, Volume 178, Issue 2, pp 591–601 | Cite as

Plant community change mediates the response of foliar δ15N to CO2 enrichment in mesic grasslands

  • H. Wayne PolleyEmail author
  • Justin D. Derner
  • Robert B. Jackson
  • Richard A. Gill
  • Andrew C. Procter
  • Philip A. Fay
Global change ecology - Original research


Rising atmospheric CO2 concentration may change the isotopic signature of plant N by altering plant and microbial processes involved in the N cycle. CO2 may increase leaf δ15N by increasing plant community productivity, C input to soil, and, ultimately, microbial mineralization of old, 15N-enriched organic matter. We predicted that CO2 would increase aboveground productivity (ANPP; g biomass m−2) and foliar δ15N values of two grassland communities in Texas, USA: (1) a pasture dominated by a C4 exotic grass, and (2) assemblages of tallgrass prairie species, the latter grown on clay, sandy loam, and silty clay soils. Grasslands were exposed in separate experiments to a pre-industrial to elevated CO2 gradient for 4 years. CO2 stimulated ANPP of pasture and of prairie assemblages on each of the three soils, but increased leaf δ15N only for prairie plants on a silty clay. δ15N increased linearly as mineral-associated soil C declined on the silty clay. Mineral-associated C declined as ANPP increased. Structural equation modeling indicted that CO2 increased ANPP partly by favoring a tallgrass (Sorghastrum nutans) over a mid-grass species (Bouteloua curtipendula). CO2 may have increased foliar δ15N on the silty clay by reducing fractionation during N uptake and assimilation. However, we interpret the soil-specific, δ15N–CO2 response as resulting from increased ANPP that stimulated mineralization from recalcitrant organic matter. By contrast, CO2 favored a forb species (Solanum dimidiatum) with higher δ15N than the dominant grass (Bothriochloa ischaemum) in pasture. CO2 enrichment changed grassland δ15N by shifting species relative abundances.


Isotope Plant productivity Soil carbon Soil type Tallgrass prairie 



Chris Kolodziejczyk operated CO2 chambers. Field and laboratory assistance from Anne Gibson, Katherine Jones, Chris Kolodziejczyk, Alicia Naranjo, Kyle Tiner, and numerous students was invaluable. Joseph Craine and Kevin Mueller provided insightful suggestions that improved the manuscript. R.J. acknowledges support from the U.S. Department of Energy (Program in Ecosystem Research #ER64242). Mention of trade names or commercial products does not imply endorsement by the US Department of Agriculture. USDA is an equal opportunity provider and employer.


  1. Bassirirad H, Constable JVH, Lussenhop J, Kimball BA, Norby RJ, Oechel WC, Reich PB, Schlesinger WH, Zitzer S, Sehtiya HL, Silim S (2003) Widespread foliage δ15N depletion under elevated CO2: inferences for the nitrogen cycle. Glob Change Biol 9:1582–1590CrossRefGoogle Scholar
  2. Bechtold JC, Naiman RJ (2006) Soil texture and nitrogen mineralization potential across a riparian toposequence in a semi-arid savanna. Soil Biol Biochem 38:1325–1333CrossRefGoogle Scholar
  3. Billings SA, Schaeffer SM, Zitzer S, Charlet T, Smith SD, Evans RD (2002) Alterations of nitrogen dynamics under elevated carbon dioxide in an intact Mojave Desert ecosystem: evidence from nitrogen-15 natural abundance. Oecologia 131:463–467CrossRefGoogle Scholar
  4. Cambardella C, Elliott E (1992) Particulate soil organic-matter changes across a grassland cultivation sequence. Soil Sci Soc Am J 56:777–783CrossRefGoogle Scholar
  5. Craine JM, Elmore AJ, Aidar MPM, Bustamante M, Dawson TE, Hobbie EA, Kahmen A, Mack MC, McLauchlan KK, Michelsen A, Nardoto GB, Pardo LH, Peñuelas J, Reich PB, Schuur EAG, Stock WD, Templer PH, Virginia RA, Welker JM, Wright IJ (2009) Global patterns of foliar nitrogen isotopes and their relationships with climate, mycorrhizal fungi, foliar nutrient concentrations, and nitrogen availability. New Phytol 183:980–992CrossRefPubMedGoogle Scholar
  6. De Graaff MA, van Groenigen KJ, Six J, Hungate B, van Kessel C (2006) Interactions between plant growth and soil nutrient cycling under elevated CO2: a meta-analysis. Glob Change Biol 12:2077–2091CrossRefGoogle Scholar
  7. Dijkstra FA, Blumenthal D, Morgan JA, Pendall E, Carrillo Y, Follett RF (2010) Contrasting effects of elevated CO2 and warming on nitrogen cycling in a semiarid grassland. New Phytol 187:426–437CrossRefPubMedGoogle Scholar
  8. Evans RD (2001) Physiological mechanisms influencing plant nitrogen isotope composition. Trends Plant Sci 6:121–126CrossRefPubMedGoogle Scholar
  9. Fay PA, Kelley AM, Procter AC, Jin VL, Jackson RB, Johnson HB, Polley HW (2009) Primary productivity and water balance of grassland vegetation on three soils in a continuous CO2 gradient: initial results from the Lysimeter CO2 Gradient Experiment. Ecosystems 12:699–714CrossRefGoogle Scholar
  10. Fay PA, Jin VL, Way DA, Potter KN, Gill RA, Jackson RB, Polley HW (2012) Soil-mediated effects of subambient to increased carbon dioxide on grassland productivity. Nat Clim Change 2:742–746CrossRefGoogle Scholar
  11. Garten CT Jr, Iversen CM, Norby RJ (2011) Litterfall 15N abundance indicates declining soil nitrogen availability in a free-air CO2 enrichment experiment. Ecology 92:133–139CrossRefPubMedGoogle Scholar
  12. Gill RA (2007) Influence of 90 years of protection from grazing on plant and soil processes in the subalpine of the Wasatch Plateau, USA. Rangeland Ecol Manag 60:88–98CrossRefGoogle Scholar
  13. Gill RA, Polley HW, Johnson HB, Anderson LJ, Maherali H, Jackson RB (2002) Nonlinear grassland responses to past and future atmospheric CO2. Nature 417:279–282CrossRefPubMedGoogle Scholar
  14. Gill RA, Anderson LJ, Polley HW, Johnson HB, Jackson RB (2006) Potential nitrogen constraints on soil carbon sequestration under low and elevated atmospheric CO2. Ecology 87:41–52CrossRefPubMedGoogle Scholar
  15. Grace JB (2006) Structural equation modeling and natural systems. Cambridge University Press, CambridgeCrossRefGoogle Scholar
  16. Gu C, Riley WJ (2010) Combined effects of short term rainfall patterns and soil texture on soil nitrogen cycling – a modeling analysis. J Contam Hydrol 112:141–154CrossRefPubMedGoogle Scholar
  17. Handley LL, Scrimgeour CM (1997) Terrestrial plant ecology and 15N natural abundance: the present limits to interpretation for uncultivated systems with original data from a Scottish old-field. Adv Ecol Res 27:133–212CrossRefGoogle Scholar
  18. Hobbie EA, Hobbie JE (2008) Natural abundance of 15N in nitrogen-limited forests and tundra can estimate nitrogen cycling through mycorhizal fungi: a review. Ecosystems 11:815–830CrossRefGoogle Scholar
  19. Hungate BA, Stiling PD, Dijkstra P, Johnson DW, Ketterer ME, Humus GJ, Hinkle CR, Drake BG (2004) CO2 elicits long-term decline in nitrogen fixation. Science 304:1291CrossRefPubMedGoogle Scholar
  20. Johnson DW, Cheng W, Ball JT (2000) Effects of CO2 and N fertilization on decomposition and N immobilization in ponderosa pine litter. Plant Soil 229:203–212Google Scholar
  21. Johnson HB, Polley HW, Whitis RP (2000) Elongated chambers for field studies across atmospheric CO2 gradients. Funct Ecol 14:388–396CrossRefGoogle Scholar
  22. Kahmen A, Wanek W, Buchmann N (2008) Foliar δ15N values characterize soil N cycling and reflect nitrate or ammonium preference of plants along a temperate grassland gradient. Oecologia 156:861–870CrossRefPubMedCentralPubMedGoogle Scholar
  23. Kalcsits LA, Buschhaus HA, Guy RD (2014) Nitrogen isotope discrimination as an integrated measure of nitrogen fluxes, assimilation and allocation in plants. Physiol Plant 151:293–304CrossRefPubMedGoogle Scholar
  24. Kelley AM, Fay PA, Polley HW, Gill RA, Jackson RB (2011) Atmospheric CO2 and soil extracellular enzyme activity: A meta-analysis and CO2 gradient experiment. Ecosphere 2(8):art96CrossRefGoogle Scholar
  25. King JY, Mosier AR, Morgan JA, LeCain DR, Milchunas DG, Parton WJ (2004) Plant nitrogen dynamics in shortgrass steppe under elevated atmospheric carbon dioxide. Ecosystems 7:147–160Google Scholar
  26. Kolb KJ, Evans RD (2003) Influence of nitrogen source and concentration on nitrogen isotope discrimination in two barley genotypes (Hordeum vulgare L.). Plant Cell Environ 16:1431–1440CrossRefGoogle Scholar
  27. Littell RS, Stroup WW, Freund RJ (2002) SAS for linear models, 4th edn. SAS Institute, CaryGoogle Scholar
  28. Luo Y, Su B, Currie WS, Dukes JS, Finzi A, 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
  29. McLauchlan KK, Ferguson CJ, Wilson IE, Ocheltree TW, Craine JM (2010) Thirteen decades of foliar isotopes indicate declining nitrogen availability in central North American grasslands. New Phytol 187:1135–1145CrossRefPubMedGoogle Scholar
  30. Mielnick PS, Dugas WA, Johnson HB, Polley HW, Sanabira J (2001) Net grassland carbon flux over a subambient to superambient CO2 gradient. Glob Change Biol 7:747–754CrossRefGoogle Scholar
  31. Nadelhoffer KJ, Fry B (1988) Controls on natural 15N and 13C abundances in forest soil organic matter. Soil Sci Soc Am J 52:1633–1640CrossRefGoogle Scholar
  32. Peñuelas J, Estiarte M (1997) Trends in plant carbon concentration and plant demand for N throughout this century. Oecologia 109:69–73CrossRefGoogle Scholar
  33. Polley HW, Johnson HB, Derner JD (2002) Soil- and plant-water dynamics in a C3/C4 grassland exposed to a subambient to superambient CO2 gradient. Glob Change Biol 8:1119–1129Google Scholar
  34. Polley HW, Johnson HB, Derner JD (2003) Increasing CO2 from subambient to superambient concentrations alters species composition and increases above-ground biomass in a C3/C4 grassland. New Phytol 160:319–327CrossRefGoogle Scholar
  35. Polley HW, Johnson HB, Fay PA, Sanabria J (2008) Initial response of evapotranspiration from tallgrass prairie vegetation to CO2 at subambient to elevated concentrations. Funct Ecol 22:163–171Google Scholar
  36. Polley HW, Fay PA, Jin VL, Combs GF Jr (2011) CO2 enrichment increases element concentrations in grass mixtures by changing species abundances. Plant Ecol 212:945–957CrossRefGoogle Scholar
  37. Polley HW, Jin VL, Fay PA (2012a) CO2-caused change in plant species composition rivals the shift in vegetation between mid-grass and tallgrass prairies. Glob Change Biol 18:700–710CrossRefGoogle Scholar
  38. Polley HW, Jin VL, Fay PA (2012b) Feedback from plant species change amplifies CO2 enhancement of grassland productivity. Glob Change Biol 18:2813–2823CrossRefGoogle Scholar
  39. Polley HW, Derner JD, Jackson RB, Wilsey BJ, Fay PA (2014) Impacts of climate change drivers on C4 grassland productivity: scaling driver effects through the plant community. J Exp Bot 65:3415–3424CrossRefPubMedGoogle Scholar
  40. Procter AC, Ellis JC, Fay PA, Polley HW, Jackson RB (2014) Fungal community responses to past and future atmospheric CO2 differ by soil type. Appl Environ Microbiol 80:7364–7377CrossRefGoogle Scholar
  41. Robinson D (2001) δ15N as an integrator of the nitrogen cycle. Trends Ecol Evol 16:153–162CrossRefPubMedGoogle Scholar
  42. Robinson D, Conroy JP (1999) A possible plant-mediated feedback between elevated CO2, denitrification and the enhanced greenhouse effect. Soil Biol Biochem 31:43–53CrossRefGoogle Scholar
  43. Shipley B (2000) Cause and correlation in biology: a user’s guide to path analysis, structural equations and causal inference. Cambridge University Press, CambridgeCrossRefGoogle Scholar
  44. Soper FM, Boutton TW, Sparks JP (2014) Investigating patterns of symbiotic nitrogen fixation during vegetation change from grassland to woodland using fine scale δ15N measurements. Plant Cell Environ. doi: 10.1111/pce.12373 PubMedGoogle Scholar
  45. Stock WD, Evans JR (2006) Effects of water availability, nitrogen supply and atmospheric CO2 concentrations on plant nitrogen natural abundance values. Funct Plant Biol 33:219–227CrossRefGoogle Scholar
  46. Tiessen H, Karamanos RE, Stewart JWB, Selles F (1984) Natural nitrogen-15 abundance as an indicator of soil organic matter transformations in native and cultivated soils. Soil Sci Soc Am J 48:312–315CrossRefGoogle Scholar
  47. Wang L, Macko SA (2011) Constrained preferences in nitrogen uptake across plant species and environments. Plant Cell Environ 34:525–534CrossRefPubMedGoogle Scholar
  48. Williams MA, Rice CW, Owensby CE (2006) Natural 15N abundances in a tallgrass prairie ecosystem exposed to 8-y of elevated atmospheric CO2. Soil Biol Biochem 28:409–412CrossRefGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg (outside the USA) 2015

Authors and Affiliations

  • H. Wayne Polley
    • 1
    Email author
  • Justin D. Derner
    • 2
  • Robert B. Jackson
    • 3
    • 4
  • Richard A. Gill
    • 5
  • Andrew C. Procter
    • 6
  • Philip A. Fay
    • 1
  1. 1.Grassland, Soil and Water Research LaboratoryUSDA-Agricultural Research ServiceTempleUSA
  2. 2.High Plains Grasslands Research StationUSDA-Agricultural Research ServiceCheyenneUSA
  3. 3.Nicholas School of the EnvironmentDuke UniversityDurhamUSA
  4. 4.School of Earth SciencesStanford UniversityStanfordUSA
  5. 5.Department of BiologyBrigham Young UniversityProvoUSA
  6. 6.US Environmental Protection AgencyResearch Triangle ParkDurhamUSA

Personalised recommendations