Skip to main content
SpringerLink
Log in

Wetting and drying cycles drive variations in the stable carbon isotope ratio of respired carbon dioxide in semi-arid grassland

  • Ecosystem Ecology - Original Paper
  • Published:
Oecologia Aims and scope Submit manuscript

Abstract

In semi-arid regions, where plants using both C3 and C4 photosynthetic pathways are common, the stable C isotope ratio (δ13C) of ecosystem respiration (δ13CR) is strongly variable seasonally and inter-annually. Improved understanding of physiological and environmental controls over these variations will improve C cycle models that rely on the isotopic composition of atmospheric CO2. We hypothesized that timing of precipitation events and antecedent moisture interact with activity of C3 and C4 grasses to determine net ecosystem CO2 exchange (NEE) and δ13CR. Field measurements included CO2 and δ13C fluxes from the whole ecosystem and from patches of different plant communities, biomass and δ13C of plants and soils over the 2000 and 2001 growing seasons. NEE shifted from C source to sink in response to rainfall events, but this shift occurred after a time lag of up to 2 weeks if a dry period preceded the rainfall. The seasonal average of δ13CR was higher in 2000 (−16‰) than 2001 (20‰), probably due to drier conditions during the 2000 growing season (79.7 mm of precipitation from April up to and including July) than in 2001 (189 mm). During moist conditions, δ13C averaged −22‰ from C3 patches, −16‰ from C4 patches, and −19‰ from mixed C3 and C4 patches. However, during dry conditions the apparent spatial differences were not obvious, suggesting reduced autotrophic activity in C4 grasses with shallow rooting depth, soon after the onset of dry conditions. Air and soil temperatures were negatively correlated with δ13CR; vapor pressure deficit was a poor predictor of δ13CR, in contrast to more mesic ecosystems. Responses of respiration components to precipitation pulses were explained by differences in soil moisture thresholds between C3 and C4 species. Stable isotopic composition of respiration in semi-arid ecosystems is more temporally and spatially variable than in mesic ecosystems owing to dynamic aspects of pulse precipitation episodes and biological drivers.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4

Similar content being viewed by others

References

  • Austin AT, Yahdjian ML, Stark JM, Belnap J, Porporato A, Norton U, Ravetta DA, Schaeffer SM (2004) Water pulses and biogeochemical cycles in arid and semiarid ecosystems. Oecologia 141:221–235

    Article  PubMed  Google Scholar 

  • Bakwin PS, Tans PP, White JWC, Andres RJ (1998) Determination of the isotopic (13C/12C) discrimination by terrestrial biology from a global network of observations. Global Biogeochem Cycles 12:555–562

    Article  CAS  Google Scholar 

  • Balesdent J, Girardin C, Mariotti A (1993) Site-related δ13C of tree leaves and soil organic matter in a temperate forest. Ecology 74:1713–1721

    Article  Google Scholar 

  • 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 287:2467–2470

    Article  PubMed  CAS  Google Scholar 

  • Berry SC, Varney GT, Flanagan LB (1997) Leaf δ13C in Pinus resinosa trees and understory plants: variation associated with light and CO2 gradient. Oecologia 109:499–506

    Article  Google Scholar 

  • Bowling DR, Baldocchi DD, Monson RK (1999) Dynamics of isotopic exchange of carbon dioxide in a Tennessee deciduous forest. Global Biogeochem Cycles 13:903–922

    Article  CAS  Google Scholar 

  • Bowling DR, Tans PP, Monson RK (2001) Partitioning net ecosystem carbon exchange with isotopic fluxes of CO2. Glob Change Biol 7:127–145

    Article  Google Scholar 

  • Bowling DR, McDowell NG, Bond BJ, Law BE, Ehleringer JR (2002) 13C content of ecosystem respiration is linked to precipitation and vapor pressure deficit. Oecologia 131:113–124

    Article  Google Scholar 

  • Brugnoli E, Farquhar GD (2000) Photosynthetic fractionation of carbon isotopes. In: Leegood RC, Sharkey TD, von Caemmerer S (eds) Photosynthesis: physiology and metabolism. Kluwer Academic, The Netherlands, pp 399–434

    Google Scholar 

  • Buchmann N, Ehleringer JR (1998) CO2 concentration profiles, and carbon and oxygen isotopes in C3 and C4 crop canopies. Agric For Meteorol 89:45–58

    Article  Google Scholar 

  • Buchmann N, Brooks JR, Rapp KD, Ehleringer JR (1996) Carbon isotope composition of C4 grasses is influenced by light and water supply. Plant Cell Environ 19:392–402

    Article  CAS  Google Scholar 

  • 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 269:1089–1102

    Article  Google Scholar 

  • Conway TJ, Tans PP, Waterman LS, Thoning KW, Kitzis DR, Masarie KA, Zhang N (1994) Evidence of interannual variability of carbon cycle from the National Oceanic and Atmospheric Administration/Climate Monitoring and Diagnosis Laboratory Global Air Sampling Network. J Geophys Res 99:22831–22855

    Article  Google Scholar 

  • Coplen TB (1996) New guidelines for reporting stable hydrogen, carbon, and oxygen isotope-ratio data. Geochem Cosmochim Acta 60:3359–3360

    Article  CAS  Google Scholar 

  • Dugas WA (1993) Micrometeorological and chamber measurements of CO2 flux from bare soil. Agric For Meteorol 67:115–128

    Article  Google Scholar 

  • Dugas WA, Heuer ML, Mayeux HS (1999) Carbon dioxide fluxes over bermudagrass, native prairie, and sorghum. Agric For Meteorol 93:121–139

    Article  Google Scholar 

  • 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 22:515–523

    Article  Google Scholar 

  • Ehleringer JR, Hall AE, Farquhar GD (1993) Stable isotopes and plant carbon-water relations. Academic, San Diego

    Google Scholar 

  • Ehleringer JR, Buchmann N, Flanagan LB (2000) Carbon isotope ratios in belowground carbon cycle processes. Ecol Appl 10:412–422

    Article  Google Scholar 

  • Ekbland A, Högberg P (2001) Natural abundance of 13C in CO2 respired from forest soils reveals speed of link between tree photosynthesis and root respiration. Oecologia 127:305–308

    Article  Google Scholar 

  • Epstein HE, Burke IC, Lauenroth WK (1999) Response of the shortgrass steppe to changes in rainfall seasonality. Ecosystems 2:139–150

    Article  Google Scholar 

  • Farquhar GD, Ehleringer JR, Hubick KT (1989) Carbon isotope discrimination and photosynthesis. Annu Rev Plant Physiol Plant Mol Biol 40:503–537

    Article  CAS  Google Scholar 

  • Fessenden JE, Ehleringer JR (2003) Temporal variation in δ13C of ecosystem respiration in the Pacific Northwest: links to moisture stress. Oecologia 136:129–136

    Article  PubMed  Google Scholar 

  • Flanagan LB, Wever LA, Carlson PJ (2002) Seasonal and interannual variation in carbon dioxide exchange and carbon balance in a northern temperate grassland. Glob Change Biol 8:599–615

    Article  Google Scholar 

  • Franklin JF, Bledsoe CS, Callahan JT (1990) Contributions of the long-term ecological research program. BioScience 40:509–523

    Article  Google Scholar 

  • 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:80–88

    CAS  Google Scholar 

  • Fung I, Field CB, Berry JA, Thompson MV, Randerson JT, Malmstrom CM, Vitousek PM, Collaz GJ, Sellers PJ, Randall DA, Denning AS, Badeck F, John J (1997) 13C exchanges between the atmosphere and biosphere. Global Biogeochem Cycles 11:507–533

    Article  CAS  Google Scholar 

  • Gemery PA, Trolier M, White JWC (1996) Oxygen isotope exchange between carbon dioxide and water following atmospheric sampling using glass flasks. J Geophys Res 101(14):415–420

    Google Scholar 

  • Ghashghaie J, Duranceau M, Badeck FW, Cornic G, Adeline MT, Deleens E (2001) Delta C13 of CO2 respired in the dark in relation to delta C13 of leaf metabolites: comparison between Nicotiana sylvestris and Helianthus annuus under drought. Plant Cell Environ 4:505–515

    Article  Google Scholar 

  • Hunt JE, Kelliher FM, McSeveny TM, Byers JN (2002) Evaporation and carbon dioxide exchange between the atmosphere and a tussock grassland during a summer drought. Agric For Meteorol 111:65–82

    Article  Google Scholar 

  • Huxman TE, Snyder KA, Tissue D, Leffler AJ, Ogle K, Pockman WT, Sandquist DR, Potts DL, Schwinning S (2004) Precipitation pulses and carbon fluxes in semiarid and arid ecosystems. Oecologia 141:254–268

    PubMed  Google Scholar 

  • Keeling CD (1958) The concentration and isotopic abundances of atmospheric carbon dioxide in rural areas. Geochem Cosmochim Acta 13:322–334

    Article  CAS  Google Scholar 

  • Keeling CD (1961) The concentration and isotopic abundance of carbon dioxide in rural and marine air. Geochem Cosmochim Acta 24:277–298

    Article  CAS  Google Scholar 

  • Keeling CD, Whorf TP, Wahlen M, van der Pflicht J (1995) Interannual extremes in the rate of rise of atmospheric carbon-di-oxide since 1980. Nature 375:666–670

    Article  CAS  Google Scholar 

  • Keitel C, Matzarakis A, Rennenberg H, Gessler A (2006) Carbon isotopic composition and oxygen isotopic enrichment in phloem and total leaf organic matter of European beech (Fagus sylvatica L.) along a climate gradient. Plant Cell Environ 29:1492–1507

    Article  PubMed  CAS  Google Scholar 

  • Kuchler AW (1974) A new vegetation map for Kansas. Ecology 55:586–604

    Article  Google Scholar 

  • Lauenroth WK, Milchunas DG (1991) Short-grass steppe. In: Coupland RT (ed) Ecosystems of the world 8A: natural grasslands. Elsevier, Amsterdam, pp 183–226

    Google Scholar 

  • Lauteri M, Brugnoli E, Spaccino L (1993) Carbon isotope discrimination in leaf soluble sugars and in whole plant dry matter in Helianthus annuus L. grown under different water conditions. In: Ehleringer JR, Hall AE, Farquhar GD (eds) Stable isotopes and plant carbon-water relations. Academic, San Diego, pp 93–108

    Google Scholar 

  • Lin G, Ehleringer JR (1997) Carbon isotopic fractionation does not occur during dark respiration in C3 and C4 plants. Plant Physiol 114:391–394

    PubMed  CAS  Google Scholar 

  • Lloyd J, Kruijt B, Hollinger DY, Grace J, Francey RJ, Wong S-C, Kelliher FM, Miranda AC, Farquhar GD, Gash JHC, Vygodskaya NN, Wright IR, Miranda HS, Schulze E-D (1996) Vegetation effects on the isotopic composition of atmospheric CO2 at local and regional scales: theoretical aspects and comparison between a rain forest in Amazonia and a boreal forest in Siberia. Aust J Plant Physiol 23:371–399

    Article  Google Scholar 

  • McDowell NG, Bowling DR, Bond BJ, Irvine J, Law BE, Anthoni P, Ehleringer JR (2004) Response of the carbon isotopic content of ecosystem, leaf, and soil respiration to meteorological and physiological driving factors in a Pinus ponderosa ecosystem. Global Biogeochem Cycles 18. doi:1029/2003GB002049

  • Milchunas DG, Lauenroth WK (2001) Belowground primary production by carbon isotope decay and long-term root biomass dynamics. Ecosystems 4:139–150

    Article  CAS  Google Scholar 

  • Monson RK, Littlejohn RO Jr, Williams GJI (1983) Photosynthetic adaptation to temperature in four species from the Colorado shortgrass steppe: a physiological model for coexistence. Oecologia 58:43–51

    Article  Google Scholar 

  • Monson RK, Turnipseed AA, Sparks JP, Harley PC, Scott-Denton LE, Sparks KL, Huxman TE (2002) Carbon sequestration in a high-elevation, subalpine forest. Glob Change Biol 8:459–478

    Article  Google Scholar 

  • Mosier AR, Parton WJ, Phongpan S (1998) Long-term large N and immediate small N addition effects on trace gas fluxes in the Colorado shortgrass steppe. Biol Fertil Soils 28:44–50

    Article  CAS  Google Scholar 

  • Nadelhoffer KJ, Fry B (1988) Controls on natural nitrogen-15 and carbon-13 abundances in forest soil organic matter. Soil Sci Soc Am J 52:1633–1640

    Google Scholar 

  • Nelson JA, Morgan JA, LeCain DR, Mosier AR, Milchunas DG, Parton WJ (2004) Elevated CO2 increases soil moisture and enhances plant water relations in a long-term field study in semi-arid shortgrass steppe of Colorado. Plant Soil 259:169–179

    Article  CAS  Google Scholar 

  • Ogle K, Reynolds JF (2004) Plant responses to precipitation in desert ecosystems: integrating functional types, pulses, thresholds, and delays. Oecologia 141:282–294

    Article  PubMed  Google Scholar 

  • Pendall E, Del Grosso S, King JY, LeCain DR, Milchunas DG, Morgan JA, Mosier AR, Ojima DS, Parton WJ, Tans PP, White JWC (2003) Elevated atmospheric CO2 effects and soil water feedbacks on soil respiration components in a Colorado grassland. Global Biogeochem Cycles 17:1–13

    Article  CAS  Google Scholar 

  • Phillips DL, Gregg JW (2001) Uncertainty in source partitioning using stable isotopes. Oecologia 127:171–179

    Article  Google Scholar 

  • Pypker TG, Hauck M, Sulzman EW, Unsworth MH, Mix AC, Kayler Z, Conklin D, Kennedy AM, Barnard HR, Philips C, Bond BJ (2008) Toward using δ13C of ecosystem respiration to monitor canopy physiology in complex terrain. Oecologia 158:399–410

    Article  PubMed  CAS  Google Scholar 

  • Reynolds JF, Kemp PR, Ogle K, Fernandez RJ (2004) Modifying the “pulse-reserve” paradigm for deserts of North America: precipitation pulses, soil water and plant responses. Oecologia 141:194–210

    Article  PubMed  Google Scholar 

  • Rosenberg NJ, Blad BL, Verma SB (1983) Microclimate: the biological environment. Wiley, New York

    Google Scholar 

  • Sala OE, Lauenroth WK, Reid CPP (1982) Water relations—a new dimension for niche separation between Bouteloua gracilis and Agropyron smithii in North-American semi-arid grasslands. J Appl Ecol 19:647–657

    Article  Google Scholar 

  • Sala OE, Lauenroth WK, Parton WJ (1992) Long-term soil water dynamics in the shortgrass steppe. Ecology 73:1175–1181

    Article  Google Scholar 

  • Scartazza A, Mata K, Matteucci G, Yakir D, Moscatello S, Brugnoli E (2004) Comparisons of δ13C of photosynthetic products and ecosystem respiratory CO2 and their responses to seasonal climate variability. Oecologia 140:340–351

    Article  PubMed  Google Scholar 

  • Schwinning S, Sala OE (2004) Hierarchy of responses to resource pulses in arid and semi-arid ecosystems. Oecologia 141:211–220

    PubMed  Google Scholar 

  • Sokal RR, Rohlf FJ (1981) Biometry. Freeman, San Francisco

    Google Scholar 

  • Still CJ, Berry JA, Ribas-Carbo M, Helliker BR (2003) The contribution of C3 and C4 plants to the carbon cycle of a tallgrass prairie: an isotopic approach. Oecologia 136:347–359

    Article  PubMed  Google Scholar 

  • Tcherkez G, Nogues S, Bleton J, Cornic G, Badeck F, Ghashghaie J (2003) Metabolic origin of carbon isotope composition of leaf dark-respired CO2 in French bean. Plant Physiol 131:237–244

    Article  PubMed  CAS  Google Scholar 

  • Tieszen LL, Boutton TW (1989) Stable isotopes in ecological research. Springer-Verlag, New York

    Google Scholar 

  • Trolier M, White JWC, Tans PP, Masarie KA, Germery PA (1996) Monitoring the isotopic composition of atmospheric CO2: measurements from the NOAA global air sampling network. J Geophys Res 101:25897–25916

    Article  CAS  Google Scholar 

  • Webb EK, Pearman GI, Leuning R (1980) Correction of flux measurements for density effects due to heat and water vapor transfer. Q J R Meteorol Soc 106:85–100

    Article  Google Scholar 

  • Xu C, Lin G, Griffin KL, Sambrotto RN (2004) Leaf respiratory CO2 is 13C-enriched relative to leaf organic components in five species of C3 plants. New Phytol 163:499–505

    Article  CAS  Google Scholar 

  • Yakir D, Wang X-F (1996) Fluxes of CO2 and water between terrestrial vegetation and the atmosphere estimated from isotope measurements. Nature 380:515–551

    Article  CAS  Google Scholar 

  • Yepez EA, Scott RL, Cable WL, Williams DG (2007) Intraseasonal variation in water and carbon dioxide flux components in a semiarid riparian woodland. Ecosystems 10:1100–1115

    Article  CAS  Google Scholar 

  • Zobitz JM, Burns SP, Ogee J, Reichstein M, Bowling R (2007) Partitioning net ecosystem exchange of CO2: a comparison of a Bayesian/isotope approach to environmental regression methods. J Geophys Res Biogeosci 112. doi:10.1029/2006JG000282

Download references

Acknowledgments

The authors thank Pieter Tans and Jim White for providing flask CO2 concentration and isotope measurements, and Arvin Mosier for providing access to a gas chromatograph. We are very grateful to D. R. LeCain and D. Smith for providing plant biomass and micrometeorological data. David Williams and two thoughtful reviewers provided helpful comments on an earlier draft. This work was supported, in part, by funding from grant National Science Foundation (NSF)-IRC DEB-9977066 001 and grant NSF NNGO4GH63G, and the Biological and Environmental Research Program, U.S. Department of Energy, through the Great Plains Regional Center of the National Institute for Global Environmental Change under Cooperative Agreement DE-FC03-90ER61010.

Author information

Authors and Affiliations

  1. Department of Forest, Rangeland, and Watershed Stewardship, Colorado State University, Fort Collins, CO, 80523, USA

    Jee H. Shim & Dennis S. Ojima

  2. Natural Resource Ecology Laboratory, Colorado State University, Fort Collins, CO, 80523, USA

    Jee H. Shim & Dennis S. Ojima

  3. Department of Botany and Program in Ecology, University of Wyoming, Laramie, WY, 82071, USA

    Elise Pendall

  4. USDA-ARS Rangeland Resources Research Unit, Crops Research Laboratory, 1701 Centre Avenue, Fort Collins, CO, 80526, USA

    Jack A. Morgan

Authors
  1. Jee H. Shim
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Elise Pendall
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Jack A. Morgan
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Dennis S. Ojima
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Elise Pendall.

Additional information

Communicated by Dan Yakir.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Shim, J.H., Pendall, E., Morgan, J.A. et al. Wetting and drying cycles drive variations in the stable carbon isotope ratio of respired carbon dioxide in semi-arid grassland. Oecologia 160, 321–333 (2009). https://doi.org/10.1007/s00442-009-1302-4

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00442-009-1302-4

Keywords

Search

Navigation