, Volume 184, Issue 3, pp 583–596 | Cite as

Plant–microbial competition for nitrogen increases microbial activities and carbon loss in invaded soils

Highlighted Student Research


Many invasive plant species show high rates of nutrient acquisition relative to their competitors. Yet the mechanisms underlying this phenomenon, and its implications for ecosystem functioning, are poorly understood, particularly in nutrient-limited systems. Here, we test the hypothesis that an invasive plant species (Microstegium vimineum) enhances its rate of nitrogen (N) acquisition by outcompeting soil organic matter-degrading microbes for N, which in turn accelerates soil N and carbon (C) cycling. We estimated plant cover as an indicator of plant N acquisition rate and quantified plant tissue N, soil C and N content and transformations, and extracellular enzyme activities in invaded and uninvaded plots. Under low ambient N availability, invaded plots had 77% higher plant cover and lower tissue C:N ratios, suggesting that invasion increased rates of plant N acquisition. Concurrent with this pattern, we observed significantly higher mass-specific enzyme activities in invaded plots as well as 71% higher long-term N availability, 21% lower short-term N availability, and 16% lower particulate organic matter N. A structural equation model showed that these changes were interrelated and associated with 27% lower particulate organic matter C in invaded areas. Our findings suggest that acquisition of N by this plant species enhances microbial N demand, leading to an increased flux of N from organic to inorganic forms and a loss of soil C. We conclude that high N acquisition rates by invasive plants can drive changes in soil N cycling that are linked to effects on soil C.


Invasive plants Nutrient uptake Soil carbon Enzyme activities Nitrogen limitation 



This project was supported by a grant from the National Science Foundation to the Coweeta Long Term Ecological Research (LTER) program (DEB-0,823,293), and by an Odell Soil Science Fellowship, Garden Club of Downer’s grove scholarship, and Spaeth-Boggess scholarship for M. Craig. We acknowledge S. Pearson for his expertise and guidance during field work. We thank M. Hamilton, E. McGrath, C. Grabowski, and J. Horton for their contributions to this work, and two anonymous reviewers and the Editor, Pascal Niklaus, for their helpful feedback on the manuscript. Finally, we thank the many landowners and agencies who allowed access to field sites.

Author contribution statement

MEC and JMF conceived and designed the study. MEC carried out the study and analyzed the data. MEC and JMF wrote the manuscript.

Supplementary material

442_2017_3861_MOESM1_ESM.docx (87 kb)
Supplementary material 1 (DOCX 88 kb)


  1. Allison SD, Vitousek PM (2004) Rapid nutrient cycling in leaf litter from invasive plants in Hawai’i. Oecologia 141:612–619CrossRefPubMedGoogle Scholar
  2. Arthur MA, Bray SR, Kuchle CR, Mcewan RW (2012) The influence of the invasive shrub, Lonicera maackii, on leaf decomposition and microbial community dynamics. Plant Ecol 213:1571–1582CrossRefGoogle Scholar
  3. Ashton IW, Hyatt LA, Howe KM, Gurevitch J, Manuel T (2005) Invasive species accelerate decomposition and litter nitrogen loss in a mixed deciduous forest. Ecol Appl 15:1263–1272CrossRefGoogle Scholar
  4. Barden LS (1987) Invasion of Microstegium vimineum (Poaceae), an exotic, annual, shade-tolerant, C4 grass, into a North Carolina floodplain. Am Midl Nat 118:40–45CrossRefGoogle Scholar
  5. Blagodatskaya EV, Blagodatsky SA, Anderson T, Kuzyakov Y (2007) Priming effects in Chernozem induced by glucose and N in relation to microbial growth strategies. Appl Soil Ecol 37:95–105CrossRefGoogle Scholar
  6. Bottollier-Curtet M, Planty-Tabacchi A-M, Tabacchi E (2013) Competition between young exotic invasive and native dominant plant species: implications for invasions within riparian areas. J Veg Sci 24:1033–1042CrossRefGoogle Scholar
  7. Bradford MA, DeVore JL, Maerz JC, McHugh JV, Smith CL, Strickland MS (2009) Native, insect herbivore communities derive a significant proportion of their carbon from a widespread invader of forest understories. Biol Invas 12:721–724CrossRefGoogle Scholar
  8. Bradford MA, Strickland MS, DeVore JL, Maerz JC (2012) Root carbon flow from an invasive plant to belowground foodwebs. Plant Soil 359:233–244CrossRefGoogle Scholar
  9. Castro-Díez P, Godoy O, Alonso A, Gallardo A, Saldaña A (2014) What explains variation in the impacts of exotic plant invasions on the nitrogen cycle? A meta-analysis. Ecol Lett 17:1–12CrossRefPubMedGoogle Scholar
  10. Chapman SK, Langley JA, Hart SC, Koch GW (2006) Plants actively control nitrogen cycling: uncorking the microbial bottleneck. New Phytol 169:27–34CrossRefPubMedGoogle Scholar
  11. Cheng L, Booker FL, Tu C, Burkey KO, Zhou L, Shew HD, Rufty TW, Hu S (2012) Arbuscular mycorrhizal fungi increase organic carbon decomposition under elevated CO2. Science 337:1084–1087CrossRefPubMedGoogle Scholar
  12. Cheplick GP, Fox J (2011) Density-dependent growth and reproduction of Microstegium vimineum in contrasting light environments. J Torrey Bot Soc 138:62–72CrossRefGoogle Scholar
  13. Corbett BF, Morrison JA (2012) The allelopathic potentials of the non-native invasive plant Microstegium vimineum and the native Ageratina altissima: two dominant species of the Eastern Forest herb layer. Northeast Nat 19:297–312CrossRefGoogle Scholar
  14. Craig ME, Pearson SM, Fraterrigo JM (2015) Grass invasion effects on forest soil carbon depend on landscape-level land use patterns. Ecology 96:2265–2279CrossRefPubMedGoogle Scholar
  15. Craine JM (2011) Resource strategies of wild plants. Princeton University Press, PrincetonGoogle Scholar
  16. Craine JM, Morrow C, Fierer N (2007) Microbial nitrogen limitation increases decomposition. Ecology 88:2105–2113CrossRefPubMedGoogle Scholar
  17. DeForest JL, Zak DR, Pregitzer KS, Burton AJ (2004) Atmospheric nitrate deposition and the microbial degradation of cellobiose and vanillin in a northern hardwood forest. Soil Biol Biochem 36:965–971CrossRefGoogle Scholar
  18. Demeester JE, Richter DD (2010) Differences in wetland nitrogen cycling between the invasive grass Microstegium vimineum and a diverse plant community. Ecol Appl 20:609–619CrossRefPubMedGoogle Scholar
  19. Drake JE, Darby BA, Giasson M, Kramer MA, Phillips RP, Finzi AC (2013) Stoichiometry constrains microbial response to root exudation- insights from a model and a field experiment in a temperate forest. Biogeosciences 10:821–838CrossRefGoogle Scholar
  20. Ehrenfeld JG, Kourtev P, Huang W (2001) Changes in soil functions following invasions of exoctic understory indeciduous forests. Ecol Appl 11:1287–1300CrossRefGoogle Scholar
  21. Fierer N, Schimel JP (2003) A proposed mechanism for the pulse in carbon dioxide production commonly observed following the rapid rewetting of a dry soil. Soil Sci Soc Am J 67:798–805CrossRefGoogle Scholar
  22. Finzi AC, Sinsabaugh RL, Long TM, Osgood MP (2006) Microbial community responses to atmospheric carbon dioxide enrichment in a warm-temperate forest. Ecosystems 9:215–226CrossRefGoogle Scholar
  23. Fontaine S, Bardoux G, Abbadie L, Mariotti A (2004) Carbon input to soil may decrease soil carbon content. Ecol Lett 7:314–320CrossRefGoogle Scholar
  24. Frank DA, Groffman PM (2009) Plant rhizospheric N processes: what we don’t know and why we should care. Ecology 90:1512–1519CrossRefPubMedGoogle Scholar
  25. Fraterrigo JM, Turner MG, Pearson SM, Dixon P (2005) Effects of past land use on spatial heterogeneity of soil nutrients in Southern Appalachian forests. Ecol Monogr 75:215–230CrossRefGoogle Scholar
  26. Fraterrigo JM, Balser TC, Turner MG (2006) Microbial community variation and its relationship with nitrogen mineralization in historically altered forests. Ecology 87:570–579CrossRefPubMedGoogle Scholar
  27. Fraterrigo JM, Strickland MS, Keiser AD, Bradford MA (2011) Nitrogen uptake and preference in a forest understory following invasion by an exotic grass. Oecologia 167:781–791CrossRefPubMedGoogle Scholar
  28. Fridley JD (2012) Extended leaf phenology and the autumn niche in deciduous forest invasions. Nature 485:359–362CrossRefPubMedGoogle Scholar
  29. Funk JL, Vitousek PM (2007) Resource-use efficiency and plant invasion in low-resource systems. Nature 446:1079–1081CrossRefPubMedGoogle Scholar
  30. Funk JL, Standish RJ, Stock WD, Valladares F (2016) Plant functional traits of dominant native and invasive species in Mediterranean-climate ecosystems. Ecology 97:75–83CrossRefPubMedGoogle Scholar
  31. Gallardo A, Schlesinger WH (1992) Carbon and nitrogen limitations of soil microbial biomass in desert ecosystems. Biogeochemistry 18:1–17CrossRefGoogle Scholar
  32. Geisseler D, Horwath WR, Joergensen RG, Ludwig B (2010) Pathways of nitrogen utilization by soil microorganisms: a review. Soil Biol Biochem 42:2058–2067CrossRefGoogle Scholar
  33. Grace JB (2006) Structural equation modelling and natural systems. Cambridge University Press, New YorkCrossRefGoogle Scholar
  34. 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
  35. Hamman OB, Rubia TDL, Martinez J (1997) Effect of carbon and nitrogen limitation on lignin peroxidase and manganese peroxidase production by Phanerochaete flavido-alba. J Appl Microbiol 83:751–757CrossRefGoogle Scholar
  36. Hart SC, Stark JM (1997) Nitrogen limitation of the microbial biomass in an old-growth forest soil. Ecoscience 4:91–98CrossRefGoogle Scholar
  37. Hawkes CV, Wren IF, Herman DJ, Firestone MK (2005) Plant invasion alters nitrogen cycling by modifying the soil nitrifying community. Ecol Lett 8:976–985CrossRefGoogle Scholar
  38. Heberling JM, Fridley JD (2013) Resource-use strategies of native and invasive plants in Eastern North American forests. New Phytol 200:523–533CrossRefPubMedGoogle Scholar
  39. Heneghan L, Fatemi F, Umek L, Grady K, Fagen K, Workman M (2006) The invasive shrub European buckthorn (Rhamnus cathartica, L.) alters soil properties in Midwestern U.S. woodlands. Appl Soil Ecol 32:142–148CrossRefGoogle Scholar
  40. Horton JL, Neufeld HS (1998) Photosynthetic responses of Microstegium vimineum (Trin.) A. Camus, a shade-tolerant, C4 grass, to variable light environments. Oecologia 114:11–19CrossRefPubMedGoogle Scholar
  41. Huebner CD (2010) Establishment of an invasive grass in closed-canopy deciduous forests across local and regional environmental gradients. Biol Invas 12:2069–2080CrossRefGoogle Scholar
  42. James JJ (2008) Leaf nitrogen productivity as a mechanism driving the success of invasive annual grasses under low and high nitrogen supply. J Arid Environ 72:1775–1784CrossRefGoogle Scholar
  43. Jo I, DA FridleyJD Frank (2016) More of the same? In situ leaf and root decomposition rates do not vary between 80 native and nonnative deciduous forest species. New Phytol 209:115–122CrossRefPubMedGoogle Scholar
  44. Jo I, Fridley JD, Frank DA (2015) Linking above- and belowground resource use strategies for native and invasive species of temperate deciduous forests. Biol Invas 17:1545–1554CrossRefGoogle Scholar
  45. Kaye JP, Hart SC (1997) Competition for nitrogen between plants and soil microorganisms. Trends Ecol Evol 12:139–143CrossRefPubMedGoogle Scholar
  46. Knops JMH, Bradley KL, Wedin DA (2002) Mechanisms of plant species impacts on ecosystem nitrogen cycling. Ecol Lett 5:454–466CrossRefGoogle Scholar
  47. Kourtev PS, Huang WZ, Ehrenfeld JG (1999) Differences in earthworm densities and nitrogen dynamics in soils under exotic and native plant species. Biol Invas 1:237–245CrossRefGoogle Scholar
  48. Kourtev PS, Ehrenfeld JG, Häggblom M (2002) Exotic plant species alter the microbial community structure and function in the soil. Ecology 83:3152–3166CrossRefGoogle Scholar
  49. Kourtev PS, Ehrenfeld JF, Ha M (2003) Experimental analysis of the effect of exotic and native plant species on the structure and function of soil microbial communities. Soil Biol Biochem 35:895–905CrossRefGoogle Scholar
  50. Kramer TD, Warren RJ, Tang Y, Bradford MA (2012) Grass invasions across a regional gradient are associated with declines in belowground carbon pools. Ecosystems 15:1271–1282CrossRefGoogle Scholar
  51. Kuzyakov Y, Xu X (2013) Competition between roots and microorganisms for nitrogen: mechanisms and ecological relevance. New Phytol 198:656–669CrossRefPubMedGoogle Scholar
  52. Laungani R, Knops JMH (2009) Species-driven changes in nitrogen cycling can provide a mechanism for plant invasions. P Natl Acad Sci USA 106:12400–12405CrossRefGoogle Scholar
  53. Lee MR, Flory SL, Phillips RP (2012) Positive feedbacks to growth of an invasive grass through alteration of nitrogen cycling. Oecologia 170:457–465CrossRefPubMedGoogle Scholar
  54. Lee MR, Tu C, Chen X, Hu S (2014) Arbuscular mycorrhizal fungi enhance P uptake and alter plant morphology in the invasive plant Microstegium vimineum. Biol Invas 16:1083–1093CrossRefGoogle Scholar
  55. Liao C, Peng R, Luo Y, Zhou X, Wu X, Fang C, Chen J, Li B (2008) Altered ecosystem carbon and nitrogen cycles by plant invasion: a meta-analysis. New Phytol 177:706–714CrossRefPubMedGoogle Scholar
  56. Manzoni S, Taylor P, Richter A, Porporato A, Agren GI (2012) Environmental and stoichiometric controls on microbial carbon-use efficiency in soils. New Phytol 196:79–91CrossRefPubMedGoogle Scholar
  57. Marriott EE, Wander MM (2006) Total and labile soil organic matter in organic and conventional farming systems. Soil Sci Soc Am J 70:950–959CrossRefGoogle Scholar
  58. McCormack ML, Dickie IA, Eissenstat DM, Fahey TJ, Fernandez CW, Guo D, Helmisaari H, Hobbie EA, Iversen CM, Jackson RB, Leppalammi-Kujansuu J, Norby RJ, Phillips RP, Pregitzer KS, Pritchard SG, Rewald B, Zadworny M (2015) Redefining fine roots improves understanding of below-ground contributions to terrestrial biosphere processes. New Phytol 207:505–518CrossRefPubMedGoogle Scholar
  59. McFarland JW, Waldrop MP, Haw M (2013) Extreme CO2 disturbance and the resilience of soil microbial communities. Soil Biol Biochem 65:274–286CrossRefGoogle Scholar
  60. McLeod ML, Cleveland CC, Lekberg Y, Maron JL, Philippot L, Bru D, Callaway RM (2016) Exotic invasive plants increase productivity, abundance of ammonia-oxidizing bacteria and nitrogen availability in intermountain grasslands. J Ecol 104:994–1002CrossRefGoogle Scholar
  61. Mooshammer M, Wanek W, Ha I, Fuchslueger L, Hofhansl F, Takriti M, Watzka M, Wild B, Keiblinger KM, Knoltsch A, Zechmeister-boltenstern S, Richter A (2014) Adjustment of microbial nitrogen use efficiency to carbon:nitrogen imbalances regulates soil nitrogen cycling. Nat Commun 5:4694CrossRefGoogle Scholar
  62. Moreau D, Pivato B, Bru D, Busset H, Deau F, Faivre C, Matejicek A, Stribik F, Philippot L, Mougel C (2015) Plant traits related to nitrogen uptake influence plant-microbe competition. Ecology 96:2300–2310CrossRefPubMedGoogle Scholar
  63. Piscitelli A, Giardina P, Lettera V, Pezzella C, Sannia G, Faraco V (2011) Induction and transcriptional regulation of laccases in fungi. Curr Genom 12:104–112CrossRefGoogle Scholar
  64. Pringle A, Bever JD, Gardes M, Parrent JL, Rillig MC, Klironomos JN (2009) Mycorrhizal Symbioses and Plant Invasions. Annu Rev Ecol Evol S 40:699–715CrossRefGoogle Scholar
  65. Reich PB (2014) The world-wide “fast–slow” plant economics spectrum: a traits manifesto. J Ecol 102:275–301CrossRefGoogle Scholar
  66. Roy J (1990) In search of the characteristics of plant invaders. In: Di Castri F, Hansen AJ, Debussche M (eds) Biological invasions in Europe and the Mediterranean basin. Kluwer Academic Publishers, Dordrecht, pp 333–352Google Scholar
  67. Scott NA, Surinder S, McIntosh PD (2001) Biogeochemical impact of Hieracium invasion in New Zealand’s grazed tussock grasslands: sustainability implications. Ecol Appl 11:1311–1322CrossRefGoogle Scholar
  68. Shannon-Firestone S, Reynolds HL, Phillips RP, Flory SL, Yannarell A (2015) The role of ammonium oxidizing communities in mediating effects of an invasive plant on soil nitrification. Soil Biol Biochem 90:266–274CrossRefGoogle Scholar
  69. Smith SE, Read DJ (2008) Mycorrhizal symbiosis, 3rd edn. Elsevier, New YorkGoogle Scholar
  70. Strickland MS, Devore JL, Maerz JC, Bradford MA (2010) Grass invasion of a hardwood forest is associated with declines in belowground carbon pools. Glob Change Biol 16:1338–1350CrossRefGoogle Scholar
  71. Tamura M, Tharayil N (2014) Plant litter chemistry and microbial priming regulate the accrual, composition and stability of soil carbon in invaded ecosystems. New Phytol 203:110–124CrossRefPubMedGoogle Scholar
  72. Van Kleunen M, Weber E, Fischer M (2010) A meta-analysis of trait differences between invasive and non-invasive plant species. Ecol Lett 13:235–245CrossRefPubMedGoogle Scholar
  73. Vila M, Weiner J (2004) Are invasive plant species better competitors than native plant species?: evidence from pair-wise experiments. Oikos 105:229–238CrossRefGoogle Scholar
  74. Vilà M, Espinar JL, Hejda M, Hulme PE, Jarošík V, Maron JL, Pergl J, Schaffner U, Sun Y, Pyšek P (2011) Ecological impacts of invasive alien plants: a meta-analysis of their effects on species, communities and ecosystems. Ecol Lett 14:702–708CrossRefPubMedGoogle Scholar
  75. Vitousek PM, Howarth RW (1991) Nitrogen limitation on land and in the sea: how can it occur? Biogeochemistry 13:87–115CrossRefGoogle Scholar
  76. Warren RJ, Wright JP, Bradford MA (2011) The putative niche requirements and landscape dynamics of Microstegium vimineum: an invasive Asian grass. Biol Invasions 13:471–483CrossRefGoogle Scholar
  77. Warren RJ, Bahn V, Bradford MA (2012) The interaction between propagule pressure, habitat suitability and density-dependent reproduction in species invasion. Oikos 121:874–881CrossRefGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2017

Authors and Affiliations

  1. 1.Department of Natural Resources and Environmental SciencesUniversity of Illinois at Urbana-ChampaignUrbanaUSA
  2. 2.Department of BiologyIndiana UniversityBloomingtonUSA

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