The rapid Cretaceous diversification of flowering plants remains Darwin’s ‘abominable mystery’ despite numerous fossil flowers discovered in recent years. Wildfires were frequent in the Cretaceous and many such early flower fossils are represented by charcoalified fragments, lacking complete delicate structures and surface textures, making their similarity to living forms difficult to discern. Furthermore, scarcity of information about the ecology of early angiosperms makes it difficult to test hypotheses about the drivers of their diversification, including the role of fire in shaping flowering plant evolution. We report the discovery of two exquisitely preserved fossil flower species, one identical to the inflorescences of the extant crown-eudicot genus Phylica and the other recovered as a sister group to Phylica, both preserved as inclusions together with burned plant remains in Cretaceous amber from northern Myanmar (~99 million years ago). These specialized flower species, named Phylica piloburmensis sp. nov. and Eophylica priscastellata gen. et sp. nov., exhibit traits identical to those of modern taxa in fire-prone ecosystems such as the fynbos of South Africa, and provide evidence of fire adaptation in angiosperms.
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The Micro-XCT scanning data are available at Zenodo (https://doi.org/10.5281/zenodo.3997200). Videos of the 3D reconstruction of internal and external structures of the fossil specimens are available at Figshare (https://doi.org/10.6084/m9.figshare.12865859.v4). High resolution images of all the figures are available at Figshare (https://doi.org/10.6084/m9.figshare.12845144).
Lloyd, G. T. et al. Dinosaurs and the Cretaceous terrestrial revolution. Proc. R. Soc. B 275, 2483–2490 (2008).
Bininda-Emonds, O. R. P. et al. The delayed rise of present-day mammals. Nature 446, 507–512 (2007).
Herrera-Flores, J. A., Stubbs, T. L. & Benton, M. J. Ecomorphological diversification of squamates in the Cretaceous. R. Soc. Open Sci. 8, 201961 (2021).
Benton, M. J. The origins of modern biodiversity on land. Phil. Trans. R. Soc. B 365, 3667–3679 (2010).
Roelants, K. et al. Global patterns of diversifcation in the history of modern amphibians. Proc. Natl Acad. Sci. USA 104, 887–892 (2007).
Grosberg, R. K., Vermeij, G. J. & Wainwright, P. C. Biodiversity in water and on land. Curr. Biol. 22, 900–903 (2012).
Condamine, F. L., Silvestro, D., Koppelhus, E. B. & Antonelli, A. The rise of angiosperms pushed conifers to decline during global cooling. Proc. Natl Acad. Sci. USA 117, 28867–28875 (2020).
Buggs, R. J. The deepening of Darwin’s abominable mystery. Nat. Ecol. Evol. 1, 0169 (2017).
Friis, E. M., Crane, P. R., Pedersen, K. R., Stampanoni, M. & Marone, F. Exceptional preservation of tiny embryos documents seed dormancy in early angiosperms. Nature 528, 551–554 (2015).
Friis, E. M., Crane, P. R. & Pedersen, K. R. Early Flowers and Angiosperm Evolution (Cambridge Univ. Press, 2011).
Friis, E. M., Pedersen, K. R. & Crane, P. R. Cretaceous angiosperm flowers: Innovation and evolution in plant reproduction. Palaeogeogr. Palaeoclimatol. Palaeoecol. 232, 251–293 (2006).
Soltis, P. S., Folk, R. A. & Soltis, D. E. Darwin review: angiosperm phylogeny and evolutionary radiations. Proc. R. Soc. B 286, 20190099 (2019).
Bond, W. J. & Scott, A. C. Fire and the spread of flowering plants in the Cretaceous. New Phytol. 188, 1137–1150 (2010).
Bond, W. J. & Midgley, J. J. Fire and the angiosperm revolutions. Int. J. Plant Sci. 173, 569–583 (2012).
Belcher, C. M. & Hudspith, V. A. Changes to Cretaceous surface fire behaviour influenced the spread of the early angiosperms. New Phytol. 213, 1521–1532 (2017).
He, T., Lamont, B. B. & Pausas, J. G. Fire as a key driver of Earth’s biodiversity. Biol. Rev. 94, 1983–2010 (2019).
Cruickshank, R. D. & Ko, K. Geology of an amber locality in the Hukawng Valley, Northern Myanmar. J. Asian Earth Sci. 21, 441–455 (2003).
Shi, G. H. et al. Age constraint on Burmese amber based on U–Pb dating of zircons. Cretac. Res. 37, 155–163 (2012).
Yu, T. et al. An ammonite trapped in Burmese amber. Proc. Natl Acad. Sci. USA 166, 11345–11350 (2019).
Xing, L. D. & Qiu, L. Zircon U–Pb age constraints on the Hkamti amber biota in northern Myanmar. Palaeogeogr. Palaeoclimatol. Palaeoecol. 558, 109960 (2020).
Xia, F. Y., Yang, G., Zhang, Q. & Shi, G. L. Amber Lives Through Time and Space (Beijing Science Press, 2015).
Poinar, G. O. & Brown, A. E. A green algae (Chaetophorales: Chaetophoraceae) in Burmese amber. Hist. Biol. 33, 323–327 (2019).
Liu, Z. J., Huang, D., Cai, C. Y. & Wang, X. The core eudicot boom registered in Myanmar amber. Sci. Rep. 8, 16765 (2018).
Poinar, G. O. & Chambers, K. L. Tropidogyne pentaptera sp. nov., a new mid-Cretaceous fossil angiosperm flower in Burmese amber. Palaeodiversity 10, 135–140 (2017).
Poinar, G. O. & Chambers, K. L. Palaeoanthella huangii gen. and sp. nov., an Early Cretaceous flower (Angiospermae) in Burmese amber. SIDA 21, 2087–2092 (2005).
Goldblatt, P. An analysis of the flora of Southern Africa: its characteristics, relationships, and orgins. Ann. Mo. Bot. Gard. 65, 369–436 (1978).
Verboom, G. A. et al. in Fynbos: Ecology, Evolution and Conservation of a Megadiverse Region (eds Allsopp, N. et al.) 93–118 (Oxford Univ. Press, 2014).
Hauenschild, F., Favre, A., Michalak, I. & Muellner-Riehl, A. N. The influence of the Gondwanan breakup on the biogeographic history of the ziziphoids (Rhamnaceae). J. Biogeogr. 45, 2669–2677 (2018).
Onstein, R. E. & Linder, H. P. Beyond climate: convergence in fast evolving sclerophylls in Cape and Australian Rhamnaceae predates the mediterranean climate. J. Ecol. 104, 665–677 (2016).
Brown, S., Scott, A. C., Glasspool, I. J. & Collinson, M. E. Cretaceous wildfires and their impact on the Earth system. Cretac. Res. 36, 162–190 (2012).
Richardson, J. E. et al. Rapid and recent origin of species richness in the Cape flora of South Africa. Nature 412, 181–183 (2001).
Pillans, N. S. The genus Phylica. J. S. Afr. Bot. 8, 1–164 (1942).
Rebelo, T. et al. in The vegetation of South Africa, Lesotho and Swaziland (eds Mucina, L. & Rutherford, M. C.) 52–219 (South African National Biodiversity Institute, 2006).
Gimingham, C. H. & Cowling, R. The ecology of fynbos: nutrients, fire and diversity. J. Ecol. 81, 195–196 (1993).
Richardson, J. E., Fay, M. F., Cronk, Q. C. B. & Cronk, M. W. Species delimitation and the origin of populations in island representatives of Phylica (Rhamnaceae). Evolution 57, 816–827 (2003).
Richardson, J. E. Molecular Systematics of the Genus Phylica L. With an Emphasis on the Island Species (Edinburgh Univ. Press, 1999).
Schirarend, C. & Köhler, E. World Pollen and Spore Flora: Rhamnaceae Juss (Scandinavian Univ. Press, 1993).
Medan, D. & Schirarend, C. in Flowering plants · Dicotyledons (ed. Kubitzki, K.) 320–338 (Springer, 2004).
Gotelli, M. M., Galati, B. G. & Medan, D. Morphological and ultrastructural studies of floral nectaries in Rhamnaceae. J. Torrey Bot. Soc. 144, 63–73 (2017).
Friedrich, O., Norris, R. D. & Erbacher, J. Evolution of middle to Late Cretaceous oceans–a 55 m.y. record of Earth’s temperature and carbon cycle. Geology 40, 107–110 (2012).
Lenton, T. M., Daines, S. J. & Mills, B. J. W. COPSE reloaded: an improved model of biogeochemical cycling over Phanerozoic time. Earth Sci. Rev. 178, 1–28 (2018).
Huber, B. T., Hodell, D. A. & Hamilton, C. P. Middle-Late Cretaceous climate of the southern high latitudes: stable isotopic evidence for minimal equator-to-pole thermal gradients. Geol. Soc. Am. Bull. 107, 1164–1191 (1995).
Belcher, C. M., Yearsley, J. M., Hadden, R. M., Mcelwain, J. C. & Rein, G. Baseline intrinsic flammability of Earth’s ecosystems estimated from paleoatmospheric oxygen over the past 350 million years. Proc. Natl Acad. Sci. USA 107, 22448–22453 (2010).
Berner, R. A., Beerling, D. J., Dudley, R., Robinson, J. M. & Wildman, R. A. Phanerozoic atmospheric oxygen. Annu. Rev. Earth Planet. Sci. 31, 105–134 (2003).
Glasspool, I. J. & Scott, A. C. Phanerozoic concentrations of atmospheric oxygen reconstructed from sedimentary charcoal. Nat. Geosci. 3, 627–630 (2010).
Poulsen, C. J., Tabor, C. & White, J. D. Long-term climate forcing by atmospheric oxygen concentrations. Science 348, 1238–1241 (2015).
Hudspith, V. A. & Belcher, C. M. Fire biases the production of charred flowers: implications for the Cretaceous fossil record. Geology 45, 727–730 (2017).
Scott, A. C. Charcoal recognition, taphonomy and uses in palaeoenvironmental analysis. Palaeogeogr. Palaeoclimatol. Palaeoecol. 291, 11–39 (2010).
Scott, A. C. The use of charcoal to interpret Cretaceous wildfires and volcanic activity. Glob. Geol. 22, 217–241 (2019).
Scott, A. C., Cripps, J. A., Nichols, G. J. & Collinson, M. E. The taphonomy of charcoal following a recent heathland fire and some implications for the interpretation of fossil charcoal deposits. Palaeogeogr. Palaeoclimatol. Palaeoecol. 164, 1–31 (2000).
Whtilock, C., Higuera, P. E., McWethy, D. B. & Briles, C. E. Paleoecological perspectives on fire ecology: revisiting the fire-regime concept. Open Ecol. J. 3, 6–23 (2010).
Bond, W. J. & Keeley, J. E. Fire as global ‘herbivore’: the ecology and evolution of flammable ecosystems. Trends Ecol. Evol. 20, 387–394 (2005).
Bowman, D. M. J. S. et al. Fire in the Earth system. Science 324, 481–484 (2009).
Crisp, M. D., Burrows, G. E., Cook, L. G., Thornhill, A. H. & Bowman, D. M. J. S. Flammable biomes dominated by eucalypts originated at the Cretaceous–Paleogene boundary. Nat. Commun. 2, 193 (2011).
Pausas, J. G. & Keeley, J. E. A burning story: the role of fire in the history of life. Bioscience 59, 593–601 (2009).
Scott, A. C. Burning Planet. The Story of Fire Through Time (Oxford Univ. Press, 2018).
Scott, A. C. Fire: A Very Short Introduction (Oxford Univ. Press, 2020).
Scott, A. C., Bowman, D. J. M. S., Bond, W. J., Pyne, S. J. & Alexander M. Fire on Earth: An Introduction (J. Wiley & Sons Press, 2014).
Keeley, J. E., Pausas, J. G., Rundel, P. W., Bond, W. J. & Bradstock, R. A. Fire as an evolutionary pressure shaping plant traits. Trends Plant Sci. 16, 406–411 (2011).
Lenton,T. M. in Fire Phenomena and the Earth System: An Interdisciplinary Guide to Fire Science (ed. Belcher, C. M.) 289–308 (J. Wiley & Sons Press, 2013).
Herendeen, P. S., Magallon-Puebla, S., Lupia, R., Crane, P. R. & Kobylinska, J. A preliminary conspectus of the Allon flora from the Late Cretaceous (Late Santonian) of the central Georgia, USA. Ann. Mo. Bot. Gard. 86, 407–471 (1999).
He, T., Pausas, J. G., Belcher, C. M., Schwilk, D. W. & Lamont, B. B. Fire-adapted traits of Pinus arose in the fiery Cretaceous. New Phytol. 194, 751–759 (2012).
Cornwell, W. K. et al. Flammability across the gymnosperm phylogeny: the importance of litter particle size. New Phytol. 206, 672–681 (2015).
Lamont, B. B. & He, T. Fire-adapted Gondwanan angiosperm floras evolved in the Cretaceous. BMC Evol. Biol. 12, 223 (2012).
He, T., Lamont, B. B. & Manning, J. A. Cretaceous origin for fire adaptations in the Cape flora. Sci. Rep. 6, 34880 (2016).
He, T., Lamont, B. B. & Downes, K. S. Banksia born to burn. New Phytol. 191, 184–196 (2011).
Midgley, J. & Bond, W. Pushing back in time, the role of fire in plant evolution. New Phytol. 191, 5–7 (2011).
Scott, A. C. The Pre-Quaternary history of fire. Palaeogeogr. Palaeoclimatol. Palaeoecol. 164, 281–329 (2000).
Midgley, J. J., Kruger, L. M. & Skelton, R. How do fires kill plants? The hydraulic death hypothesis and Cape Proteaceae “fire-resisters”. S. Afr. J. Bot. 77, 381–386 (2011).
Lamont, B. B., Groom, P. K., Williams, M. & He, T. LMA, density and thickness: recognizing different leaf shapes and correcting for their non-laminarity. New Phytol. 207, 942–947 (2015).
Lamont, B. B., He, T. & Yan, Z. Evolutionary history of fire-stimulated resprouting, flowering, seed release and germination. Biol. Rev. 94, 903–928 (2019).
Schwilk, D. W. & Kerr, B. Genetic niche-hiking: an alternative explanation for the evolution of flammability. Oikos 99, 431–442 (2002).
Kilian, D. & Cowling, R. M. Comparative seed biology and co-existence of two fynbos shrub species. J. Veg. Sci. 3, 637–646 (1992).
Hall, S. A., Newton, R. J., Holmes, P. M., Gaertner, M. & Esler, K. J. Heat and smoke pre‐treatment of seeds to improve restoration of an endangered Mediterranean climate vegetation type. Austral Ecol. 42, 354–366 (2017).
Ruprecht, E., Fenesi, A., Fodor, E. I., Kuhn, T. & Tklyi, J. Shape determines fire tolerance of seeds in temperate grasslands that are not prone to fire. Perspect. Plant Ecol. 17, 397–404 (2015).
Mohr, B. A. R. & Friis, E. M. Early angiosperms from the Lower Cretaceous Crato Formation (Brazil), a preliminary report. Int. J. Plant Sci. 161, 155–167 (2000).
Forest, F. et al. Preserving the evolutionary potential of floras in biodiversity hotspots. Nature 445, 757–760 (2007).
Linder, H. P. Evolution of diversity: the Cape flora. Trends Plant Sci. 10, 536–541 (2005).
Linder, H. P. The radiation of the Cape flora, southern Africa. Biol. Rev. 78, 597–638 (2003).
Poinar, G. O. Burmese amber: evidence of Gondwanan origin and Cretaceous dispersion. Hist. Biol. 31, 1304–1309 (2019).
Oliveira, I. D. S. et al. Earliest onychophoran in amber reveals Gondwanan migration patterns. Curr. Biol. 26, 2594–2601 (2016).
Poinar, G. O., Lambert, J. B. & Wu, Y. Araucarian source of fossiliferous Burmese amber: spectroscopic and anatomical evidence. J. Bot. Res. Inst. Tex. 1, 449–455 (2007).
Cai, C. Y. et al. Basal polyphagan beetles in mid-Cretaceous amber from Myanmar: biogeographic implications and long-term morphological stasis. Proc. R. Soc. B 286, 2175 (2019).
Zhang, W., Li, H., Shih, C., Zhang, A. & Ren, D. Phylogenetic analyses with four new Cretaceous bristletails reveal inter-relationships of Archaeognatha and Gondwana origin of Meinertellidae. Cladistics 34, 384–406 (2018).
Westerweel, J. et al. Burma Terrane part of the Trans-Tethyan Arc during collision with India according to palaeomagnetic data. Nat. Geosci. 12, 5–6 (2019).
Metcalfe, I. in Biogeography and Geological Evolution of SE Asia (eds Hall, R. & Holloway, J. D.) 25–41 (Backhuys Publishers Press,1998).
Li, J., Wu, Y., Peng, J. & Batten, D. J. Palynofloral evolution on the northern margin of the Indian Plate, southern Xizang, China during the Cretaceous period and its phytogeographic significance. Palaeogeogr. Palaeoclimatol. Palaeoecol. 515, 107–122 (2019).
Smith, A. G., Smith, D. G. & Funnell B. M. Atlas of Mesozoic and Cenozoic Coastlines (Cambridge Univ. Press, 2004).
Klages, J. P. et al. Temperate rainforests near the South Pole during peak Cretaceous warmth. Nature 580, 81–86 (2020).
Coetzee, J. A. & Muller, J. The phytogeographic significance of some extinct Gondwana pollen types from the Tertiary of the southwestern Cape (South Africa). Ann. Mo. Bot. Gard. 71, 1088–1099 (1984).
De Villiers, S. E. & Cadman, A. The palynology of Tertiary sediments from a palaeochannel in Namaqualand, South Africa. Palaeontol. Afr. 34, 69–99 (1997).
De Villiers, S. E. & Cadman, A. An analysis of the palynomorphs obtained from Tertiary sediments at Koingnaas, Namaqualand, South Africa. J. Afr. Earth Sci. 33, 17–47 (2001).
Sandersen, A., Scott, L., McLachlan, I. R. & Hancox, P. J. Cretaceous biozonation based on terrestrial palynomorphs from two wells in the offshore Orange Basin of South Africa. Palaeontol. Afr. 46, 21–41 (2011).
Hooghiemstra, H., Lézine, A. M., Leroy, S. A. G., Dupont, L. & Marret, F. Late Quaternary palynology in marine sediments: a synthesis of the understanding of pollen distribution patterns in the NW African setting. Quat. Int. 148, 29–44 (1988).
Scholtz, A. The palynology of the upper lacustrine sediments of the Arnot Pipe, Banke, Namaqualand. Ann. S. Afr. Mus. 95, 1–109 (1985).
Sciscio, L. et al. Fluctuations in Miocene climate and sea levels along the south-western South African coast: inferences from biogeochemistry, palynology and sedimentology. Palaeontol. Afr. 48, 2–18 (2013).
Roberts, D. L. et al. Miocene fluvial systems and palynofloras at the southwestern tip of Africa: implications for regional and global fluctuations in climate and ecosystems. Earth Sci. Rev. 124, 184–201 (2013).
Roberts, D. L. et al. Palaeoenvironments during a terminal Oligocene or early Miocene transgression in a fluvial system at the southwestern tip of Africa. Glob. Planet. Change 150, 1–23 (2017).
Grimaldi, D., Engel, M. S. & Nascimbene, P. Fossiliferous Cretaceous amber from Myanmar (Burma): its rediscovery, biotic diversity, and paleontological significance. Am. Mus. Novit. 3361, 1–72 (2002).
Mao, Y. et al. Various amberground marine animals on Burmese amber with discussions on its age. Palaeoentomology 1, 91–103 (2018).
Smith, R. D. & Ross, A. J. Amberground pholadid bivalve borings and inclusions in Burmese amber: implications for proximity of resin-producing forests to brackish waters, and the age of the amber. Earth Env. Sci. Trans. R. Soc. Edinb. 107, 239–247 (2018).
Schmidt, A. R. & Dilcher, D. L. Aquatic organisms as amber inclusions and examples from a modern swamp forest. Proc. Natl Acad. Sci. USA 104, 16581–16585 (2007).
Cole, L. E., Bhagwat, S. A. & Willis, K. J. Fire in the swamp forest: palaeoecological insights into natural and human-induced burning in intact tropical peatlands. Front. For. Glob. Change 2, 48 (2019).
Labandeira, C. C. in Reading and Writing of the Fossil Record: Preservational Pathways to Exceptional Fossilization. The Paleontological Society Papers (eds Laflamme, M. et al.) 163–216 (Cambridge Univ. Press, 2014).
Seyfullah, L. J. et al. Production and preservation of resins–past and present. Biol. Rev. 93, 1684–1714 (2018).
Putz, M. K. & Taylor, E. L. Wound response in fossil trees assemblages from Antarctica and its potential as a palaeoenvironmental indicator. IAWA J. 17, 77–88 (1996).
McKellar, R. C. et al. Insect outbreaks produce distinctive carbon isotope signatures in defensive resins and fossiliferous ambers. Proc. R. Soc. B 278, 3219–3224 (2011).
Pausas, J. G. Generalized fire response strategies in plants and animals. Oikos 128, 147–153 (2019).
Schmidt, A. R. et al. Arthropods in amber from the Triassic Period. Proc. Natl Acad. Sci. USA 109, 14796–14801 (2012).
Silvestro, D. et al. Fossil data support a pre-Cretaceous origin of flowering plants. Nat. Ecol. Evol. 5, 449–457 (2021).
Donoghue, P. Evolution: the flowering of land plant evolution. Curr. Biol. 29, 753–756 (2019).
Thulin, M. et al. Family relationships of the enigmatic rosid genera Barbeya and Dirachma from the Horn of Africa region. Plant Syst. Evol. 213, 103–119 (1998).
Wilf, P., Carvalho, M. R., Gandolfo, M. A. & Cúneo, N. R. Eocene lantern fruits from Gondwanan Patagonia and the early origins of Solanaceae. Science 355, 71–75 (2017).
We thank Profs. Z.-k. Zhou, P. Herendeen, S. R. Manchester, Y.-w. Xing, G.-l. Shi, H.-l. You, C. Hoorn, G. Li, Z. Feng, D. Ren, B. Wang and Z.-j. Liu for their valuable advice on earlier versions of this manuscript; J.-a. Xia for his help with drawing the palaeoenvironment reconstruction; and F.-c. Zheng for help with micro-CT data analyses. This study was supported by the National Natural Science Foundation of China (No. 31801022 for S.W. and No. 31701090 for C.S.), and co-sponsored by the National Natural Science Foundation of China (No. 41790454 and No. 41688103 for Y.D.W.), Strategic Priority Research Program (B) of the Chinese Academy of Sciences (No. XDB18000000 and No. XDB26000000 for Y.D.W.), the State Key Laboratory of Palaeobiology and Stratigraphy (No. 20191103 for Y.D.W. and No. 213119 for S.W.), the Natural Science Foundation of Shandong Province (Grant No. ZR2019BC094 for S.W.). This work is a contribution to UNESCO-IUGS IGCP Project 679.
The authors declare no competing interests.
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Supplementary Notes 1–8 and Figs. 1–30.
Videos of the 3D reconstruction of the fossil specimens QUST-AM20501–14.
Videos of the 3D reconstruction of the fossil specimens QUST-AM32413–16.
Videos of the 3D reconstruction of the fossil specimens QUST-AM32417, QUST-AM33310, QUST-AM32127 and QUST-AM33311.
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Shi, C., Wang, S., Cai, Hh. et al. Fire-prone Rhamnaceae with South African affinities in Cretaceous Myanmar amber. Nat. Plants 8, 125–135 (2022). https://doi.org/10.1038/s41477-021-01091-w
Nature Plants (2022)