Advertisement

Chapter 17 The Geologic History of C4 Plants

  • Colin P. Osborne
Chapter
Part of the Advances in Photosynthesis and Respiration book series (AIPH, volume 32)

Summary

Our understanding of C4 plant history has been revolutionized by the use of carbon isotopes to construct geologic records of photosynthetic pathway. Through isotopic analyses of fossil teeth and soils, geochemists have discovered that the dominance of low latitude ecosystems by C4 species is a relatively recent phenomenon. A major expansion of C4 grasslands occurred across four continents only during the Late Miocene and Pliocene (2–8 Myr ago, Ma), with intriguing evidence suggesting a presence of C4 plants at low abundance for at least 10 Myr before this event. Analysis of calibrated molecular phylogenies for the grasses indicates that declining atmospheric CO2 began to select for C4 photosynthesis during the Oligocene (25–30 Ma), but there remains an important gap in the geochemical data between this event and Miocene evidence of the pathway. A similar atmospheric selection pressure may have operated during the Permo-Carboniferous (270–330 Ma), but isotope surveys have so-far failed to detect any direct evidence of C4 species. Understanding when C4 plants first originated, and why they remained sub-dominant components of ecosystems for so long, therefore remain important unresolved problems in this field. However, the worldwide expansion of C4 grasslands is better understood. A range of complementary geologic data now indicate that increasing climatic seasonality or aridity caused a retraction of woodland vegetation and allowed the incursion of C4 grasses. Abrupt increases in charcoal abundance in the Late Miocene and analogies with modern fire-maintained mesic grasslands indicate an important additional role for fire in this vegetation change. However, significant uncertainties remain, especially in explaining why earlier seasonal climates did not promote C4 grassland expansion, and what drove this event in North America, where there is no evidence of abrupt climate change. I propose that the evolution of grazing resistance in C4 grasses could have promoted fires, providing a mechanism for vegetation change without the need to evoke paleoclimate change.

Keywords

Late Miocene Great Plain Middle Miocene Geologic Record Photosynthetic Pathway 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.

Abbreviations:

Ma

Myr ago

Rubisco

Ribulose-1,5-bisphospate Carboxylase/oxygenase

CA

Carbonic Anhydrase

PEPC

PhosphoenolpyruvateCarboxylase

Notes

Acknowledgments

I thank David Beerling for many stimulating discussions on this subject, Rowan Sage, Jay Quade and an anonymous reviewer for their insightful comments on the manuscript, and The Royal Society for funding through a University Research Fellowship.

References

  1. Agrawal AA (2007) Macroevolution of plant defense strategies. Tree, 22: 103–109.PubMedGoogle Scholar
  2. Agrawal AA and Fishbein M (2006) Plant defense syndromes. Ecology, 87: S132–S149.PubMedCrossRefGoogle Scholar
  3. Algeo TJ and Scheckler SE (1998) Terrestrial-marine teleconnections in the Devonian: links between the evolution of land plants, weathering processes, and marine anoxic events. Phil Trans Royal Soc B 353: 113–130.CrossRefGoogle Scholar
  4. Amundson R, Evett RR, Jahren AH and Bartolome J (1997) Stable carbon isotope composition of Poaceae pollen and its potential in paleovegetational reconstructions. Rev Pal Pal, 99: 17–24.CrossRefGoogle Scholar
  5. Archibald S, Bond WJ, Stock WD and Fairbanks DHK (2004) Shaping the landscape: fire grazer interactions in an African savanna. Ecological Applications 15: 96–109CrossRefGoogle Scholar
  6. Axelrod DI (1985) Rise of the grassland biome, central North America. Bot Rev 51: 163–201.CrossRefGoogle Scholar
  7. Beerling DJ (2005) Evolutionary responses of land plants to atmospheric CO2. Pages 114–132 in J.R. Ehleringer, T.E. Cerling, M.D. Dearing, editors, A History of Atmospheric CO 2 and its Effects on Plants, Animals, and Ecosystems. Springer, New York.Google Scholar
  8. Beerling DJ and Osborne CP (2006) The origin of the savanna biome. Global Change Biology 12: 2023–2031.CrossRefGoogle Scholar
  9. Berner RA (1999) A new look at the long-term carbon cycle. GSA Today 9: 1–6Google Scholar
  10. Berner RA (2005) The Phanerozoic Carbon Cycle. CO 2 and O 2Oxford University Press, Oxford.Google Scholar
  11. Berner RA, Petsch ST, Lake JA, Beerling DJ, Popp BN, Lane RS, Laws EA, Westley MB, Cassar N, Woodward FI, Quick WP (2000) Isotope fractionation and atmospheric oxygen: implications for Phanerozoic O2 evolution. Science, 287: 1630–1633.PubMedCrossRefGoogle Scholar
  12. Bird MI and Cali JA (1998) A million-year record of fire in sub-Saharan Africa. Nature 394: 767–769.CrossRefGoogle Scholar
  13. Bond WJ (2005) Large parts of the world are brown or black: a different view on the ‘green world’ hypothesis. J Veg Sci 16: 261–266.Google Scholar
  14. Bond WJ, Midgley GF and Woodward FI (2003) What controls South African vegetation – climate or fire? S Afr J Bot 69: 79–91.Google Scholar
  15. Bond WJ, Silander JA, Ranaivonasy J and Ratsirarson J (2008) The antiquity of Madagascar’s grasslands and the rise of C4 grassy biomes. J Biogeog 35: 1743–1758.CrossRefGoogle Scholar
  16. Bond WJ, Woodward FI and Midgley GF (2005) The global distribution of ecosystems in a world without fire. New Phytol 165: 525–538.PubMedCrossRefGoogle Scholar
  17. Bragg TB and Hulbert LC (1976) Woody plant invasion of unburned Kansas bluestem prairie. J Range Manage 29: 19–23.CrossRefGoogle Scholar
  18. Burt-Smith GS, Grime JP and Tilman D (2003) Seedling resistance to herbivory as a predictor of relative abundance in a synthesized prairie ecosystem. Oikos 101: 345–353CrossRefGoogle Scholar
  19. Cerling TE (1999) Palaeorecords of C4 plants and ecosystems. In: C 4 plant biology (eds. R.F. Sage and R.K. Monson), pp. 445–469. Academic Press, San Diego, CA.Google Scholar
  20. Cerling TE, Ehleringer JR and Harris JM (1998) Carbon dioxide starvation, the development of C4 ecosystems, and mammalian evolution. Phil Trans Royal Soc B 353: 159–171.CrossRefGoogle Scholar
  21. Cerling TE, Harris JM, MacFadden BJ, Leakey MG, Quade J, EisenmannV and Ehleringer JR (1997) Global vegetation change through the Miocene / Pliocene boundary. Nature 389: 153–158.CrossRefGoogle Scholar
  22. Cerling TE, Quade J, Wang Y and Bowman JR (1989) Carbon isotopes in soils and palaeosols as ecology and palaeoecology indicators. Nature 341: 138–139.CrossRefGoogle Scholar
  23. Chenggao G and Renaut R W (1994) The effect of Tibetan uplift on the formation and preservation of Tertiary lacustrine source-rocks in eastern China. J Paleolimnol 11: 31–40.CrossRefGoogle Scholar
  24. Christin PA, Besnard G, Samaritani E, Duvall MR, Hodkinson TR, Savolainen V and Salamin N (2008). Oligocene CO2 decline promoted C4 photosynthesis in grasses. Current Biol 18: 37–43.CrossRefGoogle Scholar
  25. Coleman M and Hodges K (2002) Evidence for Tibetan plateau uplift before 14 Myr ago from a new minimum age for east-west extension. Nature 374: 49–52.CrossRefGoogle Scholar
  26. Collins SL and Steinauer EM (1998) Disturbance, diversity, and species interactions in tallgrassprairie. Pages 140–156 in A.K. Knapp, J.M. Briggs, D.C. Hartnett and S.L. Collins, editors, Grassland Dynamics. Long-Term Ecological Research in Tallgrass Prairie. Oxford University Press, New York.Google Scholar
  27. Cornelissen JH, Pérez-Harguindeguy N, Díaz S, Grime JP, Marzano B, Cabido M, Vendramini F and Cerabolini B (1999) Leaf structure and defence control litter ­decomposition rate across species and life forms in regional floras on two continents. New Phytol 143: 191–200.CrossRefGoogle Scholar
  28. D’Antonio CM and Vitousek PM (1992) Biological invasions by exotic grasses, the grass/fire cycle, and global change. Annu Rev Ecol Syst 23: 63–87.Google Scholar
  29. DeCelles PG, Quade J, Kapp P, Fan MJ, Dettman DL and Ding L (2007) High and dry in central Tibet during the Late Oligocene. Earth Planet Sci Lett 253: 389–401.CrossRefGoogle Scholar
  30. Dettman DL, Kohn MJ, Quade J, Ryerson FJ, Ojha TP and Hamidullah S (2001) Seasonal stable isotope evidence for a strong Asian monsoon throughout the past 10.7 m.y. Geology 29: 31–34.CrossRefGoogle Scholar
  31. Ding ZL and Yang SL (2000) C3 / C4 vegetation evolution over the last 7.0 Myr in the Chinese Loess Plateau: evidence from pedogenic carbonate δ13C. Palaeogeogr ­Palaeoclimatol Palaeoecol 160: 291–299.CrossRefGoogle Scholar
  32. Dugas DP and Retallack GJ (1993) Middle Miocene fossil grasses from Fort Ternan, Kenya. J Paleon 67: 113–128.Google Scholar
  33. Dupont-Nivet G, Krijgsman W, Langereis CG, Abels HA, Dai S and Fang X (2007) Tibetan plateau aridification linked to global cooling at the Eocene-Oligocene transition. Nature 445: 635–638.PubMedCrossRefGoogle Scholar
  34. Eek KM, Sessions AL and Lies DP (2007) Carbon-isotopic analysis of microbial cells sorted by flow cytometry. Geobiology 5: 85–95.CrossRefGoogle Scholar
  35. Ehleringer J and Björkman O (1977) Quantum yields for CO2 uptake in C3 and C4 plants. Dependence on temperature, CO2, and O2 concentration. Plant Physiol 59: 86–90.PubMedCrossRefGoogle Scholar
  36. Ehleringer JR, Cerling TE and Helliker BR (1997) C4 photosynthesis, atmospheric CO2, and climate. Oecologia 112: 285–299.CrossRefGoogle Scholar
  37. Ehleringer JR, Sage RF, Flanagan LB and Pearcy RW (1991) Climate change and the evolution of C4 photosynthesis. Tree 6: 95–99.PubMedGoogle Scholar
  38. Ellis RP (1990) Tannin-like substances in grass leaves. Memoirs of the Botanical Survey of South Africa 59: 1–80.Google Scholar
  39. Farquhar GD (1983) On the nature of carbon isotope discrimination in C4 species. Aus J Plant Physiol 10: 205–226.CrossRefGoogle Scholar
  40. Farquhar GD, O’Leary MH and Berry JA (1982) On the relationship between carbon isotope discrimination and the intercellular carbon dioxide concentration in leaves. Aus J Plant Physiol 9: 121–137.CrossRefGoogle Scholar
  41. Fluteau F, Ramstein G and Besse J (1999) Simulating the evolution of the Asian and African monsoons during the past 30 Myr using an atmospheric general circulation model. J Geophys Res 104: 11995–12018.CrossRefGoogle Scholar
  42. Fox DL and Fisher DC 2004. Dietary reconstruction of Gomphotherium (Mammalia, Proboscidea) based on carbon isotope composition of tusk enamel. Palaeogeogr Palaeoclimatol Palaeoecology 206: 311–335.CrossRefGoogle Scholar
  43. Fox DL and Koch PL (2003) Tertiary history of C4 biomass in the Great Plains, USA. Geology 31: 809–812.CrossRefGoogle Scholar
  44. Fox DL and Koch PL (2004) Carbon and oxygen isotope variability in Neogene paleosol carbonates: constraints on the evolution of the C4-grasslands of the Great Plains, USA. Palaeogeogr Palaeoclimatol Palaeoecol 207: S305–S329.CrossRefGoogle Scholar
  45. Freeman KH and Colarusso LA (2001) Molecular and isotopic records of C4 grassland expansion in the late Miocene. Geochim Cosmochim Acta 65: 1439–1454.CrossRefGoogle Scholar
  46. Gheerbrant E, Sudre J and Cappetta H (1996) A Palaeocene proboscidean from Morocco. Nature 383: 68–70.CrossRefGoogle Scholar
  47. Giussani LM, Cota-Sanchez JH, Zuloaga FO and Kellogg EA (2001) A molecular phylogeny of the grass subfamily Panicoideae (Poaceae) shows multiple origins of C4 photosynthesis. Am J Bot 88: 1993–2012.PubMedCrossRefGoogle Scholar
  48. Gradstein F, Ogg J and Smith A (2004) A Geologic Timescale 2004. Cambridge University Press, Cambridge.CrossRefGoogle Scholar
  49. Grigulis K, Lavorel S, Davies ID, Dossantos A, Llorets F and Villa M (2005) Landscape-scale positive feedbacks between fire and expansion of the large tussock grass, Ampelodesmos mauritanica in Catalan shrublands. Global Change Biol 11: 1042–1053.CrossRefGoogle Scholar
  50. Grime JP (2001) Plant strategies, vegetation processes, and ecosystem properties. Wiley, Chichester, UK.Google Scholar
  51. Guo ZT, Ruddiman WF, Hao QZ, Wu HB, Qiao YS, Zhu RX, Peng SZ, Wei JJ, Yuan BY and Liu TS (2002) Onset of Asian desertification by 22 Myr ago inferred from loess deposits in China. Nature 416: 159–163.PubMedCrossRefGoogle Scholar
  52. Herring JR (1985) Charcoal fluxes into sediments of the North Pacific Ocean: the Cenozoic record of burning, The carbon cycle and atmospheric CO 2 : natural variations Archean to present (eds E. T. Sundquist and W. S. Broecker), pp. 419–442, American Geophysical Union, Washington, DC.Google Scholar
  53. Hoorn C, Ohja T and Quade J (2000) Palynological evidence for vegetation development and climatic change in the Sub-Himalayan Zone (Neogene, Central Nepal). Palaeogeogr Palaeoclimatol Palaeoecol 163: 133–161.CrossRefGoogle Scholar
  54. Horner JD, Gosz JR and Cates RG (1988) The role of carbon-based plant secondary metabolites in decomposition in terrestrial ecosystems. The American Naturalist 132: 869–883.CrossRefGoogle Scholar
  55. Huntley BJ (1984) Characteristics of South African biomes. Pages 1–17 in P. De V. Booysen, and N.M. Tainton, editors, Ecological Effects of Fire in South African Ecosystems. Springer-Verlag, Berlin, Germany.CrossRefGoogle Scholar
  56. Hutchinson JH (1982) Turtle, crocodilian, and champosaur diversity changes in the Cenozoic of the north-central region of western United States. Palaeogeogr Palaeoclimatol Palaeoecol 37: 149–164.CrossRefGoogle Scholar
  57. Jacobs BF (2004) Palaeobotanical studies from tropical Africa: relevance to the evolution of forest, woodland and savannah biomes. Phil Trans Royal Soc B 359: 1573–1583.CrossRefGoogle Scholar
  58. Jacobs BF, Kingston JD and Jacobs LL (1999) The origin of grass-dominated ecosystems. Ann Missouri Bot Gard 86: 590–643.CrossRefGoogle Scholar
  59. Jahren AH (2004) The carbon stable isotope composition of pollen. Rev Pal Pal 132: 291–313.CrossRefGoogle Scholar
  60. Jia G, Peng P, Zhao Q and Jian Z (2003) Changes in terrestrial ecosystem since 30 Ma in East Asia: stable isotope from black carbon in the South China Sea. Geology 31: 1093–1096.CrossRefGoogle Scholar
  61. Jones TP (1994) 13C enriched lower Carboniferous fossil plants from Donegal, Ireland: carbon isotope constraints on taphonomy, diagenesis and palaeoenvironments. Rev Pal Pal 81: 53–64.CrossRefGoogle Scholar
  62. Kadereit G, Borsch T, Weising K and Freitag H (2003) Phylogeny of Amaranthaceae and Chenopodiaceae and the evolution of C4 photosynthesis. Int J Plant Sci 164: 959–986.CrossRefGoogle Scholar
  63. Kappelman J, Rasmussen DT, Sanders WJ, Feseha M, Bown T, Copeland P, Crabaugh J, Fleagle J, Glantz M, Gordon A, Jacobs B, Maga M, Muldoon K, Pan A, Pyne L, Richmond B, Ryan T, Seiffert ER, Sen S, Todd L, Wiemann MC and Winkler A (2003) Oligocene mammals from Ethiopia and faunal exchange between Afro-Arabia and Eurasia. Nature 426: 549–552.PubMedCrossRefGoogle Scholar
  64. Keeley JE and Rundel PW (2003) Evolution of CAM and C4 carbon-concentrating mechanisms. Int J Plant Sci 164: S55–S77.CrossRefGoogle Scholar
  65. Keeley JE and Rundel PW (2005) Fire and the Miocene expansion of C4 grasslands. Ecology Lett 8: 683–690.CrossRefGoogle Scholar
  66. Kürchner WM, Kvaćek Z and Dilcher DL (2008) The impact of Miocene atmospheric carbon dioxide fluctuations on climate and the evolution of terrestrial ecosystems. Proc Natl Acad Sci USA 105: 449–453.CrossRefGoogle Scholar
  67. Kuypers MMM, Pancost RD and Damsté JSS (1999) A large and abrupt fall in atmospheric CO2 concentration during Cretaceous times. Nature 399: 342–345.CrossRefGoogle Scholar
  68. Latorre C, Quade J and McIntosh WC (1997) The expansion of C4 grasses and global change in the late Miocene: stable isotope evidence from the Americas. Earth Planet Sci Lett 146: 83–96.CrossRefGoogle Scholar
  69. Lee-Thorp JA and van der Merwe NJ (1987) Carbon isotope analysis of fossil bone apatite. South Afr J Sci 83: 712–715.Google Scholar
  70. Lee-Thorp JA, van der Merwe NJ and Brain CK (1989) Isotopic evidence for dietary differences between two extinct baboon species from Swartkrans J Hum Evol 18: 183–190.CrossRefGoogle Scholar
  71. Levin NE, Quade J, Simpson SW, Semaw S and Rogers M (2004) Isotopic evidence for Plio-Pleistocene environmental change at Gona, Ethiopia. Earth Planet Sci Lett 219: 93–110.CrossRefGoogle Scholar
  72. Lunt DJ, Ross I, Hopley PJ and Valdes PJ (2007) Modelling Late Oligocene C4 grasses and climate. Palaeogeogr Palaeoclimatol Palaeoecol 251: 239–253.CrossRefGoogle Scholar
  73. Massey FP, Ennos AR and Hartley SE (2007) Grasses and the resource-availability hypothesis: the importance of silica-based defences. J Ecol 95: 414–424.CrossRefGoogle Scholar
  74. Molnar P (2005) Mio-Pliocene growth of the Tibetan Plateau and evolution of the East Asian climate. Palaeontologia Electronica 8: 1–23.Google Scholar
  75. Morley RJ and Richards K (1993) Gramineae cuticle: a key indicator of Late Cenozoic climatic change in the Niger Delta. Rev Pal Pal 77: 119–127.CrossRefGoogle Scholar
  76. Mouillot F and Field CB (2005) Fire history and the global carbon budget: a 1º × 1º fire history reconstruction for the 20th century. Global Change Biol 11: 398–420.CrossRefGoogle Scholar
  77. Nambudiri EMV, Tidwell WD, Smith BN and Hebbert NP (1978) A C4 plant from the Pliocene. Nature 276: 816–817.CrossRefGoogle Scholar
  78. Nelson DM, Hu FS, Mikucki JA, Tian J and Pearson A (2007) Carbon-isotopic analysis of individual pollen grains from C3 and C4 grasses using a spooling wire microcombustion interface. Geochim Cosmochim Acta 71: 4005–4014.CrossRefGoogle Scholar
  79. Nelson DM, Hu FS, Scholes DR, Joshi N and Pearson A (2008) Using SPIRAL (Single Pollen Isotope Ratio AnaLysis) to estimate C3- and C4-grass abundance in the paleorecord. Earth Planet Sci Lett 269: 11–16.CrossRefGoogle Scholar
  80. Osborne, C.P. (2008) Atmosphere, ecology and evolution: what drove the Miocene expansion of C4 grasslands? J Ecol 96: 35–45.PubMedGoogle Scholar
  81. Osborne CP and Beerling DJ (2006) Nature’s green revolution: the remarkable evolutionary rise of C4 plants. Phil Trans R Soc Lond B 361: 173–194.CrossRefGoogle Scholar
  82. Pagani M, Freeman KH and Arthur MA (1999) Late Miocene atmospheric CO2 concentrations and the expansion of C4 grasses. Science 285: 876–879.PubMedCrossRefGoogle Scholar
  83. Pagani M, Zachos J, Freeman KH, Tipple B and Boharty S (2005) Marked decline in atmospheric carbon dioxide concentrations during the Paleogene. Science 309: 600–603.PubMedCrossRefGoogle Scholar
  84. Passey BH, Cerling TE, Perkins ME, Voorhies MR, Harris JM and Tucker ST (2002) Environmental change in the Great Plains: an isotopic record from fossil horses. J Geol 110: 123–140.CrossRefGoogle Scholar
  85. Pearson PN and Palmer MR (2000) Atmospheric carbon dioxide concentrations over the past 60 million years. Nature 406: 695–699.PubMedCrossRefGoogle Scholar
  86. Piperno DR (1988) Phytolith Analysis, an Archaeological and Geological Perspective. Academic Press, San Diego.Google Scholar
  87. Prasad V, Strömberg CAE, Alimohammadian H and Sahni A (2005) Dinosaur coprolites and the early evolution of grasses and grazers. Science 310: 1177–1180.PubMedCrossRefGoogle Scholar
  88. Quade J, Cater JML, Ojha TP, Adam J and Harrison TM (1995) Dramatic carbon and oxygen isotopic shift in paleosols from Nepal and late Miocene environmental change across the northern Indian sub-continent. GSA Bull 107: 1381–1397.CrossRefGoogle Scholar
  89. Quade J and Cerling TE (1995) Stable isotopes in paleosols and the expansion of C4 grasses in the late Miocene of Northern Pakistan. Palaeogeogr Palaeoclimatol Palaeoecol 115: 91–116.CrossRefGoogle Scholar
  90. Quade J, Cerling TE and Bowman JR (1989) Development of the Asian monsoon revealed by marked ecological shift during the latest Miocene in northern Pakistan. Nature 342: 163–166.CrossRefGoogle Scholar
  91. Quade J, Solounias N and Cerling TE (1994) Stable isotopic evidence from paleosol carbonates and fossil teeth in Greece for C3 forest or woodlands over the past 11 Ma. Palaeogeogr Palaeoclim Palaeoecol 108: 41–53.CrossRefGoogle Scholar
  92. Ramstein G, Fluteau F Besse J and Joussaume S (1997) Effect of orogeny, plate motion and land-sea distribution on Eurasian climate change over the past 30 million years. Nature 386: 788–795.CrossRefGoogle Scholar
  93. Rea DK (1994) The paleoclimatic record provided by eolian deposition in the deep-sea: the geologic history of wind. Rev Geophys 32: 159–195.CrossRefGoogle Scholar
  94. Rea DK, Snoeckx H and Joseph LH (1998) Late Cenozoic eolian deposition in the North Pacific: Asian drying, Tibetan uplift, and cooling of the Northern Hemisphere. Paleoceanography 13: 215–224.CrossRefGoogle Scholar
  95. Retallack GJ (2001a) Soils of the Past. An introduction to paleopedology. Second Ed. Blackwell Science, Oxford.CrossRefGoogle Scholar
  96. Retallack GJ (2001b) Cenozoic expansion of grasslands and climatic cooling. J Geol 109: 407–426.CrossRefGoogle Scholar
  97. Riaño D, Moreno Ruiz JA, Isidoro D and Ustin SL (2007) Global spatial patterns and temporal trends of burned area between 1981 and 2000 using NOAA-NASA Pathfinder. Global Change Biol 13: 40–50.CrossRefGoogle Scholar
  98. Roalson EH (2008) C4 photosynthesis: differentiating causation and coincidence. Current Biol 18: R167–168.CrossRefGoogle Scholar
  99. Rowley DB and Currie BS (2006) Palaeo-altimetry of the late Eocene to Miocene Lunpola basin, central Tibet. Nature 439: 677–681.PubMedCrossRefGoogle Scholar
  100. Royer DL (2006) CO2-forced climate thresholds during the Phanerozoic. Geochim Cosmochim Act 70: 5665–5675.CrossRefGoogle Scholar
  101. Royer DL, Berner RA, Montañez IP, Tabor NJ and Beerling DJ (2005) CO2 as a primary driver of Phanerozoic climate. GSA Today 14: 4–10.CrossRefGoogle Scholar
  102. Royer DL, Wing SL, Beerling DJ, Jolley DW, Koch PL, Hickey LJand Berner RA (2001) Paleobotanical evidence for near present-day levels of atmospheric CO2 during part of the Tertiary. Science 292: 2310–2313.PubMedCrossRefGoogle Scholar
  103. Sage RF (2001) Environmental and evolutionary preconditions for the origin and diversification of the C4 photosynthetic syndrome. Plant Biol 3: 202–213.CrossRefGoogle Scholar
  104. Sage RF (2004) The evolution of C4 photosynthesis. New Phytol 161: 341–370.CrossRefGoogle Scholar
  105. Sage RF and Kubien DS (2003) Quo vadis C4? An ecophysiological perspective on global change and the future of C4 plants. Photosynth Res 77: 209–225.PubMedCrossRefGoogle Scholar
  106. Sankaran M, Hanan NP Scholes RJ and 27 other authors, 2005. Determinants of woody cover in African savannas. Nature 438: 846–849.Google Scholar
  107. Sankaran M, Ratnam J and Hanan N (2008) Woody cover in African savannas: the role of resources, fire and herbivory. Global Ecology and Biogeography 17: 236–245.CrossRefGoogle Scholar
  108. Scholes RJ (1992) The influence of soil fertility on the ecology of southern African dry savannas. J Biogeog 17: 415–419.CrossRefGoogle Scholar
  109. Ségalen L, Renard M, Lee-Thorp JA, Emmanuel L, Le Callonnec L, de Rafélis M, Senut B, Pickford M and Melice J-L (2006) Neogene climate change and emergence of C4 grasses in the Namib, southwestern Africa, as reflected in ratite 13C and 18O. Earth Planet Sci Lett 244: 725–734.CrossRefGoogle Scholar
  110. Sepulchre P, Ramstein G, Fluteau F, Schuster M, Tier JJ and Brunet M (2006) Tectonic uplift and eastern African aridification. Science 313: 1419–1423.PubMedCrossRefGoogle Scholar
  111. Sessions AL, Sylva SP and Hayes JM (2005) Moving-wire device for carbon isotopic analyses of nanogram quantities of nonvolatile organic carbon. Analytical Chemistry 77: 6519–6527.PubMedCrossRefGoogle Scholar
  112. Smith FA (2002) The carbon isotope signature of fossil phytoliths: the dynamics of C3 and C4 grasses in the Neogene. PhD Thesis, University of Chicago.Google Scholar
  113. Smith FA and White JWC (2004) Modern calibration of phytolith carbon isotope signature for C3/C4 paleograssland reconstruction. Palaeogeogr Palaeoclimatol Palaeoecol 207: 277–304.CrossRefGoogle Scholar
  114. Spicer RA, Harris NBW, Widdowson M, Herman AB, Guo S, Valdes PJ, Wolfe JA and Kelley SP (2003) Constant elevation of southern Tibet over the past 15 million years. Nature 421: 622–624.PubMedCrossRefGoogle Scholar
  115. Stern LA, Johnson GD and Chamberlain CP (1994) Carbon isotope signature of environmental change found in fossil ratite eggshells from a South Asian Neogene sequence. Geology 22: 419–422.CrossRefGoogle Scholar
  116. Stewart GR, Turnbull MH, Schmidt S and Erskine PD (1995) 13C natural abundance in plant communities along a rainfall gradient: a biological integrator of water availability. Aus J Plant Physiol 22: 51–55.CrossRefGoogle Scholar
  117. Strömberg CAE (2004) Using phytolith assemblages to reconstruct the origin and spread of grass-dominated habitats in the great plains of North America during the late Eocene to early Miocene. Palaeogeogr Palaeoclimatol Palaeoecol 207: 239–275.CrossRefGoogle Scholar
  118. Strömberg CAE (2005) Decoupled taxonomic radiation and ecological expansion of open-habitat grasses in the Cenozoic of North America. Proc Natl Acad Sci USA 102: 11980–11984.PubMedCrossRefGoogle Scholar
  119. Strömberg CAE (2006) Evolution of hypsodonty in equids: testing a hypothesis of adaptation. Paleobiol 32: 236–258.CrossRefGoogle Scholar
  120. Sun X and Wang P (2005) How old is the Asian monsoon system? – Palaeobotanical records from China. Palaeogeogr Palaeoclimatol Palaeoecol 222: 181–222.CrossRefGoogle Scholar
  121. Thomasson JR, Nelson ME and Zakrzewski RJ (1986) A fossil grass (Gramineae: Chloridoideae) from the Miocene with Kranz anatomy. Science 233: 876–878.PubMedCrossRefGoogle Scholar
  122. Tipple BJ and Pagani M (2007) The early origins of terrestrial C4 photosynthesis. Annu Rev Earth Planet Sci 35: 435–461.CrossRefGoogle Scholar
  123. Vicari M and Bazely DR (1993) Do grasses fight back? The case for antiherbivore defences. TREE 8: 137–141.PubMedGoogle Scholar
  124. Vicentini A, Barber JC, Aliscioni AS, Giussani AM and Kellogg EA (2008) The age of the grasses and clusters of origins of C4 photosynthesis. Global Change Biol 14: 2963–2977.CrossRefGoogle Scholar
  125. Wang P, Clemens S, Beaufort L, Braconnot P, Ganssen G, Jian Z, Kershaw P and Sarnthein M (2005) Evolution and variability of the Asian monsoon system: state of the art and outstanding issues. Quat Sci Rev 24: 595–629.CrossRefGoogle Scholar
  126. Wolfson MM and Tainton NM (1999) The morphology and physiology of the major forage plants. Grasses. Pages 54–79 in N.M. Tainton, editor, Veld management in South Africa. University of Natal Press, Pietermaritzburg, South Africa.Google Scholar
  127. Zachos J, Pagani M, Sloan L, Thomas E and Billups K (2001) Trends, rhythms, and aberrations in global climate 65 Ma to present. Science 292: 686–693.PubMedCrossRefGoogle Scholar
  128. Zazzo A, Bocherens H, Brunet M, Beauvilian A, Billiou D, Taisso Mackaye H, Vignaud P and Mariotti A (2000) Herbivore paleodiet and paleoenvironmental changes in Chad during the Pliocene using stable carbon isotope ratios of tooth enamel carbonate. Paleobiol 26: 294–309.CrossRefGoogle Scholar
  129. Zhisheng A, Kutzbach JE, Prell WL and Porter SC (2001) Evolution of Asian monsoons :and phased uplift of the Himalaya-Tibetan plateau since Late Miocene times. Nature 411: 62–66.PubMedCrossRefGoogle Scholar
  130. Zhongshi Z, Wang H Guo Z and Jiang D (2007) What triggers the transition of palaeoenvironment patterns in China, the Tibetan Plateau uplift or the Paratethys Sea retreat? Palaeogeogr Palaeoclimatol Palaeoecol 245:317–331.CrossRefGoogle Scholar

Copyright information

© Springer Netherlands 2010

Authors and Affiliations

  1. 1.Department of Animal and Plant SciencesUniversity of SheffieldSheffieldUK

Personalised recommendations