Plant and Soil

, Volume 367, Issue 1–2, pp 437–447 | Cite as

Intermediate herbivory intensity of an aboveground pest promotes soil labile resources and microbial biomass via modifying rice growth

  • Jinghua Huang
  • Manqiang Liu
  • Xiaoyun Chen
  • Jing Chen
  • Fajun Chen
  • Huixin Li
  • Feng Hu
Regular Article


Background and Aims

The importance of aboveground herbivores for modifying belowground ecosystems has prompted numerous studies; however, studies can be biased by context dependent conditions which lead to extremely inconsistent results. So far, the impacts of herbivory intensity by important rice pests on rice paddy soil ecosystems are lacking. The aim of this study was to test the hypothesis that intermediate herbivory intensity of the brown planthopper (Nilaparvata lugens Stål) could promote soil labile resources and microbial biomass, while high intensity would show a reverse pattern, by mediating rice plant growth. This study will also help the development of integrative pest management.


Four hopper infestation density treatments (0, 4, 8 and 12 nymphs per rice plant) and two infestation duration treatments (9 and 15 days after N. lugens infestation, DAI 9 and DAI 15) were established in a glasshouse experiment. Soil and plant were sampled destructively from four replicates and analysed for soil labile resources availability, soil microbial biomass and plant performance, respectively.


The infestation density significantly affected both shoot and root mass of rice (P < 0.05), soil dissolved organic carbon (DOC) and nitrogen (DON), and microbial biomass carbon (MBC) and nitrogen (MBN), and the effects were further enhanced by prolonged infestation duration. Compared to the control (CK) without N. lugens, plant dry mass, DOC, DON, MBC and MBN increased under low (LD) and moderate hopper densities (MD) but decreased under high density (HD) on DAI 9. Moreover, the LD treatment exerted the most promotional effects on DAI 15. Rice root to shoot ratio generally increased in treatments subjected to herbivory. The labile resources and microbial biomass showed close relationships with both shoot and root mass across treatments, in particular with root mass on DAI 15. Such a trend indicated that the shift of photosynthate allocation to belowground contributed to changes of soil resource availability and microbial biomass.


Intermediate herbivory intensity showed positive effects on rice seedling performance and, further, promoted soil labile resource availability and microbial biomass. The importance of extrapolating temporal and spatial scale, i.e. from the short-term greenhouse experiment to an entire rice growing season in the field, was highlighted.


Aboveground herbivore Belowground Nilaparvata lugens Herbivory density Infestation duration Soil microbial biomass Resource availability 



Days after N. lugens infestation


Soil dissolved organic carbon


Soil dissolved organic nitrogen


Soil microbial biomass carbon


Soil microbial biomass nitrogen


Low hopper density


Moderate hopper density


High hopper density



This study was supported by the National Foundation of Sciences in China (31170487), National Key Basic Research Program of China (Grant No. 2010CB126200), the Fundamental Research Funds for the Central Universities and the PADA (Priority Academic Program Development of Jiangsu Higher Education Institutions). We thank Mr. Feng Wang and Miss Ying Tang for their laboratory work. We also thank Dr. Bryan Griffiths (SAC, Edinburgh, UK) and Dr. Anne Baily (Teagasc, Wexford, Ireland) for editing the manuscript.


  1. Alagar M, Suresh S, Samiyappan R, Saravanakumar D (2007) Reaction of resistant and susceptible rice genotypes against brown planthopper (Nilaparvata lugens). Phytoparasitica 35:346–356CrossRefGoogle Scholar
  2. Bagchi S, Ritchie ME (2010) Herbivore effects on above- and belowground plant production and soil nitrogen availability in the Trans-Himalayan shrub-steppes. Oecologia 164:1075–1082PubMedCrossRefGoogle Scholar
  3. Bardgett RD, Wardle DA (2003) Herbivore-mediated linkages between aboveground and belowground communities. Ecology 84:2258–2268CrossRefGoogle Scholar
  4. Bazot S, Mikola J, Nguyen C, Robin C (2005) Defoliation-induced changes in carbon allocation and root soluble carbon concentration in field-grown Lolium perenne plants: do they affect carbon availability, microbes and animal trophic groups in soil? Funct Ecol 19:886–896CrossRefGoogle Scholar
  5. Bezemer TM, Van Dam NM (2005) Linking aboveground and belowground interactions via induced plant defenses. Trends Ecol Evol 20:617–624PubMedCrossRefGoogle Scholar
  6. Birch ANE, Begg GS, Squire GR (2011) How agro-ecological research helps to address food security issues under new IPM and pesticide reduction policies for global crop production systems. J Exp Bot 62:3251–3261CrossRefGoogle Scholar
  7. Bottrell DG, Schoenly KG (2012) Resurrecting the ghost of green revolutions past: the brown planthopper as a recurring threat to high-yielding rice production in tropical Asia. J Asia Pac Entomol 15:122–140CrossRefGoogle Scholar
  8. Carvalho PCD, Anghinoni I, de Moraes A, de Souza ED, Sulc RM, Lang CR, Flores JPC, Lopes MLT, da Silva JLS, Conte O, Wesp CD, Levien R, Fontaneli RS, Bayer C (2010) Managing grazing animals to achieve nutrient cycling and soil improvement in no-till integrated systems. Nutr Cycl Agroecosyst 88:259–273CrossRefGoogle Scholar
  9. Chen JM (2004) Tolerance of rice varieties to the brown planthopper, Nilaparvata lugens(Stål) and its physiological mechanism. PhD dissertation, Zhejiang University, China (in Chinese with English abstract)Google Scholar
  10. Cheng J (2009) Rice planthopper problems and relevant causes in China. In: Heong KL, Hardy B (eds) Planthoppers: new threats to the sustainability of intensive rice production systems in Asia. The International Rice Research Institute (IRRI), Los Baños, pp 157–178Google Scholar
  11. Classen AT, Chapman SK, Whitham TG, Hart SC, Koch GW (2007) Genetic-based plant resistance and susceptibility traits to herbivory influence needle and root litter nutrient dynamics. J Ecol 95:1181–1194CrossRefGoogle Scholar
  12. De Deyn GB, van Ruijven J, Raaijmakers CE, de Ruiter PC, van der Putten WH (2007) Above- and belowground insect herbivores differentially affect soil nematode communities in species-rich plant communities. Oikos 116:923–930CrossRefGoogle Scholar
  13. Eisenhauer N (2012) Aboveground-belowground interactions as a source of complementarity effects in biodiversity experiments. Plant Soil 351:1–22CrossRefGoogle Scholar
  14. Fanselow N, Schonbach P, Gong XY, Lin S, Taube F, Loges R, Pan QM, Dittert K (2011) Short-term regrowth responses of four steppe grassland species to grazing intensity, water and nitrogen in Inner Mongolia. Plant Soil 340:279–289CrossRefGoogle Scholar
  15. FAO (2010) Food outlook – global market analysis.
  16. Frost CJ, Hunter MD (2008) Herbivore-induced shifts in carbon and nitrogen allocation in red oak seedlings. New Phytol 178:835–845PubMedCrossRefGoogle Scholar
  17. Fu Q, Zhang ZT, Hu C, Zhu ZW, Lai FX (2001) Effects of dietary amino acids on free amino acid pools in the body and honeydew of the brown planthopper. Nilaparvata lugens. Chin J Rice Sci 15:298–302 (in Chinese with English abstract)Google Scholar
  18. Guitian R, Bardgett RD (2000) Plant and soil microbial responses to defoliation in temperate semi-natural grassland. Plant Soil 220:271–277CrossRefGoogle Scholar
  19. Hamilton EW, Frank DA (2001) Can plants stimulate soil microbes and their own nutrient supply? Evidence from a grazing tolerant grass. Ecology 82:2397–2402CrossRefGoogle Scholar
  20. Hamilton EW, Frank DA, Hinchey PM, Murray TR (2008) Defoliation induces root exudation and triggers positive rhizospheric feedbacks in a temperate grassland. Soil Biol Biochem 40:2865–2873CrossRefGoogle Scholar
  21. Harrison KA, Bardgett RD (2004) Browsing by red deer negatively impacts on soil nitrogen availability in regenerating native forest. Soil Biol Biochem 36:115–126CrossRefGoogle Scholar
  22. Heil M (2011) Plant-mediated interactions between above- and below-ground communities at multiple trophic levels. J Ecol 99:3–6CrossRefGoogle Scholar
  23. Hladun KR, Adler LS (2009) Influence of leaf herbivory, root herbivory, and pollination on plant performance in Cucurbita moschat. Ecol Entomol 34:144–152CrossRefGoogle Scholar
  24. Holland JN, Cheng W, Crossley DA (1996) Herbivore-induced changes in plant carbon allocation: assessment of below-ground C fluxes using carbon-14. Oecologia 107:87–94CrossRefGoogle Scholar
  25. Hopkins DW, Gregorich EG (2005) Carbon as a substrate for soil organisms. In: Bardgett RD, Usher MB, Hopkins DW (eds) Biological diversity and function in soils. Cambridge University Press, Cambridge, pp 57–79CrossRefGoogle Scholar
  26. Horne PA, Page J (2008) Integrated pest management for crops and pastures. Landlinks Press, MelbourneGoogle Scholar
  27. Huang J, Liu M, Chen F, Griffiths BS, Chen X, Johnson SN, Hu F (2012) Crop resistance traits modify the effects of an aboveground herbivore, brown planthopper, on soil microbial biomass and nematode community via changes to plant performance. Soil Biol Biochem 49:157–166CrossRefGoogle Scholar
  28. Hyodo F, Kohzu A, Tayasu I (2010) Linking aboveground and belowground food webs through carbon and nitrogen stable isotope analyses. Ecol Res 25:745–756CrossRefGoogle Scholar
  29. Ilmarinen K, Mikola J, Nieminen M, Vestberg M (2005) Does plant growth phase determine the response of plants and soil organisms to defoliation? Soil Biol Biochem 37:433–443CrossRefGoogle Scholar
  30. Joergensen RG (1995) Microbial biomass. In: Alef K, Nannipieri P (eds) Methods in applied soil microbiology and biochemistry. Academic, New York, pp 375–417CrossRefGoogle Scholar
  31. Kaplan I, Halitschke R, Kessler A, Rehill BJ, Sardanelli S, Denno RF (2008) Physiological integration of roots and shoots in plant defense strategies links above- and belowground herbivory. Ecol Lett 11:841–851PubMedCrossRefGoogle Scholar
  32. Kaye JP, Hart SC (1997) Competition for nitrogen between plants and soil microorganisms. Trends Ecol Evol 12:139–143PubMedCrossRefGoogle Scholar
  33. Klumpp K, Fontaine S, Attard E, Le Roux X, Gleixner G, Soussana JF (2009) Grazing triggers soil carbon loss by altering plant roots and their control on soil microbial community. J Ecol 97:876–885CrossRefGoogle Scholar
  34. le Mellec A, Habermann M, Michalzik B (2009) Canopy herbivory altering C to N ratios and soil input patterns of different organic matter fractions in a Scots pine forest. Plant Soil 325:255–262CrossRefGoogle Scholar
  35. le Mellec A, Gerold G, Michalzik B (2011) Insect herbivory, organic matter deposition and effects on belowground organic matter fluxes in a central European oak forest. Plant Soil 342:393–403CrossRefGoogle Scholar
  36. Lessard J-P, Reynolds WN, Bunn WA, Genung MA, Cregger MA, Felker-Quinn E, Barrios-Garcia MN, Stevenson ML, Lawton RM, Brown CB, Patrick M, Rock JH, Jenkins MA, Bailey JK, Schweitzer JA (2012) Equivalence in the strength of deer herbivory on above and below ground communities. Basic Appl Ecol 13:59–66CrossRefGoogle Scholar
  37. Liu YS, Pan QM, Liu HD, Bai YF, Simmons M, Dittert K, Han XG (2011) Plant responses following grazing removal at different stocking rates in an Inner Mongolia grassland ecosystem. Plant Soil 340:199–213CrossRefGoogle Scholar
  38. Liu N, Zhang Y, Chang S, Kan H, Lin L (2012) Impact of grazing on soil carbon and microbial biomass in typical Steppe and Desert Steppe of Inner Mongolia. PLoS One 7:e36434PubMedCrossRefGoogle Scholar
  39. Macdonald LM, Paterson E, Dawson LA, McDonald AJS (2004) Short-term effects of defoliation on the soil microbial community associated with two contrasting Lolium perenne cultivars. Soil Biol Biochem 36:489–498CrossRefGoogle Scholar
  40. Mikola J, Nieminen M, Ilmarinen K, Vestberg M (2005) Belowground responses by AM fungi and animal trophic groups to repeated defoliation in an experimental grassland community. Soil Biol Biochem 37:1630–1639CrossRefGoogle Scholar
  41. Mikola J, Setälä H, Virkajärvi P, Saarijärvi K, Ilmarinen K, Voigt W, Vestberg M (2009) Defoliation and patchy nutrient return drive grazing effects on plant and soil properties in a dairy cow pasture. Ecol Monogr 79:221–224CrossRefGoogle Scholar
  42. Mollah MLR, Hossain MA, Samad MA, Khatun MF (2011) Settling and feeding responses of brown planthopper to five rice cultivars. Int J Sustain Crop Prod 6:10–13Google Scholar
  43. Murray PJ, Ostle N, Kenny C, Grant H (2004) Effect of defoliation on patterns of carbon exudation from Agrostis capillaris. J Plant Nutr Soil Sci 167:487–493CrossRefGoogle Scholar
  44. Olsen YS, Dausse A, Garbutt A, Ford H, Thomas DN, Jones DL (2011) Cattle grazing drives nitrogen and carbon cycling in a temperate salt marsh. Soil Biol Biochem 43:531–541CrossRefGoogle Scholar
  45. Pastore AI, Russell FL (2012) Insect herbivore effects on resource allocation to shoots and roots in Lespedeza capitata. Plant Ecol 213:843–851CrossRefGoogle Scholar
  46. Paterson E, Sim A (1999) Rhizodeposition and C-partitioning of Lolium perenne in axenic culture affected by nitrogen supply and defoliation. Plant Soil 216:155–164CrossRefGoogle Scholar
  47. Peng Y, Jiang G, Liu X, Niu S, Liu M, Biswas DK (2007) Photosynthesis, transpiration and water use efficiency of four plant species with grazing intensities in Hunshandak Sandland, China. J Arid Environ 70:304–315CrossRefGoogle Scholar
  48. Qi S, Zheng HX, Lin QM, Li GT, Xi ZH, Zhao XR (2011) Effects of livestock grazing intensity on soil biota in a semiarid steppe of Inner Mongolia. Plant Soil 340:117–126CrossRefGoogle Scholar
  49. Qiu HM, Wu JC, Yang GQ, Dong B, Li DH (2004) Changes in the uptake function of the rice root to nitrogen, phosphorus and potassium under brown planthopper, Nilaparvata lugens (Stål) (Homoptera: Delphacidae) and pesticide stresses, and effect of pesticides on rice-grain filling in field. Crop Prot 23:1041–1048CrossRefGoogle Scholar
  50. Rubia-Sanchez E, Suzuki Y, Miyamoto K, Watanabe T (1999) The potential for compensation of the effects of the brown planthopper Nilaparvata lugens Stål (Homoptera: Delphacidae) feeding on rice. Crop Prot 18:39–45CrossRefGoogle Scholar
  51. Rubia-Sanchez E, Suzuki Y, Arimura K, Miyamoto K, Matsumura M, Watanabe T (2003) Comparing Nilaparvata lugens (Stål) and Sogatella furcifera (Horvath) (Homoptera: Delphacidae) feeding effects on rice plant growth processes at the vegetative stage. Crop Prot 22:967–974CrossRefGoogle Scholar
  52. Saj S, Mikola J, Ekelund F (2008) Legume defoliation affects rhizosphere decomposers, but not the uptake of organic matter N by a neighbouring grass. Plant Soil 311:141–149CrossRefGoogle Scholar
  53. Schonbach P, Wan HW, Gierus M, Bai YF, Muller K, Lin LJ, Susenbeth A, Taube F (2011) Grassland responses to grazing: effects of grazing intensity and management system in an Inner Mongolian steppe ecosystem. Plant Soil 340:103–115CrossRefGoogle Scholar
  54. Shan YM, Chen DM, Guan XX, Zheng SX, Chen HJ, Wang MJ, Bai YF (2011) Seasonally dependent impacts of grazing on soil nitrogen mineralization and linkages to ecosystem functioning in Inner Mongolia grassland. Soil Biol Biochem 43:1943–1954CrossRefGoogle Scholar
  55. Sinka M, Jones TH, Hartley SE (2009) Collembola respond to aphid herbivory but not to honeydew addition. Ecol Entomol 34:588–594CrossRefGoogle Scholar
  56. Sthultz CM, Whitham TG, Kennedy K, Deckert R, Gehring CA (2009) Genetically based susceptibility to herbivory influences the ectomycorrhizal fungal communities of a foundation tree species. New Phytol 184:657–667PubMedCrossRefGoogle Scholar
  57. Tang Y, Liu MQ, Wang F, Chen FJ, Shao B, Su Y, Ge C, Huang JH, Li HX, Hu F (2010) Herbivory by the brown planthopper (Nilaparvata lugens) affects rice seedling growth and belowground soil labile organic carbon and nitrogen fractions. Acta Ecol Sin 30:2890–2898 (in Chinese with English abstract)Google Scholar
  58. Van der Putten WH, Bardgett RD, de Ruiter PC, Hol WHG, Meyer KM, Bezemer TM, Bradford MA, Christensen S, Eppinga MB, Fukami T, Hemerik L, Molofsky J, Schädler M, Scherber C, Strauss SY, Vos M, Wardle DA (2009) Empirical and theoretical challenges in aboveground-belowground ecology. Oecologia 161:1–14PubMedCrossRefGoogle Scholar
  59. Vance ED, Brookes PC, Jenkinson DS (1987) An extraction method for measuring soil microbial biomass C. Soil Biol Biochem 19:703–707CrossRefGoogle Scholar
  60. Vandegehuchte ML, Pena E, Bonte D (2010) Interactions between root and shoot herbivores of Ammophila arenaria in the laboratory do not translate into correlated abundances in the field. Oikos 119:1011–1019CrossRefGoogle Scholar
  61. Wang Y, Wang X, Yuan H, Chen R, Zhu L, He R, He G (2008) Responses of two contrasting genotypes of rice to brown planthopper. Mol Plant Microbe Interact 21:122–132PubMedCrossRefGoogle Scholar
  62. Wardle DA, Bardget RD, Klironomos JN, Setälä H, Van der Putten WH, Wall DH (2004a) Ecological linkages between aboveground and belowground biota. Science 304:1629–1633PubMedCrossRefGoogle Scholar
  63. Wardle DA, Yeates GW, Williamson WM, Bonner KI, Baker GM (2004b) Linking aboveground and belowground communities: the indirect influence of aphid species identity and diversity on a three trophic level soil food web. Oikos 107:283–294CrossRefGoogle Scholar
  64. Watanabe T, Kitagawa H (2000) Photosynthesis and translocation of assimilates in rice plants following phloem feeding by the planthopper Nilaparvata lugens (Homoptera: Delphacidae). J Econ Entomol 93:1192–1198PubMedCrossRefGoogle Scholar
  65. Wearn JA, Gange AC (2007) Above-ground herbivory causes rapid and sustained changes in mycorrhizal colonization of grasses. Oecologia 153:959–971PubMedCrossRefGoogle Scholar
  66. Wu JC, Qiu HM, Yang GQ, Dong B, Gu HN (2003) Nutrient uptake of rice roots in response to infestation of Nilaparvata lugens (Stål) (Homoptera: Delphacidae). J Econ Entomol 96:1798–1804PubMedCrossRefGoogle Scholar
  67. Yadav DS, Chander S (2010) Simulation of rice planthopper damage for developing pest management decision support tools. Crop Prot 29:267–276CrossRefGoogle Scholar
  68. Yoshida S, Forno DA, Cock JH, Gomez K (1976) Laboratory manual for physiological studies of rice, 3rd edn. The International Rice Research Institute (IRRI), Los Baños, pp 61–64Google Scholar
  69. Zhou XQ, Wang JZ, Hao YB, Wang YF (2010) Intermediate grazing intensities by sheep increase soil bacterial diversities in an Inner Mongolian steppe. Biol Fertil Soils 46:817–824CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media Dordrecht 2012

Authors and Affiliations

  • Jinghua Huang
    • 1
  • Manqiang Liu
    • 1
  • Xiaoyun Chen
    • 1
  • Jing Chen
    • 1
  • Fajun Chen
    • 2
  • Huixin Li
    • 1
  • Feng Hu
    • 1
  1. 1.Soil Ecology Lab, College of Resources and Environmental SciencesNanjing Agricultural UniversityNanjingPeople’s Republic of China
  2. 2.Department of Entomology, College of Plant ProtectionNanjing Agricultural UniversityNanjingPeople’s Republic of China

Personalised recommendations