Abstract
The CO2 concentration of the atmosphere has increased by almost 30% in the past two centuries, with most of the increase (>5 Pa) during the past 60 years. Controlled environment studies of crop plants dependent on the C3 photosynthetic pathway indicate that an increase of this magnitude would enhance net photosynthesis, reduce stomatal conductance, and increase the difference in CO2 concentration across the stomata, i.e., CO2 concentration outside the leaf to that within (c a-c i). Here we report evidence, based on stable isotope composition of tree rings from three species of field-grown, native conifer trees, that the trees have indeed responded. However, rather than increasing c a-c i, intercellular CO2 concentrations have shifted upward to match the rise in atmospheric concentrations, holding c a-c i constant. No differences were detected among Douglas-fir (Pseudotsuga menziesii), ponderosa pine (Pinus ponderosa), or western white pine (Pinus monticola). The values of c a-c i were inferred from stable carbon isotope ratio (δ13C) of tree ring holocellulose adjusted for the 0.6–2.6‰ difference between holocellulose and whole sapwood. The cellulose extraction removed contaminants deposited in the tree ring after it formed and the adjustment corrected for the enrichment of cellulose relative to whole tissue. The whole sapwood values were then adjusted for bublished estimates of past atmospheric δ13CO2 and CO2 concentrations. To avoid confounding tree age with CO2, cellulose deposited by saplings in the 1980s was compared to cellulose deposited in the inner rings of nature trees when the mature trees were saplings, between 1910–1929 and 1941–1970; thus saplings were compared to saplings. In a separate analysis, the juvenile effect, which describes the tendency for δ13C to increase in the first decades of a tree's life, was quantified independent of source CO2 effects. This study provides evidence that conifers have undergone adjustments in the intercellular CO2 concentration that have maintained c a-c i constant. Based on these results and others, we suggest that c a-c i, which has also been referred to as the intrinsic water-use efficiency, should be considered a homeostatic gas-exchange set point for these conifer species.
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References
Barnola JM, Raynaud D, Korotkevich YS, Lorius C (1987) Vostok ice core provides 160,000-year record of atmospheric CO2 Nature 329: 408–414
Beerling DJ, Mattey DP, Chaloner WG (1993) Shifts in the δ13C composition of Salix herbacea L. leaves in response to spatial and temporal gradients of atmospheric CO2 concentration. Proc R Soc Lond B 253: 53–60
Broadmeadow MSJ, Griffiths H (1993) Carbon isotope discrimination and the coupling of CO2 fluxes within forest canopies. In: Ehleringer JR, Hall AE, Farquhar GD (eds) Stable isotopes and plant carbon-water relations. Academic Press, San Diego, pp 109–129
Broadmeadow MSJ, Griffiths H, Maxwell C, Borland AM (1992) The carbon isotope ratio of plant organic material reflects temporal and spatial variations in CO2 within tropical forest formations in Trinidad. Oecologia 89: 435–441
Callaway RM, DeLucia EH, Thomas EM, Schlesinger WH (1994) Compensatory responses of CO2 exhange and biomass allocation and their effects on the relative growth rate of ponderosa pine in different CO2 and temperature regimes. Oecologia 98: 159–166
Craig H (1954) Carbon-13 variations in Sequoia rings and the atmosphere. Science 119: 141–143
Earthinfo Inc (1992) NCDC summary of the day. Boulder, Clo
Eamus D, Jarvis PG (1989) The direct effects of increase in the global atmospheric CO2 concentration on natural and commercial temperate trees and forests. Adv Ecol Res 19: 1–55
Ehleringer JR (1993) Carbon and water relations in desert plants: an isotopic perspective. In: Ehleringer JR, Hall AE, Farquhar GD (eds) Stable isotopes and plant carbon-water relations. Academic Press, San Diego, pp 155–172
Ehleringer JR, Cerling TE (1995) Atmospheric CO2 and the ratio of intercellular to ambient CO2 concentrations in plants. Tree Physiol 15: 105–111
Ehleringer JR, Field CB, Lin Z-F, Kuo C-Y (1986) Leaf carbon isotope and mineral composition in subtropical plants along an irradiance cline. Oecologia 70: 520–526
Farquhar GD, Richards RA (1984) Isotopic composition of plant carbon correlates with water-use efficiency of wheat genotypes. Aust J Plant Physiol 11: 539–552
Farquhar GD, O'Leary MH, Berry A (1982) On the relationship between carbon isotope discrimination and the intercellular carbon dioxide concentration in leaves. Aust J Plant Physiol 9: 121–137
Francey RJ (1981) Tasmanian tree rings belie suggested anthropogenic 13C/12C trends. Nature 290: 232–235
Francey RJ, Farquhar GD (1982) An explanation of 13C/12C variations in tree rings. Nature 297: 28–31
Francey RJ, Gifford RM, Sharkey TD, Weir B (1985) Physiological influences on carbon isotope discrimination in huon pine (Lagarostrobos franklinii). Oecologia 66: 211–218
Freyer HD (1979) On the 13C record in tree rings. Part I. 13C variations in northern hemispheric trees during the last 150 years. Tellus 31: 124–137
Freyer HD, Belacy N (1983) 13C/12C records in northern hemispheric trees during the past 500 years-anthropogenic impact and climatic superpositions. J Geophys Res 88: 6844–6852
Friedli H, Lotscher H, Oeschger H, Siegenthaler U (1986) Ice core record of the 13C and 12C ratio of atmospheric CO2 in the past two centuries. Nature 324: 237–238
Graumlich LJ (1991) Subalpine tree growth, climate, and increasing CO2: an assessment of recent growth trends. Ecology 72: 1–11
Graybill DA, Idso SB (1993) Detecting the acrial fertilization effect of atmospheric CO2 enrichment in tree-ring chronologies. Global Biogeochem Cycles 7: 81–95
Grulke NE, Hom JL, Roberts SW (1993) Physiological adjustment of two full-sib families of ponderosa pine to elevated CO2. Tree Physiol 12: 391–402
Hollinger DY (1987) Gas exchange and dry matter allocation responses to elevation of atmospheric CO2 concentration in seedlings of three tree species. Tree Physiol 3: 193–202
Idso SB, Kimball BA (1992) Effects of atmospheric CO2 enrichment on photosynthesis, respiration, and growth of sour orange trees. Plant Physiol 99: 341–343
Jarvis PG, McNaughton KG (1986) Stomatal control of transpiration: scaling up from leaf to region. Adv Ecol Res 15: 1–49
Keeling CD, Bacastow RB, Carter AF, Piper SC, Whorf TP, Heimann M, Mook WG, Roeloffzen H (1989). A three-dimensional model of atmpspheric CO2 transport based on observed winds. 1. Analysis of observational data. In: Peterson DH (ed) Geophysical Monograph, vol 55. American Geophysical Union, pp 165–236
Kienast F, Luxmoore RJ (1988) Tree-ring analysis and conifer growth responses to increased atmospheric CO2 levels. Oecologia 76: 487–495
Körner C, Farquhar GD, Roksandic Z (1988) A global survey of carbon isotope discrimination in plants from high altitude. Oecologia 74: 623–632
Körner C, Farquhar GD, Wong SC (1991) Carbon isotope discrimination by plants follows latitudinal and altitudinal trends. Oecologia 88: 30–40
Kramer PJ (1981) Carbon dioxide concentration, photosynthesis, and dry matter production. Bioscience 31: 29–33
La Marche VC, Graybill DA, Fritts HC, Rose MR (1984) Increasing atmospheric carbon dioxide: tree ring evidence for growth enhancement in natural vegetation. Science 225: 1019–1021
Leavitt SW, Danzer SR (1993) Method for batch processing small wood samples to holocellulose for stable-carbon isotope analysis. Anal Chem 65: 87–89
Leavitt SW, Lara A (1994) South American tree rings show declining δ13C trend. Tellus 46B: 152–157
Leavitt SW, Long A (1986) Stable-carbon isotope variability in tree foliage and wood. Ecology 67: 1002–1010
Leavitt SW, Long A (1989) The atmospheric δ13C record as derived from 56 pinyon trees at 14 sites in the southwestern United States. Radiocarbon 31: 469–474
Leavitt SW, Long A (1992) Altitudinal differences in δ13C of bristlecone pine tree rings. Naturwissenschaften 79: 179–180
Marino BD, McElroy MB (1991) Isotopic composition of atmospheric CO2 inferred from carbon in C4 plant cellulose. Nature 349: 127–131
Marshall JD, Zhang J (1994) Carbon isotope discrimination and water-use efficiency in native plants of the north-central Rockies. Ecology 75: 1887–1895
Martin B, Sutherland EK (1990) Air pollution in the past recorded in width and stable carbon isotope composition of annual growth rings of Douglas-fir. Plant Cell Environ 13: 839–844
Masle J, Farquhar GD, Gifford RM (1990) Growth and carbon economy of wheat seedlings as affected by soil resistance to penetration and ambient partial pressure of CO2. Aust J Plant Physiol 17: 465–487
Medina E, Minchin P (1980) Stratification of δ13C values of leaves in Amazonian rain forests. Oecologia 45: 377–378
Mitchell AK, Hinckley TM (1993) Effects of foliar nitrogen concentration on photosynthesis and water use efficiency in Douglas-fir. Tree Physiol 12: 403–410
Mooney HA, Drake BG, Luxmoore RJ, Oechel WC, Pitelka LF (1991) Predicting ecosystem responses to elevated CO2 concentrations. Bioscience 41: 96–104
Neftel A, Oeschger H, Schwander J, Stauffer B, Zumbrunn R (1982) Ice core sample measurements give atmospheric CO2 content during the past 40,000 yr. Nature 295: 220–223
Park R, Epstein S (1961) Metabolic fractionation of C13 & C12 in plants. Plant Physiol 36: 133–138
Pitelka LF (1994) Ecosystem response to elevated CO2. Trends Ecol Evol 9: 204–207
Polley HW, Johnson HB, Marino BD, Mayeux HS (1993) Increase in C3 plant water-use efficiency and biomass over Glacial to present CO2 concentrations. Nature 361: 61–64
Schleser GH (1990) Investigations of the δ13C patterns in leaves of Fagus sylvatica. J Exp Bot 41: 565–572
Sternberg L, Mulkey SS, Wright SJ (1989) Ecological interpretation of leaf carbon isotope ratios: influence of respired carbon dioxide. Ecology 70: 1317–1324
Stuiver M, Braziunas TF (1987) Tree cellulose 13C/12C isotope ratios and climatic change. Nature 328: 58–60
Surano KA, Daley PF, Houpis JLJ, Shinn JH, Helms JA, Palassou RJ, Costella MP (1986) Growth and physiological responses of Pinus ponderosa Dougl ex P. Laws. to long-term elevated CO2 concentrations. Tree Physiol 2: 243–259
Van de Water PK, Leavitt SW, Betancourt JL (1994) Trends in stomatal density and 13C/12C ratios of Pinus flexilis needles during last glacial-interglacial cycle. Science 264: 239–243
White J, Molfino B, Labeyrie L, Stauffer B, Farquhar GD (1993) How reliable and consistent are paleodata from continents, oceans, and ice? In: Eddy JA, Oeschger H (ed) Global changes in the perspective of the past. Wiley, New York
Wong SC, Cowan IR, Farquhar GD (1979) Stomatal conductance correlates with photosynthetic capacity. Nature 282: 424–426
Woodward FI (1987) Stomatal numbers are sensitive to increases in CO2 from pre-industrial levels. Nature 327: 617–618
Woodward FI, Bazzaz FA (1988) The responses of stomatal density to CO2 partial pressure. J Exp Bot 39: 1771–1781
Yoder BJ, Ryan MG, Waring RH, Schoettle AW, Kaufmann MR (1994) Evidence of reduced photosynthetic rates in old trees. For Sci 40: 513–527
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Marshall, J.D., Monserud, R.A. Homeostatic gas-exchange parameters inferred from 13C/12C in tree rings of conifers. Oecologia 105, 13–21 (1996). https://doi.org/10.1007/BF00328786
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DOI: https://doi.org/10.1007/BF00328786