Abstract
Leaf area index (LAI) and its seasonal dynamics are key determinants of terrestrial productivity and, therefore, of the response of ecosystems to a rising atmospheric CO2 concentration. Despite the central importance of LAI, there is very little evidence from which to assess how forest LAI will respond to increasing [CO2]. We assessed LAI and related leaf indices of a closed-canopy deciduous forest for 4 years in 25-m-diameter plots that were exposed to ambient or elevated CO2 (542 ppm) in a free-air CO2 enrichment (FACE) experiment. LAI of this Liquidambar styraciflua (sweetgum) stand was about 6 and was relatively constant year-to-year, including the 2 years prior to the onset of CO2 treatment. LAI throughout the 1999–2002 growing seasons was assessed through a combination of data on photosynthetically active radiation (PAR) transmittance, mass of litter collected in traps, and leaf mass per unit area (LMA). There was no effect of [CO2] on any expression of leaf area, including peak LAI, average LAI, or leaf area duration. Canopy mass and LMA, however, were significantly increased by CO2 enrichment. The hypothesized connection between light compensation point (LCP) and LAI was rejected because LCP was reduced by [CO2] enrichment only in leaves under full sun, but not in shaded leaves. Data on PAR interception also permitted calculation of absorbed PAR (APAR) and light use efficiency (LUE), which are key parameters connecting satellite assessments of terrestrial productivity with ecosystem models of future productivity. There was no effect of [CO2] on APAR, and the observed increase in net primary productivity in elevated [CO2] was ascribed to an increase in LUE, which ranged from 1.4 to 2.4 g MJ−1. The current evidence seems convincing that LAI of non-expanding forest stands will not be different in a future CO2-enriched atmosphere and that increases in LUE and productivity in elevated [CO2] are driven primarily by functional responses rather than by structural changes. Ecosystem or regional models that incorporate feedbacks on resource use through LAI should not assume that LAI will increase with CO2 enrichment of the atmosphere.
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References
Baldocchi DD, Hutchison BA, Matt DR, McMillen RT (1985) Canopy radiative transfer models for spherical and known leaf inclination angle distributions: a test in an oak-hickory forest. J Appl Ecol 22:539–555
Brown CL, Sommer HE (1992) Shoot growth and histogenesis of trees possessing diverse patterns of shoot development. Am J Bot 79:335–346
DeLucia EH, Thomas RB (2000) Photosynthetic responses to CO2 enrichment of four hardwood species in a forest understory. Oecologia 122:11–19
DeLucia EH, George K, Hamilton JG (2002) Radiation-use efficiency of a forest exposed to elevated concentrations of atmospheric carbon dioxide. Tree Physiol 22:1003–1010
Drake BG, Gonzàlez-Meler MA, Long SP (1997) More efficient plants: a consequence of rising atmospheric CO2? Annu Rev Plant Physiol Plant Mol Biol 48:609–639
Egli P, Maurer S, Gunthardt-Goerg MS, Körner C (1998) Effects of elevated CO2 and soil quality on leaf gas exchange and above-ground growth in beech-spruce model ecosystems. New Phytol 140:185–196
Ferris R, Sabatti M, Miglietta F, Mills RF, Taylor G (2001) Leaf area is stimulated in Populus by free air CO2 enrichment (POPFACE), through increased cell expansion and production. Plant Cell Environ 24:305–315
Gielen B, Calfapietra C, Sabatti M, Ceulemans R (2001) Leaf area dynamics in a closed poplar plantation under free-air carbon dioxide enrichment. Tree Physiol 21:1245–1255
Gower ST, Kucharik CJ, Norman JM (1999) Direct and indirect estimation of leaf area index, f(APAR), and net primary production of terrestrial ecosystems. Remote Sensing Environ 70:29–51
Gu L, Baldocchi D, Verma, SB, Black TA, Vesala T, Falge EM, Dowty PR (2002) Advantages of diffuse radiation for terrestrial ecosystem productivity. J Geophys Res 107(No D6):10.1029/2001JD001242
Gunderson CA., Sholtis JD, Wullschleger SD, Tissue DT, Hanson PJ, Norby RJ (2002) Environmental and stomatal control of photosynthetic enhancement in the canopy of a sweetgum (Liquidambar styraciflua L.) plantation during three years of CO2 enrichment. Plant Cell Environ 25:379–393
Hartz-Rubin JS, DeLucia EH (2001) Canopy development of a model herbaceous community exposed to elevated atmospheric CO2 and soil nutrients. Physiol Plant 113:258–266
Hättenschwiler S (2001) Tree seedling growth in natural deep shade: functional traits related to interspecific variation in response to elevated CO2. Oecologia 129:31–42
Hättenschwiler S, Miglietta F, Raschi A, Körner Ch. (1997) Morphological adjustments of mature Quercus ilex trees to elevated CO2. Acta Oecol 18:361–365
Haxeltine A, Prentice IC (1996) A general model for the light-use efficiency of primary production. Funct Ecol 10:551–561
Hendrey GR, Ellsworth DS, Lewin KF, Nagy J (1999) A free-air enrichment system for exposing tall forest vegetation to elevated atmospheric CO2. Global Change Biol 5:293–309
Herrick JD, Thomas RB (1999) Effects of CO2 enrichment on the photosynthetic light response of sun and shade leaves of canopy sweetgum trees (Liquidambar styraciflua) in a forest ecosystem. Tree Physiol 19:779–786
Hirose T, Ackerly DD, Traw MB, Ramseier D, Bazzaz FA (1997) CO2 elevation, canopy photosynthesis, and optimal leaf area index. Ecology 78:2339–2350
Hymus GJ, Pontailler JY, Li J, Stiling P, Hinkle CR, Drake BG (2002) Seasonal variability in the effect of elevated CO2 on ecosystem leaf area index in a scrub-oak ecosystem. Global Change Biol 8:931–940
Jach ME, Ceulemans R, Murray MB (2001) Impacts of greenhouse gases on the phenology of forest trees. In Karnosky DF, Ceulemans R, Scarascia-Mugnozza G, Innes JL (eds) The impact of carbon dioxide and other greenhouse gases on forest ecosystems. CAB International, Wallingford, pp 193–235
Kimball BA, Kobayashi K, Bindi M (2002) Responses of agricultural crops to free-air CO2 enrichment. Adv Agron 77:293–368
Körner C, Arnone JA III (1992) Responses to elevated carbon dioxide in artificial tropical ecosystems. Science 257:1672–1675
Kubiske ME, Pregitzer KS (1996) Effects of elevated CO2 and light availability on the photosynthetic light response of trees of contrasting shade tolerance. Tree Physiol 16:351–358
Lichter J, Lavine M, Mace KA, Richter DD, Schlesinger WH (2000) Throughfall chemistry in a loblolly pine plantation under elevated atmospheric CO2 concentrations. Biogeochemistry 50:73–93
Long SP (1991) Modification of the response of photosynthetic productivity to rising temperature by atmospheric CO2 concentrations—has its importance been underestimated? Plant Cell Environ 14:729–739
Long SP, Drake BG (1991) Effect of the long-term elevation of CO2 concentration in the field on the quantum yield of photosynthesis of the C3 sedge, Scirpus olneyi. Plant Physiol 96:221–226
Luo Y, Medlyn B, Hui D, Ellsworth D, Reynolds JF, Katul G (2001) Gross primary productivity in the Duke Forest: modeling synthesis of the free-air CO2 enrichment experiment and eddy-covariance measurements. Ecol Appl 11:239–252
Medlyn BE (1996) Interactive effects of atmospheric carbon dioxide and leaf nitrogen concentration on canopy light use efficiency: a modeling analysis. Tree Physiol 16:201–209
Medlyn BE (1998) Physiological basis of the light use efficiency model. Tree Physiol 18:167–176
Medlyn BE, Rey A, Barton CVM, Forstreuter M (2001) Above-ground growth response of forest trees to elevated atmospheric CO2 concentrations. In: Karnosky DF, Ceulemans R, Scarascia-Mugnozza G, Innes JL (eds) The impact of carbon dioxide and other greenhouse gases on forest ecosystems. CAB International, Wallingford, pp 127–146
Mussche S, Samson R, Nachtergale L, De Schrijver A, Lemeur R, Lust N (2001) A comparison of optical and direct methods for monitoring the seasonal dynamics of leaf area index in deciduous forests. Silva Fenn 35:373–384
Myneni RB, Keeling CD, Tucker CJ, Asrar G, Nemani RR (1997) Increased plant growth in the northern high latitudes from 1981 to 1991. Nature 386:698–702
Myneni RB, Hoffman S, Knyazikhin Y, Privette JL, Glassy J, Tian Y, Wang Y, Song X, Zhang Y, Smith GR, Lotsch A, Friedl M, Morisette JT, Votava P, Nemani RR, Running SW (2002) Global products of vegetation leaf area and fraction absorbed PAR from year one of MODIS data. Remote Sensing Environ 83:214–231
Neilson RP, Drapek RJ (1998) Potentially complex biosphere responses to transient global warming. Global Change Biol 4:505–521
Neumann HH, Den Hartog G, Shaw RH (1989) Leaf area measurements based on hemispheric photographs and leaf-litter collection in a deciduous forest during autumn leaf-fall. Agric For Meteorol 45:325–345
Niklaus PA, Spinnler D, Körner C (1998) Soil moisture dynamics of calcareous grassland under elevated CO2. Oecologia 117:201–208
Norby RJ (1996) Forest canopy productivity index. Nature 381:564
Norby RJ, Gunderson CA, Wullschleger SD, O'Neill EG, McCracken MK (1992) Productivity and compensatory responses of yellow-poplar trees in elevated CO2. Nature 357:322–324
Norby RJ, Wullschleger SD, Gunderson CA, Nietch CT (1995) Increased growth efficiency of Quercus alba trees in a CO2-enriched atmosphere. New Phytol 131:91–97
Norby RJ, Wullschleger SD, Gunderson CA, Johnson DW, Ceulemans R (1999) Tree responses to rising CO2: implications for the future forest. Plant Cell Environ 22:683–714
Norby RJ, Todd DE, Fults J, Johnson DW (2001) Allometric determination of tree growth in a CO2-enriched sweetgum stand. New Phytol 150:477–487
Norby RJ, Hanson PJ, O'Neill EG, Tschaplinski TJ, Weltzin JF, Hansen RT, Cheng W, Wullschleger SD, Gunderson CA, Edwards NT, Johnson DW (2002). Net primary productivity of a CO2-enriched deciduous forest and the implications for carbon storage. Ecol Appl 12:1261–1266.
Peterson AG, Ball JT, Luo Y, Field CB, Curtis PS, Griffin KL, Gunderson CA, Norby RJ, Tissue DT, Forstreuter M, Rey A, Vogel CS, CMEAL participants (1999) Quantifying the response of photosynthesis to changes in leaf nitrogen content and leaf mass per area in plants grown under atmospheric CO2 enrichment. Plant Cell Environ 22:1109–1119
Prioul JL, Chartier P (1977) Partitioning of transfer and carboxylation components of intracellular resistance to photosynthetic CO2 fixation: a critical analysis of the methods used. Ann Bot 41:789–800
Pritchard SG, Rogers HH, Prior SA, Peterson CM (1999) Elevated CO2 and plant structure: a review. Global Change Biol 5:807–837
Riggs JS, Tharp ML, Norby RJ (2002a) ORNL FACE CO2 Data (http://cdiac.ornl.gov/programs/FACE/ornldata/co2files.html). Carbon Dioxide Information Analysis Center, U.S. Department of Energy, Oak Ridge National Laboratory, Oak Ridge, Tennessee
Riggs JS, Tharp ML, Norby RJ (2002b) ORNL FACE Weather Data (http://cdiac.ornl.gov/programs/FACE/ornldata/weatherfiles.html). Carbon Dioxide Information Analysis Center, U.S. Department of Energy, Oak Ridge National Laboratory, Oak Ridge, Tennessee
Ruimy A, Saugier B, Dedieu G (1994) Methodology for the estimation of terrestrial net primary production from remotely sensed data. J Geophys Res 99(D3):5263–5283
Russell G, Jarvis PG, Monteith JL (1989) Absorption of radiation by canopies and stand growth. In Russell G, Marshall B, Jarvis PG (eds) Plant canopies: their growth, form and function. Cambridge University Press, Cambridge, pp 21–39
Sholtis JD (2002) Effects of elevated CO2 on sweetgum ecophysiology. PhD Dissertation, Texas Tech University, Lubbock, Texas
Woodward FI, Smith TM, Emanuel WR (1995) A global land primary productivity and phytogeography model. Global Biogeochem Cycles 9:471–490
Wullschleger SD, Norby RJ (2001) Sap velocity and canopy transpiration for a 12-year-old sweetgum stand exposed to free-air CO2 enrichment. New Phytol 150:489–498
Wullschleger SD, Gunderson CA, Hanson PJ, Wilson KB, Norby RJ (2002) Sensitivity of stomatal and canopy conductance to elevated CO2 concentration–interacting variables and perspectives of scale. New Phytol 153:485–496
Yin X (2002) Responses of leaf nitrogen concentration and specific leaf area to atmospheric CO2 enrichment: a retrospective synthesis across 62 species. Global Change Biol 8:631–642
Acknowledgements
We appreciate the critical reviews of an earlier manuscript by Stan Wullschleger and Lianhong Gu. Research was sponsored by the U.S. Department of Energy, Office of Science, Biological and Environmental Research. Oak Ridge National Laboratory is managed by UT-Battelle, LLC, for the U.S. Department of Energy under contract DE-AC05–00OR22725.
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Norby, R.J., Sholtis, J.D., Gunderson, C.A. et al. Leaf dynamics of a deciduous forest canopy: no response to elevated CO2 . Oecologia 136, 574–584 (2003). https://doi.org/10.1007/s00442-003-1296-2
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DOI: https://doi.org/10.1007/s00442-003-1296-2