Trees

, Volume 19, Issue 3, pp 251–265 | Cite as

Reconstructing atmospheric carbon dioxide with stomata: possibilities and limitations of a botanical pCO2-sensor

Original Article

Abstract

Stomatal frequency is often observed to vary inversely with atmospheric CO2 concentration (pCO2). The response is due to (1) individual phenotypic plasticity and (2) evolutionary change, depending on the time scale. Evolutionary responses occur more frequently than individual responses and individual responses are more pronounced under subambient pCO2 levels than under elevated pCO2 (“CO2 ceiling”). The evolutionary response appears therefore to be a valuable device for determining past pCO2. Since tree leaves often represent a conspicuous and rich resource of fossil material, they are increasingly important in this respect. Additionally, certain tree species are considered to represent “living fossils” and therefore valuable sources of ancient stomatal data. There are, however, numerous difficulties which have to be considered such as: (1) high variance of the data, especially for fossil material, (2) interspecific differences of the response, (3) the CO2 ceiling and (4) differences between short-term and long-term responses. Whereas the qualitative pCO2 signal of stomatal frequency appears to be reliable, quantitative pCO2 reconstruction has to be performed with caution. The results of a number of studies which used stomatal frequency as a pCO2 sensor demonstrate good agreement with the results obtained with other proxy data. Current techniques are based on “transfer functions” which calibrate the fossil data with extant material. It is suggested that a mechanistic approach including physical as well as physiological processes could improve pCO2 reconstruction. Furthermore, the topic of the influence of pCO2 on stomatal frequency is significant not only for reconstructing past pCO2 but also with respect to the climate-biosphere interrelationship.

Keywords

Stomata Stomatal density Stomatal index Atmospheric CO2 Palaeoclimate 

References

  1. Arrhenius S (1896) On the influence of carbonic acid in the air upon the temperature on the ground. Phil Mag 41:237–279Google Scholar
  2. Ball JT, Woodrow IE, Berry JA (1987) A model predicting stomatal conductance and its contribution to the control of photosynthesis under different environmental conditions. In: Biggins I (ed) Progress in photosynthesis research. Martinus Nijhoff, Netherlands, pp 221–224Google Scholar
  3. Beerling DJ (1999) Stomatal density and index: theory and applications. In: Jones TP, Rowe NP (eds) Fossil plants and spores: modern techniques. The Geological Society, London, pp 251–256Google Scholar
  4. Beerling DJ (2002) Low atmospheric CO2 levels during the Permo-Carboniferous glaciation inferred from fossil lycopsids. Proc Natl Acad Sci USA 99:12567–12571Google Scholar
  5. Beerling DJ, Chaloner WG (1993) Evolutionary responses of stomatal density to global CO2 change. Biol J Linn Soc 48:343–353CrossRefGoogle Scholar
  6. Beerling DJ, Kelly CK (1997) Stomatal density responses of temperate woodland plants over the past seven decades of CO2 increase: a comparison of Salisbury (1927) with contemporary data. Am J Bot 84:1572–1583Google Scholar
  7. Beerling DJ, Woodward FI (1997) Changes in land plant function over the Phanerozoic: reconstructions based on the fossil record. Bot J Linn Soc 124:137–153Google Scholar
  8. Beerling DJ, Royer DL (2002a) Fossil plants as indicators of the Phanerozoic global carbon cycle. Annu Rev Earth Planet Sci 30:527–556CrossRefGoogle Scholar
  9. Beerling DJ, Royer DL (2002b) Reading a CO2 signal from fossil stomata. New Phytol 153:387–397CrossRefGoogle Scholar
  10. Beerling DJ, Chaloner WG, Huntley B, Pearson JA, Tooley MJ (1993) Stomatal density responds to the glacial cycle of environmental change. Proc R Soc London B 251:133–138Google Scholar
  11. Beerling DJ, Birks HH, Woodward FI (1995) Rapid late-glacial atmospheric CO2 changes reconstructed from the stomatal density record of fossil leaves. J Quat Sci 10:379–384Google Scholar
  12. Beerling DJ, McElwain JC, Osborne CP (1998) Stomatal responses of the living fossil Ginkgo biloba L. to changes in atmospheric CO2 concentrations. J Exp Bot 49:1603–1607Google Scholar
  13. Berner RA (2001) Modeling atmospheric O2 over Phanerozoic time. Geochim Cosmochim Acta 65:685–694Google Scholar
  14. Berner RA, Canfield DE (1989) A new model for atmospheric oxygen over Phanerozoic time. Am J Sci 289:59–91Google Scholar
  15. Berner RA, Kothvala Z (2001) GEOCARB III: a revised model of atmospheric CO2 over Phanerozoic time. Am J Sci 291:339–376Google Scholar
  16. Berryman CA, Eamus D, Duff GA (1994) Stomatal responses to a range of variables in tree species grown with CO2 enrichment. J Exp Bot 45:539–546Google Scholar
  17. Boucot AJ, Gray J (2001) A critique of Phanerozoic climatic models involving changes in the CO2 content of the atmosphere. Earth-Sci Rev 56:1–159Google Scholar
  18. Brown HT, Escombe F (1900) Static diffusion of gases and liquids in relation to the assimilation of carbon and translocation in plants.Phil Trans R Soc London B 193:223–291Google Scholar
  19. Chaloner WG, McElwain J (1997) The fossil plant record and global climatic change. Rev Palaeobot Palynol 95:73–82CrossRefGoogle Scholar
  20. Chamberlin TC (1898) An attempt to frame a working hypothesis of the cause of glacial periods on an atmospheric basis. J Geol 7:545–584Google Scholar
  21. Chen L-Q, Li C-S, Chaloner WG, Beerling DJ, Sun Q-G, Collinson ME, Mitchell PL (2001) Assessing the potential for the stomatal characters of extant and fossil Ginkgo leaves to signal atmospheric CO2 change. Am J Bot 88:1309–1315PubMedGoogle Scholar
  22. Cleal CJ, James RM, Zodrow EL (1999) Variation in stomatal density in the Late Carboniferous Gymnosperm frond Neuropteris ovata. Palaios 14:180–185Google Scholar
  23. Clifford SC, Black CR Roberts JA, Stronach IM, Singleton-Jones PR, Mohamed AD, Azam-Ali SN (1995) The effect of elevated atmospheric CO2 and drought on stomatal frequency in groundnut (Arachis hypogaea) (L.)). J Exp Bot 46:847–852Google Scholar
  24. Cowan IR (1977) Stomatal behaviour and environment. Adv Bot Res 4:117–228Google Scholar
  25. Cowan IR, Farquhar GD (1977) Stomatal function in relation to leaf metabolism and environment. In: Jennings DH (ed) Integration of activity in the higher plant. Society for Experimental Biology Symposium, No. 31. Cambridge University Press, Cambridge, pp 471–505Google Scholar
  26. Croxdale JL (2000) Stomatal patterning in angiosperms. Am J Bot 87:1069–1080PubMedGoogle Scholar
  27. Demicco RV, Lowenstein TK, Hardie LA (2003) Atmospheric pCO2 since 60 Ma from records of seawater pH, calcium, and primary carbonate mineralogy. Geology 31:793–796CrossRefGoogle Scholar
  28. Denk T, Velitzelos D (2002) First evidence of epidermal structures of Ginkgo from the Mediterranean Tertiary. Rev Palaeobot Palynol 120:1–15Google Scholar
  29. Dilcher DL (1974) Approaches to the identification of Angiosperm leaf remains. Bot Rev 40:2–145Google Scholar
  30. Drake BG, Gonzàlez-Meler MA Long SP (1997) More efficient plants: a consequence of rising atmospheric CO2? Annu Rev Plant Physiol Plant Mol Biol 48:609–639CrossRefPubMedGoogle Scholar
  31. Dutton JF, Barron EJ (1997) Miocene to present vegetation changes: a possible piece of the Cenozoic puzzle. Geology 25:39–41CrossRefGoogle Scholar
  32. Edwards D (1998) Climate signals in Palaeozoic land plants. Phil Trans R Soc London B 353:141–157CrossRefGoogle Scholar
  33. Edwards D, Kerp H, Hass H (1998) Stomata in early land plants: an anatomical and ecophysiological approach. J Exp Bot 49:255–278CrossRefGoogle Scholar
  34. Farquhar GD, von Caemmerer S, Berry JA (1980) A biochemical model of photosynthetic CO2 assimilation in leaves of C3 species. Planta 149:78–90Google Scholar
  35. Ferguson DK (1985) The origin of leaf assemblages—new light on an old problem. Rev Palaeobot Palynol 46:117–188CrossRefGoogle Scholar
  36. Ferris R, Taylor G (1994) Stomatal characteristics of four native herbs following exposure to elevated CO2. Ann Bot 73:447–453CrossRefGoogle Scholar
  37. Gastaldo RA Ferguson DK, Walther H, Rabold J (1996) Criteria to distinguish parautochthonous leaves in cenophytic alluvial channel-fills. Rev Palaeobot Palynol 90:1–21Google Scholar
  38. Gray JE, Holroyd GH, van der Lee FM, Bahrami AR, Sijmons PC, Woodward FI, Schuch W, Hetherington AM (2000) The HIC signaling pathway links CO2 perception to stomatal development. Nature 408:713–716CrossRefPubMedGoogle Scholar
  39. Hetherington AM, Woodward FI (2003) The role of stomata in sensing and driving environmental change. Nature 424:901–908CrossRefPubMedGoogle Scholar
  40. Jarman PD (1974) The diffusion of carbon dioxide and water vapour through stomata. J Exp Bot 25:927–936Google Scholar
  41. Jarvis PG, McNaughton KG (1986) Stomatal control of transpiration: scaling up from leaf to region. Adv Ecol Res 15:1–49Google Scholar
  42. Jones HG (1998) Stomatal control photosynthesis and transpiration. J Exp Bot 49:387–398CrossRefGoogle Scholar
  43. Jones JH (1986) Evolution of the Fagaceae: the implications of foliar features. Ann Missouri Bot Gard 73:228–275Google Scholar
  44. Katul G, Leuning R, Oren R (2003) Relationship between plant hydraulic and biochemical properties derived from a steady-state coupled water and carbon transport model. Plant Cell Environ 26:339–350Google Scholar
  45. Keeley JE, Osmond CB, Raven JA (1984) Stylites, a vascular land plant without stomata absorbs CO2 via its roots. Nature 310:694–695Google Scholar
  46. Kergoat L, Lafont S, Douville H, Berthelot B, Dedieu G, Planton S, Royer JF (2002) Impact of doubled CO2 on global-scale leaf area index and evapotranspiration: conflicting stomatal conductance and LAI responses. J Geophys Res-Atmos 107:Art. No. 4808Google Scholar
  47. Kerstiens G (1996) Cuticular water permeability and its physiological significance. J Exp Bot 47:1813–1832Google Scholar
  48. Körner C (1988) Does global increase of CO2 alter stomatal density? Flora 181:253–257Google Scholar
  49. Konrad W, Roth-Nebelsick A, Kerp H, Hass H (2000) Transpiration and assimilation of Early Devonian land plants with axially symmetric telomes—simulations on the tissue level. J Theor Biol 206:91–107CrossRefPubMedGoogle Scholar
  50. Kouwenberg LL, McElwain JC, Kürschner W, Wagner F, Beerling DJ, Mayle FE, Visscher H (2003) Stomatal frequency adjustment of four conifer species to historical changes in atmospheric CO2. Am J Bot 90:610–619Google Scholar
  51. Kriegel K (2001) Untersuchung der Blattmorphologie und Blattanatomie von Eotrigonobalanus furcinervis (Rossmässler) Walther und Kvacek und seine Vergesellschaftung mit anderen tertiären Sippen vom Mitteleozän bis Oligo-/Miozän Mitteleuropas. Diploma thesis, Technische Universität Dresden, Fakultät für Mathematik und NaturwissenschaftenGoogle Scholar
  52. Kürschner WM (1996) Leaf stomata as biosensors of palaeoatmospheric CO2 levels. PhD thesis, Laboratory of Palaeobotany and Palynology, Utrecht UniversityGoogle Scholar
  53. Kürschner WM, van der Burgh J, Visscher H, Dilcher DL (1996) Oak leaves as biosensors of late Neogene and early Pleistocene palaeoatmospheric CO2 concentrations. Mar Micropal 27:299–312CrossRefGoogle Scholar
  54. Kürschner WM, Wagner F, Visscher EH, Visscher H (1997) Predicting the stomatal frequency response to a future CO2 enriched atmosphere: constraints from historical observations. Geol Rundsch 86:512–517CrossRefGoogle Scholar
  55. Kürschner WM, Stulen I, Wagner F, Kuiper PJC (1998) Comparison of palaeobotanical observations with experimental data on the leaf anatomy of Durmast oak [Quercus petraea (Fagaceae)] in response to environmental change. Ann Bot 81:657–664CrossRefGoogle Scholar
  56. Kürschner WM, Wagner F, Dilcher DL, Visscher H (2001) Using fossil leaves for the reconstruction of Cenozoic palaeoatmospheric CO2 concentration. In: Gerhard LC, Harrison WE, Hanson BM (eds) Geological perspectives of global climate change. Am Assoc Pet Geol, Tulsa, Okla., pp 155–176Google Scholar
  57. Kvacek Z, Walther H (1978) Anisophylly and leaf homeomorphy in some Tertiary plants. Cour Forsch-Inst Senckenberg 30:84–94Google Scholar
  58. Kvacek Z, Walther H (1989) Revision der mitteleuropäischen Fagaceen nach blattepidermalen Charakteristiken. III. T. dryophyllumDebey ex Saporta und EotrigonobalanusWalther and Kvacek. Fedd Rep 100:575–601Google Scholar
  59. Lake JA, Quick WP, Beerling DJ, Woodward FI (2001) Plant development—signals from mature to new leaves. Nature 411:154CrossRefPubMedGoogle Scholar
  60. Lake JA, Woodward FI, Quick WP (2002) Long-distance CO2 signalling in plants. J Exp Bot 53:183–193CrossRefPubMedGoogle Scholar
  61. Leuning R (1983) Transport of gases into leaves. Plant Cell Environ 6:181–194Google Scholar
  62. Leuning R (1995) A critical appraisal of a combined stomatal-photosynthesis model for C3 plants. Plant Cell Environ 18:339–355Google Scholar
  63. Madsen E (1973) Effect of CO2 concentration on the morphological, histological and cytological changes in tomato plants. Acta Agric Scand 23:241–246Google Scholar
  64. Mai DH (1995) Tertiäre Vegetationsgeschichte Europas: Methoden und Ergebnisse. Fischer, JenaGoogle Scholar
  65. Mai DH, Walther H (1991) Die oligozänen und untermiozänen Floren NW-Sachsens und des Bitterfelder Raumes. Abh Staatl Mus Mineral Geol Dresden 38:1–230Google Scholar
  66. Mai DH, Walther H (2000) Die Fundstellen eozäner Floren des Weisselster-Beckens und seiner Randgebiete. Altenburg Naturwiss Forsch 13:1–59Google Scholar
  67. McElwain JC (1998) Do fossil plants signal palaeoatmospheric CO2 concentration in the geological past? Phil Trans R Soc London B 353:83–96Google Scholar
  68. McElwain J (2002) Is the greenhouse theory a fallacy? A paleontological paradox. Palaios 17:417–418Google Scholar
  69. McElwain JC, Chaloner WG (1995) Stomatal density and index of fossil plants track atmospheric carbon dioxide in the Paleozoic. Ann Bot 76:389–395CrossRefGoogle Scholar
  70. McElwain JC, Chaloner WG (1996) The fossil cuticle as a skeletal record of environmental change. Palaios 11:376–388Google Scholar
  71. McElwain JC, Beerling DJ, Woodward FI (1999) Fossil plants and global warming at the Triassic-Jurassic boundary. Science 285:1386–1390CrossRefPubMedGoogle Scholar
  72. McElwain JC, Mayle FE, Beerling DJ (2002) Stomatal evidence for a decline in atmospheric CO2 concentrations during the Younger Dryas stadial: a comparison with Antarctic ice core records. J Quat Sci 17:21–29CrossRefGoogle Scholar
  73. Medlyn BE, Barton CVM, Broadmedow MSJ, Ceulemans R, De Angelis P, Forstreuter M, Freeman M, Jackson SB, Kellomäki S, Laitat E, Rey A, Roberntz P, Sigurdsson BD, Strassemeyer J, Wang K, Curtis PS, Jarvis PG (2001) Stomatal conductance of forest species after long-term exposure to elevated CO2 concentration: a synthesis. New Phytol 149:247–264CrossRefGoogle Scholar
  74. Micheels A (2003) Late Miocene climate modelling with ECHAM4/ML: the effects of the palaeovegetation on the Tortonian climate. PhD thesis, University of TübingenGoogle Scholar
  75. Miller KG, Fairbanks RG, Mountain GS (1987) Tertiary oxygen isotope synthesis, sea level history and continental margin erosion. Paleoceanography 2:1–19Google Scholar
  76. Moore BD, Cheng S-H, Sims D, Seemann JR (1999) The biochemical and molecular basis for photosynthetic acclimation to elevated atmospheric CO2. Plant Cell Environ 22:567–582CrossRefGoogle Scholar
  77. Morison JIL (1998) Stomatal response to increased CO2 concentration. J Exp Bot Sp Iss 49:443–452CrossRefGoogle Scholar
  78. Niklas KJ (2000) Modeling fossil plant form-function relationships: a critique. Paleobiology 26:289–304Google Scholar
  79. Nobel PS (1999) Physicochemical and environmental plant physiology. 2nd edn. Academic, New YorkGoogle Scholar
  80. O’Leary JW, Knecht GN (1981) Elevated CO2 concentration increases stomatal numbers in Phaseolus vulgaris leaves. Bot Gaz 142:438–441CrossRefGoogle Scholar
  81. Pagani M, Arthur MA, Freeman KH (1999) Miocene evolution of atmospheric carbon dioxide. Palaeoceanography 14:273–293CrossRefGoogle Scholar
  82. Pagani M, Freeman KH, Arthur MA (2000) Isotope analysis of molecular and total organic carbon from Miocene sediments. Geochim Cosmochim Acta 64:37–49CrossRefGoogle Scholar
  83. Paoletti E, Gellini R (1993) Stomatal density in beech and holm oak leaves collected over the last 200 years. Acta Oecol 14:173–178Google Scholar
  84. Parkhurst DF (1994) Tansley review No. 65. Diffusion of CO2 and other gases inside leaves. New Phytol 126:449–479Google Scholar
  85. Parkhurst DF, Mott KA (1990) Intercellular diffusion limits to CO2 uptake in leaves. Plant Physiol 94:1024–1032Google Scholar
  86. Parlange J-Y, Waggoner PE (1970) Stomatal dimensions and resistance to diffusion. Plant Physiol 46:337–342Google Scholar
  87. Pearson PE, Palmer MR (1999) Middle Eocene seawater pH and atmospheric carbon dioxide concentrations. Science 284:1824–1826CrossRefPubMedGoogle Scholar
  88. Pearson PE, Palmer MR (2000) Atmospheric carbon dioxide concentrations over the past 60 million years. Nature 406:695–699CrossRefPubMedGoogle Scholar
  89. Peñuelas J, Matamala R (1990) Changes in N and S leaf content, stomatal density and specific leaf area in 14 plant species during the last three centuries. J Exp Bot 41:1119–1124Google Scholar
  90. Petit JR, Jouzel J, Raynaud D, Barkov NI, Barnola J-M, Basile I, Bender M, Chappellaz J, Davis M, Delaygue G, Delmotte M, Kotlyakov VM, Legrand M, Lipenkov VY, Lorius C, Pépin L, Ritz C, Saltzmann E, Stievenand M (1999) Climate and atmospheric history of the past 420,000 years from the Vostok ice core, Antarctica. Nature 399:429–436CrossRefGoogle Scholar
  91. Poole I, Kürschner WM (1999) Stomatal density and index: the practice. In: Jones TP, Rowe NP (eds) Fossil plants and spores: modern techniques. The Geological Society, London, pp 257–260Google Scholar
  92. Poole I, Leyers JDB, Lawson T, Raven JA (1996) Variations in stomatal density and index: implications for palaeoclimatic reconstructions. Plant Cell Environ 19:705–712Google Scholar
  93. Poole I, Lawson T, Leyers JDB, Raven JA (2000) Effect of elevated CO2 on the stomatal distribution and leaf physiology of Alnus glutinosa. New Phytol 145:511–521CrossRefGoogle Scholar
  94. Raven JA (1977) The evolution of vascular plants in relation to supracellular transport processes. Adv Bot Res 5:153–219Google Scholar
  95. Raven JA (1984) Physiological correlates of the morphology of early vascular plants. Bot J Linn Soc 88:105–126Google Scholar
  96. Raymo ME, Grant B, Horowitz M, Rau GH (1996) Mid-Pliocene warmth: stronger greenhouse and conveyor. Mar Micropaleontol 27:312–326CrossRefGoogle Scholar
  97. Raven JA (2002) Tansley review no 131. Selection pressures on stomatal densities. New Phytol 153:371–386CrossRefGoogle Scholar
  98. Reid CD, Maherali H, Johnson HB, Smith SD, Wullschleger SD, Jackson RB (2003) On the relationship between stomatal characters and atmospheric CO2. Geophys Res Lett 30:Art. No. 1983CrossRefGoogle Scholar
  99. Retallack GJ (2001) A 300-million-year record of atmospheric carbon dioxide from fossil plant cuticles. Nature 411:287–290CrossRefPubMedGoogle Scholar
  100. Rey A, Jarvis PG (1997) Growth response of young birch trees (Betula pendula Roth.) after four and a half years of CO2 exposure. Ann Bot 80:807–816CrossRefGoogle Scholar
  101. Roth-Nebelsick A, Konrad W (2003) Assimilation and transpiration capabilities of rhyniophytic plants from the Lower Devonian and their implications for paleoatmospheric CO2 concentration. Palaeogeogr Palaeocl 302:153–178CrossRefGoogle Scholar
  102. Roth-Nebelsick A, Utescher T, Mosbrugger V, Diester-Haass L, Walther H (2004) Changes in atmospheric CO2 concentrations and climate from the Late Eocene to Early Miocene: palaeobotanical reconstruction based on fossil floras from Saxony, Germany. Palaeogeogr Palaeoecol 205:43–67CrossRefGoogle Scholar
  103. Royer DL (2001) Stomatal density and stomatal index as indicators of paleoatmospheric CO2 concentration. Rev Palaeobot Palynol 114:1–28Google Scholar
  104. Royer DL, Berner RA, Beerling DJ (2001) Phanerozoic atmospheric CO2 change: evaluating geochemical and paleobiological approaches. Earth-Sci Rev 54:349–392CrossRefGoogle Scholar
  105. Royer DL, Wing SL, Beerling DJ, Jolley DW, Koch PL, Hickey LJ, Berner RA (2001) Paleobotanical evidence for near present-day levels of atmospheric CO2 during part of the Tertiary. Science 292:2310–2313CrossRefPubMedGoogle Scholar
  106. Rundgren M, Beerling M (1999) A Holocene CO2 record from the stomatal index of subfossil Salix herbacea L. leaves from northern Sweden. Holocene 9:509–513CrossRefGoogle Scholar
  107. Salisbury EJ (1927) On the causes and ecological significance of stomatal frequency, with special reference to the woodland flora. Phil Trans R Soc London B 216:1–65Google Scholar
  108. Schulze E-D, Kelliher FM, Körner C, Lloyd J, Leuning R (1994) Relationships among maximum stomatal conductance, ecosystem surface conductance, carbon assimilation rate, and plant nitrogen nutrition: a global ecology scaling exercise. Annu Rev Ecol Syst 25:629–660CrossRefGoogle Scholar
  109. Spicer RA (1981) The sorting and deposition of allochthonous plant material in a modern environment at Silwood Lake, Silwood Park, Berkshire, England. U.S. Geol Prof Paper 1143:1–77Google Scholar
  110. Talbott LD, Rahveh E, Zeiger E (2003) Relative humidity is a key factor in the acclimation of the stomatal response to CO2. J Exp Bot 54:2141–2147CrossRefPubMedGoogle Scholar
  111. Thomas JF, Harvey CN (1983) Leaf anatomy of four species grown under continuous CO2 enrichment. Bot Gaz 144:303–309CrossRefGoogle Scholar
  112. Tichà I (1982) Photosynthetic characteristics during ontogenesis of leaves. 7. Stomatal density and size. Photosynthetica 16:375–471Google Scholar
  113. van der Burgh J (1993) Oaks related to Quercus petraea from the Upper Tertiary of the Lower Renish Basin. Palaeontographica 230:195–201Google Scholar
  114. van der Burgh J, Visscher H, Dilcher D, Kürschner W (1993) Paleoatmospheric signatures in Neogene fossil leaves. Science 260:1788–1790Google Scholar
  115. van de Water PK, Leavitt SW, Betancourt JL (1994) Trends in stomatal density and 13C/12C ratios of Pinus flexilis during last glacial-interglacial cycle. Science 264:239–242Google Scholar
  116. Veizer J, Godderis Y, Francois LM (2000) Evidence for decoupling of atmospheric CO2 and global climate during the Phanerozoic Eon. Nature 408:651–652CrossRefPubMedGoogle Scholar
  117. Wagner F, Below R, De Klerk P, Dilcher DL, Joosten H, Kürschner WM, Visscher H (1996) A natural experiment on plant acclimation: lifetime stomatal frequency response of an individual tree on annual atmospheric CO2 increase. Proc Natl Acad Sci USA 93:11705–11708Google Scholar
  118. Wagner F, Bohncke SJP, Dilcher DL, Kürschner WM, van Geel B, Visscher H (1999) Century-scale shifts in Early Holocene atmospheric CO2 concentration. Science 284:1971–1973CrossRefPubMedGoogle Scholar
  119. Wallmann K (2001) Controls on the Cretaceous and Cenozoic evolution of seawater composition, atmospheric CO2 and climate. Geochim Cosmochim Acta 65:3005–3025CrossRefGoogle Scholar
  120. Walther H (1999) Die Tertiärflora von Kleinsaubernitz bei Bautzen. Palaeontographica Abt B 249:63–174Google Scholar
  121. Wellman CH, Gray J (2000) The microfossil record of early land plants. Phil Trans R Soc London B 355:717–731CrossRefGoogle Scholar
  122. Weyers JDB, Lawson T, Peng Z-Y (1997) Variation in stomatal characters at the whole-leaf level. In: Van Gardingen PR, Foody GM, Curran PJ (eds) Scaling up from cell to landscape. SEB seminar series, 63. Cambridge University Press, Cambridge, pp 129–149Google Scholar
  123. Willmer C, Fricker M (1996) Stomata 22nd edn. Chapman and Hall, LondonGoogle Scholar
  124. Wong SC, Cowan IR, Farquhar GD (1979) Stomatal conductance correlates with photosynthetic capacity. Nature 282:424–426Google Scholar
  125. Woodrow IE (1994) Optimal acclimation of the C3 photosynthetic system under enhanced CO2. Photosynth Res 39:401–412Google Scholar
  126. Woodward FI (1987) Stomatal numbers are sensitive to increases in CO2 concentration from pre-industrial levels. Nature 327:617–618CrossRefGoogle Scholar
  127. Woodward FI, Bazzazz FA (1988) The responses of stomatal density to CO2 partial pressure. J Exp Bot 39:1771–1781Google Scholar
  128. Woodward FI, Kelly CK (1995) The influence of CO2 concentration on stomatal density. New Phytol 131:311–327Google Scholar
  129. Woodward FI, Lake JA, Quick WP (2002) Stomatal development and CO2: ecological consequences. New Phytol 153:477–484CrossRefGoogle Scholar
  130. Wullschleger SD, Gunderson CA, Hanson PJ, Wilson KB, Norby RJ (2002a) Sensitivity of stomatal and canopy conductance to elevated CO2 concentration—interacting variables and perspectives of scale. New Phytol 153:485–496CrossRefGoogle Scholar
  131. Wullschleger SD, Tschaplinski TJ, Norby RJ (2002b) Plant water relations at elevated CO2—implications for water-limited environments. Plant Cell Environ 25:319–331CrossRefPubMedGoogle Scholar
  132. Wynn JG (2003) Towards a physically based model of CO2-induced stomatal frequency response. New Phytol 157:394–398CrossRefGoogle Scholar
  133. Zachos JC, Stott LD, Lohmann KC (1994) Evolution of early Cenozoic marine temperatures. Paleoceanography 9:353–387CrossRefGoogle Scholar
  134. Zavaleta ES, Thomas BD, Chiariello NR, Asner GP, Shaw MR, Field CB (2003) Plants reverse warming effect on ecosystem water balance. Proc Natl Acad Sci USA 100:9892–9893Google Scholar

Copyright information

© Springer-Verlag 2004

Authors and Affiliations

  1. 1.Institute for GeosciencesUniversity of TübingenTübingenGermany

Personalised recommendations