, 167:771 | Cite as

The variable effects of soil nitrogen availability and insect herbivory on aboveground and belowground plant biomass in an old-field ecosystem

  • Jarrod D. Blue
  • Lara Souza
  • Aimée T. Classen
  • Jennifer A. Schweitzer
  • Nathan J. Sanders
Community ecology - Original Paper


Nutrient availability and herbivory can regulate primary production in ecosystems, but little is known about how, or whether, they may interact with one another. Here, we investigate how nitrogen availability and insect herbivory interact to alter aboveground and belowground plant community biomass in an old-field ecosystem. In 2004, we established 36 experimental plots in which we manipulated soil nitrogen (N) availability and insect abundance in a completely randomized plot design. In 2009, after 6 years of treatments, we measured aboveground biomass and assessed root production at peak growth. Overall, we found a significant effect of reduced soil N availability on aboveground biomass and belowground plant biomass production. Specifically, responses of aboveground and belowground community biomass to nutrients were driven by reductions in soil N, but not additions, indicating that soil N may not be limiting primary production in this ecosystem. Insects reduced the aboveground biomass of subdominant plant species and decreased coarse root production. We found no statistical interactions between N availability and insect herbivory for any response variable. Overall, the results of 6 years of nutrient manipulations and insect removals suggest strong bottom-up influences on total plant community productivity but more subtle effects of insect herbivores on aspects of aboveground and belowground production.


Community structure Insect herbivory Old-field ecosystems Soil nitrogen Top-down 



We thank Phillip Allen, Jacqueline Areson, Lauren Breza, Claire Brown, Windy A. Bunn, Karianne Chung, Melissa Cregger, Cavenne Engle, Colleen Iversen, Jean-Philippe Lessard, Laura Marsh, Martin Nuñez, Mariano Rodriguez-Cabal, Noelia Barrios, Tara Sackett, Tander Simberloff, Haley Smith, Katie Stuble, Heather Tran, Jeramy Webb, Jake Weltzin, and Phoebe Wright for help with field and laboratory work. Jake Weltzin was integral in establishing the experiment. The experiments described here complied with the current laws of the US. The work was partially supported by grants from Department of Ecology and Evolutionary Department at the University of Tennessee to J.B.

Supplementary material

442_2011_2028_MOESM1_ESM.doc (62 kb)
Supplementary material 1 (DOC 62 kb)


  1. Allred BW, Fuhlendorf SD, Monaco TA, Will RE (2010) Morphological and physiological traits in the success of the invasive plant Lespedeza cuneata. Biol Invasions 12:39–49CrossRefGoogle Scholar
  2. Bardgett RD, Wardle DA, Yeates GW (1998) Linking aboveground and belowground interactions: how plant responses to foliar herbivory influence soil organisms. Soil Biol Biochem 30:1867–1878CrossRefGoogle Scholar
  3. Bardgett RD, Bowman WD, Kaufmann R, Schmidt SK (2005) A temporal approach to linking aboveground and belowground ecology. Trends Ecol Evol 20:634–641PubMedCrossRefGoogle Scholar
  4. Bessler H, Temperton VM, Roscher C, Buchmann N, Schmid B, Schulze E, Weisser W, Engels C (2009) Aboveground overyielding in grassland mixtures in associated with reduced biomass partitioning to belowground organs. Ecology 90:1520–1530PubMedCrossRefGoogle Scholar
  5. Borer ET, Halpern BS, Seabloom EW (2006) Asymmetry in community regulation: effects of predators and productivity. Ecology 87:2813–2820PubMedCrossRefGoogle Scholar
  6. Brandon AL, Gibson DJ, Middleton BA (2004) Mechanisms for dominance in an early successional old field by the invasive non-native Lespedeza cuneata (Dum. Cours.) G. Don. Biol Invasions 6:483–493CrossRefGoogle Scholar
  7. Brown DG (1994) Beetle folivory increases resource availability and alters plant invasion in monocultures of goldenrod. Ecology 75:1673–1683CrossRefGoogle Scholar
  8. Buckland SM, Grime JP (2000) The effects of trophic structure and soil fertility on the assembly of plant communities: a microcosm experiment. Oikos 91:336–352CrossRefGoogle Scholar
  9. Canadell J, Jackson RB, Ehleringer JR, Mooney HA, Sala OE, Schulze ED (1996) Maximum rooting depth of vegetation types at the global scale. Oecologia 108:583–595CrossRefGoogle Scholar
  10. Carson WP, Root RB (2000) Herbivory and plant species coexistence: community regulation by an outbreaking phytophagous insect. Ecol Monogr 70:73–99CrossRefGoogle Scholar
  11. Chapman SK, Hart SC, Cobb NS, Whitham TG, Koch GW (2003) Insect herbivory increases litter quality and decomposition: an extension of the acceleration hypothesis. Ecology 84:2867–2876CrossRefGoogle Scholar
  12. 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
  13. Cleland EE, Harpole WS (2010) Nitrogen enrichment and plant communities. Ann NY Acad Sci 1195:46–61PubMedCrossRefGoogle Scholar
  14. Collins SL et al (2008) Rank clocks and plant community dynamics. Ecology 89:3534–3541PubMedCrossRefGoogle Scholar
  15. Coupe MD, Cahill JF (2003) Effects of insects on primary production in temperate herbaceous communities: a meta-analysis. Ecol Entomol 28:511–521CrossRefGoogle Scholar
  16. Coupe MD, Stacey JN, Cahill JF (2009) Limited effects of aboveground and belowground insects on community structure and function in a species-rich grassland. J Veg Sci 20:121–129CrossRefGoogle Scholar
  17. Craine JM, Reich PB, Tilman D, Ellesworth D, Fargione J, Knops J, Naeem S (2003) The role of plant species in biomass production and response to elevated CO2 and N. Ecol Lett 6:623–630CrossRefGoogle Scholar
  18. Craine JM, Morrow C, Fierer N (2007) Microbial nitrogen limitation increases decomposition. Ecology 88:2105–2113PubMedCrossRefGoogle Scholar
  19. Crawford KM, Crutsinger GM, Sanders NJ (2007) Host-plant genotypic diversity mediates the distribution of an ecosystem engineer. Ecology 88:2114–2120PubMedCrossRefGoogle Scholar
  20. Crawley MJ (1983) Herbivory: the dynamics of animal–plant interactions. Blackwell, OxfordGoogle Scholar
  21. Crutsinger GM, Souza L, Sanders NJ (2008) Intraspecific diversity and dominant genotypes resist plant invasions. Ecol Lett 11:16–23PubMedGoogle Scholar
  22. Cuevas E, Medina E (1983) Root production and organic matter decomposition in a tierra firme forest of the upper Rio Negro basin. In: Bohm W, Kutshera L, Lichtenberger E, Gumpenstein V (eds) Root ecology and its practical application. Gumpernstein, Austria. pp 653–666Google Scholar
  23. Cyr H, Pace ML (1993) Magnitude and patterns of herbivory in aquatic and terrestrial ecosystems. Nature 361:148–150CrossRefGoogle Scholar
  24. Del-Val E, Crawley MJ (2005) What limits herb biomass in grasslands: competition or herbivory. Oecologia 142:202–211PubMedCrossRefGoogle Scholar
  25. Diaz S, Symstad AJ, Chapin FS, Wardle DA, Huenneke LF (2003) Functional diversity revealed by removal experiments. Trends Ecol Evol 18:140–146CrossRefGoogle Scholar
  26. Dyer MI, Bokhari UG (1976) Plant-animal interactions: studies of the effects of grasshopper grazing on blue grama grass. Ecology 57:762–772CrossRefGoogle Scholar
  27. Eissenstat DM (1992) Costs and benefits of constructing roots of small diameter. J Plant Nutr 15:763–782CrossRefGoogle Scholar
  28. Elton CS (1927) Animal ecology. Sidgwick and Jackson, LondonGoogle Scholar
  29. Eyles A, Pinkard EA, Mohammed C (2009) Shifts in biomass and resource allocation patterns following defoliation in Eucalyptus globulus growing with varying water and nutrient supplies. Tree Phyl 29:753–764CrossRefGoogle Scholar
  30. Gao Y, Wang D, Ba L, Bai Y, Liu B (2008) Interactions between herbivory and resource availability on grazing tolerance of Leymus chinensis. Environ Exp Bot 63:113–122CrossRefGoogle Scholar
  31. Garten CT Jr, Classen AT, Norby RJ, Brice DJ, Weltzin JF, Souza L (2008) Role of N2-fixation in constructed old-field communities under different regimes of [CO2], temperature, and water availability. Ecosystems 11:125–137CrossRefGoogle Scholar
  32. Gruner DS, Smith JE, Seabloom EW, Sandin SA, Ngai JT, Hillebrand H, Harpole WS, Elser JJ, Cleland EE, Bracken MES, Borer ET, Bolker BM (2008) A cross-system synthesis of consumer and nutrient resource control on producer biomass. Ecol Lett 11:740–755PubMedCrossRefGoogle Scholar
  33. Hairston NG, Smith FE, Slobodkin LB (1960) Community structure, population control, and competition. Am Nat 94:421–425CrossRefGoogle Scholar
  34. Hillebrand H, Gruner DS, Borer ET, Bracken MES, Cleland EE, Elser JJ, Harpole WS, Ngai JT, Seabloom EW, Shurin JB, Smith JE (2007) Consumer versus resource control of producer diversity depends on ecosystem type and producer community structure. Proc Natl Acad Sci USA 104:10904–10909PubMedCrossRefGoogle Scholar
  35. Hooper DU, Chapin FS III, Ewel JJ, Hector A, Inchausti P, Lavorel S, Lawton JH, Lodge D, Loreau M, Naeem S, Schmid B, Setälä H, Symstad AJ, Vandermeer J, Wardle DA (2005) Effects of biodiversity on ecosystem functioning: a consensus of current knowledge. Ecol Monogr 75:3–35CrossRefGoogle Scholar
  36. Hunter MD (2001) Insect population dynamics meets ecosystem ecology: effects of herbivory on soil nutrient dynamics. Agric For Entomol 3:77–84CrossRefGoogle Scholar
  37. Kaplan I, Halitschke R, Kessler A, Rehill BJ, Sardanelli S, Denno RF (2008) Physiological integration of roots and shoots in plant defense strategies links aboveground and belowground herbivory. Ecol Lett 8:841–851CrossRefGoogle Scholar
  38. Kohyani PT, Bossuyt B, Bonte D, Hoffmann M (2009) Differential herbivory tolerance of dominant and subordinate plant species along gradients of nutrient availability and competition. Plant Ecol 201:611–619CrossRefGoogle Scholar
  39. Lane KE (2006) The structure and dynamics of arthropod communities in an old-field ecosystem. Thesis, Humboldt State University, ArcataGoogle Scholar
  40. Larson JL, Siemann E (1998) Legumes may be symbiont-limited during old-field succession. Am Midl Nat 140:90–95CrossRefGoogle Scholar
  41. Lauenroth WK (2000) Methods of estimating belowground net primary production. In: Sala OE, Jackson RB, Mooney HA, Howarth RW (eds) Methods in ecosystem science. Springer, New York, pp 58–69CrossRefGoogle Scholar
  42. LeBauer DS, Treseder KK (2008) Nitrogen limitation of net primary productivity in terrestrial ecosystems in globally distributed. Ecology 89:371–379PubMedCrossRefGoogle Scholar
  43. Maron JL, Crone E (2006) Herbivory: effects on plant abundance, distribution and population growth. Proc R Soc Lond B 273:2575–2584CrossRefGoogle Scholar
  44. Marshall JD, Waring RH (1985) Predicting fine root production and turnover by monitoring root starch and soil temperature. Can J For Res 15:791–800CrossRefGoogle Scholar
  45. McLendon T, Redente EF (1992) Effects of nitrogen limitation on species replacement dynamics during early secondary succession on a semiarid sagebrush site. Oecologia 91:312–317CrossRefGoogle Scholar
  46. Morghan KJR, Seastedt TR (1999) Effects of soil nitrogen reduction on nonnatibe plants in restored grasslands. Restor Ecol 7:51–55CrossRefGoogle Scholar
  47. Nadelhoffer KJ (2000) The potential effects of nitrogen deposition on fine-root production in forest ecosystems. New Phytol 147:131–139CrossRefGoogle Scholar
  48. Nishida T, Izumi N, Katayama N, Ohgushi T (2009) Short-term response of abuscular mycorrhizal association to spider mite herbivory. Popul Ecol 51:329–334CrossRefGoogle Scholar
  49. Oksanan L, Okasanen T (2000) The logic and realism of the hypothesis of exploitation ecosystems. Am Nat 155:703–723CrossRefGoogle Scholar
  50. Olson DM, Davis RF, Wackers FL, Rains GC, Potter T (2008) Plant-herbivore-carnivore interactions in cotton, Gossypium hirsutum: linking belowground and aboveground. J Chem Ecol 10:1341–1348CrossRefGoogle Scholar
  51. Phillips DH, Foss JE, Stiles CA, Trettin CC, Luxmoore RJ (2001) Soil-landscape relationships at the lower reaches of a watershed at Bear Creak near Oak Ridge, Tennessee. Castena 44:205–222Google Scholar
  52. Power ME (1992) Top-down and bottom-up forces in foodwebs: do plants have primacy? Ecology 73:733–746CrossRefGoogle Scholar
  53. Pucheta E, Bonamici I, Cabido M, Diaz S (2004) Belowground biomass and productivity of a grazed site and a neighboring ungrazed exclosure in a grassland in central Argentina. Austral Ecol 29:201–208CrossRefGoogle Scholar
  54. Root RB (1996) Herbivore pressure on goldenrods (Solidago altissima): its variation and cumulative effects. Ecology 77:1074–1087CrossRefGoogle Scholar
  55. Sanders NJ, Weltzin JF, Crutsinger GM, Fitzpatrick MC, Nuñez MA, Oswalt CM, Lane KE (2007) Insects mediate the effects of propagule supply and resource availability on a plant invasion. Ecology 89:2383–2391CrossRefGoogle Scholar
  56. Schädler M, Alphei J, Scheu S, Brandl R, Auge H (2004) Resource dynamics in an early-successional plant community are influenced by insect exclusion. Soil Biol Biochem 36:1817–1826CrossRefGoogle Scholar
  57. Schädler M, Rottstock T, Brandl R (2008) Do nutrients and invertebrate herbivory interact in an artificial plant community? Basic Appl Ecol 9:550–559CrossRefGoogle Scholar
  58. Schenk HJ, Jackson RB (2002) The global biogeography of roots. Ecol Monogr 72:311–328CrossRefGoogle Scholar
  59. Scherber C, Mwangi PN, Temperton VM, Roscher C, Schumacher J, Schmid B, Weisser WW (2006) Effects of plant diversity on invertebrate herbivory in experimental grassland. Oecologia 147:489–500PubMedCrossRefGoogle Scholar
  60. Schmitz OJ (2003) Top predator control of plant biodiversity and productivity in an old field ecosystem. Ecol Lett 6:156–163CrossRefGoogle Scholar
  61. Schmitz OJ (2006) Predators have large effects on ecosystem properties by changing plant diversity, not plant biomass. Ecology 87:1432–1437PubMedCrossRefGoogle Scholar
  62. Sih A, Crowley P, McPeek M, Petranka J, Strohmeier K (1985) Predation, competition, and prey communities: a review of field experiments. Annu Rev Ecol Syst 16:269–311CrossRefGoogle Scholar
  63. Souza L, Weltzin JF, Sanders NJ (2011) Differential effects of two dominant plant species on community structure and invasibility in an old field ecosystem. J Plant Ecol 3 (in press)Google Scholar
  64. Steen E (1984) Variation of root growth in a grass ley studied with a mesh bag technique. Swed J Agric Res 14:93–97Google Scholar
  65. Stein C, Unsicker SB, Kahmen A, Wagner M, Audorff V, Auge H, Prati D, Weisser WW (2010) Impact of invertebrate herbivory in grasslands depends on plant species diversity. Ecology 91:1639–1650PubMedCrossRefGoogle Scholar
  66. Throop HL (2005) Nitrogen deposition and herbivory affect biomass production and allocation in an annual plant. Oikos 111:91–100CrossRefGoogle Scholar
  67. Tscharntke T, Greiler HJ (1995) Insect communities, grasses, and grasslands. Annu Rev Entomol 40:535–558CrossRefGoogle Scholar
  68. Unsicker SB, Baer N, Kahmen A, Wagner M, Buchmann N, Weisser (2006) Invertebrate herbivory along a gradient of plant species diversity in extensively managed grasslands. Oecologia 150:233–246PubMedCrossRefGoogle Scholar
  69. Van der Putten WH, Vet LEM, Harvey JA, Wackers FL (2001) Linking aboveground and belowground multitrophic interactions of plants, herbivores, pathogens, and their antagonists. Trends Ecol Evol 16:547–554CrossRefGoogle Scholar
  70. Wang WJ, Baldocka JA, Dalala RC, Moody PW (2004) Decomposition dynamics of plant materials in relation to nitrogen availability and biochemistry determined by NME and wet-chemical analysis. Soil Biol Biochem 36:2045–2058CrossRefGoogle Scholar
  71. Wardle DA, Barker GA (1997) Competition and herbivory in establishing grassland communities: implications for plant biomass, species diversity and soil microbial activity. Oikos 80:470–480CrossRefGoogle Scholar
  72. Wardle DA, Bonner KI, Barker GM, Yeates GW, Nicholson KS, Bardgett RD, Watson RN, Ghani A (1999) Plant removals in perennial grassland: vegetation dynamics, decomposers, soil biodiversity, and ecosystem properties. Ecol Monogr 69:535–568CrossRefGoogle Scholar
  73. Wardle DA, Bonner KI, Barker GM (2000) Stability of ecosystem properties in response to abovegroundground functional group richness and composition. Oikos. 89:11–23CrossRefGoogle Scholar
  74. Wardle DA, Bardgett RD, Klironomos JN, Setälä H, Van der Putten WH, Wall DH (2004) Ecological linkages between aboveground and belowground biota. Science 304:1629–1633PubMedCrossRefGoogle Scholar
  75. Wedin D, Tilman D (1993) Competition among grasses along nitrogen gradient- initial conditions and mechanisms of competition. Ecol Monogr 173:199–229CrossRefGoogle Scholar
  76. Wilson SD, Gerry AK (1995) Strategies for mixed-grass prairie restoration: Herbicide, tilling, and nitrogen manipulation. Restor Ecol 3:290–298CrossRefGoogle Scholar
  77. Worm B, Lotze HK, Hillebrand H, Sommer U (2002) Consumer versus resource control of species diversity and ecosystem functioning. Nature 417:848–851PubMedCrossRefGoogle Scholar

Copyright information

© Springer-Verlag 2011

Authors and Affiliations

  • Jarrod D. Blue
    • 1
  • Lara Souza
    • 1
  • Aimée T. Classen
    • 1
  • Jennifer A. Schweitzer
    • 1
  • Nathan J. Sanders
    • 1
    • 2
  1. 1.Department of Ecology and Evolutionary BiologyUniversity of TennesseeKnoxvilleUSA
  2. 2.Department of Biology, Center for Macroecology, Climate, and EvolutionUniversity of CopenhagenCopenhagen ØDenmark

Personalised recommendations