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A paleothermometer for the northern Andes based on C3–C4 grass phytoliths
Published online by Cambridge University Press: 23 January 2023
Abstract
Grass-dominated ecosystems cover ~40% of Earth's terrestrial surface, with tropical grasses accounting for ~20% of global net primary productivity. C3 (cool/temperate) and C4 (tropical and subtropical) grass distribution is driven primarily by temperature. In this work, we used phytolith assemblages collected from vegetation plots along an elevation and temperature gradient in the northern Andes (Colombia and Ecuador) to develop a paleothermometer for the region. To accomplish this, we created a transfer function based on the inverse relationship between mean annual temperature (MAT) and the phytolith-based climatic index (Ic), which is the proportion of C3 over C4 grass phytoliths (GSSCP). To evaluate how accurately the index reflects C4–C3 grass abundance in vegetation plots, we compared it with semiquantitative floristic estimates of C4–C3 grass abundance. To further evaluate the 1 − Ic index as a proxy for C4–C3 grass abundance, we compared it with corresponding δ13C values (an independent proxy for C4–C3 vegetation). Results indicate that (1) GSSCP assemblages correctly estimate C4–C3 grass abundance in vegetation plots; (2) the Ic index outperforms the δ13C record in estimating C4–C3 grass abundance, even in open-vegetation types; and (3) our Ic index–based model accurately predicts MAT. This new calibrated proxy will help improve paleotemperature reconstructions in the northern Andes since at least the emergence and spread of C4 grasses in the region during the late Miocene.
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Literature Cited
Aleman, J. C., and Staver, A. C.. 2018. Spatial patterns in the global distributions of savanna and forest. Global Ecology and Biogeography 27:792–803.CrossRefGoogle Scholar
Aleman, J. C., Leys, B., Apema, R., Bentaleb, I., Dubois, M. A., Lamba, B., Lebamba, J., Martin, C., Ngomanda, A., Truc, L., Yangakola, J.-M., Favier, C., Bremond, L., and Woods, K.. 2012. Reconstructing savanna tree cover from pollen, phytoliths and stable carbon isotopes. Journal of Vegetation Science 23:187–197.CrossRefGoogle Scholar
Aleman, J. C., Saint-Jean, A., Leys, B., Carcaillet, C., Favier, C., and Bremond, L.. 2013. Estimating phytolith influx in lake sediments. Quaternary Research 80:341–347.CrossRefGoogle Scholar
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
An, X., Lu, H., and Chu, G.. 2015. Surface soil phytoliths as vegetation and altitude indicators: a study from the southern Himalaya. Scientific Reports 5:15523.CrossRefGoogle ScholarPubMed
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
Barreda, V., and Palazzesi, L.. 2007. Patagonian vegetation turnovers during the Paleogene–early Neogene: origin of arid-adapted floras. Botanical Review 73:31–50.CrossRefGoogle Scholar
Benvenuto, M. L., Fernández Honaine, M., Osterrieth, M. L., and Morel, E.. 2015. Differentiation of globular phytoliths in Arecaceae and other monocotyledons: morphological description for paleobotanical application. Turkish Journal of Botany 39:341–353.CrossRefGoogle Scholar
Bermúdez, M. A., Hoorn, C., Bernet, M., Carrillo, E., van der Beek, P. A., Garver, J. I., Mora, J. L., and Mehrkian, K.. 2017. The detrital record of late-Miocene to Pliocene surface uplift and exhumation of the Venezuelan Andes in the Maracaibo and Barinas foreland basins. Basin Research 29(S1):370–395.CrossRefGoogle Scholar
Biswas, O., Ghosh, R., Agrawal, S., Morthekai, P., Paruya, D. K., Mukherjee, B., Bera, M., and Bera, S.. 2021. A comprehensive calibrated phytolith based climatic index from the Himalaya and its application in palaeotemperature reconstruction. Science of the Total Environment 750:142280.CrossRefGoogle ScholarPubMed
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
Boom, A., Marchant, R., Hooghiemstra, H., and Sinninghe Damsté, J. S.. 2002. CO2- and temperature-controlled altitudinal shifts of C4- and C3-dominated grasslands allow reconstruction of palaeoatmospheric pCO2. Palaeogeography, Palaeoclimatology, Palaeoecology 177:151–168.CrossRefGoogle Scholar
Boutton, T. W. 1996. Stable carbon isotope ratios of soil organic matter and their use as indicators of vegetation and climate change. Pp. 47–82 in Boutton, T. W. and Yamasaki, S.-i., eds. Mass spectrometry of soils. Dekker, New York.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.CrossRefGoogle Scholar
Bremond, L., Alexandre, A., Peyron, O., and Guiot, J.. 2008a. Definition of grassland biomes from phytoliths in West Africa. Journal of Biogeography 35:2039–2048.CrossRefGoogle 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
Bremond, L., Boom, A., and Favier, C.. 2012. Neotropical C3/C4 grass distributions—present, past and future. Global Change Biology 18:2324–2334.CrossRefGoogle Scholar
Brightly, W. H., Hartley, S. E., Osborne, C. P., Simpson, K. J., and Strömberg, C. A. E.. 2020. High silicon concentrations in grasses are linked to environmental conditions and not associated with C4 photosynthesis. Global Change Biology 26:7128–7143.CrossRefGoogle ScholarPubMed
Castañeda, I. S., and Schouten, S.. 2011. A review of molecular organic proxies for examining modern and ancient lacustrine environments. Quaternary Science Reviews 30:2851–2891.CrossRefGoogle Scholar
Cerling, T. E., Quade, J., Wang, Y., and Bowman, J. R.. 1989. Carbon isotopes in soils and palaeosols as ecology and palaeoecology indicators. Nature 341:138–139.CrossRefGoogle Scholar
Cerling, T. E., Harris, J. M., Ambrose, S. H., Leakey, M. G., and Solounias, N.. 1997a. Dietary and environmental reconstruction with stable isotope analyses of herbivore tooth enamel from the Miocene locality of Fort Ternan, Kenya. Journal of Human Evolution 33:635–650.CrossRefGoogle ScholarPubMed
Cerling, T. E., Harris, J. M., MacFadden, B. J., Leakey, M. G., Quade, J., Eisenmann, V., and Ehleringer, J. R.. 1997b. Global vegetation change through the Miocene/Pliocene boundary. Nature 389:153–158.CrossRefGoogle 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
Chen, S. T., Smith, S. Y., Sheldon, N. D., and Strömberg, C. A. E.. 2015. Regional-scale variability in the spread of grasslands in the late Miocene. Palaeogeography, Palaeoclimatology, Palaeoecology 437:42–52.CrossRefGoogle Scholar
Collatz, G. J., Berry, J. A., and Clark, J. S.. 1998. Effects of climate and atmospheric CO2 partial pressure on the global distribution of C4 grasses: present, past, and future. Oecologia 114:441–454.CrossRefGoogle ScholarPubMed
Conley, D. J., and Carey, J. C.. 2015. Silica cycling over geologic time. Nature Geoscience 8:431–432.CrossRefGoogle Scholar
Cotton, J. M., Sheldon, N. D., and Strömberg, C. A. E.. 2012. High-resolution isotopic record of C4 photosynthesis in a Miocene grassland. Palaeogeography, Palaeoclimatology, Palaeoecology 337–338:88–98.CrossRefGoogle Scholar
Cotton, J. M., Cerling, T. E., Hoppe, K. A., Mosier, T. M., and Still, C. J.. 2016. Climate, CO2, and the history of North American grasses since the Last Glacial Maximum. Science Advances 2:e1501346.CrossRefGoogle ScholarPubMed
Crepet, W. L., and Feldman, G. D.. 1991. The earliest remains of grasses in the fossil record. American Journal of Botany 78:1010–1014.CrossRefGoogle Scholar
Crifò, C., and Strömberg, C. A. E.. 2021. Spatial patterns of soil phytoliths in a wet vs. dry Neotropical forest: implications for paleoecology. Palaeogeography Palaeoclimatology Palaeoecology 526:110100.CrossRefGoogle Scholar
Cui, Y., Schubert, B. A., and Jahren, A. H.. 2020. A 23 m.y. record of low atmospheric CO2. Geology 48:888–892.CrossRefGoogle Scholar
Diefendorf, A. F., Mueller, K. E., Wing, S. L., Koch, P. L., and Freeman, K. H.. 2010. Global patterns in leaf 13C discrimination and implications for studies of past and future climate. Proceedings of the National Academy of Sciences USA 107:5738.CrossRefGoogle ScholarPubMed
Dunn, R. E., Strömberg, C. A. E., Madden, R. H., Kohn, M. J., and Carlini, A. A.. 2015. Linked canopy, climate, and faunal change in the Cenozoic of Patagonia. Science 347:258–261.CrossRefGoogle ScholarPubMed
Edwards, E. J., and Still, C. J.. 2008. Climate, phylogeny and the ecological distribution of C4 grasses. Ecology Letters 11:266–276.CrossRefGoogle ScholarPubMed
Edwards, E. J., Osborne, C. P., Strömberg, C. A. E., Smith, S. A., Consortium, C. G., Bond, W. J., Christin, P. A., Cousins, A. B., Duvall, M. R., Fox, D. L., Freckleton, R. P., Ghannoum, O., Hartwell, J., Huang, Y., Janis, C. M., Keeley, J. E., Kellogg, E. A., Knapp, A. K., Leakey, A. D., Nelson, D. M., Saarela, J. M., Sage, R. F., Sala, O. E., Salamin, N., Still, C. J., and Tipple, B.. 2010. The origins of C4 grasslands: integrating evolutionary and ecosystem science. Science 328:587–591.CrossRefGoogle ScholarPubMed
Ehleringer, J. R., and Cerling, T. E.. 2002. C3 and C4 photosynthesis. Encyclopedia of Global Environmental Change 2(4).Google Scholar
Ehleringer, J. R., Cerling, T. E., and Helliker, B. R.. 1997. C4 photosynthesis, atmospheric CO2, and climate. Oecologia 112:285–299.CrossRefGoogle ScholarPubMed
Farquhar, G. D. 1983. On the nature of carbon isotope discrimination in C4 species. Functional Plant Biology 10:205–226.CrossRefGoogle Scholar
Favier, C., Aleman, J., Bremond, L., Dubois, M. A., Freycon, V., and Yangakola, J.-M.. 2012. Abrupt shifts in African savanna tree cover along a climatic gradient. Global Ecology and Biogeography 21:787–797.CrossRefGoogle Scholar
Fox, D. L., Pau, S., Taylor, L., Strömberg, C. A., Osborne, C. P., Bradshaw, C., Conn, S., Beerling, D. J., and Still, C. J.. 2018. Climatic controls on C4 grassland distributions during the Neogene: a model-data comparison. Frontiers in Ecology and Evolution 6:147.CrossRefGoogle Scholar
Fredlund, G. G., and Tieszen, L. T.. 1994. Modern phytolith assemblages from the North American Great Plains. Journal of Biogeography 21:321–335.CrossRefGoogle Scholar
Gallaher, T. J., Akbar, S. Z., Klahs, P. C., Marvet, C. R., Senske, A. M., Clark, L. G., and Stromberg, C. A. E.. 2020. 3D shape analysis of grass silica short cell phytoliths: a new method for fossil classification and analysis of shape evolution. New Phytol 228:376–392.CrossRefGoogle ScholarPubMed
Garzione, C. N., McQuarrie, N., Perez, N. D., Ehlers, T. A., Beck, S. L., Kar, N., Eichelberger, N., Chapman, A. D., Ward, K. M., Ducea, M. N., Lease, R. O., Poulsen, C. J., Wagner, L. S., Saylor, J. E., Zandt, G., and Horton, B. K.. 2017. Tectonic evolution of the Central Andean Plateau and implications for the growth of plateaus. Annual Review of Earth and Planetary Sciences 45:529–559.CrossRefGoogle Scholar
Gregory-Wodzicki, K. M. 2000. Uplift history of the Central and Northern Andes: a review. GSA Bulletin 112:1091–1105.2.0.CO;2>CrossRefGoogle Scholar
Harris, E. B., Strömberg, C. A. E., Sheldon, N. D., Smith, S. Y., and Vilhena, D. A.. 2017. Vegetation response during the lead-up to the middle Miocene warming event in the northern Rocky Mountains, USA. Palaeogeography, Palaeoclimatology, Palaeoecology 485:401–415.CrossRefGoogle Scholar
Hooghiemstra, H., and Van der Hammen, T.. 2004. Quaternary Ice-Age dynamics in the Colombian Andes: developing an understanding of our legacy. Philosophical Transactions of the Royal Society of London B 359:173–181.CrossRefGoogle ScholarPubMed
Hoorn, C., Wesselingh, F. P., ter Steege, H., Bermudez, M. A., Mora, A., Sevink, J., Sanmartin, I., Sanchez-Meseguer, A., Anderson, C. L., Figueiredo, J. P., Jaramillo, C., Riff, D., Negri, F. R., Hooghiemstra, H., Lundberg, J., Stadler, T., Sarkinen, T., and Antonelli, A.. 2010. Amazonia through time: Andean uplift, climate change, landscape evolution, and biodiversity. Science 330:927–931.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
Kerns, B. K., Moore, M. M., and Hart, S. C.. 2001. Estimating forest-grassland dynamics using soil phytolith assemblages and d13C of soil organic matter. Écoscience 8:478–488.CrossRefGoogle Scholar
Kirschner, J. A., and Hoorn, C.. 2020. The onset of grasses in the Amazon drainage basin, evidence from the fossil record. Frontiers of Biogeography 12(2):e44827.CrossRefGoogle Scholar
Ledru, M. P., Jomelli, V., Samaniego, P., Vuille, M., Hidalgo, S., Herrera, M., and Ceron, C.. 2013. The Medieval Climate Anomaly and the Little Ice Age in the eastern Ecuadorian Andes. Clim. Past 9:307–321.CrossRefGoogle Scholar
Livingstone, D., and Clayton, W.. 1980. An altitudinal cline in tropical African grass floras and its paleoecological significance. Quaternary Research 13:392–402.CrossRefGoogle Scholar
Lloyd, J., and Farquhar, G. D.. 1994. 13C discrimination during CO2 assimilation by the terrestrial biosphere. Oecologia 99:201–215.CrossRefGoogle ScholarPubMed
Loughney, K. M., Hren, M. T., Smith, S. Y., and Pappas, J. L.. 2019. Vegetation and habitat change in southern California through the Middle Miocene Climatic Optimum: Paleoenvironmental records from the Barstow Formation, Mojave Desert, USA. GSA Bulletin 132:113–129.CrossRefGoogle Scholar
Lupien, R. L., Russell, J. M., Yost, C. L., Kingston, J. D., Deino, A. L., Logan, J., Schuh, A., and Cohen, A. S.. 2021. Vegetation change in the Baringo Basin, East Africa across the onset of Northern Hemisphere glaciation 3.3–2.6 Ma. Palaeogeography, Palaeoclimatology, Palaeoecology 570:109426.CrossRefGoogle Scholar
Madella, M., Jones, M., 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.CrossRefGoogle Scholar
Mander, L., Li, M., Mio, W., Fowlkes, C. C., and Punyasena, S. W.. 2013. Classification of grass pollen through the quantitative analysis of surface ornamentation and texture. Proceedings of the Royal Society of London B 280:20131905.Google ScholarPubMed
Martínez, C., Jaramillo, C., Correa-Metrío, A., Crepet, W., Moreno, J. E., Aliaga, A., Moreno, F., Ibañez-Mejia, M., and Bush, M. B.. 2020. Neogene precipitation, vegetation, and elevation history of the Central Andean Plateau. Science Advances 6:eaaz4724.CrossRefGoogle ScholarPubMed
McInerney, F. A., Strömberg, C. A. E., and White, J. W. C.. 2016. The Neogene transition from C3 to C4 grasslands in North America: stable carbon isotope ratios of fossil phytoliths. Paleobiology 37:23–49.CrossRefGoogle Scholar
Meyers, P. A., and Ishiwatari, R.. 1993. Lacustrine organic geochemistry—an overview of indicators of organic matter sources and diagenesis in lake sediments. Organic Geochemistry 20:867–900.CrossRefGoogle Scholar
Miller, L. A., Smith, S. Y., Sheldon, N. D., and Stromberg, C. A. E.. 2012. Eocene vegetation and ecosystem fluctuations inferred from a high-resolution phytolith record. Geological Society of America Bulletin 124:1577–1589.CrossRefGoogle Scholar
Neumann, K., Strömberg, C. A. E., Ball, T., Albert, R. M., Vrydaghs, L., and Cummings, L. S.. 2019. International code for phytolith nomenclature (ICPN) 2.0. Annals of Botany 124:189–199.Google Scholar
Palmer, P. G. 1976. Grass cuticles: a new paleoecological tool for East African lake sediments. Canadian Journal of Botany 54:1725–1734.CrossRefGoogle Scholar
Parmenter, C., and Folger, D. W.. 1974. Eolian biogenic detritus in deep sea sediments: a possible index of equatorial ice age aridity. Science 185:695–698.CrossRefGoogle ScholarPubMed
Pau, S., Edwards, E. J., and Still, C. J.. 2013. Improving our understanding of environmental controls on the distribution of C3 and C4 grasses. Global Change Biology 19:184–196.CrossRefGoogle ScholarPubMed
Pearsall, D. M. 2000. Paleoethnobotany: a handbook of procedures. Academic Press, San Diego.Google Scholar
Piperno, D. R. 1988. Phytolyth analysis: an archaeological and geological perspective. Academic Press, San Diego.Google Scholar
Prentice, I. C. 1985. Pollen representation, source area, and basin size: toward a unified theory of pollen analysis. Quaternary Research 23:76–86.CrossRefGoogle Scholar
Quade, J., Solouniasand, N., and Cerling, T. E.. 1994. Stable isotopic evidence from paleosol carbonates and fossil teeth in Greece for forest or woodlands over the past 11 Ma. Palaeogeography, Palaeoclimatology, Palaeoecology 108:41–53.CrossRefGoogle Scholar
R Development Core Team. 2019. R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria.Google Scholar
Rieley, G., Collier, R. J., Jones, D. M., Eglinton, G., Eakin, P. A., and Fallick, A. E.. 1991. Sources of sedimentary lipids deduced from stable carbon-isotope analyses of individual compounds. Nature 352:425–427.CrossRefGoogle Scholar
Rundel, P. W. 1980. The ecological distribution of C4 and C3 grasses in the Hawaiian Islands. Oecologia 45:354–359.CrossRefGoogle ScholarPubMed
Sage, R. F., Christin, P. A., and Edwards, E. J.. 2011. The C4 plant lineages of planet Earth. Journal of Experimental Botany 62:3155–3169.CrossRefGoogle ScholarPubMed
Sage, R. F., Monson, R. K., Ehleringer, J. R., Adachi, S., and Pearcy, R. W.. 2018. Some like it hot: the physiological ecology of C4 plant evolution. Oecologia 187:941–966.CrossRefGoogle ScholarPubMed
Simpson, B. B., and Todzia, C. A.. 1990. Patterns and processes in the development of the high Andean flora. American Journal of Botany 77:1419–1432.CrossRefGoogle Scholar
Smith, B. N., and Epstein, S.. 1971. Two categories of 13C/12C ratios for higher plants. Plant Physiology 47:380–384.CrossRefGoogle Scholar
Song, Z., McGrouther, K., and Wang, H.. 2016. Occurrence, turnover and carbon sequestration potential of phytoliths in terrestrial ecosystems. Earth-Science Reviews 158:19–30.CrossRefGoogle 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):6-1-6-14.CrossRefGoogle 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.CrossRefGoogle ScholarPubMed
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. 2011. Evolution of grasses and grassland ecosystems. Annual Review of Earth and Planetary Sciences 39:517–544.CrossRefGoogle Scholar
Strömberg, C. A. E., and McInerney, F. A.. 2016. The Neogene transition from C3 to C4 grasslands in North America: assemblage analysis of fossil phytoliths. Paleobiology 37:50–71.CrossRefGoogle 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.CrossRefGoogle Scholar
Strömberg, C. A. E., Dunn, R. E., Madden, R. H., Kohn, M. J., and Carlini, A. A.. 2013. Decoupling the spread of grasslands from the evolution of grazer-type herbivores in South America. Nature Communications 4:1478.CrossRefGoogle ScholarPubMed
Strömberg, C. A. E., Di Stilio, V. S., and Song, Z.. 2016. Functions of phytoliths in vascular plants: an evolutionary perspective. Functional Ecology 30:1286–1297.CrossRefGoogle Scholar
Teeri, J., and Stowe, L.. 1976. Climatic patterns and the distribution of C4 grasses in North America. Oecologia 23:1–12.CrossRefGoogle ScholarPubMed
Thorn, V. 2001. Oligocene and early Miocene phytolits from CRP-2/2A and CRP-3, Victoria Land Basin, Antarctica. Terra Antartica 8:407–422.Google Scholar
Tieszen, L. L., Senyimba, M. M., Imbamba, S. K., and Troughton, J. H.. 1979. The distribution of C3 and C4 grasses and carbon isotope discrimination along an altitudinal and moisture gradient in Kenya. Oecologia 37:337–350.CrossRefGoogle ScholarPubMed
Trembath-Reichert, E., Wilson, J. P., McGlynn, S. E., and Fischer, W. W.. 2015. Four hundred million years of silica biomineralization in land plants. Proceedings of the National Academy of Sciences USA 112:5449–5454.CrossRefGoogle ScholarPubMed
Twiss, P. C. 1992. Predicted world distribution of C3 and C4 grass phytoliths. Pp. 113–128 in Rapp, G. and Mulholland, S. C., eds. Phytolith systematics. Springer, New York.CrossRefGoogle Scholar
Urban, M. A., Nelson, D. M., Jiménez-Moreno, G., Châteauneuf, J.-J., Pearson, A., and Hu, F. S.. 2010. Isotopic evidence of C4 grasses in southwestern Europe during the Early Oligocene–Middle Miocene. Geology 38:1091–1094.CrossRefGoogle Scholar
Winslow, J. C., Hunt, E. R. Jr., and Piper, S. C.. 2003. The influence of seasonal water availability on global C3 versus C4 grassland biomass and its implications for climate change research. Ecological Modelling 163:153–173.CrossRefGoogle Scholar
Wynn, J. G., and Bird, M. I.. 2007. C4-derived soil organic carbon decomposes faster than its C3 counterpart in mixed C3/C4 soils. Global Change Biology 13:2206–2217.CrossRefGoogle Scholar
Young, H. J., and Young, T. P.. 1983. Local distribution of C3 and C4 grasses in sites of overlap on Mount Kenya. Oecologia 58:373–377.CrossRefGoogle ScholarPubMed
Zhou, H., Helliker, B. R., Huber, M., Dicks, A., and Akcay, E.. 2018. C4 photosynthesis and climate through the lens of optimality. Proceedings of the National Academy of Sciences USA 115:12057–12062.CrossRefGoogle ScholarPubMed