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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{"title"=>"European bison as a refugee species? Evidence from isotopic data on Early Holocene bison and other large herbivores in northern Europe", "type"=>"journal", "authors"=>[{"first_name"=>"Hervé", "last_name"=>"Bocherens", "scopus_author_id"=>"7006654386"}, {"first_name"=>"Emilia", "last_name"=>"Hofman-Kamińska", "scopus_author_id"=>"55319014400"}, {"first_name"=>"Dorothée G.", "last_name"=>"Drucker", "scopus_author_id"=>"7202919808"}, {"first_name"=>"Ulrich", "last_name"=>"Schmölcke", "scopus_author_id"=>"14819778100"}, {"first_name"=>"Rafał", "last_name"=>"Kowalczyk", "scopus_author_id"=>"7006215511"}], "year"=>2015, "source"=>"PLoS ONE", "identifiers"=>{"sgr"=>"84923169873", "doi"=>"10.1371/journal.pone.0115090", "pui"=>"602263348", "pmid"=>"25671634", "scopus"=>"2-s2.0-84923169873", "issn"=>"19326203", "isbn"=>"1932-6203 (Electronic)\r1932-6203 (Linking)"}, "id"=>"682d98c3-03d7-35cd-8d40-3f017b20ad7f", "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 (δ13C and δ15N) 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 δ13C and δ15N 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 δ15N 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.", "link"=>"http://www.mendeley.com/research/european-bison-refugee-species-evidence-isotopic-data-early-holocene-bison-other-large-herbivores-no", "reader_count"=>61, "reader_count_by_academic_status"=>{"Professor > Associate Professor"=>2, "Librarian"=>1, "Researcher"=>16, "Student > Doctoral Student"=>2, "Student > Ph. D. Student"=>17, "Student > Postgraduate"=>2, "Student > Master"=>6, "Other"=>3, "Student > Bachelor"=>8, "Lecturer"=>1, "Lecturer > Senior Lecturer"=>1, "Professor"=>2}, "reader_count_by_user_role"=>{"Professor > Associate Professor"=>2, "Librarian"=>1, "Researcher"=>16, "Student > Doctoral Student"=>2, "Student > Ph. D. Student"=>17, "Student > Postgraduate"=>2, "Student > Master"=>6, "Other"=>3, "Student > Bachelor"=>8, "Lecturer"=>1, "Lecturer > Senior Lecturer"=>1, "Professor"=>2}, "reader_count_by_subject_area"=>{"Unspecified"=>2, "Environmental Science"=>13, "Biochemistry, Genetics and Molecular Biology"=>2, "Agricultural and Biological Sciences"=>27, "Arts and Humanities"=>5, "Business, Management and Accounting"=>1, "Psychology"=>2, "Social Sciences"=>2, "Earth and Planetary Sciences"=>7}, "reader_count_by_subdiscipline"=>{"Social Sciences"=>{"Social Sciences"=>2}, "Psychology"=>{"Psychology"=>2}, "Earth and Planetary Sciences"=>{"Earth and Planetary Sciences"=>7}, "Agricultural and Biological Sciences"=>{"Agricultural and Biological Sciences"=>27}, "Business, Management and Accounting"=>{"Business, Management and Accounting"=>1}, "Biochemistry, Genetics and Molecular Biology"=>{"Biochemistry, Genetics and Molecular Biology"=>2}, "Unspecified"=>{"Unspecified"=>2}, "Environmental Science"=>{"Environmental Science"=>13}, "Arts and Humanities"=>{"Arts and Humanities"=>5}}, "reader_count_by_country"=>{"Canada"=>1, "Romania"=>1, "United States"=>1, "Japan"=>1, "Poland"=>1, "United Kingdom"=>1, "Mexico"=>1, "Portugal"=>1}, "group_count"=>3}

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Figshare

  • {"files"=>["https://ndownloader.figshare.com/files/1893674"], "description"=>"<p>Shaded area denotes range of carbon isotope values characteristic for forest use. Ellipses are plotted in a way to include the extreme points of the range of measured isotopic values and to improve readability of the figure. The data used to generate the figure can be found in <a href=\"http://www.plosone.org/article/info:doi/10.1371/journal.pone.0115090#pone.0115090.t001\" target=\"_blank\">Table 1</a> and <a href=\"http://www.plosone.org/article/info:doi/10.1371/journal.pone.0115090#pone.0115090.s001\" target=\"_blank\">S1 Table</a>.</p>", "links"=>[], "tags"=>["bison", "Pleistocene steppe bison", "European bison", "habitat use", "refugee species concept", "Holocene bison", "diet"], "article_id"=>1306048, "categories"=>["Biological Sciences", "Ecology"], "users"=>["Hervé Bocherens", "Emilia Hofman-Kamińska", "Dorothée G. Drucker", "Ulrich Schmölcke", "Rafał Kowalczyk"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0115090.g002", "stats"=>{"downloads"=>3, "page_views"=>26, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Stable_13_C_coll_and_948_15_N_coll_isotope_values_for_moose_Alces_alces_aurochs_Bos_primigenius_and_European_bison_Bison_bonasus_in_Early_Holocene_in_northern_Europe_/1306048", "title"=>"Stable δ<sup>13</sup>C<sub>coll</sub> and δ<sup>15</sup>N<sub>coll</sub> isotope values for moose (<i>Alces alces</i>), aurochs (<i>Bos primigenius</i>) and European bison (<i>Bison bonasus</i>) in Early Holocene in northern Europe.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2015-02-11 03:02:49"}
  • {"files"=>["https://ndownloader.figshare.com/files/1893683"], "description"=>"<p><sup>a</sup>The following chronozones are used Younger Dryas (12,900–11,600 cal BP), Preboreal (11,600–10,640 cal. BP).</p><p><sup>b</sup>The information about datings was previously published by Hedges et al. [<a href=\"http://www.plosone.org/article/info:doi/10.1371/journal.pone.0115090#pone.0115090.ref065\" target=\"_blank\">65</a>], Bratlund [<a href=\"http://www.plosone.org/article/info:doi/10.1371/journal.pone.0115090#pone.0115090.ref067\" target=\"_blank\">67</a>], Aaris-Sørensen et al. [<a href=\"http://www.plosone.org/article/info:doi/10.1371/journal.pone.0115090#pone.0115090.ref004\" target=\"_blank\">4</a>] and Aaris-Sørensen [<a href=\"http://www.plosone.org/article/info:doi/10.1371/journal.pone.0115090#pone.0115090.ref066\" target=\"_blank\">66</a>].</p><p><sup>c</sup>Radiocarbon dates were calibrated using OxCal v4.2.3 with IntCal13 atmospheric curve [<a href=\"http://www.plosone.org/article/info:doi/10.1371/journal.pone.0115090#pone.0115090.ref083\" target=\"_blank\">83</a>], [<a href=\"http://www.plosone.org/article/info:doi/10.1371/journal.pone.0115090#pone.0115090.ref084\" target=\"_blank\">84</a>].</p><p>Results of the isotopic analysis of the collagen extracted from bones of bison, aurochs and moose, selected from different sites in northern central Europe with information on chronology and direct datings.</p>", "links"=>[], "tags"=>["bison", "Pleistocene steppe bison", "European bison", "habitat use", "refugee species concept", "Holocene bison", "diet"], "article_id"=>1306057, "categories"=>["Biological Sciences", "Ecology"], "users"=>["Hervé Bocherens", "Emilia Hofman-Kamińska", "Dorothée G. Drucker", "Ulrich Schmölcke", "Rafał Kowalczyk"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0115090.t001", "stats"=>{"downloads"=>1, "page_views"=>24, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Results_of_the_isotopic_analysis_of_the_collagen_extracted_from_bones_of_bison_aurochs_and_moose_selected_from_different_sites_in_northern_central_Europe_with_information_on_chronology_and_direct_datings_/1306057", "title"=>"Results of the isotopic analysis of the collagen extracted from bones of bison, aurochs and moose, selected from different sites in northern central Europe with information on chronology and direct datings.", "pos_in_sequence"=>0, "defined_type"=>3, "published_date"=>"2015-02-11 03:02:49"}
  • {"files"=>["https://ndownloader.figshare.com/files/1893682"], "description"=>"<p>(* denote statistically significant differences for p between 0.05 and 0.01, **—for p < 0.01). Boxes show the median, upper and lower quartiles, while the whiskers show the range of the data. The data used to generate the figure can be found in <a href=\"http://www.plosone.org/article/info:doi/10.1371/journal.pone.0115090#pone.0115090.t001\" target=\"_blank\">Table 1</a> and <a href=\"http://www.plosone.org/article/info:doi/10.1371/journal.pone.0115090#pone.0115090.s003\" target=\"_blank\">S3 Table</a>.</p>", "links"=>[], "tags"=>["bison", "Pleistocene steppe bison", "European bison", "habitat use", "refugee species concept", "Holocene bison", "diet"], "article_id"=>1306056, "categories"=>["Biological Sciences", "Ecology"], "users"=>["Hervé Bocherens", "Emilia Hofman-Kamińska", "Dorothée G. Drucker", "Ulrich Schmölcke", "Rafał Kowalczyk"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0115090.g005", "stats"=>{"downloads"=>1, "page_views"=>60, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Box_plots_of_stable_13_C_coll_values_for_Early_Holocene_Bison_bonasus_compared_to_modern_populations_of_European_Bison_bonasus_and_American_bison_Bison_bison_bison_living_in_forest_habitats_/1306056", "title"=>"Box plots of stable δ<sup>13</sup>C<sub>coll</sub> values for Early Holocene <i>Bison bonasus</i>, compared to modern populations of European (<i>Bison bonasus</i>) and American bison (<i>Bison bison bison</i>) living in forest habitats.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2015-02-11 03:02:49"}
  • {"files"=>["https://ndownloader.figshare.com/files/1893685", "https://ndownloader.figshare.com/files/1893686", "https://ndownloader.figshare.com/files/1893687", "https://ndownloader.figshare.com/files/1893688"], "description"=>"<div><p>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 (<i>Bison bonasus</i>)—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<sup>13</sup>C and δ<sup>15</sup>N) in radiocarbon dated skeletal remains of European bison and other large herbivores—aurochs (<i>Bos primigenius</i>), moose (<i>Alces alces</i>), and reindeer (<i>Rangifer tarandus</i>)—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<sup>13</sup>C and δ<sup>15</sup>N 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<sup>15</sup>N 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.</p></div>", "links"=>[], "tags"=>["bison", "Pleistocene steppe bison", "European bison", "habitat use", "refugee species concept", "Holocene bison", "diet"], "article_id"=>1306059, "categories"=>["Biological Sciences", "Ecology"], "users"=>["Hervé Bocherens", "Emilia Hofman-Kamińska", "Dorothée G. Drucker", "Ulrich Schmölcke", "Rafał Kowalczyk"], "doi"=>["https://dx.doi.org/10.1371/journal.pone.0115090.s001", "https://dx.doi.org/10.1371/journal.pone.0115090.s002", "https://dx.doi.org/10.1371/journal.pone.0115090.s003", "https://dx.doi.org/10.1371/journal.pone.0115090.s004"], "stats"=>{"downloads"=>16, "page_views"=>29, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_European_Bison_as_a_Refugee_Species_Evidence_from_Isotopic_Data_on_Early_Holocene_Bison_and_Other_Large_Herbivores_in_Northern_Europe_/1306059", "title"=>"European Bison as a Refugee Species? Evidence from Isotopic Data on Early Holocene Bison and Other Large Herbivores in Northern Europe", "pos_in_sequence"=>0, "defined_type"=>4, "published_date"=>"2015-02-11 03:02:49"}
  • {"files"=>["https://ndownloader.figshare.com/files/1893684"], "description"=>"<p>Insignificance at p > 0.05 is indicated in normal font for Mann-Whitney—Wilcoxon test. Bold indicates significant differences. Abbreviations: N = number of specimens.</p><p>Pairwise differences for δ<sup>13</sup>C carbon and δ<sup>15</sup>N nitrogen isotope values between species in Early Holocene and Pleistocene and between samples of modern <i>Bison bonasus</i> (Poland) and <i>Bison bison</i> (Prince Albert National Park, Canada) as well as between modern and Early Holocene Bison.</p>", "links"=>[], "tags"=>["bison", "Pleistocene steppe bison", "European bison", "habitat use", "refugee species concept", "Holocene bison", "diet"], "article_id"=>1306058, "categories"=>["Biological Sciences", "Ecology"], "users"=>["Hervé Bocherens", "Emilia Hofman-Kamińska", "Dorothée G. Drucker", "Ulrich Schmölcke", "Rafał Kowalczyk"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0115090.t002", "stats"=>{"downloads"=>1, "page_views"=>21, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Pairwise_differences_for_13_C_carbon_and_948_15_N_nitrogen_isotope_values_between_species_in_Early_Holocene_and_Pleistocene_and_between_samples_of_modern_Bison_bonasus_Poland_and_Bison_bison_Prince_Albert_National_Park_Canada_as_well_as_between_modern_an/1306058", "title"=>"Pairwise differences for δ<sup>13</sup>C carbon and δ<sup>15</sup>N nitrogen isotope values between species in Early Holocene and Pleistocene and between samples of modern <i>Bison bonasus</i> (Poland) and <i>Bison bison</i> (Prince Albert National Park, Canada) as well as between modern and Early Holocene Bison.", "pos_in_sequence"=>0, "defined_type"=>3, "published_date"=>"2015-02-11 03:02:49"}
  • {"files"=>["https://ndownloader.figshare.com/files/1893679"], "description"=>"<p>(* denote statistically significant differences for p between 0.05 and 0.01, **—for p < 0.01). Boxes show the median, upper and lower quartiles, while the whiskers show the range of the data. The data used to generate the figure can be found in <a href=\"http://www.plosone.org/article/info:doi/10.1371/journal.pone.0115090#pone.0115090.t001\" target=\"_blank\">Table 1</a>, <a href=\"http://www.plosone.org/article/info:doi/10.1371/journal.pone.0115090#pone.0115090.s001\" target=\"_blank\">S1</a> and <a href=\"http://www.plosone.org/article/info:doi/10.1371/journal.pone.0115090#pone.0115090.s002\" target=\"_blank\">S2</a> Tables.</p>", "links"=>[], "tags"=>["bison", "Pleistocene steppe bison", "European bison", "habitat use", "refugee species concept", "Holocene bison", "diet"], "article_id"=>1306053, "categories"=>["Biological Sciences", "Ecology"], "users"=>["Hervé Bocherens", "Emilia Hofman-Kamińska", "Dorothée G. Drucker", "Ulrich Schmölcke", "Rafał Kowalczyk"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0115090.g004", "stats"=>{"downloads"=>0, "page_views"=>13, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Comparison_of_13_C_coll_and_948_15_N_coll_values_between_European_bison_and_aurochs_in_Early_Holocene_and_Pleistocene_steppe_bison_and_aurochs_Belgium_and_Southwestern_France_/1306053", "title"=>"Comparison of δ<sup>13</sup>C<sub>coll</sub> and δ<sup>15</sup>N<sub>coll</sub> values between European bison and aurochs in Early Holocene and Pleistocene steppe bison and aurochs (Belgium and Southwestern France).", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2015-02-11 03:02:49"}
  • {"files"=>["https://ndownloader.figshare.com/files/1893675"], "description"=>"<p>(* denote statistically significant differences for p between 0.05 and 0.01, **—for p < 0.01). Boxes show the median, upper and lower quartiles while, the whiskers show the range of the data. The data used to generate the figure can be found in <a href=\"http://www.plosone.org/article/info:doi/10.1371/journal.pone.0115090#pone.0115090.t001\" target=\"_blank\">Table 1</a> and <a href=\"http://www.plosone.org/article/info:doi/10.1371/journal.pone.0115090#pone.0115090.s001\" target=\"_blank\">S1 Table</a>.</p>", "links"=>[], "tags"=>["bison", "Pleistocene steppe bison", "European bison", "habitat use", "refugee species concept", "Holocene bison", "diet"], "article_id"=>1306049, "categories"=>["Biological Sciences", "Ecology"], "users"=>["Hervé Bocherens", "Emilia Hofman-Kamińska", "Dorothée G. Drucker", "Ulrich Schmölcke", "Rafał Kowalczyk"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0115090.g003", "stats"=>{"downloads"=>1, "page_views"=>13, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Box_plots_of_stable_13_C_coll_and_948_15_N_coll_isotope_values_measured_for_Early_Holocene_moose_aurochs_European_bison_and_reindeer_/1306049", "title"=>"Box plots of stable δ<sup>13</sup>C<sub>coll</sub> and δ<sup>15</sup>N<sub>coll</sub> isotope values measured for Early Holocene moose, aurochs, European bison and reindeer.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2015-02-11 03:02:49"}
  • {"files"=>["https://ndownloader.figshare.com/files/1893673"], "description"=>"<p>Numbers in brackets indicate the number of individuals from the same location. The data used to generate the figure can be found in <a href=\"http://www.plosone.org/article/info:doi/10.1371/journal.pone.0115090#pone.0115090.t001\" target=\"_blank\">Table 1</a> and <a href=\"http://www.plosone.org/article/info:doi/10.1371/journal.pone.0115090#pone.0115090.s001\" target=\"_blank\">S1 Table</a>.</p>", "links"=>[], "tags"=>["bison", "Pleistocene steppe bison", "European bison", "habitat use", "refugee species concept", "Holocene bison", "diet"], "article_id"=>1306047, "categories"=>["Biological Sciences", "Ecology"], "users"=>["Hervé Bocherens", "Emilia Hofman-Kamińska", "Dorothée G. Drucker", "Ulrich Schmölcke", "Rafał Kowalczyk"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0115090.g001", "stats"=>{"downloads"=>1, "page_views"=>26, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Locations_of_analyzed_Early_Holocene_bone_remains_of_Bison_bonasus_Bos_primigenius_Alces_alces_and_Rangifer_tarandus_in_northern_Europe_/1306047", "title"=>"Locations of analyzed Early Holocene bone remains of <i>Bison bonasus</i>, <i>Bos primigenius</i>, <i>Alces alces</i> and <i>Rangifer tarandus</i> in northern Europe.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2015-02-11 03:02:49"}

PMC Usage Stats | Further Information

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  • {"unique-ip"=>"4", "full-text"=>"4", "pdf"=>"1", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2020", "month"=>"6"}
  • {"unique-ip"=>"9", "full-text"=>"9", "pdf"=>"2", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2020", "month"=>"7"}
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  • {"unique-ip"=>"9", "full-text"=>"9", "pdf"=>"4", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2020", "month"=>"9"}

Relative Metric

{"start_date"=>"2015-01-01T00:00:00Z", "end_date"=>"2015-12-31T00:00:00Z", "subject_areas"=>[]}
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