Skip to main content
Log in

Nitrogen uptake and preference in a forest understory following invasion by an exotic grass

  • Community ecology - Original Paper
  • Published:
Oecologia Aims and scope Submit manuscript

Abstract

Plant–soil interactions have been proposed as a causative mechanism explaining how invasive plant species impact ecosystem processes. We evaluate whether an invasive plant influences plant and soil-microbe acquisition of nitrogen to elucidate the mechanistic pathways by which invaders might alter N availability. Using a 15N tracer, we quantify differences in nitrogen uptake and allocation in communities with and without Microstegium vimineum, a shade-tolerant, C4 grass that is rapidly invading the understories of eastern US deciduous forests. We further investigate if plants or the microbial biomass exhibit preferences for certain nitrogen forms (glycine, nitrate, and ammonium) to gain insight into nitrogen partitioning in invaded communities. Understory native plants and M. vimineum took up similar amounts of added nitrogen but allocated it differently, with native plants allocating primarily to roots and M. vimineum allocating most nitrogen to shoots. Plant nitrogen uptake was higher in invaded communities due primarily to the increase in understory biomass when M. vimineum was present, but for the microbial biomass, nitrogen uptake did not vary with invasion status. This translated to a significant reduction (P < 0.001) in the ratio of microbial biomass to plant biomass nitrogen uptake, which suggests that, although the demand for nitrogen has intensified, microbes continue to be effective nitrogen competitors. The microbial biomass exhibited a strong preference for ammonium over glycine and nitrate, regardless of invasion status. By comparison, native plants showed no nitrogen preferences and M. vimineum preferred inorganic nitrogen species. We interpret our findings as evidence that invasion by M. vimineum leads to changes in the partitioning of nitrogen above and belowground in forest understories, and to decreases in the microbial biomass, but it does not affect the outcome of plant–microbe–nitrogen interactions, possibly due to functional shifts in the microbial community as a result of invasion.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4

Similar content being viewed by others

References

  • Allison SD, Vitousek PM (2004) Rapid nutrient cycling in leaf litter from invasive plants in Hawai’i. Oecologia 141:612–619

    Article  PubMed  Google Scholar 

  • Andersson T (1993) Significance of foliar nutrient absorption in nutrient-rich low-light environments as indicated by Mercurialis perennis. Flora 187:429–433

    Google Scholar 

  • Ashton IW, Hyatt LA, Howe KM, Gurevitch J, Lerdau MT (2005) Invasive species accelerate decomposition and litter nitrogen loss in a mixed deciduous forest. Ecol Appl 15:1263–1272

    Article  Google Scholar 

  • Bever JD et al (2010) Rooting theories of plant community ecology in microbial interactions. Trends Ecol Evol 25:468–478

    Article  PubMed  Google Scholar 

  • Bradford MA et al (2008) Thermal adaptation of soil microbial respiration to elevated temperature. Ecol Lett 11:1316–1327

    Article  PubMed  Google Scholar 

  • Bradford MA, DeVore JL, Maerz JC, McHugh JV, Smith CL, Strickland MS (2010) Native, insect herbivore communities derive a significant proportion of their carbon from a widespread invader of forest understories. Biol. Invasions 12:721–724

    Article  Google Scholar 

  • Cabrera ML, Beare MH (1993) Alkaline persulfate oxidation for determining total nitrogen in microbial biomass extracts. Soil Sci Soc Am J 57:1007–1012

    Article  CAS  Google Scholar 

  • Callaway RM, Thelen GC, Rodriguez A, Holben WE (2004) Soil biota and exotic plant invasion. Nature 427:731–733

    Article  PubMed  CAS  Google Scholar 

  • Carlisle A, Brown AHF, White EJ (1967) The nutrient content of tree stem flow and ground flora litter and leachates in a sessile oak (Quercus petraea) woodland. J Ecol 55:615–627

    Article  Google Scholar 

  • Chapin FS, McFarland J, McGuire AD, Euskirchen ES, Ruess RW, Kielland K (2009) The changing global carbon cycle: linking plant–soil carbon dynamics to global consequences. J Ecol 97:840–850

    Article  CAS  Google Scholar 

  • Claridge K, Franklin SB (2002) Compensation and plasticity in an invasive plant species. Biol Invasions 4:339–347

    Article  Google Scholar 

  • Cole PG, Weltzin JF (2005) Light limitation creates patchy distribution of an invasive grass in eastern deciduous forests. Biol Invasions 7:477–488

    Article  Google Scholar 

  • Collins B, Wein G (1998) Soil resource heterogeneity effects on early succession. Oikos 82:238–245

    Article  Google Scholar 

  • Crawley MJ (1987) What makes a community invasible? In: Gray AJ, Crawley MJ, Edwards PJ (eds) Colonization, succession and stability. Blackwell, Oxford, pp 429–453

    Google Scholar 

  • DeMeester JE, Richter DD (2010) Differences in wetland nitrogen cycling between the invasive grass Microstegium vimineum and a diverse plant community. Ecol Appl 20:609–619

    Article  PubMed  Google Scholar 

  • Ehleringer JR, Monson RK (1993) Evolutionary and ecological aspects of photosynthetic pathway variation. Annu Rev Ecol Syst 24:411–439

    Article  Google Scholar 

  • Ehrenfeld JG (2003) Effects of exotic plant invasions on soil nutrient cycling processes. Ecosystems 6:503–523

    Article  CAS  Google Scholar 

  • Ehrenfeld JG, Kourtev P, Huang WZ (2001) Changes in soil functions following invasions of exotic understory plants in deciduous forests. Ecol Appl 11:1287–1300

    Article  Google Scholar 

  • Ehrenfeld JG, Ravit B, Elgersma K (2005) Feedback in the plant–soil system. Annu Rev Environ Resour 30:75–115

    Article  Google Scholar 

  • Fierer N, Schimel JP (2002) Effects of drying-rewetting frequency on soil carbon and nitrogen transformations. Soil Biol Biochem 34:777–787

    Article  CAS  Google Scholar 

  • 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 67:798–805

    Article  CAS  Google Scholar 

  • Flory SL, Clay K (2010) Non-native grass invasion alters native plant composition in experimental communities. Biol Invasions 12:1285–1294

    Article  Google Scholar 

  • Fry B (2006) Stable isotope ecology. Springer, New York

    Book  Google Scholar 

  • Gagnon D, Lafond A, Amiot LP (1958) Mineral nutrient content of some forest plant leaves and of the humus layer as related to site quality. Can J Bot 36:209–220

    Article  Google Scholar 

  • Geisseler D, Horwath WR, Joergensen RG, Ludwig B (2010) Pathways of nitrogen utilization by soil microorganisms: a review. Soil Biol Biochem 42:2058–2067

    Article  CAS  Google Scholar 

  • Gilbert B, Lechowicz MJ (2005) Invasibility and abiotic gradients: the positive correlation between native and exotic plant diversity. Ecology 86:1848–1855

    Article  Google Scholar 

  • Gilliam FS (2007) The ecological significance of the herbaceous layer in temperate forest ecosystems. Bioscience 57:845–858

    Article  Google Scholar 

  • Harrison KA, Bol R, Bardgett RD (2007) Preferences for different nitrogen forms by coexisting plant species and soil microbes. Ecology 88:989–999

    Article  PubMed  Google Scholar 

  • Hawkes CV, Wren IF, Herman DJ, Firestone MK (2005) Plant invasion alters nitrogen cycling by modifying the soil nitrifying community. Ecol Lett 8:976–985

    Article  Google Scholar 

  • Hodge A, Robinson D, Fitter A (2000) Are microorganisms more effective than plants at competing for nitrogen? Trends Plant Sci 5:304–308

    Article  PubMed  CAS  Google Scholar 

  • Hogberg P, Read DJ (2006) Towards a more plant physiological perspective on soil ecology. Trends Ecol Evol 21:548–554

    Article  PubMed  Google Scholar 

  • Horton JL, Neufeld HS (1998) Photosynthetic responses of Microstegium vimineum (Trin.) A. Camus, a shade-tolerant, C4 grass, to variable light environments. Oecologia 114:11–19

    Article  Google Scholar 

  • Howard TG, Gurevitch J, Hyatt L, Carreiro M, Lerdau M (2004) Forest invasibility in communities in southeastern New York. Biol Invasions 6:393–410

    Article  Google Scholar 

  • Inderjit, van der Putten WH (2010) Impacts of soil microbial communities on exotic plant invasions. Trends Ecol Evol 25:512–519

    Article  PubMed  CAS  Google Scholar 

  • Kaye JP, Hart SC (1997) Competition for nitrogen between plants and soil microorganisms. Trends Ecol Evol 12:139–143

    Article  PubMed  CAS  Google Scholar 

  • Knops JMH, Bradley KL, Wedin DA (2002) Mechanisms of plant species impacts on ecosystem nitrogen cycling. Ecol Lett 5:454–466

    Article  Google Scholar 

  • Kourtev PS, Ehrenfeld JG, Haggblom M (2002) Exotic plant species alter the microbial community structure and function in the soil. Ecology 83:3152–3166

    Article  Google Scholar 

  • Kourtev PS, Ehrenfeld JG, Haggblom 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 35:895–905

    Article  CAS  Google Scholar 

  • Levine JM, Vila M, D’Antonio CM, Dukes JS, Grigulis K, Lavorel S (2003) Mechanisms underlying the impacts of exotic plant invasions. Proc R Soc Lond B 270:775–781

    Article  Google Scholar 

  • Liao CZ et al (2008) Altered ecosystem carbon and nitrogen cycles by plant invasion: a meta-analysis. New Phytol 177:706–714

    Article  PubMed  CAS  Google Scholar 

  • Martin PH (1999) Norway maple (Acer platanoides) invasion of a natural forest stand: understory consequence and regeneration pattern. Biol Invasions 1:215–222

    Article  Google Scholar 

  • Martin PH, Sherman RE, Fahey TJ (2004) Forty years of tropical forest recovery from agriculture: Structure and floristics of secondary and old-growth riparian forests in the Dominican Republic. Biotropica 36:297–317

    Google Scholar 

  • Martin PH, Canham CD, Marks PL (2009) Why forests appear resistant to exotic plant invasions: intentional introductions, stand dynamics, and the role of shade tolerance. Front Ecol Environ 7:142–149

    Article  Google Scholar 

  • Miller AE, Bowman WD, Suding KN (2007) Plant uptake of inorganic and organic nitrogen: neighbor identity matters. Ecology 88:1832–1840

    Article  PubMed  Google Scholar 

  • Morrison JA, Lubchansky HA, Mauck KE, McCartney KM, Dunn B (2007) Ecological comparison of two co-invasive species in eastern deciduous forests: Alliaria petiolata and Microstegium vimineum. J Torrey Bot 134:1–17

    Article  Google Scholar 

  • Muller RN (2003) Nutrient relations of the herbaceous layer in deciduous forest ecosystems. In: Gilliam FS, Roberts MR (eds) The herbaceous layer in forests of Eastern North America. Oxford University Press, New York, pp 15–37

    Google Scholar 

  • Oswalt CM, Oswalt SN, Clatterbuck WK (2007) Effects of Microstegium vimineum (Trin.) A. Camus on native woody species density and diversity in a productive mixed-hardwood forest in Tennessee. For Ecol Manag 242:727–732

    Article  Google Scholar 

  • Pollierer MM, Langel R, Korner C, Maraun M, Scheu S (2007) The underestimated importance of belowground carbon input for forest soil animal food webs. Ecol Lett 10:729–736

    Article  PubMed  Google Scholar 

  • Rodgers VL, Wolfe BE, Werden LK, Finzi AC (2008) The invasive species Alliaria petiolata (garlic mustard) increases soil nutrient availability in northern hardwood-conifer forests. Oecologia 157:459–471

    Article  PubMed  Google Scholar 

  • Schimel JP, Bennett J (2004) Nitrogen mineralization: challenges of a changing paradigm. Ecology 85:591–602

    Article  Google Scholar 

  • Scott NA, Saggar S, McIntosh PD (2001) Biogeochemical impact of Hieracium invasion in New Zealand’s grazed tussock grasslands: sustainability implications. Ecol Appl 11:1311–1322

    Article  Google Scholar 

  • Siccama TG, Bormann FH, Likens GE (1970) Hubbard Brook ecosystem study: productivity, nutrients, and phytosociology of the herbaceous layer. Ecol Monogr 40:389–402

    Article  Google Scholar 

  • 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 16:1338–1350

    Article  Google Scholar 

  • Strickland M, DeVore J, Maerz J, Bradford M (2011) Loss of faster-cycling soil carbon pools following grass invasion across multiple forest sites. Soil Biol Biochem 43:452–454

    Article  CAS  Google Scholar 

  • USDA and NRCS (2005) The PLANTS database. Version 3.5. Data compiled from various sources by Mark W. Skinner. National Plant Data Center, Baton Rouge

  • Vitousek PM (1990) Biological invasions and ecosystem processes: towards an integration of population biology and ecosystem studies. Oikos 57:7–13

    Article  Google Scholar 

  • Von Holle B, Delcourt HR, Simberloff D (2003) The importance of biological inertia in plant community resistance to invasion. J Veg Sci 14:425–432

    Article  Google Scholar 

  • Warren R, Wright J, Bradford M (2011a) The putative niche requirements and landscape dynamics of Microstegium vimineum: an invasive Asian grass. Biol Invasions 13:471–483

    Article  Google Scholar 

  • Warren RJ, Bahn V, Kramer TD, Tang Y, Bradford MA (2011b) Performance and reproduction of an exotic invader across temperate forest gradients. Ecosphere 2:14

    Article  Google Scholar 

  • Webb SL, Kaunzinger CK (1993) Biological invasion of the Drew University (New Jersey) Forest Preserve by Norway Maple (Acer platanoides L.). Bull Torrey Bot 120:343–349

    Article  Google Scholar 

  • Webb SL, Dwyer M, Kaunzinger CK, Wyckoff PH (2000) The myth of the resilient forest: case study of the invasive Norway maple (Acer platanoides). Rhodora 102:332–354

    Google Scholar 

  • Woods KD (1993) Effects of invasion by Lonicera tatarica L. on herbs and tree seedlings in 4 New England forests. Am Midl Nat 130:62–74

    Article  Google Scholar 

  • Yarie J (1980) The role of understory vegetation in the nutrient cycle of forested ecosystems in the Mountain Hemlock Biogeoclimatic Zone. Ecology 61:1498–1514

    Article  Google Scholar 

Download references

Acknowledgments

This study benefitted from discussions with Robert Warren, Tony Yannarell and Monica Turner. We also thank K. Gross and three anonymous reviewers for their comments. Funding was through the Long-Term Ecological Research (LTER) Program of the National Science Foundation (Grants DEB-0823293 and DEB-9632854) and the Andrew W. Mellon Foundation. The work conducted complied with all current laws and regulations of the US, where the study was conducted.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Jennifer M. Fraterrigo.

Additional information

Communicated by Tim Seastedt.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Fraterrigo, J.M., Strickland, M.S., Keiser, A.D. et al. Nitrogen uptake and preference in a forest understory following invasion by an exotic grass. Oecologia 167, 781–791 (2011). https://doi.org/10.1007/s00442-011-2030-0

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00442-011-2030-0

Keywords

Navigation