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.
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.
引文
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Bardgett RD,van der Putten WH(2014)Belowground biodiversity and ecosystem functioning.Nature,515,505-511.
Barrios E(2007)Soil biota,ecosystem services and land productivity.Ecological Economics,64,269-285.
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.
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.
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.
Bj?rnlund L,Liu MQ,R?nn 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.
Bongers T(1988)De Nematoden Van Nederland.(in Dutch)Stichting Uitgeverij Koninklijke Nederlandse Natuurhistorische Vereniging,Utrecht.
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.
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.
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.
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.]
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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.
Faucon MP,Houben D,Lambers H(2017)Plant functional traits:Soil and ecosystem services.Trends in Plant Science,22,385-394.
Ferris H,Griffiths BS,Porazinska DL,Powers TO,Wang KH,Tenuta M(2012a)Reflections on plant and soil nematode ecology:Past,present and future.Journal of Nematology,44,115-126.
Ferris H,Sánchez-Moreno S,Brennan EB(2012b)Structure,functions and interguild relationships of the soil nematode assemblage in organic vegetable production.Applied Soil Ecology,61,16-25.
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.
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.
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.]
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.
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.]
Johnson SN,Clark KE,Hartley SE,Jones TH,Mckenzie SW,Koricheva J(2012)Aboveground-belowground herbivore interactions:A meta-analysis.Ecology,93,2208-2215.
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:Ameta-analytical review.Oikos,123,1409-1419.
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.]
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.
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.]
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.]
Milcu A,Allan E,Roscher C,Jenkins T,Meyer S T,Flynn D,Bessler H,Buscot F,Engels C,Gubsch M,K?nig 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.
Moretti M,Dias ATC,De Bello F,Altermatt F,Chown SL,Azcárate FM,Bell JR,Fournier B,Hedde M,Hortal J,Ibanez S,?ckinger E,Sousa JP,Ellers J,Berg MP(2017)Handbook of protocols for standardized measurement of terrestrial invertebrate functional traits.Functional Ecology,31,558-567.
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.
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.
Pineda A,Kaplan I,Bezemer TM(2017)Steering soil microbiomes to suppress aboveground insect pests.Trends in Plant Science,22,770-778.
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.]
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.
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.]
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.
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.
Wardle DA(2006)The influence of biotic interactions on soil biodiversity.Ecology Letters,9,870-886.
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