Leaf economic traits from fossils support a weedy habit for early angiosperms.

Many key aspects of early angiosperms are poorly known, including their ecophysiology and associated habitats. Evidence for fast-growing, weedy angiosperms comes from the Early Cretaceous Potomac Group, where angiosperm fossils, some of them putative herbs, are found in riparian depositional settings. However, inferences of growth rate from sedimentology and growth habit are somewhat indirect; also, the geographic extent of a weedy habit in early angiosperms is poorly constrained. Using a power law between petiole width and leaf mass, we estimated the leaf mass per area (LMA) of species from three Albian (110-105 Ma) fossil floras from North America (Winthrop Formation, Patapsco Formation of the Potomac Group, and the Aspen Shale). All LMAs for angiosperm species are low (<125 g/m(2); mean = 76 g/m(2)) but are high for gymnosperm species (>240 g/m(2); mean = 291 g/m(2)). On the basis of extant relationships between LMA and other leaf economic traits such as photosynthetic rate and leaf lifespan, we conclude that these Early Cretaceous landscapes were populated with weedy angiosperms with short-lived leaves (<12 mo). The unrivalled capacity for fast growth observed today in many angiosperms was in place by no later than the Albian and likely played an important role in their subsequent ecological success.

[1]  C. Labandeira,et al.  Late Paleocene fossils from the Cerrejón Formation, Colombia, are the earliest record of Neotropical rainforest , 2009, Proceedings of the National Academy of Sciences.

[2]  T. Brodribb,et al.  Angiosperm leaf vein evolution was physiologically and environmentally transformative , 2009, Proceedings of the Royal Society B: Biological Sciences.

[3]  L. Poorter,et al.  Causes and consequences of variation in leaf mass per area (LMA): a meta-analysis. , 2009, The New phytologist.

[4]  T. Brodribb,et al.  Ancestral xerophobia: a hypothesis on the whole plant ecophysiology of early angiosperms , 2009, Geobiology.

[5]  T. Taylor,et al.  Paleobotany: The Biology and Evolution of Fossil Plants , 2008 .

[6]  L. Hickey,et al.  The Fossil Flora of the Winthrop Formation (Albian–Early Cretaceous) of Washington State, USA. Part I: Bryophyta and Pteridophytina , 2008 .

[7]  W. Green,et al.  A Morphotype Catalogue, Floristic Analysis and Stratigraphic Description of the Aspen Shale Flora(Cretaceous–Albian) of Southwestern Wyoming , 2008 .

[8]  Sandra Díaz,et al.  Plant species traits are the predominant control on litter decomposition rates within biomes worldwide. , 2008, Ecology letters.

[9]  R. Müller,et al.  Global plate motion frames: Toward a unified model , 2008 .

[10]  R. B. Jackson,et al.  The Global Stoichiometry of Litter Nitrogen Mineralization , 2008, Science.

[11]  D. Royer,et al.  Sharply increased insect herbivory during the Paleocene–Eocene Thermal Maximum , 2008, Proceedings of the National Academy of Sciences.

[12]  Leo J. Hickey,et al.  Early cretaceous fossil evidence for angiosperm evolution , 2008, The Botanical Review.

[13]  Pamela S Soltis,et al.  Using plastid genome-scale data to resolve enigmatic relationships among basal angiosperms , 2007, Proceedings of the National Academy of Sciences.

[14]  Ü. Niinemets,et al.  Fossil leaf economics quantified: calibration, Eocene case study, and implications , 2007, Paleobiology.

[15]  L. Santiago,et al.  Extending the leaf economics spectrum to decomposition: evidence from a tropical forest. , 2007, Ecology.

[16]  U. Heimhofer,et al.  New records of Early Cretaceous angiosperm pollen from Portuguese coastal deposits: Implications for the timing of the early angiosperm radiation , 2007 .

[17]  B. G. Briggs,et al.  Hydatellaceae identified as a new branch near the base of the angiosperm phylogenetic tree , 2007, Nature.

[18]  T. Feild,et al.  The ecophysiology of early angiosperms. , 2007, Plant, cell & environment.

[19]  Mark E. Harmon,et al.  Global-Scale Similarities in Nitrogen Release Patterns During Long-Term Decomposition , 2007, Science.

[20]  Eric Garnier,et al.  From Plant Traits to Plant Communities: A Statistical Mechanistic Approach to Biodiversity , 2006, Science.

[21]  J. P. Grime,et al.  Plant Strategies, Vegetation Processes, and Ecosystem Properties , 2006 .

[22]  U. Heimhofer,et al.  Timing of early angiosperm radiation: recalibrating the classical succession , 2006, Journal of the Geological Society.

[23]  Frans Bongers,et al.  Leaf traits are good predictors of plant performance across 53 rain forest species. , 2006, Ecology.

[24]  L. Hickey,et al.  Using leaf margin analysis to estimate the mid-Cretaceous (Albian) paleolatitude of the Baja BC block , 2006 .

[25]  M. Westoby,et al.  Bivariate line‐fitting methods for allometry , 2006, Biological reviews of the Cambridge Philosophical Society.

[26]  P. Reich,et al.  Fundamental trade-offs generating the worldwide leaf economics spectrum. , 2006, Ecology.

[27]  Sandra Díaz,et al.  Specific leaf area and dry matter content estimate thickness in laminar leaves. , 2005, Annals of botany.

[28]  William G. Lee,et al.  Modulation of leaf economic traits and trait relationships by climate , 2005 .

[29]  D. Royer,et al.  Correlations of climate and plant ecology to leaf size and shape: potential proxies for the fossil record. , 2005, American journal of botany.

[30]  T. Feild,et al.  Form, function and environments of the early angiosperms: merging extant phylogeny and ecophysiology with fossils. , 2005, The New phytologist.

[31]  N. Holbrook,et al.  Leaf hydraulic capacity in ferns, conifers and angiosperms: impacts on photosynthetic maxima. , 2004, The New phytologist.

[32]  M. Donoghue,et al.  Dark and disturbed: a new image of early angiosperm ecology , 2004, Paleobiology.

[33]  J. P. Grime,et al.  The plant traits that drive ecosystems: Evidence from three continents , 2004 .

[34]  Sean C. Thomas,et al.  The worldwide leaf economics spectrum , 2004, Nature.

[35]  S. Beavington‐Penney Analysis of the Effects of Abrasion on the Test of Palaeonummulites venosus: Implications for the Origin of Nummulithoclastic Sediments , 2004 .

[36]  L. Hickey,et al.  Phylogenetic evidence for the herbaceous origin of angiosperms , 1992, Plant Systematics and Evolution.

[37]  P. Reich,et al.  The Evolution of Plant Functional Variation: Traits, Spectra, and Strategies , 2003, International Journal of Plant Sciences.

[38]  B. Housen,et al.  Paleomagnetism of the Mt. Stuart Batholith Revisited Again: What Has Been Learned Since 1972? , 2003 .

[39]  P. Barrett,et al.  An exceptionally preserved Lower Cretaceous ecosystem , 2003, Nature.

[40]  M. Westoby,et al.  ECOLOGICAL STRATEGIES : Some Leading Dimensions of Variation Between Species , 2002 .

[41]  D. Ellsworth,et al.  Dependence of needle architecture and chemical composition on canopy light availability in three North American Pinus species with contrasting needle length. , 2002, Tree physiology.

[42]  K. Nixon,et al.  Archaefructaceae, a New Basal Angiosperm Family , 2002, Science.

[43]  E. M. Friis,et al.  Fossil evidence of water lilies (Nymphaeales) in the Early Cretaceous , 2001, Nature.

[44]  Ülo Niinemets,et al.  GLOBAL-SCALE CLIMATIC CONTROLS OF LEAF DRY MASS PER AREA, DENSITY, AND THICKNESS IN TREES AND SHRUBS , 2001 .

[45]  F. Woodward,et al.  Vegetation and the terrestrial carbon cycle:Modelling the first 400 million years , 2001 .

[46]  J. Doyle,et al.  Morphological Phylogenetic Analysis of Basal Angiosperms: Comparison and Combination with Molecular Data , 2000, International Journal of Plant Sciences.

[47]  Mark W. Chase,et al.  The earliest angiosperms: evidence from mitochondrial, plastid and nuclear genomes , 1999, Nature.

[48]  P. Reich,et al.  Convergence and correlations among leaf size and function in seed plants: a comparative test using independent contrasts. , 1999, American journal of botany.

[49]  Volker Mosbrugger,et al.  Leaf venation density as a climate and environmental proxy: a critical review and new data , 1999 .

[50]  P. Reich,et al.  From tropics to tundra: global convergence in plant functioning. , 1997, Proceedings of the National Academy of Sciences of the United States of America.

[51]  Roderick Hunt,et al.  Seedling growth, allocation and leaf attributes in a wide range of woody plant species and types , 1996 .

[52]  G. J. Brenner Evidence for the Earliest Stage of Angiosperm Pollen Evolution: A Paleoequatorial Section from Israel , 1996 .

[53]  L. Hickey,et al.  Evidence for and Implications of an Herbaceous Origin for Angiosperms , 1996 .

[54]  A. Drinnan,et al.  The Megaflora from the Quantico Locality (Upper Albian), Lower Cretaceous Potomac Group of Virginia , 1994 .

[55]  C. Swisher,et al.  Implications of an exceptional fossil flora for Late Cretaceous vegetation , 1993, Nature.

[56]  J. Doyle Revised palynological correlations of the lower Potomac group (USA) and the cocobeach sequence of Gabon (Barremian-Aptian) , 1992 .

[57]  S. Lidgard,et al.  Angiosperm diversification and Cretaceous floristic trends: a comparison of palynofloras and leaf macrofloras , 1990, Paleobiology.

[58]  W. Bond The tortoise and the hare: ecology of angiosperm dominance and gymnosperm persistence , 1989 .

[59]  E. M. Gifford,et al.  Morphology and evolution of vascular plants , 1989 .

[60]  G. Rex,et al.  Further experimental investigations on the formation of plant compression fossils , 1986 .

[61]  P. Coley,et al.  HERBIVORY AND DEFENSIVE CHARACTERISTICS OF TREE SPECIES IN A LOWLAND TROPICAL FOREST , 1983 .

[62]  K. Niklas Morphometric Relationships and Rates of Evolution among Paleozoic Vascular Plants , 1978 .

[63]  L. Hickey,et al.  Pollen and leaves from the Mid-Cretaceous Potomac group and their bearing on early angiosperm evolution , 1976 .

[64]  G. Ledyard Stebbins,et al.  Flowering Plants: Evolution Above the Species Level , 1975 .

[65]  G. Stebbins THE PROBABLE GROWTH HABIT OF THE EARLIEST FLOWERING PLANTS , 1965 .

[66]  G. J. Brenner The spores and pollen of the Potomac group of Maryland , 1963 .

[67]  R. Brown Fossil plants from the Aspen shale of southwestern Wyoming , 1933 .

[68]  F. H. Knowlton The Lower Cretaceous Deposits of Maryland , 1912 .