Plant and Soil

, Volume 365, Issue 1–2, pp 41–57

Different plant traits affect two pathways of riparian nitrogen removal in a restored freshwater wetland

  • A. E. Sutton-Grier
  • J. P. Wright
  • C. J. Richardson
Regular Article

Abstract

Background & aims

Plants may have dissimilar effects on ecosystem processes because they possess different attributes. Given increasing biodiversity losses, it is important to understand which plant traits are key drivers of ecosystem functions. To address this question, we studied the response of two ecosystem functions that remove nitrogen (N) from wetland soils, the accumulation of N in plant biomass and denitrification potential (DNP), to variation in plant trait composition.

Methods

Our experiment manipulated plant composition in a riparian wetland. We determined relative importance of plant traits and environmental variables as predictors of each ecosystem function.

Results

We demonstrate that Water Use Efficiency (WUE) had a strong negative effect on biomass N. Root porosity and belowground biomass were negatively correlated with DNP. Trait ordination indicated that WUE was largely orthogonal to traits that maximized DNP.

Conclusions

These results indicate that plant species with different trait values are required to maintain multiple ecosystem functions, and provide a more mechanistic, trait-based link between the recent findings that higher biodiversity is necessary for multi-functionality. While we selected plant traits based on ecological theory, several of the plant traits were not good predictors of each ecosystem function suggesting the ecological theory linking traits to function is incomplete and requires strengthening.

Keywords

Biodiversity and ecosystem function Denitrification potential (DNP) North Carolina Plant traits Wetland restoration 

Abbreviations

AGB

aboveground biomass

AGCN

aboveground biomass carbon to nitrogen ratio

BEF

biodiversity and ecosystem function

BGB

belowground biomass

BGCN

belowground biomass carbon to nitrogen ratio

BGR

Below-ground Rooting Ratio

C

carbon

CO2

carbon dioxide

DEA

Denitrification Enzyme Assay

DNP

denitrification potential

N

nitrogen

NH4-N

extractable ammonium

NO3-N

extractable nitrate + nitrite

POR

root porosity

SEM

structural equation modeling

SLA

specific leaf area

SRL

specific root length

WUE

water use efficiency

References

  1. Arbuckle JL 1995 Amos User’s Guide 7.0. Amos Development Corporation, Spring House, PA.Google Scholar
  2. Balvanera P, Pfisterer AB, Buchmann N, He JS, Nakashizuka T, Raffaelli D, Schmid B (2006) Quantifying the evidence for biodiversity effects on ecosystem functioning and services. Ecol Lett 9:1146–1156PubMedCrossRefGoogle Scholar
  3. Barden LS (1987) Invasion of Microstegium-Vimineum (Poaceae), an Exotic, Annual, Shade-Tolerant, C-4 Grass, into a North-Carolina Floodplain. Am Midl Nat 118:40–45CrossRefGoogle Scholar
  4. Bardgett RD, Mawdsley JL, Edwards S, Hobbs PJ, Rodwell JS, Davies WJ (1999) Plant species and nitrogen effects on soil biological properties of temperate upland grasslands. Funct Ecol 13:650–660CrossRefGoogle Scholar
  5. Brady NC, Weil RR (1999) The Nature and Properties of Soils. Prentice Hall, Upper Saddle River, NJGoogle Scholar
  6. Burke IC, Lauenroth WK, Vinton MA, Hook PB, Kelly RH, Epstein HE, Aguiar MR, Robles MD, Aguilera MO, Murphy KL, Gill RA (1998) Plant-soil interactions in temperate grasslands. Biogeochemistry 42:121–143CrossRefGoogle Scholar
  7. Byrne B M 2010 Structural Equation Modeling with AMOS: Basic concepts, applications, and programming. Routledge, New York, NY, U.S.A.Google Scholar
  8. Callaway JC, Sullivan G, Zedler JB (2003a) Species-Rich Plantings Increase biomass and Nitrogen Accumulation in a Wetland Restoration Experiment. Ecol Appl 13:1626–1639CrossRefGoogle Scholar
  9. Callaway RM, Pennings SC, Richards CL (2003b) Phenotypic plasticity and interactions among plants. Ecology 84:1115–1128CrossRefGoogle Scholar
  10. Cardinale BJ, Srivastava DS, Duffy JE, Wright JP, Downing AL, Sankaran M, Jouseau C (2006) Effects of biodiversity on the functioning of trophic groups and ecosystems. Nature 443:989–992PubMedCrossRefGoogle Scholar
  11. Cavigelli MA, Robertson GP (2000) The functional significance of denitrifier community composition in a terrestrial ecosystem. Ecology 81:1402–1414CrossRefGoogle Scholar
  12. Cavigelli MA, Robertson GP (2001) Role of denitrifier diversity in rates of nitrous oxide consumption in a terrestrial ecosystem. Soil Biol Biochem 33:297–310CrossRefGoogle Scholar
  13. Chapin FS (2003) Effects of plant traits on ecosystem and regional processes: a conceptual framework for predicting the consequences of global change. Ann Bot 91:455–463PubMedCrossRefGoogle Scholar
  14. Chapin FS III, Reynolds HL, D’Antonio CM, Eckhart VM (1996) The functional role of species in terrestrial ecosystems. In: Walker B, Steffan W (eds) Global Change and Terrestrial Ecosystems. Cambridge University Press, Cambridge, U.K, pp 403–428Google Scholar
  15. Chapin FS, Zavaleta ES, Eviner VT, Naylor RL, Vitousek PM, Reynolds HL, Hooper DU, Lavorel S, Sala OE, Hobbie SE, Mack MC, Diaz S (2000) Consequences of changing biodiversity. Nature 405:234–242PubMedCrossRefGoogle Scholar
  16. Cornelissen JHC, Lavorel S, Garnier E, Diaz S, Buchmann N, Gurvich DE, Reich PB, ter Steege H, Morgan HD, van der Heijden MGA, Pausas JG, Poorter H (2003) A handbook of protocols for standardised and easy measurement of plant functional traits worldwide. Aust J Bot 51:335–380CrossRefGoogle Scholar
  17. Cornwell WK, Cornelissen JHC, Amatangelo K, Dorrepaal E, Eviner VT, Godoy O, Hobbie SE, Hoorens B, Kurokawa H, Perez-Harguindeguy N, Quested HM, Santiago LS, Wardle DA, Wright IJ, Aerts R, Allison SD, van Bodegom P, Brovkin V, Chatain A, Callaghan TV, Diaz S, Garnier E, Gurvich DE, Kazakou E, Klein JA, Read J, Reich PB, Soudzilovskaia NA, Vaieretti MV, Westoby M (2008) Plant species traits are the predominant control on litter decomposition rates within biomes worldwide. Ecol Lett 11:1065–1071PubMedCrossRefGoogle Scholar
  18. Craine JM, Tilman D, Wedin D, Reich P, Tjoelker M, Knops J (2002) Functional traits, productivity and effects on nitrogen cycling of 33 grassland species. Funct Ecol 16:563–574CrossRefGoogle Scholar
  19. Cronk JK and Fennessy MS 2001 Adaptations to Growth Conditions in Wetlands. In Wetland Plants: Biology and Ecology. pp 87-145. Lewis Publishers, Boca Raton.Google Scholar
  20. Crush JR (1998) Effect of different forage plants on denitrification potential of Horotiu soil. N Z J Agric Res 41:421–426CrossRefGoogle Scholar
  21. Culley JLB (1993) Density and Compressibility. In: Carter MR (ed) Soil sampling and methods of analysis. Lewis Publishers, Boca Raton, FL, pp 529–539Google Scholar
  22. Diaz S (2001) Ecosystem Function, Measurement, Terrestrial communities. In: Levin SA (ed) Encyclopedia of Biodiversity. Academic, San Diego, pp 321–344CrossRefGoogle Scholar
  23. Diaz S, Cabido M (1997) Plant functional types and ecosystem function in relation to global change. J Veg Sci 8:463–474Google Scholar
  24. Diaz S, Hodgson JG, Thompson K, Cabido M, Cornelissen JHC, Jalili A, Montserrat-Marti G, Grime JP, Zarrinkamar F, Asri Y, Band SR, Basconcelo S, Castro-Diez P, Funes G, Hamzehee B, Khoshnevi M, Perez-Harguindeguy N, Perez-Rontome MC, Shirvany FA, Vendramini F, Yazdani S, Abbas-Azimi R, Bogaard A, Boustani S, Charles M, Dehghan M, de Torres-Espuny L, Falczuk V, Guerrero-Campo J, Hynd A, Jones G, Kowsary E, Kazemi-Saeed F, Maestro-Martinez M, Romo-Diez A, Shaw S, Siavash B, Villar-Salvador P, Zak MR (2004) The plant traits that drive ecosystems: Evidence from three continents. J Veg Sci 15:295–304Google Scholar
  25. Drury CF, McKenney DJ, Findlay WI (1991) Relationships between Denitrification, Microbial Biomass and Indigenous Soil Properties. Soil Biol Biochem 23:751–755CrossRefGoogle Scholar
  26. Duffy JE (2009) Why biodiversity is important to the functioning of real-world ecosystems. Front Ecol Environ 7:437–444CrossRefGoogle Scholar
  27. Dukes JS (2000) Will the increasing atmospheric CO2 concentration affect the success of invasive species? In: Mooney HA, Hobbs RJ (eds) In Invasive species in a changing world. Island Press, Washington, D.C, pp 95–113Google Scholar
  28. Ehrenfeld JG, Ravit B, Elgersma K (2005) Feedback in the plant-soil system. Annu Rev Environ Res 30:75–115CrossRefGoogle Scholar
  29. Engelhardt KA, Ritchie ME (2001) Effects of macrophyte species richness on wetland ecosystem functioning and services. Nature 411:687–689PubMedCrossRefGoogle Scholar
  30. Ettema CH, Lowrance R, Coleman DC (1999) Riparian soil response to surface nitrogen input: temporal changes in denitrification, labile and microbial C and N pools, and bacterial and fungal respiration. Soil Biol Biochem 31:1609–1624CrossRefGoogle Scholar
  31. Eviner VT (2004) Plant traits that influence ecosystem processes vary independently among species. Ecology 85:2215–2229CrossRefGoogle Scholar
  32. Eviner VT, Chapin FS (2003) Functional matrix: A conceptual framework for predicting multiple plant effects on ecosystem processes. Annu Rev Ecol Evol Syst 34:455–485CrossRefGoogle Scholar
  33. Farrar J, Hawes M, Jones D, Lindow S (2003) How roots control the flux of carbon to the rhizosphere. Ecology 84:827–837CrossRefGoogle Scholar
  34. Fornara DA, Tilman D (2008) Plant functional composition influences rates of soil carbon and nitrogen accumulation. J Ecol 96:314–322CrossRefGoogle Scholar
  35. Fornara DA, Tilman D, Hobbie SE (2009) Linkages between plant functional composition, fine root processes and potential soil N mineralization rates. J Ecol 97:48–56CrossRefGoogle Scholar
  36. Gamfeldt L, Hillebrand H, Jonsson PR (2008) Multiple functions increase the importance of biodiversity for overall ecosystem functioning. Ecology 89:1223–1231PubMedCrossRefGoogle Scholar
  37. Grace JB (2006) Structural Equation Modeling and Natural Systems. Cambridge University Press, CambridgeCrossRefGoogle Scholar
  38. Grime JP (1998) Benefits of plant diversity to ecosystems: immediate, filter and founder effects. J Ecol 86:902–910CrossRefGoogle Scholar
  39. Groffman PM (1987) Nitrification and denitrification in soil - A comparison of enzyme assay, incubation and enumeration methods. Plant Soil 97:445–450CrossRefGoogle Scholar
  40. Groffman PM (1994) Denitrification in Freshwater Wetlands. Curr Topics Wetland Biogeochem 1:15–35Google Scholar
  41. Groffman PM, Crawford MK (2003) Denitrification potential in urban riparian zones. J Environ Qual 32:1144–1149PubMedCrossRefGoogle Scholar
  42. Groffman PM, Axelrod EA, Lemunyon JL, Sullivan WM (1991) Denitrification in grass and forest vegetated filter strips. J Environ Qual 20:671–674CrossRefGoogle Scholar
  43. Groffman PN, Holland EA, Myrold DD, Robertson GP, Zou X (1999) Denitrification. In: Robertson GP, Coleman DC, Bledsoe CS, Sollins P (eds) Standard Soil Methods for Long-Term Ecological Research. Oxford University Press, Oxford, U.K, pp 272–288Google Scholar
  44. Hall K 2003 Recommended Native Plant Species for Stream Restoration in North Carolina. North Carolina Stream Restoration Institute, North Carolina State University, Raleigh.Google Scholar
  45. Hector A, Bagchi R (2007) Biodiversity and ecosystem multifunctionality. Nature 448:188–191PubMedCrossRefGoogle Scholar
  46. Hector A, Schmid B, Beierkuhnlein C, Caldeira MC, Diemer M, Dimitrakopoulos PG, Finn JA, Freitas H, Giller PS, Good J, Harris R, Hogberg P, Huss-Danell K, Joshi J, Jumpponen A, Korner C, Leadley PW, Loreau M, Minns A, Mulder CPH, O’Donovan G, Otway SJ, Pereira JS, Prinz A, Read DJ, Scherer-Lorenzen M, Schulze ED, Siamantziouras ASD, Spehn EM, Terry AC, Troumbis AY, Woodward FI, Yachi S, Lawton JH (1999) Plant diversity and productivity experiments in European grasslands. Science 286:1123–1127PubMedCrossRefGoogle Scholar
  47. Hernandez ME, Mitsch WJ (2007) Denitrification potential and organic matter as affected by vegetation community, wetland age, and plant introduction in created wetlands. J Environ Qual 36:333–342PubMedCrossRefGoogle Scholar
  48. Hill AR (1996) Nitrate removal in stream riparian zones. J Environ Qual 25:743–755CrossRefGoogle Scholar
  49. Hill AR, Cardaci M (2004) Denitrification and organic carbon availability in riparian wetland soils and subsurface sediments. Soil Sci Soc Am J 68:320–325CrossRefGoogle Scholar
  50. Hobbie SE (1992) Effects of Plant-Species on Nutrient Cycling. Trends Ecol Evol 7:336–339PubMedCrossRefGoogle Scholar
  51. Hooper DU, Vitousek PM (1997) The effects of plant composition and diversity on ecosystem processes. Science 277:1302–1305CrossRefGoogle Scholar
  52. Hooper DU, Chapin FS, Ewel JJ, Hector A, Inchausti P, Lavorel S, Lawton JH, Lodge DM, Loreau M, Naeem S, Schmid B, Setala H, Symstad AJ, Vandermeer J, Wardle DA (2005) Effects of biodiversity on ecosystem functioning: A consensus of current knowledge. Ecol Monogr 75:3–35CrossRefGoogle Scholar
  53. Houghton JT, Ding Y, Griggs DJ, Noguer M, van der Linden PJ, Dai X, Maskell K, Johnson CA (2001) Technical Summary. In: Houghton JT, Ding Y, Griggs DJ, Noguer M, van der Linden PJ, Dai X, Maskell K, Johnson CA (eds) Climate Change 2001: the Scientific Basis. Contribution of Working Group I to the Third Assessment Report of the Intergovernmental Panel on Climate Change. Cambridge University Press, Cambridge, pp 22–83Google Scholar
  54. Hume NP, Fleming MS, Horne AJ (2002) Denitrification potential and carbon quality of four aquatic plants in wetland microcosms. Soil Sci Soc Am J 66:1706–1712CrossRefGoogle Scholar
  55. Jensen CR, Luxmoore RJ, Vangundy SD, Stolzy LH (1969) Root Air Space Measurements by a Pycnometer Method. Agron J 61:474CrossRefGoogle Scholar
  56. Kerkhoff AJ, Enquist BJ, Elser JJ, Fagan WF (2005) Plant allometry, stoichiometry and the temperature-dependence of primary productivity. Global Ecol Biogeogr 14:585–598CrossRefGoogle Scholar
  57. Kirby R M 1971 Soil Survey of Durham County, North Carolina. USDA Soil Conservation Service.Google Scholar
  58. Knops JMH, Bradley KL, Wedin DA (2002) Mechanisms of plant species impacts on ecosystem nitrogen cycling. Ecol Lett 5:454–466CrossRefGoogle Scholar
  59. Lavorel S, Garnier E (2002) Predicting changes in community composition and ecosystem functioning from plant traits: revisiting the Holy Grail. Funct Ecol 16:545–556CrossRefGoogle Scholar
  60. Lin YF, Jing SR, Wang TW, Lee DY (2002) Effects of macrophytes and external carbon sources on nitrate removal from Zgroundwater in constructed wetlands. Environ Pollut 119:413–420PubMedCrossRefGoogle Scholar
  61. Lowrance R, Hubbard RK (2001) Denitrification from a swine lagoon overland flow treatment system at a pasture-riparian zone interface. J Environ Qual 30:617–624PubMedCrossRefGoogle Scholar
  62. Mack RN, Simberloff D, Lonsdale WM, Evans H, Clout M, Bazzaz FA (2000) Biotic invasions: Causes, epidemiology, global consequences, and control. Ecol Appl 10:689–710CrossRefGoogle Scholar
  63. Martin K, Parsons LL, Murray RE, Smith MS (1988) Dynamics of soil denitrifier populations - Relationships between enzyme-activity, most-probably-number counts, and actual N-gas loss. Appl Environ Microbiol 54:2711–2716PubMedGoogle Scholar
  64. Maynard DG, Kalra YP (1993) Nitrate and Exchangeable Ammonium Nitrogen. In: Carter MR (ed) Soil Sampling and Methods of Analysis. Lewis Publishers, Boca Raton, USA, pp 25–38Google Scholar
  65. McCune B and Grace J B 2002 Structural Equation Modeling. In Analysis of Ecological Communities. MjM Software Design, Gleneden Beach, Oregon.Google Scholar
  66. McCune B and Mefford MJ 1999 PC-ORD. Multivariate Analysis of Ecological Data. Version 4.41. MjM Software, Gleneden Beach, Oregon, U.S.A.Google Scholar
  67. McGill BJ, Enquist BJ, Weiher E, Westoby M (2006) Rebuilding community ecology from functional traits. Trends Ecol Evol 21:178–185PubMedCrossRefGoogle Scholar
  68. McGill BM, Sutton-Grier AE, Wright JP (2010) Plant trait diversity buffers variability in denitrification potential over changes in season and soil conditions. PLoS One 5:e11618PubMedCrossRefGoogle Scholar
  69. Melillo JM, Aber JD, Muratore JF (1982) Nitrogen and Lignin Control of Hardwood Leaf Litter Decomposition Dynamics. Ecology 63:621–626CrossRefGoogle Scholar
  70. Millennium Ecosystem Assessment 2005 Ecosystems and Human Well-Being: Biodiversity Synthesis. World Resources Institute.Google Scholar
  71. Mitsch WJ, Gosselink JG (2000) Wetlands, 3rd edn. John Wiley and Sons, Inc., New York, NY, USAGoogle Scholar
  72. Moraghan JT, Buresh R (1977) Correction for Dissolved Nitrous-Oxide in Nitrogen Studies. Soil Sci Soc Am J 41:1201–1202CrossRefGoogle Scholar
  73. Naeem S, Wright JP (2003) Disentangling biodiversity effects on ecosystem functioning: deriving solutions to a seemingly insurmountable problem. Ecol Lett 6:567–579CrossRefGoogle Scholar
  74. Owensby CE, Ham JM, Knapp AK, Auen LM (1999) Biomass production and species composition change in a tallgrass prairie ecosystem after long-term exposure to elevated atmospheric CO2. Global Change Biol 5:497–506CrossRefGoogle Scholar
  75. Parsons LL, Murray RE, Smith MS (1991) Soil denitrification dynamics - Spatial and temporal variations of enzyme-activity, populations, and nitrogen gas loss. Soil Sci Soc Am J 55:90–95CrossRefGoogle Scholar
  76. Patra AK, Abbadie L, Clays-Josserand A, Degrange V, Grayston SJ, Guillaumaud N, Loiseau P, Louault F, Mahmood S, Nazaret S, Philippot L, Poly F, Prosser JI, Le Roux X (2006) Effects of management regime and plant species on the enzyme activity and genetic structure of N-fixing, denitrifying and nitrifying bacterial communities in grassland soils. Environ Microbiol 8:1005–1016PubMedCrossRefGoogle Scholar
  77. Pinay G, Barbera P, Carreras-Palou A, Fromin N, Sonie L, Couteaux MM, Roy J, Philippot L, Lensi R (2007) Impact of atmospheric CO2 and plant life forms on soil microbial activities. Soil Biol Biochem 39:33–42CrossRefGoogle Scholar
  78. R Development Core Team (2008) R: A Language and Environment for Statistical Computing. R Foundation for Statistical Computing, Vienna, AustriaGoogle Scholar
  79. Reddy KR, Patrick WH, Lindau CW (1989) Nitrification-Denitrification at the Plant Root-Sediment Interface in Wetlands. Limnol Oceanogr 34:1004–1013CrossRefGoogle Scholar
  80. Reich PB, Walters MB, Ellsworth DS (1992) Leaf Life-Span in Relation to Leaf, Plant, and Stand Characteristics among Diverse Ecosystems. Ecol Monogr 62:365–392CrossRefGoogle Scholar
  81. Reich PB, Tjoelker MG, Machado JL, Oleksyn J (2006) Universal scaling of respiratory metabolism, size and nitrogen in plants. Nature 439:457–461PubMedCrossRefGoogle Scholar
  82. Schipper LA, Harfoot CG, McFarlane PN, Cooper AB (1994) Anaerobic decomposition and denitrification during plant decomposition in an organic soil. J Environ Qual 23:923–928CrossRefGoogle Scholar
  83. Smith MS, Tiedje JM (1979) Phases of denitrification following oxygen depletion in soil. Soil Biol Biochem 11:261–267CrossRefGoogle Scholar
  84. Steers RJ, Funk JL, Allen EB (2011) Can resource-use traits predict native vs. exotic plant success in carbon amended soils? Ecol Appl 21:1211–1224PubMedCrossRefGoogle Scholar
  85. Steltzer H, Bowman WD (1998) Differential influence of plant species on soil nitrogen transformations within moist meadow Alpine tundra. Ecosystems 1:464–474CrossRefGoogle Scholar
  86. Storer DA (1984) A simple high sample volume ashing procedure for determination of soil organic matter. Communications in Soil Sciene and Plant Analysis 15:759–772CrossRefGoogle Scholar
  87. Suding KN, Lavorel S, Chapin FS, Cornelissen JHC, Diaz S, Garnier E, Goldberg D, Hooper DU, Jackson ST, Navas ML (2008) Scaling environmental change through the community-level: a trait-based response-and-effect framework for plants. Global Change Biol 14:1125–1140CrossRefGoogle Scholar
  88. Sutherst RW (2000) Climate change and invasive species: A conceptual framework. In: Mooney HA, Hobbs RJ (eds) Invasive species in a changing world. Island Press, Washington, D.C, pp 211–240Google Scholar
  89. Sutton-Grier AE, Megonigal JP (2011) Plant species traits regulate methane production in freshwater wetland soils. Soil Biol Biochem 43:413–420CrossRefGoogle Scholar
  90. Sutton-Grier AE, Ho M, Richardson CJ (2009) Organic amendments improve soil conditions and denitrification in a restored riparian wetland. Wetlands 29:343–352CrossRefGoogle Scholar
  91. Sutton-Grier AE, Wright JP, McGilll BM, Richardson CJ (2011) Environmental Conditions Influence the Plant Functional Diversity Effect on Potential Denitrification. PLoS One 6:e16584PubMedCrossRefGoogle Scholar
  92. Templer P, Findlay S, Lovett G (2003) Soil microbial biomass and nitrogen transformations among five tree species of the Catskill Mountains, New York, USA. Soil Biol Biochem 35:607–613CrossRefGoogle Scholar
  93. Tilman D, Knops J, Wedin D, Reich P, Ricthie M, Siemann E (1997) The Influence of Functional Diversity and Composition on Ecosystem Processes. Science 277:1300–1302CrossRefGoogle Scholar
  94. Tilman D, Reich PB, Knops J, Wedin D, Mielke T, Lehman C (2001) Diversity and Productivity in a Long-Term Grassland Experiment. Science 294:843–845PubMedCrossRefGoogle Scholar
  95. Verville JH, Hobbie SE, Chapin FS, Hooper DU (1998) Response of tundra CH4 and CO2 flux to manipulation of temperature and vegetation. Biogeochemistry 41:215–235CrossRefGoogle Scholar
  96. Vitousek PM (1997) Human domination of Earth’s ecosystems (vol 277, pg 494, 1997). Science 278:21–21Google Scholar
  97. Wardle DA (2002) Communities and Ecosystems: Linking the Aboveground and Belowground Components. Princeton University Press, PrincetonGoogle Scholar
  98. Wardle DA, Barker GM, Bonner KI, Nicholson KS (1998) Can comparative approaches based on plant ecophysiological traits predict the nature of biotic interactions and individual plant species effects in ecosystems? J Ecol 86:405–420CrossRefGoogle Scholar
  99. Wardle DA, Bardgett RD, Klironomos JN, Setala H, van der Putten WH, Wall DH (2004) Ecological linkages between aboveground and belowground biota. Science 304:1629–1633PubMedCrossRefGoogle Scholar
  100. Wedin DA, Tilman D (1990) Species Effects on Nitrogen Cycling - a Test with Perennial Grasses. Oecologia 84:433–441Google Scholar
  101. Westoby M, Wright IJ (2006) Land-plant ecology on the basis of functional traits. Trends Ecol Evol 21:261–268PubMedCrossRefGoogle Scholar
  102. Wittebolle L, Marzorati M, Clement L, Balloi A, Daffonchio D, Heylen K, De Vos P, Verstraete W, Boon N (2009) Initial community evenness favours functionality under selective stress. Nature 458:623–626PubMedCrossRefGoogle Scholar
  103. Wright IJ, Reich PB, Westoby M, Ackerly DD, Baruch Z, Bongers F, Cavender-Bares J, Chapin T, Cornelissen JHC, Diemer M, Flexas J, Garnier E, Groom PK, Gulias J, Hikosaka K, Lamont BB, Lee T, Lee W, Lusk C, Midgley JJ, Navas ML, Niinemets U, Oleksyn J, Osada N, Poorter H, Poot P, Prior L, Pyankov VI, Roumet C, Thomas SC, Tjoelker MG, Veneklaas EJ, Villar R (2004) The worldwide leaf economics spectrum. Nature 428:821–827PubMedCrossRefGoogle Scholar
  104. Zak DR, Holmes WE, White DC, Peacock AD, Tilman D (2003) Plant diversity, soil microbial communities, and ecosystem function: Are there any links? Ecology 84:2042–2050CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media B.V. 2012

Authors and Affiliations

  • A. E. Sutton-Grier
    • 1
  • J. P. Wright
    • 2
  • C. J. Richardson
    • 3
  1. 1.Nicholas School of the Environment and Earth SciencesDuke UniversityDurhamUSA
  2. 2.Biology DepartmentDuke UniversityDurhamUSA
  3. 3.Nicholas School of the Environment and Earth SciencesDuke UniversityDurhamUSA

Personalised recommendations