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      Extinction Risk and Diversification Are Linked in a Plant Biodiversity Hotspot

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          There is no author summary for this article yet. Authors can add summaries to their articles on ScienceOpen to make them more accessible to a non-specialist audience.

          Abstract

          Plant extinction risks in the Cape, South Africa differ from those for vertebrates worldwide, with young and fast-evolving plant lineages marching towards extinction at the fastest rate, but independently of human effects.

          Abstract

          It is widely recognized that we are entering an extinction event on a scale approaching the mass extinctions seen in the fossil record. Present-day rates of extinction are estimated to be several orders of magnitude greater than background rates and are projected to increase further if current trends continue. In vertebrates, species traits, such as body size, fecundity, and geographic range, are important predictors of vulnerability. Although plants are the basis for life on Earth, our knowledge of plant extinctions and vulnerabilities is lagging. Here, we disentangle the underlying drivers of extinction risk in plants, focusing on the Cape of South Africa, a global biodiversity hotspot. By comparing Red List data for the British and South African floras, we demonstrate that the taxonomic distribution of extinction risk differs significantly between regions, inconsistent with a simple, trait-based model of extinction. Using a comprehensive phylogenetic tree for the Cape, we reveal a phylogenetic signal in the distribution of plant extinction risks but show that the most threatened species cluster within short branches at the tips of the phylogeny—opposite to trends in mammals. From analyzing the distribution of threatened species across 11 exemplar clades, we suggest that mode of speciation best explains the unusual phylogenetic structure of extinction risks in plants of the Cape. Our results demonstrate that explanations for elevated extinction risk in plants of the Cape flora differ dramatically from those recognized for vertebrates. In the Cape, extinction risk is higher for young and fast-evolving plant lineages and cannot be explained by correlations with simple biological traits. Critically, we find that the most vulnerable plant species are nonetheless marching towards extinction at a more rapid pace but, surprisingly, independently from anthropogenic effects. Our results have important implications for conservation priorities and cast doubts on the utility of current Red List criteria for plants in regions such as the Cape, where speciation has been rapid, if our aim is to maximize the preservation of the tree-of-life.

          Author Summary

          The rapid loss of biodiversity is the most significant ecological challenge we face today. Over the past few years, the International Union for Conservation of Nature has published Red Lists documenting the inexorable slide towards extinction of species; recent losses include the Hawaiian crow, golden toad, Baiji dolphin, and the West African black rhino. In groups we know well, such as mammals, the risk of extinction has been related to biology, with the most vulnerable species tending to be large, slow breeding, and narrowly distributed. Although plants are the basis for life on Earth, our knowledge of the drivers of plant extinctions is poor. Here, we disentangle the causes of plant extinctions. We show that the processes linked with extinction risks in plants of the Cape, South Africa differ from those for vertebrates more generally. The most vulnerable species are found within young and fast-evolving plant lineages, opposite to patterns in vertebrates. Our results illustrate the intricate link between the processes of speciation and extinction. We also show that the most threatened species are marching towards extinction at faster rates, but surprisingly, the risk appears independent of human effects.

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          Testing for phylogenetic signal in comparative data: behavioral traits are more labile.

          The primary rationale for the use of phylogenetically based statistical methods is that phylogenetic signal, the tendency for related species to resemble each other, is ubiquitous. Whether this assertion is true for a given trait in a given lineage is an empirical question, but general tools for detecting and quantifying phylogenetic signal are inadequately developed. We present new methods for continuous-valued characters that can be implemented with either phylogenetically independent contrasts or generalized least-squares models. First, a simple randomization procedure allows one to test the null hypothesis of no pattern of similarity among relatives. The test demonstrates correct Type I error rate at a nominal alpha = 0.05 and good power (0.8) for simulated datasets with 20 or more species. Second, we derive a descriptive statistic, K, which allows valid comparisons of the amount of phylogenetic signal across traits and trees. Third, we provide two biologically motivated branch-length transformations, one based on the Ornstein-Uhlenbeck (OU) model of stabilizing selection, the other based on a new model in which character evolution can accelerate or decelerate (ACDC) in rate (e.g., as may occur during or after an adaptive radiation). Maximum likelihood estimation of the OU (d) and ACDC (g) parameters can serve as tests for phylogenetic signal because an estimate of d or g near zero implies that a phylogeny with little hierarchical structure (a star) offers a good fit to the data. Transformations that improve the fit of a tree to comparative data will increase power to detect phylogenetic signal and may also be preferable for further comparative analyses, such as of correlated character evolution. Application of the methods to data from the literature revealed that, for trees with 20 or more species, 92% of traits exhibited significant phylogenetic signal (randomization test), including behavioral and ecological ones that are thought to be relatively evolutionarily malleable (e.g., highly adaptive) and/or subject to relatively strong environmental (nongenetic) effects or high levels of measurement error. Irrespective of sample size, most traits (but not body size, on average) showed less signal than expected given the topology, branch lengths, and a Brownian motion model of evolution (i.e., K was less than one), which may be attributed to adaptation and/or measurement error in the broad sense (including errors in estimates of phenotypes, branch lengths, and topology). Analysis of variance of log K for all 121 traits (from 35 trees) indicated that behavioral traits exhibit lower signal than body size, morphological, life-history, or physiological traits. In addition, physiological traits (corrected for body size) showed less signal than did body size itself. For trees with 20 or more species, the estimated OU (25% of traits) and/or ACDC (40%) transformation parameter differed significantly from both zero and unity, indicating that a hierarchical tree with less (or occasionally more) structure than the original better fit the data and so could be preferred for comparative analyses.
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            The future of biodiversity.

            Recent extinction rates are 100 to 1000 times their pre-human levels in well-known, but taxonomically diverse groups from widely different environments. If all species currently deemed "threatened" become extinct in the next century, then future extinction rates will be 10 times recent rates. Some threatened species will survive the century, but many species not now threatened will succumb. Regions rich in species found only within them (endemics) dominate the global patterns of extinction. Although new technology provides details of habitat losses, estimates of future extinctions are hampered by our limited knowledge of which areas are rich in endemics.
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              Quantifying and mapping the human appropriation of net primary production in earth's terrestrial ecosystems.

              Human appropriation of net primary production (HANPP), the aggregate impact of land use on biomass available each year in ecosystems, is a prominent measure of the human domination of the biosphere. We present a comprehensive assessment of global HANPP based on vegetation modeling, agricultural and forestry statistics, and geographical information systems data on land use, land cover, and soil degradation that localizes human impact on ecosystems. We found an aggregate global HANPP value of 15.6 Pg C/yr or 23.8% of potential net primary productivity, of which 53% was contributed by harvest, 40% by land-use-induced productivity changes, and 7% by human-induced fires. This is a remarkable impact on the biosphere caused by just one species. We present maps quantifying human-induced changes in trophic energy flows in ecosystems that illustrate spatial patterns in the human domination of ecosystems, thus emphasizing land use as a pervasive factor of global importance. Land use transforms earth's terrestrial surface, resulting in changes in biogeochemical cycles and in the ability of ecosystems to deliver services critical to human well being. The results suggest that large-scale schemes to substitute biomass for fossil fuels should be viewed cautiously because massive additional pressures on ecosystems might result from increased biomass harvest.
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                Author and article information

                Contributors
                Role: Academic Editor
                Journal
                PLoS Biol
                plos
                plosbiol
                PLoS Biology
                Public Library of Science (San Francisco, USA )
                1544-9173
                1545-7885
                May 2011
                May 2011
                24 May 2011
                : 9
                : 5
                : e1000620
                Affiliations
                [1 ]National Center for Ecological Analysis and Synthesis, University of California, Santa Barbara, California, United States of America
                [2 ]Department of Biology, McGill University, Montreal, Quebec, Canada
                [3 ]South African National Biodiversity Institute, Biosystematics Research and Biodiversity Collections, Pretoria, South Africa
                [4 ]Schweickerdt Herbarium, Department of Plant Science, University of Pretoria, Pretoria, South Africa
                [5 ]Department of Biochemistry, University of Stellenbosch, Stellenbosch, South Africa
                [6 ]Compton Herbarium, South African National Biodiversity Institute, Cape Town, South Africa
                [7 ]Department of Botany and Plant Biotechnology, University of Johannesburg, Johannesburg, South Africa
                [8 ]Bews Herbarium, School of Biological and Conservation Sciences, University of KwaZulu-Natal, Pietermaritzburg, South Africa
                [9 ]Botany Department, Nelson Mandela Metropolitan University, Port Elizabeth, South Africa
                [10 ]Royal Botanic Gardens, Kew, Richmond, Surrey, United Kingdom
                [11 ]Department of Biological Sciences, University of Idaho, Moscow, Idaho, United States of America
                [12 ]Department of Botany and Bolus Herbarium, University of Cape Town, Western Cape, Rondebosch, South Africa
                [13 ]Imperial College London, Silwood Park Campus, Ascot, Berkshire, United Kingdom
                The University of North Carolina, United States of America
                Author notes

                The author(s) have made the following declarations about their contributions: Conceived and designed the experiments: TJD RMC VS. Performed the experiments: TJD. Analyzed the data: TJD LJH. Contributed reagents/materials/analysis tools: GFS DUB JSB BB RMC FF LJH AMM BS YS MvdB VS. Wrote the paper: TJD VS.

                Article
                10-PLBI-RA-8856R3
                10.1371/journal.pbio.1000620
                3101198
                21629678
                9a7e5732-77c7-43df-a0ee-c23e557efb00
                Davies et al. This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
                History
                : 9 August 2010
                : 14 April 2011
                Page count
                Pages: 9
                Categories
                Research Article
                Ecology/Conservation and Restoration Ecology
                Ecology/Evolutionary Ecology
                Ecology/Global Change Ecology
                Evolutionary Biology/Evolutionary Ecology

                Life sciences
                Life sciences

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