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The Neogene transition from C3 to C4 grasslands in North America: assemblage analysis of fossil phytoliths

Published online by Cambridge University Press:  08 April 2016

Caroline A. E. Strömberg  and
Francesca A. McInerney
Caroline A. E. Strömberg
Affiliation:
Department of Biology and the Burke Museum of Natural History and Culture, University of Washington, Box 351800, Seattle, Washington 98195. E-mail: caestrom@u.washington.edu
Francesca A. McInerney
Affiliation:
Department of the Geophysical Sciences, University of Chicago, 5734 South Ellis Avenue, Chicago, Illinois 60637
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Abstract

The rapid ecological expansion of grasses with C4 photosynthesis at the end of the Neogene (8–2 Ma) is well documented in the fossil record of stable carbon isotopes. As one of the most profound vegetation changes to occur in recent geologic time, it paved the way for modern tropical grassland ecosystems. Changes in CO2 levels, seasonality, aridity, herbivory, and fire regime have all been suggested as potential triggers for this broadly synchronous change, long after the evolutionary origin of the C4 pathway in grasses. To date, these hypotheses have suffered from a lack of direct evidence for floral composition and structure during this important transition. This study aimed to remedy the problem by providing the first direct, relatively continuous record of vegetation change for the Great Plains of North America for the critical interval (ca. 12–2 Ma) using plant silica (phytolith) assemblages.

Phytoliths were extracted from late Miocene-Pliocene paleosols in Nebraska and Kansas. Quantitative phytolith analysis of the 14 best-preserved assemblages indicates that habitats varied substantially in openness during the middle to late Miocene but became more uniformly open, corresponding to relatively open grassland or savanna, during the late Miocene and early Pliocene. Phytolith data also point to a marked increase of grass short cells typical of chloridoid and other potentially C4 grasses of the PACMAD clade between 8 and 5 Ma; these data suggest that the proportion of these grasses reached up to ∼50–60% of grasses, resulting in mixed C3-C4 and highly heterogeneous grassland communities by 5.5 Ma. This scenario is consistent with interpretations of isotopic records from paleosol carbonates and ungulate tooth enamel. The rise in abundance of chloridoids, which were present in the central Great Plains since the early Miocene, demonstrates that the “globally” observed lag between C4 grass evolution/taxonomic diversification and ecological expansion occurred at the regional scale. These patterns of vegetation alteration imply that environmental change during the late Miocene-Pliocene played a major role in the C3-C4 shift in the Great Plains. Specifically, the importance of chloridoids as well as a decline in the relative abundance of forest indicator taxa, including palms, point to climatic drying as a key trigger for C4 dominance.

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Articles
Information
Paleobiology , Volume 37 , Issue 1 , Winter 2011 , pp. 50 - 71
Copyright
Copyright © The Paleontological Society 

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References

Literature Cited

Alexandre, A., Meunier, J.-D., Lezine, A.-M., Vincens, A., and Schwartz, D. 1997. Phytoliths: indicators of grassland dynamics during the late Holocene in intertropical Africa. Palaeogeography, Palaeoclimatology, Palaeoecology 136:213–229.CrossRefGoogle Scholar
Barboni, D., Bremond, L., and Bonnefille, R. 2007. Comparative study of modern phytolith assemblages from inter-tropical Africa. Palaeogeography, Palaeoclimatology, Palaeoecology 246:454–470.CrossRefGoogle Scholar
Behrensmeyer, A. K., Quade, J., Ceding, T. E., Kappelman, J., Khan, I. A., Copeland, P., Roe, L., Hicks, J., Stubblefield, P., Willis, B. J., and Latorre, C. 2007. The structure and rate of late Miocene expansion of C4 plants: evidence from lateral variation in stable isotopes in paleosols of the Siwalik Group, northern Pakistan. Geological Society of America Bulletin 119:1486–1505.CrossRefGoogle Scholar
Björkman, O. 1971. Comparative photosynthetic CO2 exchange in higher plants. Pp. 18–32 in Hatch, M. D., Osmond, C. B., and Slatyer, R. O., eds. Photosynthesis and photorespiration. Wiley, New York.Google Scholar
Blinnikov, M. S. 2005. Phytoliths in plants and soils of the interior Pacific Northwest, USA. Review of Palaeobotany and Palynology 135:71–98.CrossRefGoogle Scholar
Boellstorff, J. B. 1978. Chronology of some late Cenozoic deposits from the central United States and the Ice Ages. Transactions of the Nebraska Academy of Sciences 6:35–49.Google Scholar
Bond, W. J., Woodward, F. I., and Midgley, G. F. 2005. The global distribution of ecosystems in a world without fire. New Phytologist 165:525–538.CrossRefGoogle Scholar
Bouchenak-Khelladi, Y., Salamin, N., Savolainen, V., Forest, F., van der Bank, M., Chase, M. W., and Hodkinson, T. R. 2008. Large multigene phylogenetic trees of the grasses (Poaceae): progress towards complete tribal and generic level sampling. Molecular Phylogenetics and Evolution 47:488–505.Google Scholar
Bouchenak-Khelladi, Y., Verboom, G. A., Hodkinson, T. R., Salamin, N., Francois, O., Chonghaile, G. N., and Savolainen, V. 2009. The origins and diversification of C4 grasses and savanna adapted ungulates. Global Change Biology 15:2397–2417.CrossRefGoogle Scholar
Bozarth, S. R. 1992. Classification of opal phytoliths formed in selected dicotyledons native to the Great Plains. Pp. 193–214 in Rapp, G. J. and Mulholland, S. C., eds. Phytolith systematics: emerging issues. Plenum, New York.CrossRefGoogle Scholar
Bremond, L., Alexandre, A., Hély, C., and Guiot, J. 2005a. A phytolith index as a proxy of tree cover density in tropical areas: calibration with Leaf Area Index along a forest-savanna transect in southeastern Cameroon. Global and Planetary Change 45:277–293.CrossRefGoogle Scholar
Bremond, L., Alexandre, A., Peyron, O., and Guiot, J. 2005b. Grass water stress estimated from phytoliths in West Africa. Journal of Biogeography 32:311–327.CrossRefGoogle Scholar
Brown, D. A. 1984. Prospects and limits of a phytolith key for grasses in the Central United States. Journal of Archaeological Science 11:345–368.CrossRefGoogle Scholar
Buol, S. W., Southard, R. J., Graham, R. C., and McDaniel, P. A. 2003. Soil genesis and classification 5th ed. University of Iowa Press, Ames.Google Scholar
Cabido, M., Pons, E., Cantero, J. J., Lewis, J. P., and Anton, A. 2007. Photosynthetic pathway variation among C4 grasses along a precipitation gradient in Argentina. Journal of Biogeography 35:131–140.CrossRefGoogle Scholar
Carnelli, A. L., Theurillat, J.-P., and Madella, M. 2004. Phytolith types and type-frequencies in subalpine–alpine plant species of the European Alps. Review of Palaeobotany and Palynology 129:39–65.CrossRefGoogle Scholar
Cerling, T. E., Harris, J. M., MacFadden, B. J., Leakey, M. G., Quade, J., Eisenmann, V., and Ehleringer, J. R. 1997. Global vegetation change through the Miocene/Pliocene boundary. Nature 389:153–158.CrossRefGoogle Scholar
Cerling, T. E., Ehleringer, J. R., and Harris, J. M. 1998. Carbon dioxide starvation, the development of C4 ecosystems, and mammalian evolution. Philosophical Transactions of the Royal Society of London B 353:159–171.CrossRefGoogle ScholarPubMed
Christin, P.-A., Besnard, G., Samaritani, E., Duvall, M. R., Hodkinson, T. R., Savolainen, V., and Salamin, N. 2008. Oligocene CO2 decline promoted C4 photosynthesis in grasses. Current Biology 18:37–43.Google Scholar
Clements, F. E., Weaver, J. E., and Hanson, H. C. 1929. Plant competition: an analysis of community functions. Carnegie Institution, Washington D.C. Google Scholar
Crowley, T. J., and North, G. R. 1991. Paleoclimatology. Oxford University Press, New York.Google Scholar
Damuth, J. D., Fortelius, M., Andrews, P., Badgley, C., Hadley, E. A., Hixon, S., Janis, C. M., Madden, R. H., Reed, K., Smith, J. M., Theodor, J. M., van Dam, J. A., Van Valkenburgh, B., and Werdelin, L. 2002. Reconstructing mean annual precipitation based on mammalian dental morphology and local species richness. Journal of Vertebrate Paleontology 22(Suppl. to No. 3):48A.Google Scholar
Dettman, D. L., Kohn, M. J., Quade, J., Ryerson, F. J., Ojha, T. P., and Hamidullah, S. 2001. Seasonal stable isotope evidence for a strong Asian monsoon throughout the past 10.7 m.y. Geology 29:31–34.Google Scholar
Diffendal, R. F. Jr. 1990. The Sidney Gravel and Kimball Formation, supposed parts of the Ogallala Group (Neogene), are not objectively mappable units. Pp. 23–38 in Gustavson, T. C., ed. Geologic framework and regional hydrology: Upper Cenozoic Blackwater Draw and Ogallala formations, Great Plains. Texas Bureau of Economic Geology, University of Texas, Austin.Google Scholar
Diffendal, R. F. Jr. 1995. Geology of the Ogallala-High Plains Regional Aquifer System in Nebraska. Pp. 61–75 in Diffendal, R. F. Jr. and Flowerday, C. F., eds. Geologic field trips in Nebraska and adjacent parts of Kansas and South Dakota. Conservation and Survey Division, Univerisity of Nebraska, Lincoln.Google Scholar
Diffendal, R. F. Jr., Pabian, R. K., and Thomasson, J. R. 1996. Geologic history of Ash Hollow State Historical Park, Nebraska. Conservation and Survey Division, University of Nebraska, Lincoln.Google Scholar
Dugas, D. P., and Retallack, G. J. 1993. Middle Miocene fossil grasses from Fort Ternan, Kenya. Journal of Paleontology 67:113–128.CrossRefGoogle Scholar
Duvall, M., Davis, J. I., Clark, L. G., Goldman, D. H., and Sanchez-Ken, J. G. 2007. Phylogeny of the grasses (Poaceae) revisited. Aliso 23:237–247.Google Scholar
Edwards, E. J., and Still, C. J. 2008. Climate, phylogeny, and the ecological distribution of C4 grasses. Ecology Letters 11:266–276.Google Scholar
Edwards, E. J., and Smith, S. A. 2010. Phylogenetic analyses reveal the shady history of C4 grasses. Proceedings of the National Academy of Sciences USA 107:2532–2537.Google Scholar
Edwards, E. J., Osborne, C. P., Strömberg, C. A. E., S. A. Smith, and C4 Grasses Consortium. 2010. The origins of C4 grasslands: integrating evolutionary and ecosystem science. Science 328:587–591.Google Scholar
Ehleringer, J. R. 1978. Implications of quantum yield differences on distributions of C3 and C4 grasses. Oecologia 31:255–267.CrossRefGoogle Scholar
Ehleringer, J. R., Sage, R. F., Flanagan, L. B., and Pearcy, R. W. 1991. Climate change and the evolution of C4 photosynthesis. Trends in Ecology and Evolution 6:95–99.CrossRefGoogle Scholar
Epstein, H. E., Lauenroth, W. K., Burke, I. C., and Coffin, D. P. 1997. Productivity patterns of C3 and C4 functional types in the U.S. Great Plains. Ecology 78:722–731.Google Scholar
Fortelius, M., Eronen, J. T., Jernvall, J., Liu, L., Pushkina, D., Rinne, J., Tesakov, A., Vislobokova, I. A., Zhang, Z., and Zhou, L. 2002. Fossil mammals resolve regional patterns of Eurasian climate change during 20 million years. Evolutionary Ecology Research 4:1005–1016.Google Scholar
Fortelius, M., Eronen, J., Liu, L. P., Pushkina, D., Tesakov, A., Vislobokova, I., and Zhang, Z. Q. 2003. Continental-scale hypsodonty patterns, climatic paleobiogeography and dispersal of Eurasian Neogene large mammal herbivores. in Reumer, J. W. F. and Wessels, W., eds. Distribution and migration of Tertiary mammals in Eurasia. A volume in honour of Hans de Bruijn. Deinsea 10:1–11.Google Scholar
Fox, D. L., and Koch, P. L. 2003. Tertiary history of C4 biomass in the Great Plains, USA. Geology 31:809–812.CrossRefGoogle Scholar
Fox, D. L. 2004. Carbon and oxygen isotope variability in Neogene paleosol carbonates: constraints on the evolution of the C4-grasslands of the Great Plains, USA. Palaeogeography, Palaeoclimatology, Palaeoecology 207:305–329.Google Scholar
Fredlund, G. G., and Tieszen, L. L. 1994. Modern phytolith assemblages from the North American Great Plains. Journal of Biogeography 21:321–335.CrossRefGoogle Scholar
Fredlund, G. G. 1997. Calibrating grass phytolith assemblages in climatic terms: application to late Pleistocene assemblages from Kansas and Nebraska. Palaeogeography, Palaeoclimatology, Palaeoecology 136:199–211.CrossRefGoogle Scholar
Gardner, L. R., Diffendal, R. F. Jr., and Williams, D. F. 1992. Stable isotope composition of calcareous paleosols and ground-water cements from the Ogallala Group (Neogene), western Nebraska. Contributions to Geology, University of Wyoming 29:97–109.Google Scholar
Gibson, D. J. 2009. Grasses and grassland ecology. Oxford University Press, Oxford.Google Scholar
GPWG (Grass Phylogeny Working Group). 2001. Phylogeny and subfamilial classification of the grasses (Poaceae). Annals of the Missouri Botanical Garden 88:373–457.Google Scholar
Hartley, W. 1973. Studies on the origin, evolution, and distribution of the Gramineae. V. The subfamily Festucoideae. Australian Journal of Botany 21:201–234.Google Scholar
Hattersley, P. W. 1983. The distribution of C3-grass and C4-grasses in Australia in relation to climate. Oecologia 57:113–128.Google Scholar
Hattersley, P. W., and Watson, L. 1992. Diversification of photosynthesis. Pp. 38–11 in Chapman, G. P., ed. Grass evolution and domestication. Cambridge University Press, Cambridge.Google Scholar
Herring, J. R. 1985. Charcoal fluxes into sediments of the North Pacific Ocean: the Cenozoic record of burning. Pp. 419–442 in Sundquist, E. T. and Broecker, W. S., eds. The carbon cycle and atmospheric CO2: natural variations Archean to present. American Geophysical Union, Washington, D.C. Google Scholar
Huang, Y., Clemens, S. C., Wang, Y., and Prell, W. L. 2007. Large-scale hydrological change drove the late Miocene C4 plant expansion in the Himalayan foreland and Arabian Peninsula. Geology 35:531–534.CrossRefGoogle Scholar
Hutchison, J. H. 1982. Turtle, crocodilian and champsosaur diversity changes in the Cenozoic of the north-central region of western United States. Palaeogeography, Palaeoclimatology, Palaeoecology 37:149–164.Google Scholar
ICPN Working Group (Madella, M., Alexandre, A., and Ball, T. B.) 2005. International code for phytolith nomenclature 1.0. Annals of Botany 96:253–260.CrossRefGoogle ScholarPubMed
Jacobs, B. F., Kingston, J. D., and Jacobs, L. L. 1999. The origin of grass-dominated ecosystems. Annals of the Missouri Botanical Garden 86:590–643.CrossRefGoogle Scholar
Janis, C. M. 1993. Tertiary mammal evolution in the context of changing climates, vegetation, and tectonic events. Annual Review of Ecology and Systematics 24:467–500.Google Scholar
Janis, C. M., Scott, K. M., and Jacobs, L. L. 1998. Evolution of Tertiary mammals in North America. 1. Terrestrial carnivores, ungulates and ungulatelike mammals. Cambridge University Press, Cambridge.Google Scholar
Janis, C. M., Damuth, J., and Theodor, J. M. 2000. Miocene ungulates and terrestrial primary productivity: where have all the browsers gone? Proceedings of the National Academy of Sciences USA 97:237–261.Google Scholar
Janis, C. M. 2002. The origins and evolution of the North American grassland biome: the story from the hoofed mammals. Palaeogeography, Palaeoclimatology, Palaeoecology 177:183–198.Google Scholar
Janis, C. M. 2004. The species richness of Miocene browsers, and implications for habitat type and primary productivity in the North American grassland biome. Palaeogeography, Palaeoclimatology, Palaeoecology 207:371–398.Google Scholar
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.Google Scholar
Kealhofer, L. 1996. The human environment during the terminal Pleistocene and Holocene in northeastern Thailand: phytolith evidence from Lake Kumphawapi. Asian Perspectives 35:229–254.Google Scholar
Kealhofer, L., and Piperno, D. 1998. Opal phytoliths in Southeastern Asian Flora. Smithsonian Contributions to Botany 88:1–39.CrossRefGoogle Scholar
Keeley, J. E., and Rundel, P. W. 2003. Evolution of CAM and C4 carbon-concentrating mechanisms. International Journal of Plant Sciences 164(3 Suppl.):S55–S77.Google Scholar
Keeley, J. E. 2005. Fire and the Miocene expansion of C4 grasslands. Ecology Letters 8:683–690.Google Scholar
Kelly, E. F. 1989. A study of the influence of climate and vegetation on the stable isotope chemistry of soils in grassland ecosystems of the Great Plains. Ph.D dissertation. University of California, Berkeley.Google Scholar
Kennett, J. P. 1995. A review of polar climatic evolution during the Neogene, based on the marine sediment record. Pp. 49–64 in Vrba, E. S., Denton, G. H., Partridge, T. C., and Burckle, L. H., eds. Paleoclimate and evolution, with emphasis on human origins. Yale University Press, New Haven, Conn. Google Scholar
Kingston, J. D., Marino, B. D., and Hill, A. 1994. Isotopic evidence for Neogene Hominid paleoenvironments in the Kenya Rift Valley. Science 264:955–959.Google Scholar
Kondo, R., Childs, C., and Atkinson, I. 1994. Opal phytoliths of New Zealand. Manaaki Whenua, Canterbury, New Zealand. Google Scholar
Kucera, C. L. 1981. Grasslands and fire. Pp. 90–111 in Mooney, H. A., Bonnicksen, T. M., Christensen, N. L., Lotan, J. E., and Reiners, W. A., eds. Fire regimes and ecosystem properties. U.S. Department of Agriculture, Forest Service, Washington, D.C. Google Scholar
Kürschner, W. M. 1997. The anatomical diversity of recent and fossil leaves of the durmast oak (Quercus petraea Lieblein/Q. pseudocastanea Goeppert)—implications for their use as biosensors of palaeoatmospheric CO2 levels. Palaeogeography, Palaeoclimatology, Palaeoecology 96:1–30.Google Scholar
Kürschner, W. M., Kvaček, Z., and Dilcher, D. 2008. The impact of Miocene atmospheric carbon dioxide fluctuations on climate and the evolution of terrestrial ecosystems. Proceedings of the National Academy of Sciences USA 105:449–453.Google Scholar
Levin, N. E. 2004. Isotopic evidence for Plio-Pleistocene environmental change at Gona, Ethiopia. Earth and Planetary Science Letters 219:93–110.CrossRefGoogle Scholar
MacFadden, B. J., Ceding, T. E., and Prado, J. 1996. Cenozoic terrestrial ecosystem evolution in Argentina: evidence from carbon isotopes of fossil mammal teeth. Palaios 11:319–327.Google Scholar
Madella, M., Jones, M. K., Echlin, P., Powers-Jones, A., and Moore, M. 2009. Plant water availability and analytical microscopy of phytoliths: Implications for ancient irrigation in arid zones. Quaternary International 193:32–40.Google Scholar
Martin, R. A., Honey, J. G., Peláez-Campomanes, P., Goodwin, H. T., Baskin, J. A., and Zakrzewski, R. J. 2002. Blancan lagomorphs and rodents of the Deer Park assemblages, Meade County, Kansas. Journal of Paleontology 76:1072–1090.Google Scholar
Martin, R. A., Peláez-Campomanes, P., Honey, J. G., Fox, D. L., Zakrzewski, R. J., Albright, L. B., Lindsay, E. H., Opdyke, N. D., and Goodwin, H. T. 2008. Rodent community change at the Pliocene-Pleistocene transition in southwestern Kansas and identification of the Microtus immigration event on the Central Great Plains. Palaeogeography, Palaeoclimatology, Palaeoecology 267:196–207.Google Scholar
McClaran, M. P., and Umlauf, M. 2000. Desert grassland dynamics estimated from carbon isotopes in grass phytoliths and soil organic matter. Journal of Vegetation Science 11:71–76.Google Scholar
McInerney, F. A., Strömberg, C. A. E., and White, J. W. C. 2011. The Neogene transition from C3 to C4 grasslands in North America: stable carbon isotope ratios of fossil phytoliths. Paleobiology 37:23–49 (this volume).CrossRefGoogle Scholar
Morgan, M. E., Kingston, J. D., and Marino, B. D. 1994. Carbon isotopic evidence for the emergence of C4 plants in the Neogene from Pakistan and Kenya. Nature 367:162–165.Google Scholar
Morley, R. J., and Richards, K. 1993. Gramineae cuticle: a key indicator of Late Cenozoic climatic change in the Niger Delta. Review of Palaeobotany and Palynology 77:119–127.Google Scholar
Mulholland, S. C. 1989. Phytolith shape frequencies in North Dakota grasses: a comparison to general patterns. Journal of Archaeological Science 16:489–511.Google Scholar
Nambudiri, E. M. V., Tidwell, W. D., Smith, B. N., and Hebbert, N. P. 1978. A C4 plant from the Pliocene. Nature 276:816–817.CrossRefGoogle Scholar
Nelson, D. M., Hu, F. S., Mikucki, J., Tian, J., and Pearson, A. 2007. Carbon isotopic analysis of individual pollen grains from C3 and C4 grasses using a spooling wire microcombustion interface. Geochimica et Cosmochimica Acta 71:4005–4014.Google Scholar
Osborne, C. P. 2008. Atmosphere, ecology and evolution: what drove the Miocene expansion of C4 grasslands? Journal of Ecology 96:35–45.Google Scholar
Osborne, C. P., and Beerling, D. J. 2006. Nature's green revolution: the remarkable evolutionary rise of C4 plants. Philosophical Transactions of the Royal Society of London B 361:173–194.Google Scholar
Pagani, M., Freeman, K. H., and Arthur, M. A. 1999. Late Miocene atmospheric CO2 concentrations and the expansion of C4 grasses. Science 285:876–879.Google Scholar
Parry, D. W., and Smithson, F. 1966. Opal silica in the inflorescences of some British grasses and cereals. Annals of Botany 30:525–538.Google Scholar
Paruelo, J. M., Jobbágy, E. G., Sala, O. E., Lauenroth, W. K., and Burke, I. C. 1998. Functional and structural convergence of temperate grassland and shrubland ecosystems. Ecological Applications 8:194–206.CrossRefGoogle Scholar
Paruelo, J. M., and Lauenroth, W. K. 1996. Relative abundance of plant functional types in grasslands and shrublands of North America. Ecological Applications 6:1212–1224.CrossRefGoogle Scholar
Passey, B. H., Cerling, T. E., Perkins, M. E., Voorhies, M. R., Harris, J. M., and Tucker, S. T. 2002. Environmental change in the Great Plains: an isotopic record from fossil horses. Journal of Geology 110:123–140.Google Scholar
Passey, B. H., Ayliffe, L. K., Kaakinen, A., Eronen, J. T., Zhang, Z. Q., Cerling, T. E., and Fortelius, M. 2009. Strengthened East Asian summer monsoons during a period of high-latitude warmth? Isotopic evidence from Mio-Pliocene fossil mammals and soil carbonates from northern China. Earth and Planetary Science Letters 277:443–452.Google Scholar
Pearson, P. N., and Palmer, M. R. 1999. Middle Eocene seawater pH and atmospheric carbon dioxide concentrations. Science 284:1824–1826.Google Scholar
Piperno, D. R. 1988. Phytolith analysis, an archaeological and geological perspective. Academic Press, San Diego.Google Scholar
Piperno, D. R. 1993. Phytolith and charcoal records from deep lake cores in the American tropics. Pp. 58–71 in Pearsall, D. M. and Piperno, D. R., eds. Current research in phytolith analysis: applications in archaeology and paleoecology. University Museum of Archaeology and Anthropology, University of Pennsylvania, Philadelphia.Google Scholar
Piperno, D. R. 2006. Phytoliths: a comprehensive guide for archaeolo gists and paleoecologists. AltaMira, New York.Google Scholar
Piperno, D. R., and Pearsall, D. M. 1998. The silica bodies of tropical American grasses: morphology, taxonomy, and implications for grass systematics and fossil phytolith identification. Smithsonian Contributions to Botany 85:1–40.CrossRefGoogle Scholar
Postek, M. T. 1981. The occurrence of silica in the leaves of Magnolia grandiflora L. Botanical Gazette 142:124–134.Google Scholar
Prasad, V., Strömberg, C. A. E., Alimohammadian, H., and Sahni, A. 2005. Dinosaur coprolites and the early evolution of grasses and grazers. Science 310:1177–1180.Google Scholar
Punyasena, S. W., Eshel, G., and McElwain, J. C. 2008. The influence of climate on the spatial patterning of Neotropical plant families. Journal of Biogeography 35:117–130.CrossRefGoogle Scholar
Quade, J., and Cerling, T. E. 1995. Expansion of C4 grasses in the late Miocene of northern Pakistan: Evidence from stable isotopes in paleosols. Palaeogeography, Palaeoclimatology, Palaeoecology 115:91–116.Google Scholar
Quade, J., Ceding, T. E., and Bowman, J. R. 1989. Development of Asian monsoon revealed by marked ecological shift during the latest Miocene in northern Pakistan. Nature 342:163–164.CrossRefGoogle Scholar
Retallack, G. J. 1983. Late Eocene and Oligocene paleosols from Badlands National Park, South Dakota. Geological Society of America Special Paper 193:1–82.Google Scholar
Retallack, G. J. 1997. Neogene expansion of the North American prairie. Palaios 12:380–390.Google Scholar
Retallack, G. J. 2001. Cenozoic expansion of grasslands and climatic cooling. Journal of Geology 109:407–426.Google Scholar
Retallack, G. J. 2007. Cenozoic paleoclimate on land in North America. Journal of Geology 115:271–294.Google Scholar
Royer, D. L. 2006. CO2-forced climate thresholds during the Phanerozoic. Geochimica Cosmochimica Acta 70:5665–5675.Google Scholar
Royer, D. L., Osborne, C. P., and Beerling, D. J. 2002. High CO2 increases the freezing sensitivity of plants: Implications for paleoclimatic reconstructions from fossil floras. Geology 30:963–966.Google Scholar
Runge, F. 1996. Opal Phytolithe in Pflantzen aus dem humiden und semi-ariden Osten Afrikas und ihre Bedeutung fur die Klima- und Vegetationsgeschichte. Botanische Jahrbuch Syst. 118:303–363.Google Scholar
Runge, F. 2001. Evidence for land use history by opal phytolith analysis: examples from the central African tropics (eastern Kivu, Congo, D. R.). Pp. 73–85 in Meunier, J. D. and Colin, F., eds. Phytoliths: applications in Earth sciences and human history. A.A. Balkema Publishers, Lisse, Netherlands.Google Scholar
Sage, R. F. 2004. The evolution of C4 photosynthesis. New Phytologist 161:341–370.Google Scholar
Sakai, A., and Larcher, W. 1987. Frost survival of plants: Responses and adaptation to freezing stress. Springer, Berlin.Google Scholar
Sánchez-Ken, J. G., Clark, L. G., Kellogg, E. A., and Kay, E. E. 2007. Reinstatement and emendation of subfamily Micrairoideae (Poaceae). Systematic Botany 32:71–80.Google Scholar
Sankaran, M., Hanan, N. P., Scholes, R. J., Ratnam, J., Augustine, D. J., Cade, B. S., Gignoux, J., Higgins, S. I., Le Roux, X., Ludwig, F., Ardo, A., Banyikwa, F., Bronn, A., Bucini, G., Caylor, K. K., Coughenour, M. B., Diouf, A., Ekaya, W., Feral, C. J., February, E. C., Frost, P. G. H., Hiernaux, P., Hrabar, H., Metzger, K. L., Prins, H. H. T., Ringrose, S., Sea, W., Tews, J., Worden, J., and Zambatis, N. 2005. Determinants of woody cover in African savannas. Nature 438:846–849.Google Scholar
Sankaran, M., Ratnam, J., and Hanan, N. 2007. Woody cover in African savannas: the role of resources, fire and herbivory. Global Ecology and Biogeography 2007:1–10.Google Scholar
Ségalen, L., Lee-Thorp, J. A., and Cerling, T. E. 2007. Timing of C4 grass expansion across sub-Saharan Africa. Journal of Human Evolution 53:549–559.Google Scholar
Sepulchre, P., Ramstein, G., Fluteau, F., Schuster, M., Tier, J. J., and Brunet, M. 2006. Tectonic uplift and eastern African aridification. Science 313:1419–1423.Google Scholar
Simon, J. L. 1997. Resampling: the new statistics. Duxbury, Belmont, Calif. Google Scholar
Skinner, M. F., and Hibbard, C. W. 1972. Early Pleistocene pre-glacial and glacial rocks and faunas of North-Central Nebraska. Bulletin of the American Museum of Natural History 148:1–148.Google Scholar
Still, C. J., Berry, J. A., Collatz, G. J., and DeFries, R. S. 2003. Global distribution of C3 and C4 vegetation: carbon cycle implications. Global Biogeochemical Cycles 17:1–6.Google Scholar
Strömberg, C. A. E. 2002. The origin and spread of grass-dominated ecosystems in the Late Tertiary of North America: preliminary results concerning the evolution of hypsodonty. Palaeogeography, Palaeoclimatology, Palaeoecology 177:59–75.Google Scholar
Strömberg, C. A. E. 2003. The origin and spread of grass-dominated ecosystems during the Tertiary of North America and how it relates to the evolution of hypsodonty in equids. Ph.D. dissertation. University of California, Berkeley.Google Scholar
Strömberg, C. A. E. 2004. Using phytolith assemblages to reconstruct the origin and spread of grass-dominated habitats in the Great Plains during the late Eocene to early Miocene. Palaeogeography, Palaeoclimatology, Palaeoecology 207:239–275.Google Scholar
Strömberg, C. A. E. 2005. Decoupled taxonomic radiation and ecological expansion of open-habitat grasses in the Cenozoic of North America. Proceedings of the National Academy of Sciences USA 102:11980–11984.Google Scholar
Strömberg, C. A. E. 2006. The evolution of hypsodonty in equids: testing a hypothesis of adaptation. Paleobiology 32:236–258.Google Scholar
Strömberg, C. A. E. 2009. Methodological concerns for analysis of phytolith assemblages: does count size matter? Quaternary International 193:124–140.CrossRefGoogle Scholar
Strömberg, C. A. E., Werdelin, L., Friis, E. M., and Saraç, G. 2007. The spread of grass-dominated habitats in Turkey and surrounding areas during the Cenozoic: phytolith evidence. Palaeogeography, Palaeoclimatology, Palaeoecology 250:18–49.Google Scholar
Taub, D. R. 2001. Climate and the U.S. distribution of C4 grass subfamilies and decarboxylation variants of C4 photosynthesis. American Journal of Botany 87:1211–1215.Google Scholar
Thomasson, J. R. 1979. Late Cenozoic grasses and other Angiosperms from Kansas, Nebraska and Colorado: biostratigraphy and relationships to living taxa. Kansas Geological Survey Bulletin 218:1–68.Google Scholar
Thomasson, J. R. 1984. Miocene grass (Gramineae: Arundinoideae) leaves showing external micromorphological and internal anatomical features. Botanical Gazette 145:204–209.Google Scholar
Thomasson, J. R. 1985. Miocene fossil grasses: possible adaptation in reproductive bracts (lemma and palea). Annals of the Missouri Botanical Garden 72:843–851.Google Scholar
Thomasson, J. R. 1987. Fossil grasses: 1820–1986 and beyond. Pp. 159–167 in Soderstrom, T. R., Hilu, K. W., Campbell, C. S., and Barkworth, M. E., eds. Grass systematics and evolution. Smithsonian Institution Press, Washington, D.C. Google Scholar
Thomasson, J. R. 1990. Fossil plants from the Late Miocene Ogallala Formation of central North America: possible paleoenvironmental and biostratigraphic significance. Pp. 99–114 in Gustavson, T. C., ed. Geologic framework and regional hydrology: Upper Cenozoic Blackwater Draw and Ogallala Formations, Great Plains. Bureau of Economic Geology. University of Texas at Austin, Austin.Google Scholar
Thomasson, J. R., Nelson, M. E., and Zakrzewski, R. J. 1986. A fossil grass (Gramineae; Chloridoideae) from the Miocene with Kranz anatomy. Science 233:876–878.Google Scholar
Thompson, R. S. 1991. Pliocene environments and climates in the western United States. Quaternary Science Reviews 10:115–132.Google Scholar
Thorn, V. C. 2004. Phytoliths from subantarctic Campbell Island: plant production and soil surface spectra. Review of Paleobotany and Palynology 132:37–59.Google Scholar
Tidwell, W. D., and Nambudiri, E. M. V. 1989. Thomlinsonia thomassonii, gen, et sp. nov., a permineralized grass from the upper Miocene Ricardo Formation, California. Review of Palaeobotany and Palynology 60:165–177.Google Scholar
Tieszen, L. L., Reed, B. C., Bliss, N. B., Wylie, B. K., and DeJong, D. D. 1997. NDVI, C3 and C4 production, and distributions in Great Plains grassland land cover classes. Ecological Applications 7:59–78.Google Scholar
Tipple, B. J., and Pagani, M. 2007. The early origins of terrestrial C4 photosynthesis. Annual Review of Ecology, Evolution and Systematics 35:435–461.Google Scholar
Tripati, A. K., Roberts, C. D., and Eagle, R. A. 2009. Coupling of CO2 and ice sheet stability over major climate transitions of the last 20 million years. Science 326:1394–1397.Google Scholar
Twiss, P. C., Suess, E., and Smith, R. M. 1969. Morphological classification of grass phytoliths. Soil Science Society of America, Proceedings 33:109–115.Google Scholar
Vicentini, A., Barber, J. C., Aliscioni, S. S., Giussani, L. M., and Kellogg, E. A. 2008. The age of the grasses and clusters of origins of C4 photosynthesis. Global Change Biology 14:2963–2977.CrossRefGoogle Scholar
Voorhies, M. R. 1977. Fossil Moles of late Hemphillian age from northeastern Nebraska. Transactions of the Nebraska Academy of Sciences 4:129–137.Google Scholar
Voorhies, M. R. 1990. Vertebrate biostratigraphy of the Ogallala Group in Nebraska. Pp. 115–151 in Gustavson, T. C., ed. Geologic framework and regional hydrology: Uppor Cenozoic Blackwater Draw and Ogallala Formations, Great Plains. Bureau of Economic Geology, University of Texas, Austin.Google Scholar
Vrba, E. S. 1993. Mammal Evolution in the African Neogene and a new look at the Great American Interchange. Pp. 393–432 in Goldblatt, P., ed. Biological relationships between Africa and South America. Yale Univeristy Press, New Haven, Conn. Google Scholar
Wallis, L. A. 2003. An overview of leaf phytolith production patterns in selected northwest Australian flora. Review of Palaeobotany and Palynology 125:201–248.Google Scholar
Wang, Y., Cerling, T. E., MacFadden, B. J., and Bryant, J. D. 1994. Fossil horses and carbon isotopes: new evidence for Cenozoic dietary, habitat, and ecosystem changes in North America. Palaeogeography, Palaeoclimatology, Palaeoecology 107:269–280.Google Scholar
Watson, L., and Dallwitz, M. J. 1992 onward. Grass genera of the world: descriptions, illustrations, identification, and information retrieval; including synonyms, morphology, anatomy, physiology, phytochemistry, cytology, classification, pathogens, world and local distribution, and references. http://delta-intkey.com/.Google Scholar
Webb, T. III, Crowley, T. J., Frenzel, B., Gliemeroth, A.-K., Jouzel, J., Labeyrie, L., Prentice, I. C., Rind, D., Ruddiman, W. F., Sarnthein, M., and Zwick, A. 1993. Group report: paleoclimate data as analogs for understanding future global changes. Pp. 51–71 in Eddy, J. A. and Oeschger, H., eds. Global changes in the perspective of the past. Wiley, New York.Google Scholar
Wing, S. L., and Greenwood, D. R. 1995. Eocene continental climates and latitudinal temperature gradients. Geology 23:1044–1048.Google Scholar
Woodburne, M. O., ed. 2004. Late Cretaceous and Cenozoic mammals of North America: biostratigraphy and geochronology. Columbia University Press, New York.Google Scholar
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.Google Scholar
Zubakov, V. A., and Borzenkova, I. I. 1988. Pliocene paleoclimates: past climates as possible analogs of mid-twenty-first century climate. Palaeogeography, Palaeoclimatology, Palaeoecology 65:35–49.Google Scholar
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