Skip to main content
Log in

Quo vadis C4? An ecophysiological perspective on global change and the future of C4 plants

  • Published:
Photosynthesis Research Aims and scope Submit manuscript

Abstract

C4 plants are directly affected by all major global change parameters, often in a manner that is distinct from that of C3 plants. Rising CO2 generally stimulates C3 photosynthesis more than C4, but C4 species still exhibit positive responses, particularly at elevated temperature and arid conditions where they are currently common. Acclimation of photosynthesis to high CO2 occurs in both C3 and C4 plants, most notably in nutrient-limited situations. High CO2 aggravates nitrogen limitations and in doing so may favor C4 species, which have greater photosynthetic nitrogen use efficiency. C4 photosynthesis is favored by high temperature, but global warming will not necessarily favor C4 over C3 plants because the timing of warming could be more critical than the warming itself. C3 species will likely be favored where harsh winter climates are moderated, particularly where hot summers also become drier and less favorable to C4 plant growth. Eutrophication of soils by nitrogen deposition generally favors C3 species by offsetting the superior nitrogen use efficiency of C4 species; this should allow C3 species to expand at the expense of C4 plants. Land-use change and biotic invasions are also important global change factors that affect the future of C4 plants. Human exploitation of forested landscapes favors C4 species at low latitude by removing woody competitors and opening gaps in which C4 grasses can establish. Invasive C4 grasses are causing widespread forest loss in Asia, the Americas and Oceania by accelerating fire cycles and reducing soil nutrient status. Once established, weedy C4 grasses can prevent woodland establishment, and thus arrest ecological succession. In sum, in the future, certain C4 plants will prosper at the expense of C3 species, and should be able to adjust to the changes the future brings.

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

Access this article

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

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

References

  • Aide TM and Cavelier JC (1994) Barriers to lowland tropical forest restoration in the Sierra Nevada de Santa Marta, Colombia. Restoration Ecol 2: 219–229

    Article  Google Scholar 

  • Anderson LJ, Maherali H, Johnson HB, Polley HW and Jackson RB (2001) Gas exchange and photosynthetic acclimation over subambient to elevated CO2 in a C3-C4 grassland. Global Change Biol 7: 693–707

    Article  Google Scholar 

  • Archer S and Stokes C (2000) Stress, Disturbance and Change in Rangeland Ecosystems. In: Arnalds O and Archer S (eds) Rangeland Desertification, pp 17–38. Kluwer Academic Publishers, Dordrecht, The Netherlands

    Google Scholar 

  • Archer S, Schimel DS and Holland EA (1995) Mechanisms of shrubland expansion: Land use, climate or CO2? Climatic Change 29: 91–99

    Article  Google Scholar 

  • Ball AS (1997) Microbial decomposition at elevated CO2 levels: Effect of litter quality. Global Change Biol 3: 379–386

    Article  Google Scholar 

  • Baruch Z, Ludlow MM and Davis R (1985) Photosynthetic responses of native and introduced C4 grasses from Venezuelan savannas. Oecologia 67: 388–393

    Article  Google Scholar 

  • Bond WJ and Midgley GF (2001) A proposed CO2-controlled mechanism of woody plant invasion in grasslands and savannas. Global Change Biol 6: 865–870

    Article  Google Scholar 

  • Bond WJ and van Wilgen BW (1996) Fire and Plants. Chapman & Hall, London

    Google Scholar 

  • Brown RH (1978) A difference in N use efficiency in C3 and C4plants and its implications in adaptation and evolution. Crop Sci 18: 93–98

    Article  CAS  Google Scholar 

  • Brown WV (1977) The Kranz syndrome and its subtypes in grass systematics. Mem Torrey Bot Club 23: 1–97

    CAS  Google Scholar 

  • Clark JS, Grimm EC, Lynch J and Mueller PG (2001) Effects of Holocene climate change on the C4 grassland/woodland boundary in the Northern Plains, USA. Ecology 82: 620–636

    Article  Google Scholar 

  • Cochrane MA and Schulze MD (1999) Fire as a recurrent event in tropical forests of the eastern Amazon: Effects on forest structure, biomass, and species composition. Biotropica 31: 2–16

    Google Scholar 

  • Cochrane MA, Alencar A, Schulze MD, Souza Jr. CM, Nepstad DC, Lefebvre P and Davidson EA (1999) Positive feedbacks in the fire dynamic of closed canopy tropical forests. Science 284: 1832–1835

    Article  PubMed  CAS  Google Scholar 

  • Cure JD, Acock B (1986) Crop responses to carbon dioxide doubling: A literature survey. Agric Forest Meteorol 38: 127–145

    Article  Google Scholar 

  • D'Antonio CM and Vitousek PM (1992) Biological invasions by exotic grasses, the grass/fire cycle, and global change. Ann Rev Ecol Syst 23: 63–87

    Google Scholar 

  • Dakora FD and Drake BG (2000) Elevated CO2 stimulates associative N2 fixation in a C3 plant of the Chesapeake Bay wetland. Plant Cell Environ 23: 943–953

    Article  CAS  Google Scholar 

  • Diaz S, Grime JP, Harris J and McPherson E (1993) Evidence of a feedback mechanism limiting plant response to elevated carbon dioxide. Nature 364: 616–617

    Article  CAS  Google Scholar 

  • Dijkstra P, Hymus G, Colavito D, Vieglais DA, Cundari CM, Johnson DP, Hungate BA, Hinkle CR and Drake BG (2002) Elevated atmospheric CO2 stimulates aboveground biomass in a fire-regenerated scrub-oak ecosystem. Global Change Ecol 8: 90–103

    Article  Google Scholar 

  • Dublin HT, Sinclair ARE and MacGlade J (1990) Elephants and fire as causes of multiple stable states in the Serengeti-Mara woodlands. J Anim Ecol 59: 1147–64

    Article  Google Scholar 

  • Edwards GE, Furbank RT, Hatch MD and Osmond CB (2001) What does it take to be C4? Lessons from the evolution of C4 photosynthesis. Plant Physiol 125: 46–49

    Article  PubMed  CAS  Google Scholar 

  • Ehleringer JR (1978) Implications of quantum yield differences on the distributions of C3 and C4 grasses. Oecologia 31: 255–267

    Article  Google Scholar 

  • Ehleringer J and Pearcy RW (1983) Variation in quantum yield for CO2 uptake among C3 and C4 plants. Plant Physiol 73: 555–559

    PubMed  CAS  Google Scholar 

  • Ehleringer JR, Cerling TE and Helliker BR (1997) C4 photosynthesis, atmospheric CO2, and climate. Oecologia 112: 285–299

    Article  Google Scholar 

  • Epstein HE, Lauenroth WK, Burke IC and Coffin DP (1997) Productivity patterns of C3 and C4 functional types in the US Great Plains. Ecology 78: 722–731

    Article  Google Scholar 

  • Farquhar GD and Sharkey TD (1982) Stomatal conductance and photosynthesis. Annu Rev Plant Physiol 33: 317–345

    Article  CAS  Google Scholar 

  • Flannigan MD, Stocks BJ and Wotton BM (2000) Climate change and forest fires. Sci Total Environ 262: 221–229

    Article  PubMed  CAS  Google Scholar 

  • Frost PGH and Robertson F (1987) Fire, the ecological effects of fire in savannas. In: Walker BH (ed) Determinants of Tropical Savannas, pp 93–140. IRL Press, Oxford

    Google Scholar 

  • Gascoigne-Owens JS, Press MC and Quick WP (2002) Elevated CO2: effects on C4 photosynthesis. Comp Biochem Physiol 132A (Suppl 1): S150

    Google Scholar 

  • Ghannoum O, von Caemmerer S, Ziska LH and Conroy JP (2000) The growth response of C4 plants to rising atmospheric CO2 partial pressure: A reassessment. Plant Cell Environ 23: 931–942

    Article  CAS  Google Scholar 

  • Ghannoum O, von Caemmerer S and Conroy JP (2001) Plant water use efficiency of 17 Australian NAD-ME and NADP-ME C4 grasses at ambient and elevated CO2 partial pressure. Aust J Plant Physiol 28: 1207–1217

    CAS  Google Scholar 

  • Gibson DJ, Seastedt TR, Briggs JM (1993) Management practices in tallgrass prairie: large-and small-scale experimental effects on species composition. J Appl Ecol 30: 247–255.

    Article  Google Scholar 

  • Gillison AN (1983) Tropical savannas of Australia and the southwest Pacific. In: Bourliere F (ed) Ecosystems of the World 13: Tropical Savannas, pp 183–243. Elsevier, Amsterdam

    Google Scholar 

  • Goldammer JG (ed) (1990) Fire in the Tropical Biota: Ecosystem Processes and Global Challenges. Springer-Verlag, Berlin

    Google Scholar 

  • Goldammer JG (1993) Historical biogeography of fire: Tropical and subtropical. In: Crutzen PJ and Goldammer JG (eds) The Ecological, Atmospheric, and Climatic Importance of Vegetation Fire, pp 297–314. John Wiley and Sons, New York

    Google Scholar 

  • Goldstein G and Sarmiento G (1987) Water relations of trees and grasses and their consequences for the structure of savanna vegetation. In: Walker BH (ed) Determinations of Tropical Savannas, pp 13–38. IRL Press, Oxford

    Google Scholar 

  • Grise DJ (1996) Effects of elevated CO2 and high temperature on the relative growth rates and competitive interactions between a C3 (Chenopodium album) and a C4 (Amaranthus hybridus) annual. PhD thesis, University of Georgia, Athens, Georgia

    Google Scholar 

  • Harris W, Forde BJ and Hardacre AK (1981) Temperature and cutting effects on the growth and competitive interaction of ryegrass and paspalum. II. Interspecific competition. N Z J Agric Res 24: 309–320

    Google Scholar 

  • Hatch MD (1987) C4 photosynthesis: A unique blend of modified biochemistry, anatomy and ultrastructure. Biochim Biophys Acta 895: 81–106

    CAS  Google Scholar 

  • Hattersley PW (1983) The distribution of C3 and C4 grasses in Australia in relation to climate. Oecologia 57: 113–128

    Article  Google Scholar 

  • Henderson S, Hattersley P, von Caemmerer S and Osmond CB (1994) Are C4 pathway plants threatened by global climatic change? In: Schulze E-D and Caldwell MM(eds) Ecophysiology of Photosynthesis, pp 529–549. Springer-Verlag, New York

    Google Scholar 

  • Hoffmann WA, Bazzaz FA, Chatterton NJ, Harrison PA and Jackson RB (2000) Elevated CO2 enhances resprouting of a tropical savanna tree. Oecologia 123: 312–317

    Article  Google Scholar 

  • Hopkins B (1983) Successional processes. In: Bourliere F (ed) Ecosystems of the World 13: Tropical Savannas, pp 605–616. Elsevier, Amsterdam

    Google Scholar 

  • Horton JL and Neufeld HS (1998) Photosynthetic responses of Microstegium vimineum (Trin.) A. Camus, a shade-tolerant, C4 grass, to variable light environments. Oecologia 114: 11–19

    Article  Google Scholar 

  • Houghton JT, Ding Y, Griggs DJ, Noguer M, van der Linden PJ and Ziaosu D (2001) Climate Change 2001: the Scientific Basis (Contribution of Working Group I to the Third Assessment Report of the Intergovernmental Panel on Climate Change (IPCC)). Cambridge University Press, Cambridge

    Google Scholar 

  • Hungate BA (1999) Ecosystem responses to rising atmospheric CO2: Feedbacks through the nitrogen cycle. In: Luo Y and Mooney HA (eds) Carbon Dioxide and Environmental Stress. pp 265–285. Academic Press, San Diego, California

    Google Scholar 

  • Johnson NC and Wedin DA (1997) Soil carbon, nutrients, and mycorrhizae during conversion of a dry tropical forest to grassland. Ecol Appl 7: 171–182

    Google Scholar 

  • Jordan DB, Ogren WL (1984) The CO2/O2 specificity of ribulose-1,5-bisphosphate carboxylase/oxygenase. Planta 161: 308–313

    Article  CAS  Google Scholar 

  • Kattenberg A, Giorgi F, Grassl H, Meehl GA, Mitchell JFB, Stouffer RJ, Tokioka T, Weaver AJ and Wigley TML(1996) Climate models - projections of future climate. In: Houghton JT, Filho LGM, Callander BA, Harris N, Kattenberg A and Maskell K (eds) Climate Change 1995: the Science of Climate Change, pp 285–357. Cambridge University Press, Cambridge, UK

    Google Scholar 

  • Kauffman JB, Cummings DL, Ward DE and Babbitt R (1995) Fire in the Brazilian Amazon: 1. Biomass, nutrient pools, and losses in slashed primary forests. Oecologia 104: 397–408

    Article  Google Scholar 

  • Knapp AK and Medina E (1999) Success of C4 photosynthesis in the field: Lessons from communities dominated by C4 plants. In: Sage RF and Monson RK (eds) C4 Plant Biology, pp 251–283. Academic Press, San Diego, California

    Google Scholar 

  • Knapp AK, Hamerlynck EP, Ham JM and Owensby CE (1996) Responses in stomatal conductance to elevated CO2 in 12 grassland species that differ in form. Vegetatio 125: 31–41

    Article  Google Scholar 

  • Ko LJ and Reich PB (1993) Oak tree effects on soil and herbaceous vegetation in savannas and pastures in Wisconsin. Am Midl Nat 130: 31–42

    Article  Google Scholar 

  • Koch GW and Mooney HA (eds) (1996) Carbon Dioxide and Terrestrial Ecosystems. Academic Press, San Diego, California

    Google Scholar 

  • Krall JP and Pearcy RW (1993) Concurrent measurements of oxygen and carbon dioxide exchange during lightflecks in maize (Zea mays L.). Plant Physiol 103: 823–828

    PubMed  CAS  Google Scholar 

  • Ku S-B and Edwards GE (1977) Oxygen inhibition of photosynthesis. I. Temperature dependence and relation to O2/CO2 solubility ratio. Plant Physiol 59: 986–990

    PubMed  CAS  Google Scholar 

  • Kubien DS (2003) On the performance of C4 photosynthesis at low temperatures and its relationship to the ecology of C4 plants in cool climates. PhD dissertation. University of Toronto, Canada

    Google Scholar 

  • Kucera CL (1992) Tall-grass prairie. In: Coupland RT (ed) Ecosystems of the World, Vol8A: Natural Grasslands, Introduction and Western Hemisphere, pp 227–268. Elsevier, Amsterdam

    Google Scholar 

  • LeCain DR and Morgan JA (1998) Growth, gas exchange, leaf nitrogen and carbohydrate concentrations in NAD-ME and NADPME C4 grasses in elevated CO2. Physiol Plant 102: 297–306

    Article  CAS  Google Scholar 

  • Lee TD, Tjoelker MG, Ellsworth DS and Reich PB (2001) Leaf gas exchange responses of 13 prairie grassland species to elevated CO2 and increased nitrogen supply. New Phytol 150: 405–418

    Article  CAS  Google Scholar 

  • Leegood RC and Edwards GE (1996) Carbon metabolism and photorespiration: temperature dependence in relation to other environmental factors. In: Baker NR (ed) Photosynthesis and the Environment, pp 191–221. Kluwer Academic Publishers, Dordrecht, The Netherlands

    Google Scholar 

  • Lin G, Philips SL and Ehleringer JR (1996) Monsoonal precipitation responses of shrubs in a cold desert community on the Colorado Plateau. Oecologia 106: 8–17

    Google Scholar 

  • Long SP (1983) C4 Photosynthesis at low temperatures. Plant Cell Environ 6: 345–363

    CAS  Google Scholar 

  • 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: 729–740

    Article  CAS  Google Scholar 

  • Long SP (1999) Environmental responses. In: Sage RF and Monson RK (eds) The Biology of C4 Photosynthesis, pp. 215–249. Academic Press, San Diego, California

    Google Scholar 

  • Ludlow MM (1985) Photosynthesis and dry matter production in C3 and C4 pasture plants, with special emphasis on tropical C3legumes and grasses. Aust J Plant Physiol 12: 557–572

    Article  Google Scholar 

  • Maas JM (1995) Conversion of tropical dry forest to pasture and agriculture. In: Bullock SH, Mooney HA and Medina E (eds) Seasonal Dry Tropical Forests, pp 399–422. Cambridge University Press, Cambridge, UK

    Google Scholar 

  • Maherali H, Reid CD, Polley HW, Johnson HB and Jackson RB (2002) Stomatal acclimation over a subambient to elevated CO2 gradient in a C3/C4 grassland. Plant Cell Environ 25: 557–566

    Article  CAS  Google Scholar 

  • Means DB (1997) Wiregrass restoration: Probable shading effects in a slash pine plantation. Restoration Manage Notes 15: 52–55

    Google Scholar 

  • Monson RK, Littlejohn RO Jr and Williams GJ III (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 

  • Morgan JA, LeCain DR, Read JJ, Hunt HW and Knight WG (1998) Photosynthetic pathway and ontogeny affect water relations and the impact of CO2 on Bouteloua gracilis (C4) and Pascopyrum smithii (C3). Oecologia 114: 483–493

    Article  Google Scholar 

  • Morgan JA, LeCain DR, Mosier AR and Milchunas DG (2001) Elevated CO2 enhances water relations and productivity and affects gas exchange in C3 and C4 grasses of the Colorado shortgrass steppe. Global Change Biol 7: 451–466

    Article  Google Scholar 

  • Mueller-Dombois D and Goldammer JB (1990) Fire in tropical ecosystems and global environmental change: an introduction. In: Goldammer, JG (ed) Fire in the Tropical Biota - Ecosystem Processes and Global Challenges, pp 1–10. Springer-Verlag, Berlin

    Google Scholar 

  • Ode DJ, Tieszen LL and Lerman JC (1980) The seasonal contribution of C3 and C4 plant species to primary production in a mixed prairie. Ecology 61: 1304–1311

    Article  Google Scholar 

  • Osmond CB, Winter K and Ziegler H (1982) Functional significance of different pathways of CO2 fixation in photosynthesis. In: Lange OL, Nobel PS, Osmond CB and Ziegler H (eds) Encyclopedia of Plant Physiology, New Series, Vol 12B. Physiological Plant Ecology II. Water Relations and Carbon Assimilation, pp 479–547. Springer-Verlag, Berlin

    Google Scholar 

  • Owensby CE, Ham JM, Knapp A, Rice CW, Coyne PI and Auen LM(1996) Ecosystem-level responses of tallgrass prairie to elevated CO2. In: Koch GW and Mooney HA (eds) Carbon Dioxide and Terrestrial Ecosystems, pp 147–162. Academic Press, San Diego, California

    Google Scholar 

  • Owensby CE, Ham JM, Knapp A, Bremer D and Auen LM (1997) Water vapor fluxes and their impact under elevated CO2 in a C4-tallgrass prairie. Global Change Biol 3: 189–195

    Article  Google Scholar 

  • Patterson DT (1995) Weeds in a changing climate. Weed Sci 43: 685–701

    CAS  Google Scholar 

  • Patterson DT and Flint EP (1990) Implications of increasing carbon dioxide and climate change for plant communities and competition in natural and managed ecosystems. In: Impact of Carbon Dioxide, Trace Gases, and Climate Change on Global Agriculture, Special publication 53, pp 83–109. Am Soc Agron, Madison, Wisconsin

    Google Scholar 

  • Pearcy RW and Calkin HW (1983) Carbon dioxide exchange of C3 and C4 tree species in the understory of a Hawaiian forest. Oecologia 58: 26–32

    Article  Google Scholar 

  • Pearcy RW and Ehleringer J (1984) Comparative ecophysiology of C3 and C4 plants. Plant Cell Environ 7: 1–13

    Article  CAS  Google Scholar 

  • Pearcy RW, Tumosa N and Williams K (1981) Relationships between growth, photosynthesis and competitive interactions for a C3 and a C4 plant. Oecologia 48: 371–376

    Article  Google Scholar 

  • Pearcy RW, Osteryoung K and Calkin HW (1985) Photosynthetic responses to dynamic light environments by Hawaiian trees. Plant Physiol 79: 896–902

    Article  PubMed  CAS  Google Scholar 

  • Peat HCL (1997) Dynamics of C3 and C4 productivity in northern mixed grass prairie. MSc thesis, University of Toronto, Canada

    Google Scholar 

  • Pittermann J and Sage RF (2001) The response of the high altitude C4 grass Muhlenbergia montana (Nutt.) A.S. Hitchc. to long and short-term chilling. J Exp Bot 52: 829–838

    PubMed  CAS  Google Scholar 

  • Polley HW (1997) Implications of rising atmospheric carbon dioxide concentration for rangelands. J Range Manage 50: 561–577

    Google Scholar 

  • Polley HW, Johnson HB and Mayeux HS (1994) Increasing CO2: Comparative responses of the C4 grass Schizachyrium and grassland invader Prosopis. Ecology 75: 976–988

    Article  Google Scholar 

  • Polley HW, Johnson HB and Derner JD (2002) Soil-and plant water dynamics in a C3/C4 grassland exposed to a subambient to superambient CO2 gradient. Global Change Biol 8: 1118–1129

    Article  Google Scholar 

  • Pyne SJ (1990) Fire conservancy: the origins of wildland fire protection in British India, America and Australia. In: Goldammer JG (ed) Fire in the Tropical Biota - Ecosystem Processes and Global Challenges, pp 319–336. Springer-Verlag, Berlin

    Google Scholar 

  • Reich PB, Tilman D, Craine J, Ellsworth D, Tjoelker MG, Knops J, Wedin D, Naeem S, Bahauddin D, Goth J, Bengtson W and Lee TD (2001) Do species and functional groups differ in acquisition and use of C, N and water under varying atmospheric CO2 and N availability regimes? A field test with 16 grassland species. N Phytol 150: 435–448

    Article  CAS  Google Scholar 

  • Sage RF (1994) Acclimation of photosynthesis to increasing atmospheric CO2: the gas exchange perspectives. Photosynth Res 39: 351–368

    Article  CAS  Google Scholar 

  • Sage RF (1996) Modification of fire disturbance by elevated CO2. In: Korner CH and F Bazzaz (eds) Carbon Dioxide, Populations, and Communities, pp 231–249. Academic Press, San Diego, California

    Google Scholar 

  • Sage RF (2001) C4 plants. In: Encyclopedia of Biodiversity, Vol I, pp 575–598. Academic Press, San Diego, California

    Google Scholar 

  • Sage RF (2002) Variation in the kcat of Rubisco in C3 and C4 plants and some implications for photosynthetic performance at high and low temperature. J Exp Bot 53: 609–620

    Article  PubMed  CAS  Google Scholar 

  • Sage RF and Coleman JR (2001) Low CO2 effects on plants: more than a thing of the past. Trends Plant Sci 6: 18–24

    Article  PubMed  CAS  Google Scholar 

  • Sage RF and Pearcy RW (1987) The nitrogen use efficiency of C3 and C4 plants. II. Leaf nitrogen effects on the gas exchange characteristics of Chenopodium album L. and Amaranthus retroflexus L. Plant Physiol 84: 959–963

    PubMed  CAS  Google Scholar 

  • Sage RF and Pearcy RW (2000) The physiological ecology of C4 photosynthesis. In: Leegood RC, Sharkey TD and von Caemmerer S (eds) Photosynthesis: Physiology and Metabolism, pp 497–532. Kluwer Academic Publishers, Dordrecht, The Netherlands

    Google Scholar 

  • Sage RF and Sage TL (2002) Microsite characteristics of Muhlenbergia richardsonis (Trin.) Rydb., an alpine C4 grass from the White Mountains, California. Oecologia 132: 501–508

    Article  Google Scholar 

  • Sage RF, Santrucek J and Grise DJ (1995) Temperature effects on the photosynthetic response of C3 plants to long-term CO2 enrichment. Vegetatio 121: 67–77

    Article  Google Scholar 

  • Sage RF, Wedin DA and Li M-R (1999) The biogeography of C4 photosynthesis: patterns and controlling factors. In: Sage RF and Monson RK (eds) C4 Plant Biology, pp 313–373. Academic Press, San Diego, California

    Google Scholar 

  • Sala OE, Chapin III FS and Huber-Sannwald E (2001) Potential biodiversity change: Global patterns and biome comparisons. In: Chapin III FS, Sala OE, Huber-Sannwald E (eds) Global Biodiversity in a Changing Environment: Scenarios for the 21st Century, pp 351–367. Springer-Verlag, New York

    Google Scholar 

  • San Jose JJ, Farinas MR (1991) Temporal changes in the structure of a Trachypogon savanna protected for 25 years. Acta Oecol 12: 237–247

    Google Scholar 

  • Schortemeyer M, Atkin OK, McFarlane N and Evans JR (2002) N2 fixation by Acacia species increases under elevated atmospheric CO2. Plant Cell Environ 25: 567–579

    Article  CAS  Google Scholar 

  • Schüle W(1990) Landscapes and climate in prehistory: interactions of wildlife, man and fire. In: Goldammer JG (ed) Fire in the Tropical Biota - Ecosystem Processes and Global Challenges, pp 373–318. Springer-Verlag, Berlin

    Google Scholar 

  • Schulze E-D and Hall AE (1982) Stomatal responses, water loss, and CO2 assimilation rates of plants in contrasting environments. In: Lange OL, Nobel PS, Osmond CB and Ziegler H (eds) Encyclopedia of Plant Physiology, New Series, Vol 12B. Physiological Plant Ecology II. Water Relations and Carbon Assimilation, pp 181–230. Springer-Verlag, Berlin

    Google Scholar 

  • Sharkey TD (1988) Estimating the rate of photorespiration in leaves. Physiol Plant 73: 147–152

    CAS  Google Scholar 

  • Snowden SW, Press MC and Quick WP (2002) How does elevated CO2 impact C3, C3-C4 and C4 photosynthesis of Flaveria species? Comp Biochem Physiol 132A (Suppl 1): S155

    Google Scholar 

  • Soares RV (1990) Fire in some tropical and subtropical South American vegetation types: An overview. In: Goldammer JG (ed) Fire in the Tropical Biota - Ecosystem Processes and Global Challenges, pp 63–81. Springer-Verlag, Berlin

    Google Scholar 

  • Stitt M (1991) Rising CO2 levels and their potential significance for carbon flow in photosynthetic cells. Plant Cell Environ 14: 741–762

    Article  CAS  Google Scholar 

  • Teeri JA and Stowe LG (1976) Climatic patterns and the distribution of C4 grasses in North America. Oecologia 23: 1–12

    Google Scholar 

  • Tieszen LL, Reed BC, Bliss NB, Wylie BK and DeJong DD (1997) NDVI, C3 and C4 production, and distributions in Great Plains grassland land cover classes. Ecol Appl 7: 59–78

    Article  Google Scholar 

  • Tissue DT, Griffen KL, Thomas RB and Strain BR (1995) Effects of low and elevated CO2 on C3 and C4 annuals. II. Photosynthesis and leaf biochemistry. Oecologia 101: 21–28

    Article  Google Scholar 

  • Tissue DT, Megonigal JP and Thomas RB (1997) Nitrogenase activity and N2 fixation are stimulated by elevated CO2 in a tropical N2-fixing tree. Oecologia 109: 28–33

    Article  Google Scholar 

  • Uhl C and Buschbacher R (1985) A disturbing synergism between cattle ranch burning practices and selective tree harvesting in the eastern Amazon. Biotropica 17: 265–268

    Article  Google Scholar 

  • Uhl C and Kauffman JB (1990) Deforestation, fire susceptibility, and potential tree responses to fire in the eastern Amazon. Ecology 71: 437–449

    Article  Google Scholar 

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

    Article  Google Scholar 

  • Vitousek PM (1994) Beyond global warming: ecology and global change. Ecology 75: 1861–1876

    Article  Google Scholar 

  • Vitousek PM, Aber JD, Howarth RW, Linkens GE, Matson PA, Schindler DW, Schlesinger WH and Tilman DG (1997) Human alteration of the global nitrogen cycle: sources and consequences. Ecol Appl 7: 737–750

    Google Scholar 

  • Vogel CS, Curtis PS and Thomas RB (1997) Growth and nitrogen accretion of dinitrogen-fixing Alnus glutinosa (L.) Gaertn. under elevated carbon dioxide. Plant Ecol 130: 63–70

    Article  Google Scholar 

  • von Caemmerer S (2000) Biochemical Models of Leaf Photosynthesis. CSIRO, Canberra, Australia

    Google Scholar 

  • Wan CSM, Sage RF (2001) Climate and the distribution of C4 grasses along the Atlantic and Pacific coasts of North America. Can J Bot 79: 474–486

    Article  Google Scholar 

  • Wand SJE, Midgley GF, Jones MH and Curtis PS (1999) Responses of wild C4 and C3 grass (Poaceae) species to elevated atmospheric CO2 concentration: a meta-analytic test of current theories and perceptions. Global Change Biol 5: 723–741

    Article  Google Scholar 

  • Watling JR, Press MC and Quick WP (2000) Elevated CO2 induces biochemical and ultrastructural changes in leaves of the C4 cereal sorghum. Plant Physiol 123: 1143–1152

    Article  PubMed  CAS  Google Scholar 

  • Wedin DA and Tilman D (1993) Competition among grasses along a nitrogen gradient: initial conditions and mechanisms of competition. Ecol Monogr 63: 199–229

    Article  Google Scholar 

  • Wedin DA and Tilman D (1996) Influence of nitrogen loading and species composition on the carbon balance of grasslands. Science 274: 1720–1723

    Article  PubMed  CAS  Google Scholar 

  • Weltzin JF and Coughenour MB (1990) Savanna tree influence on understory vegetation and soil nutrients in northwestern Kenya. J Veg Sci 1: 325–334

    Article  Google Scholar 

  • White TA, Campbell BD, Kemp PD and Hunt CL (2000) Sensitivity of three grassland communities to simulated extreme temperature and rainfall events. Global Change Biol 6: 671–684

    Article  Google Scholar 

  • White TA, Campbell BD, Kemp PD and Hunt CL (2001) Impacts of extreme climatic events on competition during grassland invasions. Global Change Biol 7: 1–13

    Article  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Rights and permissions

Reprints and permissions

About this article

Cite this article

Sage, R.F., Kubien, D.S. Quo vadis C4? An ecophysiological perspective on global change and the future of C4 plants. Photosynthesis Research 77, 209–225 (2003). https://doi.org/10.1023/A:1025882003661

Download citation

  • Issue Date:

  • DOI: https://doi.org/10.1023/A:1025882003661

Navigation