Hostname: page-component-586b7cd67f-t8hqh Total loading time: 0 Render date: 2024-11-27T11:15:53.406Z Has data issue: false hasContentIssue false
  • English
  • Français

The Neogene transition from C3 to C4 grasslands in North America: stable carbon isotope ratios of fossil phytoliths

Published online by Cambridge University Press:  08 April 2016

Francesca A. McInerney ,
Caroline A. E. Strömberg  and
James W. C. White
Francesca A. McInerney
Affiliation:
Department of the Geophysical Sciences, University of Chicago, 5734 South Ellis Avenue, Chicago, Illinois 60637
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: [email protected]
James W. C. White
Affiliation:
Institute for Arctic and Alpine Research, University of Colorado at Boulder, Campus Box 450, Boulder, Colorado 80309-0450
Get access Rights & Permissions [Opens in a new window]

Abstract

C4 grasses form the foundation of warm-climate grasslands and savannas and provide important food crops such as corn, but their Neogene rise to dominance is still not fully understood. Carbon isotope ratios of tooth enamel, soil carbonate, carbonate cements, and plant lipids indicate a late Miocene-Pliocene (8–2 Ma) transition from C3 vegetation to dominantly C4 grasses at many sites around the world. However, these isotopic proxies cannot identify whether the C4 grasses replaced woody vegetation (trees and shrubs) or C3 grasses. Here we propose a method for reconstructing the carbon isotope ratio of Neogene grasses using the carbon isotope ratio of organic matter trapped in plant silica bodies (phytoliths). Although a wide range of plants produce phytoliths, we hypothesize that in grass-dominated ecosystems the majority of phytoliths will be derived from grasses, and will yield a grass carbon isotope signature. Phytolith extracts can be contaminated by non-phytolith silica (e.g., volcanic ash). To test the feasibility of the method given these potential problems, we examined sample purity (phytolith versus non-phytolith silica), abundance of grass versus non-grass phytoliths, and carbon isotope ratios of phytolith extracts from late Miocene-Pliocene paleosols of the central Great Plains. Isotope results from the purest samples are compared with phytolith assemblage analysis of these same extracts. The dual record spans the interval of focus (ca. 12–2 Ma), allowing us, for the first time, to investigate how isotopic shifts correlate with floral change.

We found that many samples contained high abundances of non-biogenic silica; therefore, only a small subset of “pure” samples (>50% of phytoliths by volume) with good preservation were considered to provide reliable carbon isotope ratios. All phytolith assemblages contained high proportions (on average 85%) of grass phytoliths, supporting our hypothesis for grass-dominated communities. Therefore, the carbon isotope ratio of pure, well-preserved samples that are dominated by grass biosilica is considered a reliable measure of the proportion of C3 and C4 grasses in the Neogene.

The carbon isotope ratios of the pure fossil phytolith samples indicate a transition from predominantly C3 grasses to mixed C3-C4 grasses by 5.5 Ma and then a shift to more than 80% C4 grasses by 3–2 Ma. With the exception of the Pliocene sample, these isotopic data are broadly concordant with phytolith assemblages that show a general increase in C4 grasses in the late Miocene. However, phytolith assemblage analysis indicates lower relative abundance of C4 grasses in overall vegetation than do the carbon isotopes from the same phytolith assemblages. The discrepancy may relate to either (1) incomplete identification of (C4) PACMAD phytoliths, (2) higher production of non-diagnostic phytoliths in C4 grasses compared to C3 grasses, or (3) biases in the isotope record toward grasses rather than overall vegetation. The impact of potential incomplete characterization of (C4) PACMAD phytoliths on assemblage estimates of proportion of C4, though important, cannot reconcile discrepancies between the methods. We explore hypothesis (2) by analyzing a previously published data set of silica content in grasses and a small data set of modern grass leaf assemblage composition using analysis of variance, independent contrasts, and sign tests. These tests suggest that C4 grasses do not have more silica than C3 grasses; there is also no difference with regard to production of non-diagnostic phytoliths. Thus, it is most likely that the discrepancy between phytolith assemblages and isotope ratios is a consequence of hypothesis (3), that the isotope signature is influenced by the contribution of non-diagnostic grass phytoliths, whereas the assemblage composition is not. Assemblage-based estimates of % C4 within grasses, rather than overall vegetation, are in considerably better agreement with the isotope-based estimates. These results support the idea that, in grass-dominated assemblages, the phytolith carbon isotope method predominantly records shifts in dominant photosynthetic pathways among grasses, whereas phytolith assemblage analysis detects changes in overall vegetation. Carbon isotope ratios of fossil phytoliths in conjunction with phytolith assemblage analysis suggest that the late Neogene expansion of C4 grasses was largely at the expense of C3 grasses rather than C3 shrubs/trees. Stable isotopic analysis of phytoliths can therefore provide unique information about grass community changes during the Neogene, as well as help test how grass phytolith morphology relates to photosynthetic pathway.

Type
Articles
Information
Paleobiology , Volume 37 , Issue 1 , Winter 2011 , pp. 23 - 49
Copyright
Copyright © The Paleontological Society 

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

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
Baker, R. G., Fredlund, G. G., Mandel, R. D., and Bettis, E. A. III. 2000. Holocene environments of the central Great Plains: multi-proxy evidence from alluvial sequences, southeastern Nebraska. Quaternary International 67:75–88.Google Scholar
Barboni, D., Bonnefille, R., Alexandre, A., and Meunier, J.-D. 1999. Phytoliths as paleoenvironmental indicators, West Side Middle Awash Valley, Ethiopia. Palaeogeography, Palaeoclimatology, Palaeoecology 152:87–100.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.Google Scholar
Bates, C. D., Coxon, P., and Gibbard, P. L. 1978. A new method for the preparation of clay-rich sediment samples for palynological investigation. New Phytologist 81:459–463.CrossRefGoogle Scholar
Blackman, E., and Parry, D. W. 1968. Opaline silica deposition in rye (Secale cereale L.). Annals of Botany 32:199–206.Google Scholar
Blinnikov, M. S., Busacca, A., and Whitlock, C. 2002. Reconstruction of the Late Pleistocene grassland of the Columbia basin, Washington, U.S.A., based on phytolith records in loess. Palaeogeography, Palaeoclimatology, Palaeoecology 177:77–101.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
Boutton, T. W., Harrison, A. T., and Smith, B. N. 1980. Distribution of biomass of species differing in photosynthetic pathway along altitudinal transects in southeastern Wyoming grassland. Oecologia 45:287–298.CrossRefGoogle ScholarPubMed
Boyd, W. E., Lentfer, C. J., and Torrence, R. 1998. Phytolith analysis for a wet tropics environment: methodological issues and implications for the archaeology of Garua Island, West New Britain, Papa New Guinea. Palynology 22:213–228.Google 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.Google Scholar
Bremond, L. 2008a. Definition of grassland biomes from phytoliths in West Africa. Journal of Biogeography 35:2039–2048.Google Scholar
Bremond, L., Alexandre, A., Wooller, M. J., Hély, C., Williamson, D., Schäfer, P. A., Majule, A., and Guiot, J. 2008b. Phytolith indices as proxies of grass subfamilies on East African tropical mountains. Global and Planetary Change 61:209–224.CrossRefGoogle Scholar
Broadley, M. R., Willey, N. J., Wilkins, J. C., Baker, A. J. M., Mead, A., and White, P. J. 2001. Phylogenetic variation in heavy metal accumulation in angiosperms. New Phytologist 152:9–27.Google Scholar
Broadley, M. R., Bowen, H. C., Cotterill, H. L., Hammond, J. P., Meacham, M. C., Mead, A., and White, P. J. 2003. Variation in the shoot calcium content of angiosperms. Journal of Experimental Botany 54:1431–1446.Google 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.Google Scholar
Cerling, T. E., Wang, Y., and Quade, J. 1993. Expansion of C4 ecosystems as an indicator of global ecological change in the late Miocene. Nature 361:344–345.Google 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.Google Scholar
Chadwick, O. A., Hendricks, D. M., and Nettleton, W. D. 1989. Division S-5-Soil genesis, morphology, and classification: Silicification of Holocene soils in northern Monitor Valley, Nevada. Soil Science Society of America Journal 53:158–164.Google Scholar
Chazdon, R. L. 1978. Ecological aspects of the distribution of C4 grasses in selected habitats of Costa Rica. Biotropica 10:265–269.CrossRefGoogle Scholar
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
Delhon, C., Alexandre, A., Berger, J.-F., Thiébault, S., Brochier, J.-L., and Meunier, J.-D. 2003. Phytolith assemblages as a promising tool for reconstructing Mediterranean Holocene vegetation. Quaternary Research 59:48–60.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
Dorweiler, J. E., and Doebley, J. 1997. Developmental analysis of Teosinte Glume Architecture1: a key locus in the evolution of maize (Poaceae). American Journal of Botany 84:1313–1322.CrossRefGoogle ScholarPubMed
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 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., C. P. Osborne, C. A. E. Strömberg, 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., Buchmann, N., and Flanagan, L. B. 2000. Carbon isotope ratios in belowground carbon cycle processes. Ecological Applications 10:412–422.Google Scholar
Epstein, E. 1999. Silicon. Annual Review of Plant Physiology and Plant Molecular Biology 50:641–664.Google 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
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
Freckleton, R. P., Harvey, P. H., and Pagel, M. 2002. Phylogenetic analysis and comparative data: a test and review of the evidence. American Naturalist 160:712–726.Google Scholar
Fredlund, G. G. 1993. Paleoenvironmental interpretations of stable carbon, hydrogen, and oxygen isotopes from opal phytoliths, Eustis Ash Pit, Nebraska. Pp. 37–46 in Pearsall, and Piperno, 1993.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.Google Scholar
Fredlund, G. G. 1997a. Calibrating grass phytolith assemblages in climatic terms: application to late Pleistocene assemblages from Kansas and Nebraska. Palaeogeography, Palaeoclimatology, Palaeoecology 136:199–211.CrossRefGoogle Scholar
Fredlund, G. G. 1997b. Phytolith and carbon evidence for Late Quaternary vegetation and climate change in the Southern Black Hills, South Dakota. Quaternary Research 47:206–217.Google Scholar
Freeman, K. H., and Colarusso, L. A. 2001. Molecular and isotopic records of C4 grassland expansion in the late Miocene. Geochimica et Cosmochimica Acta 65:1439–1454.Google Scholar
Gibson, D. J. 2009. Grasses and grassland ecology. Oxford University Press, New York.Google Scholar
GPWG. 2001. Phylogeny and subfamilial classification of the grasses (Poaceae). Annals of the Missouri Botanical Garden 88:373–457.Google Scholar
Hattersley, P. W. 1983. The distribution of C3 and C4 grasses in Australia in relation to climate. Oecologia 57:113–128.Google Scholar
Hodson, M. J., White, P. J., Mead, A., and Broadley, M. R. 2005. Phylogenetic variation in the silicon composition of plants. Annals of Botany 96:1027–1046.Google Scholar
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.Google 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
Jones, L. H. P., and Handreck, K. A. 1965. Studies of silica in the oat plant. 3. Uptake of silica from soils by the plant. Plant Soil 23:79–95.Google Scholar
Katz, O., Cabanes, D., Weiner, S., Maeir, A. M., Boaretto, E., and Shahack-Gross, R. 2010. Rapid phytolith extraction for analysis of phytolith concentrations and assemblages during an excavation: an application at Tell es-Safi/Gath, Israel. Journal of Archaeological Science 37:1557–1563.Google Scholar
Kaufman, P. B., Dayanandan, P., and Franklin, C. I. 1985. Structure and function of silica bodies in the epidermal system of grass bodies. Annals of Botany 55:487–507.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
Kelly, E. F., Amundson, R. G., Marino, B. D., and Deniro, M. J. 1991. Stable isotope ratios of carbon in phytoliths as a quantitative method for monitoring vegetational and climate change. Quaternary Research 35:222–233.Google Scholar
Kelly, E. F., Blecker, S. W., Yonker, C. M., Olson, C. G., Wohl, E. E., and Todd, L. C. 1998. Stable isotope composition of soil organic matter and phytoliths as paleoenvironmental indicators. Geoderma 82:59–81.CrossRefGoogle Scholar
Kerns, B. K., Moore, M. M., and Hart, S. C. 2001. Estimating forest-grassland dynamics using soil phytolith assemblages and δ13C of soil organic matter. Ecoscience 8:478–488.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
Lü, H., Wang, Y., Wang, G., Yang, H., and Li, Z. 2000. Analysis of carbon isotope in phytoliths from C3 and C4 plants and modern soil. Chinese Science Bulletin 45:1804–1808.Google Scholar
MacFadden, B. J., Cerling, 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
Maddison, W. P., and Maddison, D. R. 2009. Mesquite: a modular system for evolutionary analysis, Version 2.6. http://mesquiteproject.org .Google Scholar
Madella, M., Powers-Jones, A. H., and Jones, M. K. 1998. A simple method of extraction of opal phytoliths from sediment using a non-toxic heavy liquid. Journal of Archaeological Science 25:801–803.CrossRefGoogle 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., 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
McClaren, 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.CrossRefGoogle Scholar
Rosen, A. Miller, and Weiner, S. 1994. Identifying ancient irrigation: a new method using opaline phytoliths from emmer wheat. Journal of Archaeological Science 21:125–132.Google 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.CrossRefGoogle 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
Mulholland, S. C., and Prior, C. 1993. AMS Radiocarbon dating of phytoliths. Pp. 21–24 in Pearsall, and Piperno, 1993.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
Osborne, C. P., and Freckleton, R. P. 2009. Ecological selection pressures for C4 photosynthesis in the grasses. Proceedings of the Royal Society of London B 276:1753–1760.Google Scholar
Pagel, M. 1999. Inferring the historical patterns of biological evolution. Nature 401:877–884.Google 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
Pearsall, D. M., and Piperno, D. R., eds. 1993. 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. 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, and Piperno, 1993.Google Scholar
Piperno, D. R. 2006. Phytoliths: a comprehensive guide for archaeologists and paleoecologists AltaMira, New York.Google Scholar
Piperno, D. R., and Becker, P. 1996. Vegetational history of a site in the central Amazon basin derived from phytolith and charcoal records from natural soils. Quaternary Research 45:202–209.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.Google 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., Cerling, 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.Google Scholar
Retallack, G. J. 1997. Neogene expansion of the North American prairie. Palaios 12:380–390.Google Scholar
Rovner, I. 1971. Potential of opal phytoliths for use in paleoecological reconstruction. Quaternary Research 1:343–359.Google Scholar
Rundel, P. W. 1980. The ecological distribution of C3 and C4 grasses in the Hawaiian Islands. Oecologia 45:354–359.Google Scholar
Runge, F. 1999. The opal phytolith inventory of soils in central Africa—quantities, shapes, classification, and spectra. Review of Palaeobotany and Palynology 107:23–53.Google Scholar
Sage, R. F., Wedin, D. A., and Li, M. 1999. The biogeography of C4 photosynthesis: pattern and controlling factors. Pp. 313–373 in Sage, R. F. and Monson, R. K., eds. C4 plant biology. Academic Press, San Diego.Google Scholar
Sanchez-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
Sangster, A. G., and Parry, D. W. 1969. Some factors in relation to bulliform cell silicification in the grass leaf. Annals of Botany 33:315–323.Google Scholar
Sanyal, P., Bhattacharya, S. K., Kumar, R., Ghosh, S. K., and Sangode, S. J. 2005. Paleovegetational reconstruction in Late Miocene: a case study based on early diagenetic carbonate cement from the Indian Siwalik. Palaeogeography, Palaeoclimatology, Palaeoecology 228:245–259.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
Sinha, N. R., and Kellogg, E. A. 1996. Parallelism and diversity in multiple origins of C4 photosynthesis in the grass family. American Journal of Botany 83:1458–1470.Google Scholar
Smith, F. A., and Anderson, K. B. 2001. Characterization of organic compounds in phytoliths: improving the resolving power of phytolith δ13C as a tool for paleoecological reconstruction of C3 and C4 grasses. Pp. 317–327 in Meunier, J. D. and Colin, F., eds. Phytoliths: applications in Earth science and human history. A. A. Balkema, Rotterdam.Google Scholar
Smith, F. A., and White, J. W. C. 2004. Modern calibration of phytolith carbon isotope signatures for C3/C4 paleograssland reconstruction. Palaeogeography, Palaeoclimatology, Palaeoecology 207:277–304.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., and McInerney, F. A. 2011. The Neogene transition from C3 to C4 grasslands in North America: assemblage analysis of fossil phytoliths. Paleobiology 37:50–71 (this volume).Google Scholar
Strömberg, C. A. E., Friis, E. M., Liang, M.-M., Werdelin, L., and Zhang, Y.-l. 2007a. Palaeoecology of an Early-Middle Miocene lake in China: preliminary interpretations based on phytoliths from the Shanwang Basin. Vertebrata PalAsiatica 45:145–160.Google Scholar
Strömberg, C. A. E., Werdelin, L., Friis, E. M., and Saraç, G. 2007b. The spread of grass-dominated habitats in Turkey and surrounding areas during the Cenozoic: phytolith evidence. Palaeogeography, Palaeoclimatology, Palaeoecology 250:18–49.Google Scholar
Teeri, J. A., and Stowe, L. G. 1976. Climatic patterns and the distribution of C4 grasses in North America. Oecologia 23:1–12.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
Tieszen, L. L., Senyimba, M. M., and Imbamba, S. K. 1979. The distribution of C3 and C4 grasses and carbon isotope discrimination along an altitudinal and moisture gradient in Kenya. Oecologia 37:337–350.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
Twiss, P. C. 1992. Predicting the world distribution of C3 and C4 grass phytoliths. Pp. 113–128 in Rapp, G. Jr. and Mulholland, S. C., eds. Phytolith systematics: emerging issues. Plenum, New York.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.Google Scholar
Vogel, J. C. 1993. Variability of carbon isotope fractionation during photosynthesis. Pp. 29–46 in Ehleringer, J. R., Hall, A. E., and Farquhar, G. D., eds. Stable isotopes and plant carbon-water relations. Academic Press, New York.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.CrossRefGoogle Scholar
Webb, C. O., Ackerly, D. D., and Kembel, S. W. 2008. Phylocom: software for the analysis of phylogenetic community structure and trait evolution. Bioinformatics 24:2098–2100.Google Scholar
Wilding, L. P. 1967. Radiocarbon dating of biogenic opal. Science 156:66–67.Google Scholar
Zheng, Y., Dong, Y., Matsui, A., Udatsu, T., and Fujiwara, H. 2003. Molecular genetic basis of determining subspecies of ancient rice using the shape of phytoliths. Journal of Archaeological Science 30:1215–1221.CrossRefGoogle Scholar
Supplementary material: PDF

McInerney et al. supplementary material

Supplementary Material

Download McInerney et al. supplementary material(PDF)
PDF 3.2 MB