Abstract
Many studies have linked the spread of exotic, invasive species to high nitrogen supply, but most of this work does not distinguish between various inorganic forms and different concentrations of available nitrogen. Previous research has suggested that exotic, invasive species common in eastern deciduous forests may preferentially utilize nitrate in contrast to native species that preferentially make use of ammonium. We tested this hypothesis by comparing the growth response of two common forest invaders, Berberis thunbergii and Microstegium vimineum, and two co-occurring native species (Vaccinium pallidum and Hamamelis virginiana) to different forms of nitrogen under varying concentrations in a greenhouse experiment. Two forms of nitrogen (nitrate or ammonium) were added at different concentrations (22, 106, and 212 mg N l−1) to all species. Growth response variables included survival, stem length, stem diameter, above and belowground biomass, and estimated seed production (Microstegium only). Unexpectedly the exotic species did not respond preferentially to nitrate addition. Microstegium responded most strongly to both nitrogen forms depending on the response variable. Berberis and Hamamelis surprisingly reacted similarly to nitrogen additions. As expected, Vaccinium fared poorly under most treatment conditions, but did show some growth in NH4 + treatments. Our findings suggest species response to nitrogen addition is complex, and that exotic species do not all respond similarly to nitrogen inputs. In this study, the response of exotic and native species to available nutrients does not provide a general mechanism of invasion success.
Similar content being viewed by others
References
Aerts R (1999) Interspecific competition in natural plant communities: mechanisms, trade-offs and plant-soil feedbacks. J Exp Bot 50(330):29–37
Aerts R, Chapin FSI (2000) The mineral nutrition of wild plants revisited: a re-evaluation of processes and patterns. Adv Ecol Res 30:1–67
Allcock KG (2002) Effects of phosphorus on growth and competitive interactions of native and introduced species found in white box woodlands. Aust Ecol 27:638–646
Aronson MFJ, Handel SN, Clemants SE (2007) Fruit type, life form and origin determine the success of woody plant invaders in an urban landscape. Biol Invasions 9(3):465–475
Baiser B, Lockwood JL, La Puma D, Aronson MFJ (2008) A perfect storm: two ecosystem engineers interact to degrade deciduous forests of New Jersey. Biol Invasions 10(6):785–795
Barden LS (1987) Invasion of Microstegium vimineum, an exotic, annual, shade-tolerant, C4 grass, into a North Carolina floodplain. Am Midl Nat 118(1):40–45
Bashkin M, Stohlgren TJ, Otsuki Y, Lee M, Evangelista P, Belnap V (2003) Soil characteristics and plant exotic species invasions in the Grand Staircase-Escalante National Monument, Utah USA. Appl Soil Ecol 22:67–77
Bobbink R, Hornung M, Roelofs JM (1998) The effects of air-borne nitrogen pollutants on species diversity in natural and semi-natural European vegetation. J Ecol 86:717–738
Brooks ML (2003) Effects of increased soil nitrogen on the dominance of alien annual plants in the Mojave Desert. J Appl Ecol 40:344–353
Burns JH, Halpern SL, Winn AA (2007) A test for a cost of opportunism in invasive species in the Commelinaceae. Biol Invasions 9:213–225
Cassidy TM, Fownes JH, Harrington RA (2004) Nitrogen limits an invasive perennial shrub in forest understory. Biol Invasions 6:113–121
Cheplick G (2005) Biomass partitioning and reproductive allocation in the invasive, cleistogamous grass Microstegium vimineum: Influence of the light environment. J Torrey Bot Soc 132(2):214–224
Claridge K, Franklin SB (2002) Compensation and plasticity in an invasive plant species. Biol Invasions 4:339–347
Claussen W, Lenz F (1999) Effect of ammonium or nitrate nutrition on net photosynthesis, growth, and activity of the enzymes nitrate reductase and glutamine synthetase in blueberry, raspberry and strawberry. Plant Soil 208:95–102
Cole PG, Weltzin JF (2004) Environmental correlates of the distribution and abundance of Microstegium vimineum, in East Tennessee. Southeast Nat 3(3):545–562
Cui X, Song J (2007) Soil NH4 +/NO3 − nitrogen characteristics in primary forests and the adaptability of some coniferous species. Front For China 2(1):1–10
Daehler CC (2003) Performance comparisons of co-occurring native and alien invasive plants: implications for conservation and restoration. Annu Rev Ecol Evol Syst 34:183–211
Davis MA, Grime JP, Thompson K (2000) Fluctuating resources in plant communities: a general theory of invisibility. J Ecol 88:528–534
DeGasperis BG, Motzkin G (2007) Windows of opportunity: historical and ecological controls on Berberis thunbergii invasions. Ecology 88(12):3115–3125
Ehrenfeld JG (1997) Invasion of deciduous forest preserves in the New York metropolitan region by Japanese barberry (Berberis thunbergii DC.). J Torrey Bot Soc 124(2):210–215
Ehrenfeld JG (1999a) Distribution and dynamics of two exotic species, Berberis thunbergii and Microstegium vimineum. In: Morristown national historical park, national park service. Report for Morristown National Historical Park, Morris County, NJ
Ehrenfeld JG (1999b) Structure and dynamics of populations of Japanese barberry (Berberis thunbergii DC.) in deciduous forests of New Jersey. Biol Invasions 1:203–213
Ehrenfeld JG (2010) Ecosystem consequences of biological invasions. Annu Rev Ecol Evol Syst 41:59–80
Ehrenfeld JG, Kourtev P, Huang W (2001) Changes in soil functions following invasions of exotic understory plants in deciduous forests. Ecol Appl 11(5):1287–1300
Elgersma K, Ehrenfeld JG, Yu S, Vor T Legacy effects overwhelm the short-term effects of exotic plant invasion and restoration on soil microbial community structure, enzyme activities, and nitrogen cycling. Oecologia. doi:10.1007/s00442-011-2022-0
Eschtruth AK, Battles JJ (2009) Acceleration of exotic plant invasion in a forested ecosystem by a generalist herbivore. Conserv Biol 23:388–399
Fang YY, Babourina O, Rengel Z, Yang XE, Pul PM (2007) Ammonium and nitrate uptake by the floating plant Landoltia punctata. Ann Bot 99:365–370
Funk JL, Vitousek PM (2007) Resource-use efficiency and plant invasion in low-resource systems. Nature 446:1079–1081
Gibson DJ, Spyreas G, Benedict J (2002) Life history of Microstegium vimineum (Poaceae), an invasive grass in southern Illinois. J Torrey Bot Soc 129(3):207–219
Gilliam FS (2006) Response of the herbaceous layer of forest ecosystems to excess nitrogen deposition. J Ecol 94:1176–1191
Gilliam FS (2007) The ecological significance of the herbaceous layer in temperate forest ecosystems. Bioscience 57(10):845–858
Green EK, Galatowitsch SM (2001) Differences in wetland plant community establishment with additions of nitrate-n and invasive species (Phalaris arundinacea and Typha x glauca). Can J Bot 79:170–178
Grime JP (1979) Plant strategies and vegetation processes. Wiley, New York
Gurevitch J, Howard TG, Ashton IW, Leger EA, Howe KM, Woo E, Lerdau M (2008) Effects of experimental manipulation of light and nutrients on establishment of seedlings of native and invasive woody species in Long Island, NY forests. Biol Invasions 10:821–831
Harrington RA, Fownes JH, Cassidy TM (2004) Japanese barberry (Berberis thunbergii) in forest understory: leaf and whole plant responses to nitrogen availability. Am Midl Nat 151:206–216
Hewins D, Hyatt L (2010) Flexible N uptake and assimilation mechanisms may assist biological invasion by Alliaria petiolata. Biol Invasions 12:2639–2647
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
Howard TG, Gurevitch J, Hyatt L, Carriero M, Lerdau M (2004) Forest invasibility in communities in southeastern New York. Biol Invasions 6:393–410
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 72:1775–1784
Knight TM, Dunn JL, Smith LA, Davis J, Kalisz S (2009) Deer facilitate invasive plant success in a Pennsylvania forest understory. Nat Areas J 29:110–116
Kourtev PS, Ehrenfeld JG, Huang WZ (1998) Effects of exotic plant species on soil properties in hardwood forests of New Jersey. Water Air Soil Pollut 105:493–501
Kourtev PS, Huang WZ, Ehrenfeld JG (1999) Differences in earthworm densities and nitrogen dynamics in soils under exotic and native plant species. Biol Invasions 1:237–245
Kourtev PS, Ehrenfeld JG, Haggblom M (2002) Exotic plant species alter the microbial community structure and function in the soil. Ecology 83(11):3152–3166
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
Kronzucker HJ, Anthony DM, Glass M, Siddiqi Y (1995) Nitrate induction in spruce: an approach using compartmental analysis. Planta 196:683–690
Kronzucker HJ, Siddiqi MY, Glass ADM (1997) Conifer root discrimination against soil nitrate and the ecology of forest succession. Nature 385:59–61
Leicht SA, Silander JA Jr, Greenwood K (2005) Assessing the competitive ability of Japanese stilt grass, Microstegium vimineum (Trin.) A. Camus. J Torrey Bot Soc 132(4):573–580
Liao CZ et al (2008) Altered ecosystem carbon and nitrogen cycles by plant invasion: a meta-analysis. New Phytol 177:706–714
Lowe PN, Lauenroth WK, Burke IC (2003) Effects of nitrogen availability on competition between Bromus tectorum and Bouteloua gracilis. Plant Ecol 167:247–254
Marschner H (1986) Mineral nutrition of higher plants. Academic Press, Sand Diego
Marshall JM, Buckley DS, Franklin JA (2009) Competitive interaction between Microstegium vimineum and first-year seedlings of three central hardwoods. J Torrey Bot Soc 136(3):342–349
McDonald RI, Motzkin G, Foster DR (2008) Assessing the influence of historical factors, contemporary processes, and environmental conditions on the distribution of invasive species. J Torrey Bot Soc 135:260–271
Miller AE, Bowman WD (2002) Variation in nitrogen-15 natural abundance and nitrogen uptake traits among co-occurring alpine species: do species partition by nitrogen form? Oecologia 130:609–616
Miller AE, Bowman WD, Suding KN (2007) Plant uptake of inorganic and organic nitrogen: neighbor identity matters. Ecology 88(7):1832–1840
Newingham BA, Belnap J (2006) Direct effects of soil amendments on field emergence and growth of the invasive annual grass Bromus tectorum L. and the native perennial grass Hilaria jamesii (Torr.) Benth. Plant Soil 280:29–40
Nordin A, Strengbom J, Witzell J, Näsholm T, Ericson L (2005) Nitrogen deposition and the biodiversity of boreal forests: implications for the nitrogen critical load. Ambio 34(1):20–24
Ostertag R, Verville JH (2002) Fertilization with nitrogen and phosphorus increases abundance of non-native species in Hawaiian montane forests. Plant Ecol 162:77–90
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
Persson J, Högberg P, Ekblad A, Högberg MN, Nordgren A, Näsholm T (2003) Nitrogen acquisition from inorganic and organic sources by boreal forest plants in the field. Oecologia 137:252–257
Pouyat RV, McDonnell MJ, Picket STA (1997) Litter decomposition and nitrogen mineralization in oak stands along an urban-rural land use gradient. Urban Ecosyst 1:117–131
QuikChem Systems (1986) QuikChem method no. 12-107-04-1-A. QuikChem Systems. Division of Lachat Chemicals Inc., Mequon, WI
QuikChem Systems (1987) QuikChem method no. 12-107-06-A. QuikChem Systems. Division of Lachat Chemicals Inc., Mequon, WI
Read DJ (1991) Mycorrhizas in ecosystems. Experientia 47:376–391
Roper MM, Ophel-Keller KM (1997) Soil microflora as bioindicators of soil health. In: Pankhurst CE, Doube BM, Gupta VVSR (eds) Biological Indicators of soil health. CAB International, New York
Russell FL, Zippin DB, Fowler NL (2001) Effects of white-tailed deer (Odocoileus virginianus) on plants, plant populations and communities: a review. Am Midl Nat 146(1):1–26
SAS Institute Inc. (2003) Cary, NC
Scheffe H (1959) The analysis of variance. Wiley, New York
Silander JA, Klepeis DM (1999) The invasion ecology of Japanese barberry (Berberis thunbergii) in the New England landscape. Biol Invasions 1:189–201
USDA (2008) Plants database. Retrieved 20 Feb 2008. http://plants.usda.gov
USDA Forest Service (2008) Fire effects information system. Retrieved 22 Apr 2008. http://www.fs.fed.us/database/feis/plants/shrub/vacpal/all.html
Vitousek PM, Walker LR (1989) Biological invasion by Myrica faya in hawai’i: Plant demography, nitrogen fixation, ecosystem effects. Ecol Monogr 59(3):247–265
Wardle DA (2002) Communities and ecosystems: linking aboveground and belowground components. Princeton University Press, Princeton
Wedin D, Tilman D (1993) Competition among grasses along a nitrogen gradient: initial conditions and mechanisms of competition. Ecol Monogr 63:199–229
Zhu WX, Carriero MM (1999) Chemoautotrophic nitrification in acidic forest soils along an urban-to-rural transect. Soil Biol Biochem 31:1091–1100
Acknowledgments
We thank past and present members of the J. Ehrenfeld lab at Rutgers including K. Elgersma, M. Palta, A. Wen, and L. Shapelle for valuable comments/suggestions on early drafts. We especially thank W. Landesman who provided extremely helpful comments on later drafts. In addition, we appreciate comments from several anonymous reviewers that greatly improved the manuscript. For help with data collection we thank M. Bartels, A. Wen, and L. Rohleder. We thank Joe Florentine for support in the greenhouse. Thanks also to Dow AgroSciences for donation of N-Serve 24E™. Funding was provided by US Department of Agriculture National Research Initiative grant # 2002-35320-12416.
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Ross, K.A., Ehrenfeld, J.G. & Patel, M.V. The effects of nitrogen addition on the growth of two exotic and two native forest understory plants. Biol Invasions 13, 2203–2216 (2011). https://doi.org/10.1007/s10530-011-0034-7
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10530-011-0034-7