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Nocturnal and seasonal patterns of carbon isotope composition of leaf dark-respired carbon dioxide differ among dominant species in a semiarid savanna

  • Physiological ecology - Original Paper
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Abstract

The C isotope composition of leaf dark-respired CO2 (δ13Cl) integrates short-term metabolic responses to environmental change and is potentially recorded in the isotopic signature of ecosystem-level respiration. Species differences in photosynthetic pathway, resource acquisition and allocation patterns, and associated isotopic fractionations at metabolic branch points can influence δ13Cl, and differences are likely to be modified by seasonal variation in drought intensity. We measured δ13Cl in two deep-rooted C3 trees (Prosopis velutina and Celtis reticulata), and two relatively shallow-rooted perennial herbs (a C3 dicot Viguiera dentata and a C4 grass Sporobolus wrightii) in a floodplain savanna ecosystem in southeastern Arizona, USA during the dry pre-monsoon and wet monsoon seasons. δ13Cl decreased during the nighttime and reached minimum values at pre-dawn in all species. The magnitude of nocturnal shift in δ13Cl differed among species and between pre-monsoon and monsoon seasons. During the pre-monsoon season, the magnitude of the nocturnal shift in δ13Cl in the deep-rooted C3 trees P. velutina (2.8 ± 0.4‰) and C. reticulata (2.9 ± 0.2‰) was greater than in the C3 herb V. dentata (1.8 ± 0.4‰) and C4 grass S. wrightii (2.2 ± 0.4‰). The nocturnal shift in δ13Cl in V. dentata and S. wrightii increased to 3.2 ± 0.1‰ and 4.6 ± 0.6‰, respectively, during the monsoon season, but in C3 trees did not change significantly from pre-monsoon values. Cumulative daytime net CO2 uptake was positively correlated with the magnitude of the nocturnal decline in δ13Cl across all species, suggesting that nocturnal δ13Cl may be controlled by 13C/12C fractionations associated with C substrate availability and C metabolite partitioning. Nocturnal patterns of δ13Cl in dominant plant species in the semiarid savanna apparently have predictable responses to seasonal changes in water availability, which is important for interpreting and modeling the C isotope signature of ecosystem-respired CO2.

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Abbreviations

A :

Leaf net CO2 assimilation rate (μmol m−2 s−1)

a :

Fractionation against 13C during CO2 diffusion through air (‰)

Acetyl CoA:

Acetyl coenzyme A

b :

Net fractionation against 13C associated with carboxylation in C3 plants (‰)

b 3 :

Fractionation against 13C associated with Rubisco carboxylation in C4 plants (‰)

b 4 :

Fractionation against 13C associated with dissolution of CO2 to HCO3 − and fixation by PEPc (‰)

c a :

Ambient air CO2 concentration (ppm)

c i :

CO2 concentration in the leaf internal air space (ppm)

δ13Ca :

C isotope composition of atmospheric CO2 (‰)

δ13Cb :

C isotope composition of bulk leaf biomass (‰)

δ13Cl :

C isotope composition of leaf dark-respired CO2 (‰)

δ13Clipid :

C isotope composition of leaf lipids (‰)

δ13Clw :

C isotope composition of nighttime leaf-respired CO2 weighted by respiration flux rate (‰)

δ13Cp :

C isotope composition of photosynthate (‰)

δ13Cpw :

Cumulative C isotope composition of the recently fixed photosynthate weighted by net photosynthesis flux rate (‰)

δ13CR :

C isotope composition of ecosystem respiration (‰)

δ13Cs :

C isotope composition of starch (‰)

ΔP :

Photosynthetic C isotope discrimination (‰)

ΔR,biomass :

Respiratory apparent 13C/12C fractionation with leaf biomass as putative respiratory substrate (‰)

ΔR,lipid :

Respiratory apparent 13C/12C fractionation with leaf lipids as putative respiratory substrate (‰)

ΔR,photosynthate :

Respiratory apparent 13C/12C fractionation with cumulative photosynthates at 1800 hours as putative respiratory substrate (‰)

ΔR,starch :

Respiratory apparent 13C/12C fractionation with leaf starch as putative respiratory substrate (‰)

D l :

Leaf-to-air vapor pressure deficit (kPa)

g s :

Stomatal conductance (mol m−2 s−1)

NAD-ME:

Nicotinamide adenine dinucleotide malic enzyme

NEE:

Net ecosystem CO2 exchange

PAR:

Photosynthetically active radiation (μmol m−2 s−1)

PDH:

Pyruvate dehydrogenase

PEPc:

Phosphoenolpyruvate carboxylase

ϕ :

Leakiness of the bundle sheath to CO2 in C4 plants (unitless)

Ψ :

Leaf water potential (MPa)

Ψ pd :

Pre-dawn leaf water potential (MPa)

R :

Leaf respiration rate (μmol m−2 s−1)

Rubisco:

Ribulose-1,5-bisphosphate carboxylase/oxygenase

s :

Fractionation against 13C associated with diffusion of CO2 out of bundle sheath cells in C4 plants (‰)

TCA cycle:

Tricarboxylic acid cycle

References

  • Archer S, Boutton TW, Hibbard KA (2001) Trees in grasslands: biogeochemical consequences of woody plant expansion. In: Schulze E-D et al (eds) Global biogeochemical cycles in the climate system. Academic Press, San Diego, pp 115–137

    Chapter  Google Scholar 

  • Benner R, Fogel ML, Sprague EK, Hodson RE (1987) Depletion of 13C in lignin and its implications for stable carbon isotope studies. Nature 329:708–710

    Article  CAS  Google Scholar 

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

    Article  Google Scholar 

  • Bowling DR, Sargent SD, Tanner BD, Ehleringer JR (2003) Tunable diode laser absorption spectroscopy for stable isotope studies of ecosystem-atmosphere CO2 exchange. Agric For Meteorol 118:1–19

    Article  Google Scholar 

  • Bowling DR, Pataki DE, Randerson JT (2008) Carbon isotopes in terrestrial ecosystem pools and CO2 fluxes. New Phytol 178:24–40

    Article  CAS  PubMed  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 

  • Chikaraishi Y, Naraoka H (2001) Organic hydrogen-carbon isotope signatures of terrestrial higher plants during biosynthesis for distinctive photosynthetic pathways. Geochem J 35:451–458

    CAS  Google Scholar 

  • Collister JW, Rieley G, Stern B, Eglinton G, Fry B (1994) Compound-specific δ13C analyses of leaf lipids from plants with differing carbon dioxide metabolisms. Org Geochem 21:619–627

    Article  CAS  Google Scholar 

  • Deniro MJ, Epstein S (1977) Mechanism of carbon isotope fractionation associated with lipid-synthesis. Science 197:261–263

    Article  CAS  PubMed  Google Scholar 

  • Duranceau M, Ghashghaie J, Badeck F, Deleens E, Cornic G (1999) δ13C of CO2 respired in the dark in relation to δ13C of leaf carbohydrates in Phaseolus vulgaris L. under progressive drought. Plant Cell Environ 22:515–523

    Article  Google Scholar 

  • Edwards G, Walker DA (1983) C3, C4: mechanisms, and cellular and environmental regulation, of photosynthesis. University of California Press, Berkeley

    Google Scholar 

  • Farquhar GD (1983) On the nature of carbon isotope discrimination in C4 species. Aust J Plant Physiol 10:205–226

    Article  CAS  Google Scholar 

  • Farquhar GD, O’Leary MH, Berry JA (1982) On the relationship between carbon isotope discrimination and the intercellular carbon dioxide concentration in leaves. Aust J Plant Physiol 9:121–137

    Article  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Gessler A et al (2009) On the metabolic origin of the carbon isotope composition of CO2 evolved from darkened light-acclimated leaves in Ricinus communis. New Phytol 181:374–386

    Article  CAS  PubMed  Google Scholar 

  • Ghashghaie J, Duranceau M, Badeck F-W (2001) δ13C of CO2 respired in the dark in relation to δ13C of leaf metabolites: comparison between Nicotiana sylvestris and Helianthus annuus under drought. Plant Cell Environ 24:505–515

    Article  CAS  Google Scholar 

  • Ghashghaie J, Badeck F-M, Lanigan G (2003) Carbon isotope fractionation during dark respiration and photorespiration in C3 plants. Phytochem Rev 2:145–161

    Article  CAS  Google Scholar 

  • Gleixner G, Schmidt HL (1997) Carbon isotope effects on the fructose-1, 6-bisphosphate aldolase reaction, origin for non-statistical 13C distributions in carbohydrates. J Biol Chem 272:5382–5387

    Article  CAS  PubMed  Google Scholar 

  • Göttlicher S, Knohl A, Wanek W, Buchmann N, Richter A (2006) Short-term changes in carbon isotope composition of soluble carbohydrates and starch: from canopy leaves to the root system. Rapid Commun Mass Spectrom 20:653–660

    Article  PubMed  Google Scholar 

  • Grover HD, Musick HB (1990) Shrubland and encroachment in southern New Mexico, USA: an analysis of desertification processes in the American Southwest. Clim Change 17:305–330

    Article  Google Scholar 

  • Hattersley PW (1992) C4 photosynthetic pathway variation in grasses (Poaceae): its significance for arid and semi-arid lands. In: Chapman GP (ed) Desertified grassland: their biology and management. Academic Press, London, pp 181–212

    Google Scholar 

  • Hobbie EA, Werner RA (2004) Intramolecular, compound-specific, and bulk carbon isotope patterns in C3 and C4 plants: a review and synthesis. New Phytol 161:371–385

    Article  CAS  Google Scholar 

  • Hultine KR, Williams DG, Burgess SSO, Keefer TO (2003) Contrasting patterns of hydraulic redistribution in three desert phreatophytes. Oecologia 135:167–175

    CAS  PubMed  Google Scholar 

  • Hymus GJ, Maseyk K, Valentini R, Yakir D (2005) Large daily variation in 13C-enrichment of leaf-respired CO2 in two Quercus forest canopies. New Phytol 167:377–384

    Article  CAS  PubMed  Google Scholar 

  • Jackson RB, Banner JL, Jobbagy EG, Pockman WT, Wall DH (2002) Ecosystem carbon loss with woody plant invasion of grasslands. Nature 418:623–626

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Knapp AK et al (2008) Shrub encroachment in North American grasslands: shifts in growth form dominance rapidly alters control of ecosystem carbon inputs. Glob Change Biol 14:615–623

    Article  Google Scholar 

  • Knohl A, Werner RA, Brand WA, Buchmann N (2005) Short-term variations in δ13C of ecosystem respiration reveals link between assimilation and respiration in a deciduous forest. Oecologia 142:70–82

    Article  PubMed  Google Scholar 

  • Lai CT, Schauer AJ, Owensby C, Ham JM, Ehleringer JR (2003) Isotopic air sampling in a tallgrass prairie to partition net ecosystem CO2 exchange. J Geophys Res Atmos 108:D18(4566)

    Google Scholar 

  • Mook WG, Bommerso JC, Staverma WH (1974) Carbon isotope fractionation between dissolved bicarbonate and gaseous carbon dioxide. Earth Planet Sci Lett 22:169–176

    Article  CAS  Google Scholar 

  • Ogee J et al (2003) Partitioning net ecosystem carbon exchange into net assimilation and respiration using 13CO2 measurements: a cost-effective sampling strategy. Glob Biogeochem Cycles 17:1070

    Article  Google Scholar 

  • Ohlrogge JB, Jaworski JG (1997) Regulation of fatty acid synthesis. Annu Rev Plant Physiol Plant Mol Biol 48:109–136

    Article  CAS  PubMed  Google Scholar 

  • Pacala SW et al (2001) Consistent land- and atmosphere-based US carbon sink estimates. Science 292:2316–2320

    Article  CAS  PubMed  Google Scholar 

  • Park R, Epstein S (1961) Metabolic fractionation of 13C and 12C in plants. Plant Physiol 36:133–138

    Article  CAS  PubMed  Google Scholar 

  • Pataki DE et al (2003) The application and interpretation of Keeling plots in terrestrial carbon cycle research. Glob Biogeochem Cycles 17:1022

    Article  Google Scholar 

  • Peisker M, Henderson SA (1992) Carbon: terrestrial C4 plants. Plant Cell Environ 15:987–1004

    Article  CAS  Google Scholar 

  • Peylin P et al (2005) Multiple constraints on regional CO2 flux variations over land and oceans. Glob Biogeochem Cycles 19:GB221

    Article  Google Scholar 

  • Poorter R (1989) Interspecific variation in relative growth rate: on ecological cause and physiological consequences. In: Lambers H, Cambridge ML, Konings H, Pons TL (eds) Causes and consequences of variation in growth rate and productivity of higher plants. SPB, The Hague, pp 45–68

    Google Scholar 

  • Potts DL, Huxman TE, Scott RL, Williams DG, Goodrich DC (2006) The sensitivity of ecosystem carbon exchange to seasonal precipitation and woody plant encroachment. Oecologia 150:453–463

    Article  CAS  PubMed  Google Scholar 

  • Prater JL, Behzad M, Jeffery PC (2006) Diurnal variation of the δ13CR of pine needle respired CO2 evolved in darkness. Plant Cell Environ 29:202–211

    Article  CAS  PubMed  Google Scholar 

  • Prentice IC, Farquhar GD, Fasham MJR (2001) The carbon cycle and atmospheric carbon dioxide. In: Houghton JT, Ding Y (eds) Climate change 2001: the scientific basis. Contribution of Working Group I to the third assessment report of the Intergovermental Panel on Climate Change. Cambridge University Press, Cambridge, pp 183–237

    Google Scholar 

  • Priault P, Wegener F, Werner C (2009) Pronounced differences in diurnal variation of carbon isotope composition of leaf respired CO2 among functional groups. New Phytol 181:400–412

    Article  CAS  PubMed  Google Scholar 

  • Rossmann A, Butzenlechner M, Schmidt HL (1991) Evidence for a nonstatistical carbon isotope distribution in natural glucose. Plant Physiol 96:609–614

    Article  CAS  PubMed  Google Scholar 

  • Schnyder H, Lattanzi FA (2005) Partitioning respiration of C3–C4 mixed communities using the natural abundance 13C approach—testing assumptions on a controlled environment. Plant Biol 7:592–600

    Article  CAS  PubMed  Google Scholar 

  • Scott RL, Edwards EA, Shuttleworth WJ, Huxman TE, Watts C, Goodrich DC (2004) Interannual and seasonal variation in fluxes of water and carbon dioxide from a riparian woodland ecosystem. Agric For Meteorol 122:65–84

    Article  Google Scholar 

  • Scott RL, Huxman TS, Williams DG, Goodrich DC (2006) Ecohydrological impacts of woody-plant encroachment: seasonal patterns of water and carbon dioxide exchange within a semiarid riparian environment. Glob Change Biol 12:311–324

    Article  Google Scholar 

  • Shimoda S, Murayama S, Mo W, Oikawa T (2009) Seasonal contribution of C3 and C4 species to ecosystem respiration and photosynthesis estimated from isotopic measurements of atmospheric CO2 at a grassland in Japan. Agric For Meteorol 149:603–613

    Article  Google Scholar 

  • Snyder KA, Williams DG (2000) Water sources used by riparian trees varies among stream types on the San Pedro River, Arizona. Agric For Meteorol 105:227–240

    Article  Google Scholar 

  • Still CJ, Berry JA, Collatz GJ, DeFries RS (2003a) Global distribution of C3 and C4 vegetation: carbon cycle implications. Glob Biogeochem Cycles 17:1006

    Article  Google Scholar 

  • Still CJ, Berry JA, Ribas-Carbo M, Helliker BR (2003b) 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 

  • Sun W, Resco V, Williams DG (2009) Diurnal and seasonal variation in the carbon isotope composition of leaf dark-respired CO2 in velvet mesquite (Prosopis velutina). Plant Cell Environ 32:1390–1400

    Article  CAS  PubMed  Google Scholar 

  • Tazoe Y, Hanba YT, Furumoto T, Noguchi K, Terashima I (2008) Relationships between quantum yield for CO2 assimilation, activity of key enzymes and CO2 leakiness in Amaranthus cruentus, a C4 dicot, grown in high or low light. Plant Cell Physiol 49:19–29

    Article  CAS  PubMed  Google Scholar 

  • Tcherkez G, Farquhar GD (2005) Carbon isotope effect predictions for enzymes involved in the primary carbon metabolism of plant leaves. Funct Plant Biol 32:277–291

    Article  CAS  Google Scholar 

  • Van Auken OW (2000) Shrub invasions of North American semiarid grasslands. Annu Rev Ecol Syst 31:197–215

    Article  Google Scholar 

  • Wanek W, Heintel S, Richter A (2001) Preparation of starch and other carbon fractions from higher plant leaves for stable carbon isotope analysis. Rapid Commun Mass Spectrom 15:1136–1140

    Article  CAS  PubMed  Google Scholar 

  • Werner C et al (2006) Importance of short-term dynamics in carbon isotope ratios of ecosystem respiration (δ13CR) in a Mediterranean oak woodland and linkage to environmental factors. New Phytol 172:330–346

    Article  CAS  PubMed  Google Scholar 

  • Werner C, Hasenbein N, Maia R, Beyschlag W, Maguas C (2007) Evaluating high time-resolved changes in carbon isotope ratio of respired CO2 by a rapid in-tube incubation technique. Rapid Commun Mass Spectrom 21:1353–1360

    Article  Google Scholar 

  • Williams DG et al (2001) Carbon isotope discrimination by Sorghum bicolor under CO2 enrichment and drought. New Phytol 150:285–293

    Article  CAS  Google Scholar 

  • Xu C, Lin GH, Griffin K, 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, Sternberg LDL (2000) The use of stable isotopes to study ecosystem gas exchange. Oecologia 123:297–311

    Article  Google Scholar 

  • Yakir D, Wang XF (1996) Fluxes of CO2 and water between terrestrial vegetation and the atmosphere estimated from isotope measurements. Nature 380:515–517

    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 

  • Zeeman SC, Smith SM, Smith AM (2007) The diurnal metabolism of leaf starch. Biochem J 401:13–28

    Article  CAS  PubMed  Google Scholar 

  • Zhang J, Griffis TJ, Baker JM (2006) Using continuous stable isotope measurements to partition net ecosystem CO2 exchange. Plant Cell Environ 29:483–496

    Article  CAS  PubMed  Google Scholar 

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Acknowledgments

This research was supported by NSF (DEB-0414680). We thank C. Werner for providing valuable comments on an earlier version of this manuscript. S. Sharma and W. Cable helped with C isotope analysis and R. Scott, T. Huxman, S. Chen and G. Barron-Gafford supported the field work.

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Author notes

  1. Wei Sun

    Present address: School of Biological Sciences, Washington State University, Pullman, WA, 99164-4236, USA

  2. Víctor Resco

    Present address: Centro de Investigación del Fuego, Fundación General de Medio Ambiente de Castilla-La Mancha, 45071, Toledo, Spain

Authors and Affiliations

  1. Department of Renewable Resources, University of Wyoming, Laramie, WY, 82071, USA

    Wei Sun & Víctor Resco

  2. Departments of Renewable Resources and Botany, University of Wyoming, Laramie, WY, 82071, USA

    David G. Williams

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  1. Wei Sun
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Correspondence to Wei Sun.

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Communicated by Marilyn Ball.

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Sun, W., Resco, V. & Williams, D.G. Nocturnal and seasonal patterns of carbon isotope composition of leaf dark-respired carbon dioxide differ among dominant species in a semiarid savanna. Oecologia 164, 297–310 (2010). https://doi.org/10.1007/s00442-010-1643-z

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