Rise to dominance of angiosperm pioneers in European Cretaceous environments Clément Coiffard a , Bernard Gomez b,1 , Véronique Daviero-Gomez b , and David L. Dilcher c,1 a Museum für Naturkunde, Leibniz Institut für Evolutions und Biodiversitätsforschung, Invalidenstrasse 43, D-10115 Berlin, Germany; b Centre National de la Recherche Scientifique Unité Mixte de Recherche 5276, Laboratoire de Géologie de Lyon–Terre, Planètes, Environnement, Université Lyon 1 (Claude Bernard), F-69622 Villeurbanne Cedex, France; and c Department of Geology, Indiana University, Bloomington, IN 47405-7005 Contributed by David L. Dilcher, November 2, 2012 (sent for review June 20, 2012) The majority of environments are dominated by flowering plants today, but it is uncertain how this dominance originated. This increase in angiosperm diversity happened during the Cretaceous period (ca. 145–65 Ma) and led to replacement and often extinction of gymnosperms and ferns. We propose a scenario for the rise to dominance of the angiosperms from the Barremian (ca. 130 Ma) to the Campanian (ca. 84 Ma) based on the European megafossil plant record. These megafossil data demonstrate that angiosperms mi- grated into new environments in three phases: (i ) Barremian (ca. 130–125 Ma) freshwater lake-related wetlands; (ii ) Aptian–Albian (ca. 125–100 Ma) understory floodplains (excluding levees and back swamps); and (iii ) Cenomanian–Campanian (ca. 100–84 Ma) natural levees, back swamps, and coastal swamps. This scenario allows for the measured evolution of angiosperms in time and space synthe- sizing changes in the physical environment with concomitant changes in the biological environment. This view of angiosperm radiation in three phases reconciles previous scenarios based on the North American record. The Cretaceous plant record that can be observed in Europe is exceptional in many ways. (i ) Angiosperms are well preserved from the Barremian to the Maastrichtian (ca. 65 Ma). (ii ) Deposits are well constrained and dated stratigraphically. (iii ) They encompass a full range of environments. (iv) European paleobotany provides many detailed studies of Cretaceous floras for analysis. These factors make a robust dataset for the study of angiosperm evolution from the Barremian to the Campanian that can be traced through various ecosystems and related to other plant groups occupying the same niches. vegetation turnover | early angiosperms | ecology | evolution in time and space L ess than 20 y after the publication of The Origin of Species, Charles Darwin wrote to Oswald Heer in a letter dated March 8, 1875: “The sudden appearance of so many Dicotyledons in the Upper Chalk appears to me a perplexing phenomenon” (1, p 539). A few years later, he wrote to Joseph Dalton Hooker in a letter dated July 22, 1879: “The rapid development as far as we can judge of all the higher plants within recent geological times is an abominable mystery” (1, p 378). Darwin was referring to the fre- quent appearance of leaves of the flowering plants with the be- ginning of the Late Cretaceous (Cenomanian Stage), as it was known at that time. Since then, paleobotanists have attempted to explain the “sudden” appearance of angiosperms in the fossil re- cord based either on the present percentage and distribution of living primitive taxa in the tropics (2) or on fossils from the middle Cretaceous of North America (3–6). These publications have in- cluded many new finds on somewhat older Cretaceous strata. We present here a unique interpretation of the European Cretaceous record of angiosperms in their paleoenvironmental context. Our synthesis demonstrates that early angiosperms were at first suc- cessful invaders in only certain environments but expanded into others over an interval of ∼45 million y (7). Three phases are clearly recognizable that represent different stages in the success story of flowering plants. Phase 1: Barremian–Aptian Freshwater Lake-Related Wetlands Worldwide, Barremian (ca. 130–125 Ma) angiosperm megafossils are very rare, represented by 11 genera, 5 of which apparently lived in freshwater lake/wetland habitats (8–15, *). In an aquatic com- munity, these angiosperms competed with charophytes that dom- inated macrophytic associations since the Permian (10, 11, 13). In the Barremian of Europe (Figs. 1 and 2A), chloranthoid/Afropollis pollen indicate the presence of terrestrial angiosperms (16), al- though matoniaceous fern thickets and open conifer woodlands in floodplains dominated the terrestrial vegetation. The physiog- nomy of the megafossil plants from the Barremian (ca. 130 Ma) to the middle Aptian (ca. 118 Ma) is consistent with the fact that during that time Western Europe underwent an arid phase (17, 18). Diversified aquatic angiosperm megafossils (19) and terrestrial chloranthoid, lauralean, and magnolialean fossil pollen (16) appear in the late Aptian (Fig. 2B). This diversification was accompanied by the closure of canopy woodland, with conifers spreading over most environments and the near extinction of matoniaceous ferns (ref. 19; Fig. 2B). In contrast, terrestrial angiosperm leaf mega- fossils are very rare except for Quercophyllum from the Aptian/ Albian of Arnal (Portugal) that probably grew along freshwater lakes or pond margins. Phase 2: Albian Understory Floodplains (Excluding Levees and Back Swamps) The total taxa count in the vegetation of Europe became very di- verse during the Albian (ca. 112–100 Ma). For example in the floodplains, there were ca. 4 angiosperms per 11 taxa in total per locality during the Albian vs. 0 angiosperms per 8 taxa in total during the Barremian and 0 angiosperms per 6 taxa in total during the Aptian. This angiosperm increase coincided with a warming period beginning in the early Albian (20, 21), when angiosperms exhibited widening ecological ranges (Fig. 2C). They continued to dominate the aquatic vegetation (22, 23) but also occurred in significant numbers in the floodplains for the first time (ref. 19; Fig. 2C). From the Barremian, angiosperms competed with Osmun- daceae taxa (e.g., Cladophlebis Brongniart), which nearly dis- appeared during the Albian. In contrast to the small-leafed, highly ramified angiospermous habit, the ferns and gymnosperms, which were replaced by the angiosperms, often showed a large-leafed, monocaulous habit. The small-leafed, ramified habit is more resilient than those with a sin- gle apical meristem that may be damaged or lost. If the meristem of a monocaulous plant is destroyed, it may die or recover only very slowly, whereas a ramified plant can use many active meristems that Author contributions: C.C. and B.G. designed research; C.C., B.G., and V.D.-G. performed research; C.C., B.G., and D.L.D. analyzed data; and C.C., B.G., V.D.-G., and D.L.D. wrote the paper. The authors declare no conflict of interest. 1 To whom correspondence may be addressed. E-mail: dilcher@indiana.edu or bernard. gomez@univ-lyon1.fr. *Gomez B, Daviero-Gomez V, Martín-Closas C, de la Fuente M, Montsechia vidalii, an early aquatic angiosperm from the Barremian of Spain. Seventh European Palaeobotany and Palynology Conference, September 6–11, 2006, Prague, p 49 (abstr). www.pnas.org/cgi/doi/10.1073/pnas.1218633110 PNAS | December 18, 2012 | vol. 109 | no. 51 | 20955–20959 ECOLOGY