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      European Bison as a Refugee Species? Evidence from Isotopic Data on Early Holocene Bison and Other Large Herbivores in Northern Europe

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          Abstract

          According to the refugee species concept, increasing replacement of open steppe by forest cover after the last glacial period and human pressure had together forced European bison ( Bison bonasus)—the largest extant terrestrial mammal of Europe—into forests as a refuge habitat. The consequent decreased fitness and population density led to the gradual extinction of the species. Understanding the pre-refugee ecology of the species may help its conservation management and ensure its long time survival. In view of this, we investigated the abundance of stable isotopes (δ 13C and δ 15N) in radiocarbon dated skeletal remains of European bison and other large herbivores—aurochs ( Bos primigenius), moose ( Alces alces), and reindeer ( Rangifer tarandus)—from the Early Holocene of northern Europe to reconstruct their dietary habits and pattern of habitat use in conditions of low human influence. Carbon and nitrogen isotopic compositions in collagen of the ungulate species in northern central Europe during the Early Holocene showed significant differences in the habitat use and the diet of these herbivores. The values of the δ 13C and δ 15N isotopes reflected the use of open habitats by bison, with their diet intermediate between that of aurochs (grazer) and of moose (browser). Our results show that, despite the partial overlap in carbon and nitrogen isotopic values of some species, Early Holocene large ungulates avoided competition by selection of different habitats or different food sources within similar environments. Although Early Holocene bison and Late Pleistocene steppe bison utilized open habitats, their diets were significantly different, as reflected by their δ 15N values. Additional isotopic analyses show that modern populations of European bison utilize much more forested habitats than Early Holocene bison, which supports the refugee status of the species.

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          Global patterns of foliar nitrogen isotopes and their relationships with climate, mycorrhizal fungi, foliar nutrient concentrations, and nitrogen availability.

          Ratios of nitrogen (N) isotopes in leaves could elucidate underlying patterns of N cycling across ecological gradients. To better understand global-scale patterns of N cycling, we compiled data on foliar N isotope ratios (delta(15)N), foliar N concentrations, mycorrhizal type and climate for over 11,000 plants worldwide. Arbuscular mycorrhizal, ectomycorrhizal, and ericoid mycorrhizal plants were depleted in foliar delta(15)N by 2 per thousand, 3.2 per thousand, 5.9 per thousand, respectively, relative to nonmycorrhizal plants. Foliar delta(15)N increased with decreasing mean annual precipitation and with increasing mean annual temperature (MAT) across sites with MAT >or= -0.5 degrees C, but was invariant with MAT across sites with MAT < -0.5 degrees C. In independent landscape-level to regional-level studies, foliar delta(15)N increased with increasing N availability; at the global scale, foliar delta(15)N increased with increasing foliar N concentrations and decreasing foliar phosphorus (P) concentrations. Together, these results suggest that warm, dry ecosystems have the highest N availability, while plants with high N concentrations, on average, occupy sites with higher N availability than plants with low N concentrations. Global-scale comparisons of other components of the N cycle are still required for better mechanistic understanding of the determinants of variation in foliar delta(15)N and ultimately global patterns in N cycling.
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            Global patterns in leaf 13C discrimination and implications for studies of past and future climate.

            Fractionation of carbon isotopes by plants during CO(2) uptake and fixation (Delta(leaf)) varies with environmental conditions, but quantitative patterns of Delta(leaf) across environmental gradients at the global scale are lacking. This impedes interpretation of variability in ancient terrestrial organic matter, which encodes climatic and ecological signals. To address this problem, we converted 3,310 published leaf delta(13)C values into mean Delta(leaf) values for 334 woody plant species at 105 locations (yielding 570 species-site combinations) representing a wide range of environmental conditions. Our analyses reveal a strong positive correlation between Delta(leaf) and mean annual precipitation (MAP; R(2) = 0.55), mirroring global trends in gross primary production and indicating stomatal constraints on leaf gas-exchange, mediated by water supply, are the dominant control of Delta(leaf) at large spatial scales. Independent of MAP, we show a lesser, negative effect of altitude on Delta(leaf) and minor effects of temperature and latitude. After accounting for these factors, mean Delta(leaf) of evergreen gymnosperms is lower (by 1-2.7 per thousand) than for other woody plant functional types (PFT), likely due to greater leaf-level water-use efficiency. Together, environmental and PFT effects contribute to differences in mean Delta(leaf) of up to 6 per thousand between biomes. Coupling geologic indicators of ancient precipitation and PFT (or biome) with modern Delta(leaf) patterns has potential to yield more robust reconstructions of atmospheric delta(13)C values, leading to better constraints on past greenhouse-gas perturbations. Accordingly, we estimate a 4.6 per thousand decline in the delta(13)C of atmospheric CO(2) at the onset of the Paleocene-Eocene Thermal Maximum, an abrupt global warming event approximately 55.8 Ma.
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              Conservation paleobiology: putting the dead to work.

              Geohistorical data and analyses are playing an increasingly important role in conservation biology practice and policy. In this review, we discuss examples of how the near-time and deep-time fossil record can be used to understand the ecological and evolutionary responses of species to changes in their environment. We show that beyond providing crucial baseline data, the conservation paleobiology perspective helps us to identify which species will be most vulnerable and what kinds of responses will be most common. We stress that inclusion of geohistorical data in our decision-making process provides a more scientifically robust basis for conservation policies than those dependent on short-term observations alone. © 2010 Elsevier Ltd. All rights reserved.
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                Author and article information

                Contributors
                Role: Academic Editor
                Journal
                PLoS One
                PLoS ONE
                plos
                plosone
                PLoS ONE
                Public Library of Science (San Francisco, CA USA )
                1932-6203
                11 February 2015
                2015
                : 10
                : 2
                : e0115090
                Affiliations
                [1 ]Fachbereich Geowissenschaften, Forschungsbereich Paläobiologie, Universität Tübingen, Hölderlinstr. 12, D-72074 Tübingen, Germany
                [2 ]Senckenberg Center for Human Evolution and Palaeoecology (HEP), Universität Tübingen, Hölderlinstr. 12, D-72074 Tübingen, Germany
                [3 ]Mammal Research Institute Polish Academy of Sciences, Gen. Waszkiewicza 1c, 17-230 Białowieża, Poland
                [4 ]Centre for Baltic and Scandinavian Archaeology (ZBSA), Schloss Gottorf, D-24837 Schleswig, Germany
                NYIT College of Osteopathic Medicine, UNITED STATES
                Author notes

                Competing Interests: The authors have declared that no competing interests exist.

                Conceived and designed the experiments: EHK RK HB DGD. Performed the experiments: EHK HB DGD RK. Analyzed the data: EHK HB RK. Contributed reagents/materials/analysis tools: EHK HB RK US DGD. Wrote the paper: EHK HB RK.

                Article
                PONE-D-14-34609
                10.1371/journal.pone.0115090
                4324907
                25671634
                2b0d1546-7ecf-4978-bae0-851c832c5d2a
                Copyright @ 2015

                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
                : 1 August 2014
                : 18 November 2014
                Page count
                Figures: 5, Tables: 2, Pages: 19
                Funding
                This study was financed by the Polish National Science Centre grant no. N N304 301940 (to RK) and the budget of the Mammal Research Institute PAS in Białowieża (to RK and EHK). The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.
                Categories
                Research Article
                Custom metadata
                All relevant data are within the paper and its Supporting Information files.

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