Oecologia

, Volume 136, Issue 3, pp 347–359 | Cite as

The contribution of C3 and C4 plants to the carbon cycle of a tallgrass prairie: an isotopic approach

  • Christopher J. Still
  • Joseph A. Berry
  • Miquel Ribas-Carbo
  • Brent R. Helliker
Ecophysiology

Abstract

The photosynthetic pathway composition (C3:C4 mixture) of an ecosystem is an important controller of carbon exchanges and surface energy flux partitioning, and therefore represents a fundamental ecophysiological distinction. To assess photosynthetic mixtures at a tallgrass prairie pasture in Oklahoma, we collected nighttime above-canopy air samples along concentration and isotopic gradients throughout the 1999 and 2000 growing seasons. We analyzed these samples for their CO2 concentration and carbon isotopic composition and calculated C3:C4 proportions with a two-source mixing model. In 1999, the C4 percentage increased from 38% in spring (late April) to 86% in early fall (mid-September). The C4 percentages inferred from ecosystem respiration measurements in 2000 indicate a smaller shift, from 67% in spring (early May) to 77% in mid-summer (late July). We also sampled daytime CO2 concentration and carbon isotope gradients above the canopy to determine ecosystem discrimination against 13CO2 during net uptake. These discrimination values were always lower than corresponding nighttime ecosystem respiration isotopic signatures would suggest. After accounting for the isotopic disequilibria between respiration and photosynthesis resulting from seasonal variations in the C3:C4 mixture, we estimated canopy photosynthetic discrimination. The C4 percentage calculated from this approach agrees with the percentage determined from nighttime respiration for sampling periods in both growing seasons. Isotopic imbalances between photosynthesis and respiration are likely to be common in mixed C3:C4 ecosystems and must be considered when using daytime isotopic measurements to constrain ecosystem physiology. Given the global extent of such ecosystems, isotopic imbalances likely contribute to global variations in the carbon isotopic composition of atmospheric CO2.

Keywords

C4 photosynthesis Grassland Carbon isotopes Isotope disequilibrium Discrimination 

References

  1. Battle M, Bender ML, Tans PP, White JWC, Ellis JT, Conway T, Francey RJ (2000) Global carbon sinks and their variability inferred from atmospheric O2 and δ13C. Science 287:2467–2470CrossRefPubMedGoogle Scholar
  2. Benner R, Fogel ML, Sprague EK, Hodson RE (1987) Depletion of C-13 in lignin and its implications for stable carbon isotope studies. Nature 329:708–710Google Scholar
  3. Bowling DR, Baldocchi DD, Monson RK (1999) Dynamics of isotope exchange of carbon dioxide in a Tennessee deciduous forest. Global Biogeochem Cycles 13:903–922CrossRefGoogle Scholar
  4. Bowling DR, McDowell NG, Bond BJ, Law BE, Ehleringer JR (2002) C-13 content of ecosystem respiration is linked to precipitation and vapor pressure deficit. Oecologia 131:113–124CrossRefGoogle Scholar
  5. Buchmann N, Ehleringer JR (1998) CO2 concentration profiles, and carbon and oxygen isotopes in C3 and C4 crop canopies. Agric For Meteorol 89:45–58CrossRefGoogle Scholar
  6. Buchmann N, Brooks JR, Rapp KD, Ehleringer JR (1996) Carbon isotopic composition of C4 grasses is influenced by light and water supply. Plant Cell Environ 19:392–402Google Scholar
  7. Ciais P, Tans PP, Trolier M, White JWC, Francey RJ (1995) A large northern hemisphere terrestrial CO2 sink indicated by the 13C/12C ratio of atmospheric CO2. Science 269:1098–1102Google Scholar
  8. Colello GD, Grivet C, Sellers PJ, Berry JA (1998) Modeling of energy, water, and CO2 flux in a temperate grassland ecosystem with SiB2: May–October 1987. J Atmos Sci 55:1141–1169CrossRefGoogle Scholar
  9. Collatz GJ, Berry JA, Clark JS (1998) Effects of climate and atmospheric CO2 partial pressure on the global distribution of C4 grasses: present, past, and future. Oecologia 114:441–454CrossRefGoogle Scholar
  10. Collins SL, Knapp AK, Briggs JM, Blair JM, Steinauer EM (1998) Modulation of diversity by grazing and mowing in native tallgrass prairie. Science 280:745–747CrossRefPubMedGoogle Scholar
  11. Daniels F, Williams JW, Bender P, Alberty RA (eds) (1962) Experimental physical chemistry. McGraw-Hill, New York, USA, pp 393–417Google Scholar
  12. Duranceau M, Ghashghaie J, Badeck F, Deleens E, Cornic G (1999) Delta C-13 of CO2 respired in the dark in relation to delta C-13 of leaf carbohydrates in Phaseolus vulgaris L-under progressive drought. Plant Cell Environ 22:515–523CrossRefGoogle Scholar
  13. Ehleringer JR (1978) Implications of quantum yield differences to the distributions of C3 and C4 grasses. Oecologia 31:255–267Google Scholar
  14. Ehleringer JR, Cerling TE, Helliker BR (1997) C-4 photosynthesis, atmospheric CO2 and climate. Oecologia 112:285-299CrossRefGoogle Scholar
  15. Ehleringer JR, Buchmann N, Flanagan LB (2000) Carbon isotope ratios in belowground carbon cycle processes. Ecol Appl 10:412–422Google Scholar
  16. Ekblad A, Hogberg P (2001) Natural abundance of C-13 in CO2 respired from forest soils reveals speed of link between tree photosynthesis and root respiration. Oecologia 127:305–308CrossRefGoogle Scholar
  17. Evans JR, Sharkey TD, Berry JA, Farquhar GD (1986) Carbon isotope discrimination measured concurrently with gas-exchange to investigate CO2 diffusion in leaves of higher-plants. Aust J Plant Physiol 13:281–292Google Scholar
  18. Farquhar GD, Ehleringer JR, Hubick KT (1989). Carbon isotope discrimination and photosynthesis. Annu Rev Plant Physiol Mol Biol 40:503–537Google Scholar
  19. Flanagan LB, Ehleringer JR (1998) Ecosystem-atmosphere CO2 exchange: interpreting signals of change using stable isotope ratios. Trends Ecol Evol 13:10–14CrossRefGoogle Scholar
  20. Flanagan LB, Brooks JR, Varney GT, Berry SC, Ehleringer JR (1996) Carbon isotope discrimination during photosynthesis and the isotope ratio of respired CO2 in boreal forest ecosystems. Global Biogeochem Cycles 10:629–40Google Scholar
  21. Francey RJ, Tans PP, Allison C, Enting IG, White JWC, Trolier M (1995) Changes in oceanic and terrestrial carbon uptake since 1982. Nature 373:326–330Google Scholar
  22. Freeman CC (1998) The flora of Konza prairie: a historical review and contemporary patterns. In: Knapp AK, Briggs JM, Hartnett DC, Collins SL (eds) Grassland dynamics. Oxford University Press, New York, pp 69–80Google Scholar
  23. Friedli H, Siegenthaler U, Rauber D, Oeschger H (1987) Measurements of concentration, 13C/12C and 18O/16O ratios of tropospheric carbon dioxide over Switzerland. Tellus 39B:80–88Google Scholar
  24. Ghashghaie J, Duranceau M, Badeck FW, Cornic G, Adeline MT, Deleens E (2001) Delta C-13 of CO2 respired in the dark in relation to delta C-13 of leaf metabolites: comparison between Nicotiana sylvestris and Helianthus annuus under drought. Plant Cell Environ 4:505–515CrossRefGoogle Scholar
  25. Harwood KG, Gillon JS, Roberts A, Griffiths H (1999) Determinants of isotope coupling of CO2 and water vapour within a Quercus petraea forest canopy. Oecologia 119:109–119CrossRefGoogle Scholar
  26. Henderson SA, von Caemmerer S, Farquhar GD (1992) Short-term measurements of carbon isotope discrimination in several C4 species. Aust J Plant Physiol 19:263–285Google Scholar
  27. Keeling CD (1958) The concentrations and isotope abundances of atmospheric carbon dioxide in rural areas. Geochem Cosmochim Acta 13:322–334Google Scholar
  28. Keeling CD (1961) The concentrations and isotope abundances of atmospheric carbon dioxide in rural and marine air. Geochem Cosmochim Acta 24:277–298Google Scholar
  29. Keeling CD, Whorf TP, Wahlen M, Vanderplicht J (1995) Interannual extremes in the rate of rise of atmospheric carbon-dioxide since 1980. Nature 375:666-670Google Scholar
  30. Kemp PR, Williams GJ (1980) A physiological basis for niche separation between Agropyron smythii (C3) and Bouteloua gracilis (C4). Ecology 61:846–858Google Scholar
  31. Knapp AK, Briggs JM, Blair JM, Turner CL (1998) Patterns and controls of aboveground net primary production in tallgrass prairie, In: Knapp AK, Briggs JM, Hartnett DC, Collins SL (eds) grassland dynamics. Oxford University Press, New York, pp193-221Google Scholar
  32. Laws E (1997) Mathematical methods for oceanographers. Wiley, New YorkGoogle Scholar
  33. Lin GH, Ehleringer JR (1997) Carbon isotopic fractionation does not occur during dark respiration in C-3 and C-4 plants. Plant Physiol 114:391-394Google Scholar
  34. Lloyd J, Kruijt B, Hollinger DY, Grace J, Francey RJ, Wong SC, Kelliher FM, Miranda AC, Farquhar GD, Gash JHC, Vygodskaya NN, Wright IR, Miranda HS, Schulze ED (1996) Vegetation effects on the isotopic composition of atmospheric CO2 at local and regional scales: theoretical aspects and a comparison between rain forest in Amazonia and a boreal forest in Siberia. Aust J Plant Physiol 23:371–399Google Scholar
  35. Long SP (1999) Environmental responses. In: Sage RF, Monson RK (eds) C4 plant biology. Academic Press, New York, pp 215–249Google Scholar
  36. Miranda AC, Miranda HS, Lloyd J, Grace J, Francey RJ, McIntyre JA, Meir P, Riggan P, Lockwood R, Brass J (1997) Fluxes of carbon, water and energy over Brazilian cerrado: an analysis using eddy covariance and stable isotopes. Plant Cell Environ 20:315–328Google Scholar
  37. Mole S, Joern A, O'Leary MH, Madhaven S (1994) Spatial and temporal variation in carbon isotope discrimination in prairie graminoids. Oecologia 97:316–321Google Scholar
  38. Morgan MG, Henrion M (1990) Uncertainty: a guide to dealing with uncertainty in quantitative risk and policy analysis. Cambridge University Press, CambridgeGoogle Scholar
  39. Ode DJ, Tieszen Ll, Lerman JC (1980) The seasonal contribution of C-3 and C-4 plant-species to primary production in a mixed prairie. Ecology 61:1304-1311Google Scholar
  40. Pataki DE, Ehleringer JR, Flanagan LB, Yakir D, Bowling DR, Still CJ, Buchmann N, Berry JA (2003) The application and interpretation of Keeling plots in terrestrial carbon cycle research. Global Biogeochem Cycles (in press)Google Scholar
  41. Peisker M, Henderson SA (1992) Carbon: terrestrial C4 plants. Plant Cell Environ 15:987–1004Google Scholar
  42. Raich JW, Schlesinger WH (1992) The global carbon dioxide flux in soil respiration and its relationship to vegetation and climate. Tellus 44B:81–99Google Scholar
  43. Randerson JT, Collatz GJ, Fessenden JE, Munoz AD, Still CJ, Berry JA, Fung IY, Suits N, Denning AS (2002a) A possible global covariance between terrestrial gross primary production and 13C discrimination: consequences for the atmospheric 13C budget and its response to ENSO. Global Biogeochem Cycles 16:1136CrossRefGoogle Scholar
  44. Randerson JT, Still CJ, Balle JJ, Fung IY, Doney SC, Tans PP, Conway TJ, White JWC, Vaughn B, Suits N, Denning AS (2002b) Carbon isotope discrimination of arctic and boreal biomes inferred from remote atmospheric measurements and a biosphere-atmosphere model. Global Biogeochem Cycles 16:1028CrossRefGoogle Scholar
  45. Ribas-Carbo M, Still CJ, Berry JA (2002) An automated system for simultaneous analysis of δ13C, δ18O, and CO2 concentration in small air samples. Rapid Commun Mass Spectrom 16:339–345CrossRefPubMedGoogle Scholar
  46. Sage RF, Wedin DA, Li M (1999) The biogeography of C4 photosynthesis: patterns and controlling factors In: Sage RF, Monson RK (eds) C4 plant biology. Academic Press, New York, pp 313–373Google Scholar
  47. Sokal RR, Rohlf FJ (1995) Biometry: the principles and practice of statistics in biological research. W.H. Freeman, New YorkGoogle Scholar
  48. Still CJ, Berry JA, Collatz GJ, DeFries RS (2003) Global distribution of C3 and C4 vegetation: Carbon cycle implications. Global Biogeochem Cycles 17:1006CrossRefGoogle Scholar
  49. Suyker AE, Verma SB (2001) Year-round observations of the net ecosystem exchange of carbon dioxide in a native tallgrass prairie. Global Change Biol 7:279–289CrossRefGoogle Scholar
  50. Tieszen LL, Reed BC, Bliss NB, Wylie BK, DeJong DD (1997) NDVI, C3 and C4 production, and distributions in Great Plains grassland land cover classes. Ecol Appl 7:59–78CrossRefGoogle Scholar
  51. Yakir D, Sternberg LDL (2000) The use of stable isotopes to study ecosystem gas exchange. Oecologia 123:297–311CrossRefGoogle Scholar
  52. Yakir D, Wang XF (1996) Fluxes of CO2 and water between terrestrial vegetation and the atmosphere estimated from isotope measurements. Nature 380:515–517Google Scholar

Copyright information

© Springer-Verlag 2003

Authors and Affiliations

  • Christopher J. Still
    • 1
    • 3
  • Joseph A. Berry
    • 1
  • Miquel Ribas-Carbo
    • 1
    • 4
  • Brent R. Helliker
    • 2
    • 5
  1. 1.Department of Plant BiologyCarnegie Institution of WashingtonStanfordUSA
  2. 2.Department of BiologyUniversity of UtahSalt Lake CityUSA
  3. 3.Geography DepartmentUC Santa BarbaraSanta BarbaraUSA
  4. 4.Departament de Biologia, Area de Fisiologia VegetalUniversitat de les Illes BalearsIlles BalearsSpain
  5. 5.Department of Plant BiologyCarnegie Institution of WashingtonStanfordUSA

Personalised recommendations