Biological Invasions

, Volume 18, Issue 9, pp 2619–2631 | Cite as

Deep rooting and global change facilitate spread of invasive grass

  • Thomas J. Mozdzer
  • J. Adam Langley
  • Peter Mueller
  • J. Patrick Megonigal


Abiotic global change factors, such as rising atmospheric CO2, and biotic factors, such as exotic plant invasion, interact to alter the function of terrestrial ecosystems. An invasive lineage of the common reed, Phragmites australis, was introduced to North America over a century ago, but the belowground mechanisms underlying Phragmites invasion and persistence in natural systems remain poorly studied. For instance, Phragmites has a nitrogen (N) demand higher than native plant communities in many of the ecosystems it invades, but the source of the additional N is not clear. We exposed introduced Phragmites and native plant assemblages, containing Spartina patens and Schoenoplectus americanus, to factorial treatments of CO2 (ambient or +300 ppm), N (0 or 25 g m−2 year−1), and hydroperiod (4 levels), and focused our analysis on changes in root productivity as a function of depth and evaluated the effects of introduced Phragmites on soil organic matter mineralization. We report that non-native invasive Phragmites exhibited a deeper rooting profile than native marsh species under all experimental treatments, and also enhanced soil organic matter decomposition. Moreover, exposure to elevated atmospheric CO2 induced a sharp increase in deep root production in the invasive plant. We propose that niche separation accomplished through deeper rooting profiles circumvents nutrient competition where native species have relatively shallow root depth distributions; deep roots provide access to nutrient-rich porewater; and deep roots further increase nutrient availability by enhancing soil organic matter decomposition. We expect that rising CO2 will magnify these effects in deep-rooting invasive plants that compete using a tree-like strategy against native herbaceous plants, promoting establishment and invasion through niche separation.


Invasive Elevated carbon dioxide Priming Rooting depth Nitrogen Marsh organ Phragmites Schoenoplectus americanus Spartina patens 



We thank, J. Duls, A. Peresta, G. Peresta, M.I. Seal, K. Shepard, A. Teasley, S. Hagerty, M. O’Donoghue, K. Pannier, and B. Kelly for field and laboratory assistance. We also thank J.S. Caplan for feedback on the manuscript. The field study was supported by the USGS Global Change Research Program (cooperative agreement 06ERAG0011), the US Department of Energy (DE-FG02-97ER62458), US Department of Energy’s Office of Science (BER) through the Coastal Center of the National Institute of Climate Change Research at Tulane University, the National Science Foundation’s Long-Term Research Environmental Biology program (DEB-0950080, DEB-1457100, & DEB-1557009), Maryland Sea Grant (SA7528082 & SA7528114-WW), Research Experience for Undergraduates (REU) program, and the Smithsonian Institution. Use of trade, product, or firm names does not imply endorsement by the U.S. Government.


  1. Amsberry L, Baker MA, Ewanchuk PJ, Bertness MD (2000) Clonal integration and the expansion of Phragmites australis. Ecol Appl 10:1110–1118CrossRefGoogle Scholar
  2. Arnone JA, Zaller JG, Spehn EM, Niklaus PA, Wells CE, Korner C (2000) Dynamics of root systems in native grasslands: effects of elevated atmospheric CO2. New Phytol 147:73–86CrossRefGoogle Scholar
  3. Bertness MD, Callaway R (1994) Positive Interactions in Communities. Trends Ecol Evol 9:191–193CrossRefPubMedGoogle Scholar
  4. Bertness MD, Ellison AM (1987) Determinants of pattern in a New-England salt-marsh plant community. Ecol Monogr 57:129–147CrossRefGoogle Scholar
  5. Bertness MD, Ewanchuk PJ, Silliman BR (2002) Anthropogenic modification of New England salt marsh landscapes. Proc Natl Acad Sci USA 99:1395–1398CrossRefPubMedPubMedCentralGoogle Scholar
  6. Bowling DR, Pataki DE, Randerson JT (2008) Carbon isotopes in terrestrial ecosystem pools and CO2 fluxes. New Phytol 178:24–40CrossRefPubMedGoogle Scholar
  7. Burke DJ, Hamerlynck EP, Hahn D (2002) Interactions among plant species and microorganisms in salt marsh sediments. Appl Environ Microbiol 68:1157–1164CrossRefPubMedPubMedCentralGoogle Scholar
  8. Caplan JS, Wheaton C, Mozdzer TJ (2014) Belowground advantages in construction cost facilitate a cryptic plant invasion. AoB Plants 6:plu020. doi: 10.1093/aobpla/plu020
  9. Caplan JS, Hager RN, Megonigal JP, Mozdzer TJ (2015) Global change accelerates carbon assimilation by a wetland ecosystem engineer. Environ Res Lett 10:115006CrossRefGoogle Scholar
  10. Carney KM, Hungate BA, Drake BG, Megonigal JP (2007) Altered soil microbial community at elevated CO2 leads to loss of soil carbon. Proc Natl Acad Sci USA 104:4990–4995CrossRefPubMedPubMedCentralGoogle Scholar
  11. Chambers RM, Mozdzer TJ, Ambrose JC (1998) Effects of salinity and sulfide on the distribution of Phragmites australis and Spartina alterniflora in a tidal saltmarsh. Aquat Bot 62:161–169CrossRefGoogle Scholar
  12. Chambers RM, Osgood DT, Bart DJ, Montalto F (2003) Phragmites australis invasion and expansion in tidal wetlands: interactions among salinity, sulfide, and hydrology. Estuaries 26:398–406CrossRefGoogle Scholar
  13. Cheng WX (2009) Rhizosphere priming effect: its functional relationships with microbial turnover, evapotranspiration, and C–N budgets. Soil Biol Biochem 41:1795–1801CrossRefGoogle Scholar
  14. Daehler CC, Strong DR (1996) Status, prediction and prevention of introduced cordgrass Spartina spp. invasions in Pacific estuaries, USA. Biol Conserv 78:51–58CrossRefGoogle Scholar
  15. Deegan LA, Johnson DS, Warren RS, Peterson BJ, Fleeger JW, Fagherazzi S, Wollheim WM (2012) Coastal eutrophication as a driver of salt marsh loss. Nature 490:388CrossRefPubMedGoogle Scholar
  16. Dukes JS, Mooney HA (1999) Does global change increase the success of biological invaders? Trends Ecol Evol 14:135–139CrossRefPubMedGoogle Scholar
  17. Ehrenfeld JG (2003) Effects of exotic plant invasions on soil nutrient cycling processes. Ecosystems 6:503–523CrossRefGoogle Scholar
  18. Ewanchuk PJ, Bertness MD (2004) Structure and organization of a northern New England salt marsh plant community. J Ecol 92:72–85CrossRefGoogle Scholar
  19. Fu SL, Cheng WX (2002) Rhizosphere priming effects on the decomposition of soil organic matter in C-4 and C-3 grassland soils. Plant Soil 238:289–294CrossRefGoogle Scholar
  20. Gale MR, Grigal DF (1987) Vertical root distributions of Northern tree species in relation to successional status. Can J For Res 17:829–834CrossRefGoogle Scholar
  21. Holdredge C, Bertness MD (2011) Litter legacy increases the competitive advantage of invasive Phragmites australis in New England wetlands. Biol Invasions 13:423–433CrossRefGoogle Scholar
  22. Hooper DU, Adair EC, Cardinale BJ, Byrnes JEK, Hungate BA, Matulich KL, Gonzalez A, Duffy JE, Gamfeldt L, O’Connor MI (2012) A global synthesis reveals biodiversity loss as a major driver of ecosystem change. Nature 486:U105–U129Google Scholar
  23. Iversen CM (2010) Digging deeper: fine-root responses to rising atmospheric CO2 concentration in forested ecosystems. New Phytol 186:346–357CrossRefPubMedGoogle Scholar
  24. Jackson RB, Canadell J, Ehleringer JR, Mooney HA, Sala OE, Schulze ED (1996) A global analysis of root distributions for terrestrial biomes. Oecologia 108:389–411CrossRefGoogle Scholar
  25. Keller JK, Wolf AA, Weisenhorn PB, Drake BG, Megonigal JP (2009) Elevated CO2 affects porewater chemistry in a brackish marsh. Biogeochemistry 96:101–117CrossRefGoogle Scholar
  26. Kettenring KM, Whigham DF (2009) Seed viability and seed dormancy of non-native Phragmites australis in suburbanized and forested watersheds of the Chesapeake Bay, USA. Aquat Bot 91:199–204CrossRefGoogle Scholar
  27. Kirwan ML, Megonigal JP (2013) Tidal wetland stability in the face of human impacts and sea-level rise. Nature 504(7478):53–60Google Scholar
  28. Koop-Jakobsen K, Wenzhöfer F (2015) The dynamics of plant-mediated sediment oxygenation in Spartina anglica rhizospheres-a planar optode study. Estuaries Coasts 38:951–963CrossRefGoogle Scholar
  29. Langley JA, Megonigal JP (2010) Ecosystem response to elevated CO2 levels limited by nitrogen-induced plant species shift. Nature 466:96–99CrossRefPubMedGoogle Scholar
  30. Langley JA, Mckee KL, Cahoon DR, Cherry JA, Megonigal JP (2009) Elevated CO2 stimulates marsh elevation gain, counterbalancing sea-level rise. Proc Natl Acad Sci USA 106:6182–6186CrossRefPubMedPubMedCentralGoogle Scholar
  31. Langley JA, Mozdzer TJ, Shepard KA, Hagerty SB, Megonigal JP (2013) Tidal marsh plant responses to elevated CO2, nitrogen fertilization, and sea level rise. Global Change Biol 19(5):1495–1503Google Scholar
  32. Luo Y, Su B, Currie WS, Dukes JS, Finzi AC, Hartwig U, Hungate B, McMurtrie RE, Oren R, Parton WJ, Pataki DE, Shaw MR, Zak DR, Field CB (2004) Progressive nitrogen limitation of ecosystem responses to rising atmospheric carbon dioxide. Bioscience 54:731–739CrossRefGoogle Scholar
  33. McCormick MK, Kettenring KM, Baron HM, Whigham DF (2010) Spread of invasive Phragmites australis in estuaries with differing degrees of development: genetic patterns, Allee effects and interpretation. J Ecol 98:1369–1378CrossRefGoogle Scholar
  34. McKinley DC, Romero JC, Hungate BA, Drake BG, Megonigal JP (2009) Does deep soil N availability sustain long-term ecosystem responses to elevated CO2? Global Change Biol 15:2035–2048CrossRefGoogle Scholar
  35. Megonigal JP, Neubauer SC (2009) Biogeochemistry of tidal freshwater wetlands. In: Gerardo EW, Perillo ME, Cahoon DR, Brinson MM (eds) Coastal wetlands: an integrated ecosystem approach, Elsevier, The Netherlands, pp 535–562Google Scholar
  36. Meschter J (2015) Effects of phragmites australis (Common Reed) invasion on nitrogen cycling: porewater chemistry and vegetation structure in a Brackish Tidal Marsh of the Rhode River, Maryland. M.S. Thesis. University of Maryland, College Park, MD. doi: 10.13016/M20W78
  37. Meyerson LA, Vogt KA, Chambers RM (2000) Linking the success of Phragmites to the alteration of ecosystem nutrient cycles. In: Weinstein MP, Kreeger DA (eds) Concepts and controversies in tidal marsh ecology. Kluwer Academic Publishers, Dordrecht, pp 827–844Google Scholar
  38. Moore GE, Burdick DM, Peter CR, Keirstead DR (2012) Belowground biomass of Phragmites australis in coastal marshes. Northeast Nat 19:611–626CrossRefGoogle Scholar
  39. Mozdzer TJ, Megonigal JP (2012) Jack-and-master trait responses to elevated CO2 and N: a comparison of native and introduced Phragmites australis. Plos One 7(10):1–10. doi: 10.1371/journal.pone.0042794
  40. Mozdzer TJ, Zieman JC (2010) Ecophysiological differences between genetic lineages facilitate the invasion of non-native Phragmites australis in North American Atlantic coast wetlands. J Ecol 98:451–458CrossRefGoogle Scholar
  41. Mozdzer TJ, Patrick MJ (2013) Increased methane emissions by an introduced phragmites australis lineage under global change. Wetlands 33(4):609–615. doi: 10.1007/s13157-013-0417-x
  42. Mueller P, Hager RN, Meschter JE, Mozdzer TJ, Langley JA, Jensen K, Megonigal JP (2016) Complex invader-ecosystem interactions and seasonality mediate the impact of non-native phragmites on CH4 emissions. Biol Invasions. doi: 10.1007/s10530-016-1093-6 Google Scholar
  43. Nehring S, Hesse KJ (2008) Invasive alien plants in marine protected areas: the Spartina anglica affair in the European Wadden Sea. Biol Invasions 10:937–950CrossRefGoogle Scholar
  44. Norby RJ, Warren JM, Iversen CM, Medlyn BE, McMurtrie RE (2010) CO2 enhancement of forest productivity constrained by limited nitrogen availability. Proc Natl Acad Sci USA 107:19368–19373CrossRefPubMedPubMedCentralGoogle Scholar
  45. Pimentel D, Zuniga R, Morrison D (2005) Update on the environmental and economic costs associated with alien-invasive species in the United States. Ecol Econ 52:273–288CrossRefGoogle Scholar
  46. Qin P, Zong CX (1992) Applied studies on Spartina. Ocean Press, BeijingGoogle Scholar
  47. Rooth JE, Stevenson JC, Cornwall JC (2003) Increased sediment accretion rates following invasion by Phragmites australis: the role of litter. Estuaries 26:475–483CrossRefGoogle Scholar
  48. Ruhl H, Rybicki N (2010) Long-term reductions in anthropogenic nutrients link to improvements in Chesapeake Bay habitat. Proc Natl Acad Sci USA 107(38):16566–16570Google Scholar
  49. Rundel PW, Dickie IA, Richardson DM (2014) Tree invasions into treeless areas: mechanisms and ecosystem processes. Biol Invasions. doi: 10.1007/s10530-013-0614-9 Google Scholar
  50. Saltonstall K (2002) Cryptic invasion by a non-native genotype of the common reed, Phragmites australis, into North America. Proc Natl Acad Sci USA 99:2445–2449CrossRefPubMedPubMedCentralGoogle Scholar
  51. Saunders CJ, Megonigal JP, Reynolds JF (2006) Comparison of belowground biomass in C3- and C4- dominated mixed communities in a Chesapeake Bay brackish marsh. Plant Soil 280(1–2):305–322Google Scholar
  52. Sorte CJB, Ibáñez I, Blumenthal DM, Molinari NA, Miller LP, Grosholz ED, Diez JM, D’Antonio CM, Olden JD, Jones SJ, Dukes JS (2013) Poised to prosper? A cross-system comparison of climate change effects on native and non-native species performance. Ecol Lett 16:261–270CrossRefPubMedGoogle Scholar
  53. 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
  54. van Groenigen KJ, Osenberg CW, Hungate BA (2011) Increased soil emissions of potent greenhouse gases under increased atmospheric CO(2). Nature 475:214CrossRefPubMedGoogle Scholar
  55. Vitousek PM, D’antonio CM, Loope LL, Rejmanek M, Westbrooks R (1997) Introduced species: a significant component of human-caused global change. NZ J Ecol 21:1–16Google Scholar
  56. Wang Q, Wang CH, Zhao B, Ma ZJ, Luo YQ, Chen JK, Li B (2006) Effects of growing conditions on the growth of and interactions between salt marsh plants: implications for invasibility of habitats. Biol Invasions 8:1547–1560CrossRefGoogle Scholar
  57. Windham L, Ehrenfeld JG (2003) Net impact of a plant invasion on nitrogen-cycling processes within a brackish tidal marsh. Ecol Appl 13:883–896CrossRefGoogle Scholar
  58. Windham L, Lathrop RG (1999) Effects of Phragmites australis (common reed) invasion on aboveground biomass and soil properties in brackish tidal marsh of the Mullica River, New Jersey. Estuaries 22:927–935CrossRefGoogle Scholar
  59. Windham L, Meyerson LA (2003) Effects of common reed (Phragmites australis) expansions on nitrogen dynamics of tidal marshes of the northeastern US. Estuaries 26:452–464CrossRefGoogle Scholar
  60. Wolf AA, Drake BG, Erickson JE, Megonigal JP (2007) An oxygen-mediated positive feedback between elevated carbon dioxide and soil organic matter decomposition in a simulated anaerobic wetland. Glob Change Biol 13:2036–2044CrossRefGoogle Scholar
  61. Zhu BA, Cheng WX (2011) C-13 isotope fractionation during rhizosphere respiration of C-3 and C-4 plants. Plant Soil 342:277–287CrossRefGoogle Scholar

Copyright information

© Springer International Publishing Switzerland (outside the USA) 2016

Authors and Affiliations

  • Thomas J. Mozdzer
    • 1
  • J. Adam Langley
    • 2
  • Peter Mueller
    • 3
  • J. Patrick Megonigal
    • 4
  1. 1.Department of BiologyBryn Mawr CollegeBryn MawrUSA
  2. 2.Department of BiologyVillanova UniversityVillanovaUSA
  3. 3.Applied Plant Ecology, Biocenter Klein FlottbekUniversity of HamburgHamburgGermany
  4. 4.Smithsonian Environmental Research CenterEdgewaterUSA

Personalised recommendations