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      Plant Ecological Strategies Shift Across the Cretaceous–Paleogene Boundary

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          Abstract

          The End-Cretaceous Impact Winter Killed Off Slow-Growing Plants The end-Cretaceous mass extinction caused the selective extinction of plant species with slow-growth strategies, consistent with an impact winter hypothesis.

          Abstract

          The Chicxulub bolide impact caused the end-Cretaceous mass extinction of plants, but the associated selectivity and ecological effects are poorly known. Using a unique set of North Dakota leaf fossil assemblages spanning 2.2 Myr across the event, we show among angiosperms a reduction of ecological strategies and selection for fast-growth strategies consistent with a hypothesized recovery from an impact winter. Leaf mass per area (carbon investment) decreased in both mean and variance, while vein density (carbon assimilation rate) increased in mean, consistent with a shift towards “fast” growth strategies. Plant extinction from the bolide impact resulted in a shift in functional trait space that likely had broad consequences for ecosystem functioning.

          Author Summary

          Sixty-six million years ago the Chicxulub bolide impacted the Earth, marking the Cretaceous–Paleogene boundary (KPB). This event caused the planet's most recent mass extinction, but the selectivity and functional consequences of the extinction on terrestrial plants has been largely unknown. A key untested hypothesis has been that a subsequent impact winter would have selected against slow-growing evergreen species, a possible cause of the modern dominance of high-productivity deciduous angiosperm forests. We tested this hypothesis using fossil leaf assemblages across a 2-million-year interval spanning the KPB. We assess two key ecological strategy axes—carbon assimilation rate and carbon investment—using leaf minor vein density and leaf mass per area as proxies, respectively. We show that species that survive the KPB have fast-growth ecological strategies corresponding to high assimilation rates and low carbon investment. This finding is consistent with impact winter leading to the nonrandom loss of slow-growing evergreen species. Our study reveals a dramatic example of the effect of rapid catastrophic environmental change on biodiversity.

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          Most cited references15

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          Rebuilding community ecology from functional traits.

          There is considerable debate about whether community ecology will ever produce general principles. We suggest here that this can be achieved but that community ecology has lost its way by focusing on pairwise species interactions independent of the environment. We assert that community ecology should return to an emphasis on four themes that are tied together by a two-step process: how the fundamental niche is governed by functional traits within the context of abiotic environmental gradients; and how the interaction between traits and fundamental niches maps onto the realized niche in the context of a biotic interaction milieu. We suggest this approach can create a more quantitative and predictive science that can more readily address issues of global change.
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            From tropics to tundra: global convergence in plant functioning.

            Despite striking differences in climate, soils, and evolutionary history among diverse biomes ranging from tropical and temperate forests to alpine tundra and desert, we found similar interspecific relationships among leaf structure and function and plant growth in all biomes. Our results thus demonstrate convergent evolution and global generality in plant functioning, despite the enormous diversity of plant species and biomes. For 280 plant species from two global data sets, we found that potential carbon gain (photosynthesis) and carbon loss (respiration) increase in similar proportion with decreasing leaf life-span, increasing leaf nitrogen concentration, and increasing leaf surface area-to-mass ratio. Productivity of individual plants and of leaves in vegetation canopies also changes in constant proportion to leaf life-span and surface area-to-mass ratio. These global plant functional relationships have significant implications for global scale modeling of vegetation-atmosphere CO2 exchange.
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              Plant species traits are the predominant control on litter decomposition rates within biomes worldwide.

              Worldwide decomposition rates depend both on climate and the legacy of plant functional traits as litter quality. To quantify the degree to which functional differentiation among species affects their litter decomposition rates, we brought together leaf trait and litter mass loss data for 818 species from 66 decomposition experiments on six continents. We show that: (i) the magnitude of species-driven differences is much larger than previously thought and greater than climate-driven variation; (ii) the decomposability of a species' litter is consistently correlated with that species' ecological strategy within different ecosystems globally, representing a new connection between whole plant carbon strategy and biogeochemical cycling. This connection between plant strategies and decomposability is crucial for both understanding vegetation-soil feedbacks, and for improving forecasts of the global carbon cycle.
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                Author and article information

                Contributors
                Role: Academic Editor
                Journal
                PLoS Biol
                PLoS Biol
                plos
                plosbiol
                PLoS Biology
                Public Library of Science (San Francisco, USA )
                1544-9173
                1545-7885
                September 2014
                16 September 2014
                : 12
                : 9
                : e1001949
                Affiliations
                [1 ]Department of Ecology and Evolutionary Biology, University of Arizona, Tucson, Arizona, United States of America
                [2 ]Rocky Mountain Biological Laboratory, Gothic, Colorado, United States of America
                [3 ]Department of Earth and Environmental Sciences, Wesleyan University, Middletown, Connecticut, United States of America
                [4 ]National Museum of Natural History, Smithsonian Institution, Washington, DC, United States of America
                [5 ]Denver Museum of Nature and Science, Denver, Colorado, United States of America
                [6 ]The Santa Fe Institute, Santa Fe, New Mexico, United States of America
                University of California, Berkeley, United States of America
                Author notes

                The authors have declared that no competing interests exist.

                The author(s) have made the following declarations about their contributions: Conceived and designed the experiments: BB DR BE. Performed the experiments: BB DR. Analyzed the data: BB DR. Contributed reagents/materials/analysis tools: KJ IM BE. Contributed to the writing of the manuscript: BB DR KJ IM BE.

                Article
                PBIOLOGY-D-14-01131
                10.1371/journal.pbio.1001949
                4165584
                25225914
                a88d1dee-2c85-4b3f-981d-7785d661d857
                Copyright @ 2014

                This is an open-access article, free of all copyright, and may be freely reproduced, distributed, transmitted, modified, built upon, or otherwise used by anyone for any lawful purpose. The work is made available under the Creative Commons CC0 public domain dedication.

                History
                : 28 March 2014
                : 7 August 2014
                Page count
                Pages: 7
                Funding
                BB was supported by a Rocky Mountain Biological Laboratory graduate research fellowship, a Geological Society of America student research grant, and a NSF pre-doctoral fellowship. BE was supported by an NSF ATB and Macrosystems award (Grant numbers: Macrosystems - NSF DEB 1065861; ATB - NSF EF 0742800). The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.
                Categories
                Research Article
                Biology and Life Sciences
                Ecology
                Biodiversity
                Ecological Niches
                Ecophysiology
                Macroecology
                Paleoecology
                Plant Ecology
                Paleontology
                Paleobiology
                Paleobotany
                Paleoclimatology
                Earth Sciences
                Ecology and Environmental Sciences
                Custom metadata
                The authors confirm that all data underlying the findings are fully available without restriction. All relevant data are within the paper and its Supporting Information files.

                Life sciences
                Life sciences

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