Biological Invasions

, Volume 18, Issue 8, pp 2349–2364 | Cite as

Nitrogen enrichment contributes to positive responses to soil microbial communities in three invasive plant species

  • Justin M. ValliereEmail author
  • Edith B. Allen
Original Paper


Increased resource availability and feedbacks with soil biota have both been invoked as potential mechanisms of plant invasion. Nitrogen (N) deposition can enhance invasion in some ecosystems, and this could be the result of increased soil N availability as well as shifts in soil biota. In a two-phase, full-factorial greenhouse experiment, we tested effects of N availability and N-impacted soil communities on growth responses of three Mediterranean plant species invasive in California: Bromus diandrus, Centaurea melitensis, and Hirschfeldia incana. In the first phase, plants were grown individually in pots and inoculated with sterile soil, soil from control field plots or soil from high N addition plots, and with or without supplemental N. In the second phase, we grew the same species in soils conditioned in the first phase. We hypothesized growth responses would differ across species due to species-specific relationships with soil biota, but overall increased N availability and N-impacted soil communities would enhance plant growth. In the first phase, Centaurea had the greatest growth response when inoculated with N-impacted soil, while Bromus and Hirschfeldia performed best in low N soil communities. However, in phase two all species exhibited positive growth responses in N-impacted soil communities under high N availability. While species may differ in responses to soil biota and N, growth responses to soils conditioned by conspecifics appear to be most positive in all species under high N availability and/or in soil communities previously impacted by simulated N deposition. Our results suggest N deposition could facilitate invasion due to direct impacts of soil N enrichment on plant growth, as well as through feedbacks with the soil microbial community.


Nitrogen deposition Plant–soil feedbacks Arbuscular mycorrhizal fungi Invasive species Coastal sage scrub 



We would like to thank Dr. Irina Irvine for field and logistical support. Dr. Michael Allen, Dr. Jodie Holt and Dr. Louis Santiago provided valuable feedback regarding the design of this experiment and Erin Reilly and Amanda Haraksin assisted with greenhouse and laboratory work. We greatly appreciate all their contributions to this project. We are also grateful to two anonymous reviewers for feedback on an earlier draft of this paper. This research was supported in part by the National Park Service Air Resources Division (TASK AGREEMENT NO. J8C07110022).


  1. Agrawal AA, Kotanen PM, Mitchell CE, Power AG, Godsoe W, Klironomos J (2005) Enemy release? An experiment with congeneric plant pairs and diverse above-and belowground enemies. Ecology 86:2979–2989CrossRefGoogle Scholar
  2. Allen EB, Padgett PE, Bytnerowicz A, Minnich R (1996) Nitrogen deposition effects on coastal sage vegetation of southern California. In: Bytnerowicz A, Arbaugh MJ, Schilling S (tech. coords) Proceedings of the international symposium on air pollution and climate change effects on forest ecosystems, Riverside, California. General Technical Report PSW-GTRGoogle Scholar
  3. Belnap J, Phillips SL, Sherrod SK, Moldenke A (2005) Soil biota can change after exotic plant invasion: does this affect ecosystem processes? Ecology 86:3007–3017CrossRefGoogle Scholar
  4. Bennett AE, Strauss SY (2013) Response to soil biota by native, introduced non-pest, and pest grass species: is responsiveness a mechanism for invasion? Biol Invasions 15:1343–1353CrossRefGoogle Scholar
  5. Bertrand H, Plassard C, Pinochet X, Touraine B, Normand P, Cleyet-Marel J (2000) Stimulation of the ionic transport system in Brassica napus by a plant growth-promoting rhizobacterium (Achromobacter sp.). Can J Microbiol 46:229–236CrossRefPubMedGoogle Scholar
  6. Bever JD (2002) Negative feedback within a mutualism: host-specific growth of mycorrhizal fungi reduces plant benefit. Proc R Soc Lond B Biol Sci 269:2595–2601CrossRefGoogle Scholar
  7. Bever JD, Westover KM, Antonovics J (1997) Incorporating the soil community into plant population dynamics: the utility of the feedback approach. J Ecol 85:561–573CrossRefGoogle Scholar
  8. Bonanomi G, Chiurazzi M, Caporaso S, Del Sorbo G, Moschetti G, Felice S (2008) Soil solarization with biodegradable materials and its impact on soil microbial communities. Soil Biol Biochem 40:1989–1998CrossRefGoogle Scholar
  9. Bozzolo FH, Lipson DA (2013) Differential responses of native and exotic coastal sage scrub plant species to N additions and the soil microbial community. Plant Soil 371:37–51CrossRefGoogle Scholar
  10. Bradley BA, Blumenthal DM, Wilcove DS, Ziska LH (2010) Predicting plant invasions in an era of global change. Trends Ecol Evol 25:310–318CrossRefPubMedGoogle Scholar
  11. Brooks ML (2003) Effects of increased soil nitrogen on the dominance of alien annual plants in the Mojave Desert. J Appl Ecol 40:344–353CrossRefGoogle Scholar
  12. Burke MJ, Grime J (1996) An experimental study of plant community invasibility. Ecology 77:776–790CrossRefGoogle Scholar
  13. Callaway R, Newingham B, Zabinski CA, Mahall BE (2001) Compensatory growth and competitive ability of an invasive weed are enhanced by soil fungi and native neighbours. Ecol Lett 4:429–433CrossRefGoogle Scholar
  14. Callaway RM, Mahall BE, Wicks C, Pankey J, Zabinski C (2003) Soil fungi and the effects of an invasive forb on grasses: neighbor identity matters. Ecology 84:129–135CrossRefGoogle Scholar
  15. Callaway RM, Thelen GC, Rodriguez A, Holben WE (2004) Soil biota and exotic plant invasion. Nature 427:731–733CrossRefPubMedGoogle Scholar
  16. Callaway RM et al (2008) Novel weapons: invasive plant suppresses fungal mutualists in America but not in its native Europe. Ecology 89:1043–1055CrossRefPubMedGoogle Scholar
  17. Chapin FS (1980) The mineral nutrition of wild plants. Annu Rev Ecol Syst 11:233–260CrossRefGoogle Scholar
  18. Cione NK, Padgett PE, Allen EB (2002) Restoration of a native shrubland impacted by exotic grasses, frequent fire, and nitrogen deposition in southern California. Restor Ecol 10:376–384. doi: 10.1046/j.1526-100X.2002.02038.x CrossRefGoogle Scholar
  19. Corkidi L, Rowland DL, Johnson NC, Allen EB (2002) Nitrogen fertilization alters the functioning of arbuscular mycorrhizas at two semiarid grasslands. Plant Soil 240:299–310. doi: 10.1023/A:1015792204633 CrossRefGoogle Scholar
  20. Cox RD, Preston KL, Johnson RF, Minnich RA, Allen EB (2014) Influence of landscape-scale variables on vegetation conversion to exotic annual grassland in southern California, USA. Glob Ecol Conserv 2:190–203CrossRefGoogle Scholar
  21. Davis MA, Grime JP, Thompson K (2000) Fluctuating resources in plant communities: a general theory of invasibility. J Ecol 88:528–534CrossRefGoogle Scholar
  22. de la Pena E, De Clercq N, Bonte D, Roiloa S, Rodríguez-Echeverría S, Freitas H (2010) Plant–soil feedback as a mechanism of invasion by Carpobrotus edulis. Biol Invasions 12:3637–3648CrossRefGoogle Scholar
  23. Dukes JS, Mooney HA (1999) Does global change increase the success of biological invaders? Trends Ecol Evol 14:135–139CrossRefPubMedGoogle Scholar
  24. Egerton-Warburton LM, Allen EB (2000) Shifts in arbuscular mycorrhizal communities along an anthropogenic nitrogen deposition gradient. Ecol Appl 10:484–496CrossRefGoogle Scholar
  25. Egerton-Warburton LM, Graham RC, Allen EB, Allen MF (2001) Reconstruction of the historical changes in mycorrhizal fungal communities under anthropogenic nitrogen deposition. Proc R Soc Lond B Biol Sci 268:2479–2484CrossRefGoogle Scholar
  26. Ehrenfeld JG, Ravit B, Elgersma K (2005) Feedback in the plant–soil system. Annu Rev Environ Resour 30:75–115CrossRefGoogle Scholar
  27. Elton CS (2000) The ecology of invasions by animals and plants. University of Chicago Press, ChicagoGoogle Scholar
  28. Fenn ME et al (2003) Ecological effects of nitrogen deposition in the western United States. Bioscience 53:404–420CrossRefGoogle Scholar
  29. Fenn ME et al (2010) Nitrogen critical loads and management alternatives for N-impacted ecosystems in California. J Environ Manag 91:2404–2423. doi: 10.1016/j.jenvman.2010.07.034 CrossRefGoogle Scholar
  30. Galloway JN et al (2004) Nitrogen cycles: past, present, and future. Biogeochemistry 70:153–226CrossRefGoogle Scholar
  31. Gerdemann J (1968) Vesicular–arbuscular mycorrhiza and plant growth. Annu Rev Phytopathol 6:397–418CrossRefGoogle Scholar
  32. Going BM, Hillerislambers J, Levine JM (2009) Abiotic and biotic resistance to grass invasion in serpentine annual plant communities. Oecologia 159:839–847CrossRefPubMedGoogle Scholar
  33. Goldstein LJ, Suding KN (2014) Applying competition theory to invasion: resource impacts indicate invasion mechanisms in California shrublands. Biol Invasions 16:191–203CrossRefGoogle Scholar
  34. Gustafson DJ, Casper BB (2004) Nutrient addition affects AM fungal performance and expression of plant/fungal feedback in three serpentine grasses. Plant Soil 259:9–17CrossRefGoogle Scholar
  35. 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
  36. Hilbig BE, Allen EB (2015) Plant–soil feedbacks and competitive interactions between invasive Bromus diandrus and native forb species. Plant Soil 392:1–13Google Scholar
  37. Hoeksema JD et al (2010) A meta-analysis of context-dependency in plant response to inoculation with mycorrhizal fungi. Ecol Lett 13:394–407CrossRefPubMedGoogle Scholar
  38. Huenneke LF, Hamburg SP, Koide R, Mooney HA, Vitousek PM (1990) Effects of soil resources on plant invasion and community structure in Californian serpentine grassland. Ecology 71:478–491CrossRefGoogle Scholar
  39. Innes L, Hobbs PJ, Bardgett RD (2004) The impacts of individual plant species on rhizosphere microbial communities in soils of different fertility. Biol Fert Soils 40:7–13CrossRefGoogle Scholar
  40. Johnson N, Graham JH, Smith F (1997) Functioning of mycorrhizal associations along the mutualism–parasitism continuum*. New Phytol 135:575–585CrossRefGoogle Scholar
  41. Johnson NC, Wilson GW, Bowker MA, Wilson JA, Miller RM (2010) Resource limitation is a driver of local adaptation in mycorrhizal symbioses. Proc Natl Acad Sci 107:2093–2098CrossRefPubMedPubMedCentralGoogle Scholar
  42. Kardol P, Martijn Bezemer T, van der Putten WH (2006) Temporal variation in plant–soil feedback controls succession. Ecol Lett 9:1080–1088CrossRefPubMedGoogle Scholar
  43. Kaye JP, Hart SC (1997) Competition for nitrogen between plants and soil microorganisms. Trends Ecol Evol 12:139–143CrossRefPubMedGoogle Scholar
  44. Keane RM, Crawley MJ (2002) Exotic plant invasions and the enemy release hypothesis. Trends Ecol Evol 17:164–170CrossRefGoogle Scholar
  45. Kimball S, Goulden ML, Suding KN, Parker S (2014) Altered water and nitrogen input shifts succession in a Southern California coastal sage community. Ecol Appl 24:1390–1404CrossRefGoogle Scholar
  46. Klironomos JN (2002) Feedback with soil biota contributes to plant rarity and invasiveness in communities. Nature 417:67–70CrossRefPubMedGoogle Scholar
  47. Klironomos JN (2003) Variation in plant response to native and exotic arbuscular mycorrhizal fungi. Ecology 84:2292–2301CrossRefGoogle Scholar
  48. Koske R, Gemma J (1989) A modified procedure for staining roots to detect VA mycorrhizas. Mycol Res 92:486–488CrossRefGoogle Scholar
  49. 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
  50. Kulmatiski A, Beard KH, Stevens JR, Cobbold SM (2008) Plant–soil feedbacks: a meta-analytical review. Ecol Lett 11:980–992CrossRefPubMedGoogle Scholar
  51. Levine JM, Vila M, Antonio CM, Dukes JS, Grigulis K, Lavorel S (2003) Mechanisms underlying the impacts of exotic plant invasions. Proc R Soc Lond B Biol Sci 270:775–781CrossRefGoogle Scholar
  52. Levine JM, Adler PB, Yelenik SG (2004) A meta-analysis of biotic resistance to exotic plant invasions. Ecol Lett 7:975–989CrossRefGoogle Scholar
  53. Levine JM, Pachepsky E, Kendall BE, Yelenik SG, Lambers JHR (2006) Plant–soil feedbacks and invasive spread. Ecol Lett 9:1005–1014CrossRefPubMedGoogle Scholar
  54. Manning P, Morrison S, Bonkowski M, Bardgett RD (2008) Nitrogen enrichment modifies plant community structure via changes to plant–soil feedback. Oecologia 157:661–673CrossRefPubMedGoogle Scholar
  55. McGonigle T, Miller M, Evans D, Fairchild G, Swan J (1990) A new method which gives an objective measure of colonization of roots by vesicular–arbuscular mycorrhizal fungi. New Phytol 115:495–501CrossRefGoogle Scholar
  56. Mills KE, Bever JD (1998) Maintenance of diversity within plant communities: soil pathogens as agents of negative feedback. Ecology 79:1595–1601CrossRefGoogle Scholar
  57. Mitchell CE, Power AG (2003) Release of invasive plants from fungal and viral pathogens. Nature 421:625–627CrossRefPubMedGoogle Scholar
  58. Oliveira R, Vosátka M, Dodd J, Castro P (2005) Studies on the diversity of arbuscular mycorrhizal fungi and the efficacy of two native isolates in a highly alkaline anthropogenic sediment. Mycorrhiza 16:23–31CrossRefPubMedGoogle Scholar
  59. Owen SM, Sieg CH, Johnson NC, Gehring CA (2013) Exotic cheatgrass and loss of soil biota decrease the performance of a native grass. Biol Invasions 15:2503–2517CrossRefGoogle Scholar
  60. Padgett PE, Allen EB (1999) Differential responses to nitrogen fertilization in native shrubs and exotic annuals common to Mediterranean coastal sage scrub of California. Plant Ecol 144:93–101CrossRefGoogle Scholar
  61. Parker SS, D’antonio CM (2008) The role of mycorrhizal fungi in promoting exotic grass persistence. Paper presented at the Ecological Society of America 93rd annual meeting, Milwaukee, WisconsinGoogle Scholar
  62. Pernilla Brinkman E, Van der Putten WH, Bakker EJ, Verhoeven KJ (2010) Plant–soil feedback: experimental approaches, statistical analyses and ecological interpretations. J Ecol 98:1063–1073CrossRefGoogle Scholar
  63. Pimentel D, Lach L, Zuniga R, Morrison D (2000) Environmental and economic costs of nonindigenous species in the United States. Bioscience 50:53–65CrossRefGoogle Scholar
  64. Pringle A, Bever JD, Gardes M, Parrent JL, Rillig MC, Klironomos JN (2009) Mycorrhizal symbioses and plant invasions. Annu Rev Ecol Evol Syst 40:699–715CrossRefGoogle Scholar
  65. Rao LE, Allen EB (2010) Combined effects of precipitation and nitrogen deposition on native and invasive winter annual production in California deserts. Oecologia 162:1035–1046CrossRefPubMedGoogle Scholar
  66. Reinhart KO, Callaway RM (2006) Soil biota and invasive plants. New Phytol 170:445–457CrossRefPubMedGoogle Scholar
  67. Schimel JP, Jackson LE, Firestone MK (1989) Spatial and temporal effects on plant-microbial competition for inorganic nitrogen in a California annual grassland. Soil Biol Biochem 21:1059–1066CrossRefGoogle Scholar
  68. Sigüenza C, Corkidi L, Allen EB (2006a) Feedbacks of soil inoculum of mycorrhizal fungi altered by N deposition on the growth of a native shrub and an invasive annual grass. Plant Soil 286:153–165CrossRefGoogle Scholar
  69. Sigüenza C, Crowley DE, Allen EB (2006b) Soil microorganisms of a native shrub and exotic grasses along a nitrogen deposition gradient in southern California. Appl Soil Ecol 32:13–26CrossRefGoogle Scholar
  70. Smith SE, Read DJ (2010) Mycorrhizal symbiosis. Academic press, CambridgeGoogle Scholar
  71. Stinson KA et al (2006) Invasive plant suppresses the growth of native tree seedlings by disrupting belowground mutualisms. PLoS Biol 4:727CrossRefGoogle Scholar
  72. Talluto MV, Suding KN (2008) Historical change in coastal sage scrub in southern California, USA in relation to fire frequency and air pollution. Landsc Ecol 23:803–815CrossRefGoogle Scholar
  73. Theoharides KA, Dukes JS (2007) Plant invasion across space and time: factors affecting nonindigenous species success during four stages of invasion. New Phytol 176:256–273CrossRefPubMedGoogle Scholar
  74. Tonnesen GS, Wang ZW, Omary M, Vhien CJ (2007) Assessment of nitrogen deposition: modeling and habitat assessment. California Energy Commission, SacramentoGoogle Scholar
  75. van der Heijden MG et al (1998) Mycorrhizal fungal diversity determines plant biodiversity, ecosystem variability and productivity. Nature 396:69–72CrossRefGoogle Scholar
  76. van der Putten WH (2010) Impacts of soil microbial communities on exotic plant invasions. Trends Ecol Evol 25:512–519CrossRefPubMedGoogle Scholar
  77. Van der Putten WH, Klironomos JN, Wardle DA (2007) Microbial ecology of biological invasions. ISME J 1:28–37CrossRefPubMedGoogle Scholar
  78. Vitousek PM, Walker LR (1989) Biological invasion by Myrica faya in Hawai’i: plant demography, nitrogen fixation, ecosystem effects. Ecol Monogr 59:247–265CrossRefGoogle Scholar
  79. Vitousek PM et al (1997a) Human alteration of the global nitrogen cycle: sources and consequences. Ecol Appl 7:737–750Google Scholar
  80. Vitousek PM, D’antonio CM, Loope LL, Rejmanek M, Westbrooks R (1997b) Introduced species: a significant component of human-caused global change. N Z J Ecol 21:1–16Google Scholar
  81. Vogelsang KM (2004) The use of mycorrhizal fungi in erosion control applications. California Department of Transportation Sacramento, CaliforniaGoogle Scholar
  82. Vogelsang KM, Bever JD (2009) Mycorrhizal densities decline in association with nonnative plants and contribute to plant invasion. Ecology 90:399–407CrossRefPubMedGoogle Scholar
  83. Wedin DA, Tilman D (1996) Influence of nitrogen loading and species composition on the carbon balance of grasslands. Science 274:1720–1723CrossRefPubMedGoogle Scholar
  84. Weiss SB (1999) Cars, cows, and checkerspot butterflies: nitrogen deposition and management of nutrient-poor grasslands for a threatened species. Conserv Biol 13:1476–1486CrossRefGoogle Scholar
  85. Wood YA, Meixner T, Shouse PJ, Allen EB (2006) Altered ecohydrologic response drives native shrub loss under conditions of elevated nitrogen deposition. J Environ Qual 35:76–92. doi: 10.2134/jecl2004.0465 CrossRefPubMedGoogle Scholar
  86. Yoshida LC, Allen EB (2001) Response to ammonium and nitrate by a mycorrhizal annual invasive grass and native shrub in southern California. Am J Bot 88:1430–1436CrossRefPubMedGoogle Scholar
  87. Zhang Q, Yang R, Tang J, Yang H, Hu S, Chen X (2010) Positive feedback between mycorrhizal fungi and plants influences plant invasion success and resistance to invasion. PLoS ONE 5:e12380CrossRefPubMedPubMedCentralGoogle Scholar

Copyright information

© Springer International Publishing Switzerland 2016

Authors and Affiliations

  1. 1.Department of Botany and Plant SciencesUniversity of CaliforniaRiversideUSA
  2. 2.Center for Conservation BiologyUniversity of CaliforniaRiversideUSA

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