Evolution of High Tooth Replacement Rates in Sauropod Dinosaurs
Publication Date
July 17, 2013
Journal
PLOS ONE
Authors
Michael D. D’emic, John A. Whitlock, Kathlyn M. Smith, Daniel C. Fisher, et al
Volume
8
Issue
7
Pages
e69235
DOI
https://dx.plos.org/10.1371/journal.pone.0069235
Publisher URL
http://journals.plos.org/plosone/article?id=10.1371%2Fjournal.pone.0069235
PubMed
http://www.ncbi.nlm.nih.gov/pubmed/23874921
PubMed Central
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC3714237
Europe PMC
http://europepmc.org/abstract/MED/23874921
Web of Science
000322000600047
Scopus
84880426659
Mendeley
http://www.mendeley.com/research/evolution-high-tooth-replacement-rates-sauropod-dinosaurs
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{"title"=>"Evolution of High Tooth Replacement Rates in Sauropod Dinosaurs", "type"=>"journal", "authors"=>[{"first_name"=>"Michael D.", "last_name"=>"D'Emic", "scopus_author_id"=>"26532443000"}, {"first_name"=>"John A.", "last_name"=>"Whitlock", "scopus_author_id"=>"7102828707"}, {"first_name"=>"Kathlyn M.", "last_name"=>"Smith", "scopus_author_id"=>"37056787400"}, {"first_name"=>"Daniel C.", "last_name"=>"Fisher", "scopus_author_id"=>"7403343411"}, {"first_name"=>"Jeffrey A.", "last_name"=>"Wilson", "scopus_author_id"=>"7407983842"}], "year"=>2013, "source"=>"PLoS ONE", "identifiers"=>{"sgr"=>"84880426659", "pmid"=>"23874921", "isbn"=>"1932-6203 (Electronic)\\r1932-6203 (Linking)", "pui"=>"369378588", "issn"=>"19326203", "scopus"=>"2-s2.0-84880426659", "doi"=>"10.1371/journal.pone.0069235"}, "id"=>"186c0633-0120-378d-87f5-70d0fbf5d7a7", "abstract"=>"BACKGROUND: Tooth replacement rate can be calculated in extinct animals by counting incremental lines of deposition in tooth dentin. Calculating this rate in several taxa allows for the study of the evolution of tooth replacement rate. Sauropod dinosaurs, the largest terrestrial animals that ever evolved, exhibited a diversity of tooth sizes and shapes, but little is known about their tooth replacement rates. METHODOLOGY/PRINCIPAL FINDINGS: We present tooth replacement rate, formation time, crown volume, total dentition volume, and enamel thickness for two coexisting but distantly related and morphologically disparate sauropod dinosaurs Camarasaurus and Diplodocus. Individual tooth formation time was determined by counting daily incremental lines in dentin. Tooth replacement rate is calculated as the difference between the number of days recorded in successive replacement teeth. Each tooth family in Camarasaurus has a maximum of three replacement teeth, whereas each Diplodocus tooth family has up to five. Tooth formation times are about 1.7 times longer in Camarasaurus than in Diplodocus (315 vs. 185 days). Average tooth replacement rate in Camarasaurus is about one tooth every 62 days versus about one tooth every 35 days in Diplodocus. Despite slower tooth replacement rates in Camarasaurus, the volumetric rate of Camarasaurus tooth replacement is 10 times faster than in Diplodocus because of its substantially greater tooth volumes. A novel method to estimate replacement rate was developed and applied to several other sauropodomorphs that we were not able to thin section. CONCLUSIONS/SIGNIFICANCE: Differences in tooth replacement rate among sauropodomorphs likely reflect disparate feeding strategies and/or food choices, which would have facilitated the coexistence of these gigantic herbivores in one ecosystem. Early neosauropods are characterized by high tooth replacement rates (despite their large tooth size), and derived titanosaurs and diplodocoids independently evolved the highest known tooth replacement rates among archosaurs.", "link"=>"http://www.mendeley.com/research/evolution-high-tooth-replacement-rates-sauropod-dinosaurs", "reader_count"=>54, "reader_count_by_academic_status"=>{"Unspecified"=>1, "Professor > Associate Professor"=>5, "Librarian"=>1, "Researcher"=>9, "Student > Doctoral Student"=>3, "Student > Ph. D. Student"=>14, "Student > Postgraduate"=>1, "Other"=>5, "Student > Master"=>5, "Student > Bachelor"=>7, "Lecturer"=>1, "Professor"=>2}, "reader_count_by_user_role"=>{"Unspecified"=>1, "Professor > Associate Professor"=>5, "Librarian"=>1, "Researcher"=>9, "Student > Doctoral Student"=>3, "Student > Ph. D. Student"=>14, "Student > Postgraduate"=>1, "Other"=>5, "Student > Master"=>5, "Student > Bachelor"=>7, "Lecturer"=>1, "Professor"=>2}, "reader_count_by_subject_area"=>{"Engineering"=>1, "Unspecified"=>1, "Agricultural and Biological Sciences"=>21, "Arts and Humanities"=>1, "Computer Science"=>2, "Earth and Planetary Sciences"=>28}, "reader_count_by_subdiscipline"=>{"Engineering"=>{"Engineering"=>1}, "Earth and Planetary Sciences"=>{"Earth and Planetary Sciences"=>28}, "Agricultural and Biological Sciences"=>{"Agricultural and Biological Sciences"=>21}, "Computer Science"=>{"Computer Science"=>2}, "Unspecified"=>{"Unspecified"=>1}, "Arts and Humanities"=>{"Arts and Humanities"=>1}}, "reader_count_by_country"=>{"Argentina"=>1, "Spain"=>2}, "group_count"=>0}

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Figshare

  • {"files"=>["https://ndownloader.figshare.com/files/1121301"], "description"=>"<p>Thin sections of <i>Camarasaurus</i> (<b>A</b>, <b>C</b>) and <i>Diplodocus</i> (<b>B</b>, <b>D</b>) premaxillary teeth showing incremental lines of von Ebner (white arrowheads) in dentin. Teeth are oriented with their long axis horizontal and the occlusal surface directed to the right. <b>A</b> shows the tip of tooth 3iii of <i>Camarasaurus</i>, and <b>B</b> shows the tip of tooth 4iv of <i>Diplodocus</i>. <b>C</b> and <b>D</b> are enlarged images of one ‘limb’ of tooth 3ii and 4iii, respectively. Abbreviations: <b>edj</b>, enamel-dentin junction; <b>en</b>, enamel; <b>pc</b>, pulp cavity. [planned for page width].</p>", "links"=>[], "tags"=>["Evolutionary biology", "Paleontology", "paleobiology", "paleoecology", "Vertebrate paleontology", "Evolutionary ecology", "histology", "Zoology", "Comparative anatomy", "sauropod", "dinosaurs"], "article_id"=>747396, "categories"=>["Biological Sciences", "Earth and Environmental Sciences"], "users"=>["Michael D. D’Emic", "John A. Whitlock", "Kathlyn M. Smith", "Daniel C. Fisher", "Jeffrey A. Wilson"], "doi"=>["https://dx.doi.org/10.1371/journal.pone.0069235.g001"], "stats"=>{"downloads"=>0, "page_views"=>0, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Dental_histology_of_the_sauropod_dinosaurs_Camarasaurus_and_Diplodocus_/747396", "title"=>"Dental histology of the sauropod dinosaurs <i>Camarasaurus</i> and <i>Diplodocus</i>.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2013-07-17 02:24:41"}
  • {"files"=>["https://ndownloader.figshare.com/files/1121306"], "description"=>"<p>Reconstructed skulls (<b>A</b>, <b>D</b>) and premaxillary teeth (<b>B</b>, <b>C</b>) of <i>Camarasaurus</i> (<b>A</b>, <b>B</b>) and <i>Diplodocus</i> (<b>C</b>, <b>D</b>). <b>B</b> and <b>C</b> include CT-generated sagittal and transverse sections of premaxillary alveoli and photographs of thin sections of <i>Camarasaurus</i> (UMNH 5527) and <i>Diplodocus</i> (YMP 4677). Premaxillae show replacement teeth in each of the four alveoli adjacent to the symphysis labelled by their position along the tooth row (1–4) and their position in the replacement sequence at each tooth position (i–v). Sagittal sections in <b>B</b> and <b>C</b> were taken at premaxillary tooth position 4 in <i>Camarasaurus</i> and premaxillary tooth position 1 in <i>Diplodocus</i>. The symphysis faces the bottom of the page in transverse sections. Photographs of thin sections of <i>Diplodocus</i> and <i>Camarasaurus</i> teeth show enamel (<b>en</b>), the pulp cavity (<b>pc</b>), daily-deposited incremental lines of von Ebner (arrowheads mark every other line) in the dentin (<b>den</b>), and the crown-root junction (<b>crj</b>). The 20 mm scale bar is for the premaxilla and tooth images in (<b>B</b>); 10 mm scale bar is for premaxilla and tooth images in (<b>C</b>). Skull reconstructions are from <a href=\"http://www.plosone.org/article/info:doi/10.1371/journal.pone.0069235#pone.0069235-Wilson1\" target=\"_blank\">[19]</a>, <a href=\"http://www.plosone.org/article/info:doi/10.1371/journal.pone.0069235#pone.0069235-Whitlock2\" target=\"_blank\">[46]</a>[planned for page width].</p>", "links"=>[], "tags"=>["Evolutionary biology", "Paleontology", "paleobiology", "paleoecology", "Vertebrate paleontology", "Evolutionary ecology", "histology", "Zoology", "Comparative anatomy", "sauropod", "dinosaurs"], "article_id"=>747397, "categories"=>["Biological Sciences", "Earth and Environmental Sciences"], "users"=>["Michael D. D’Emic", "John A. Whitlock", "Kathlyn M. Smith", "Daniel C. Fisher", "Jeffrey A. Wilson"], "doi"=>["https://dx.doi.org/10.1371/journal.pone.0069235.g002"], "stats"=>{"downloads"=>0, "page_views"=>0, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Tooth_replacement_in_the_sauropod_dinosaurs_Camarasaurus_and_Diplodocus_/747397", "title"=>"Tooth replacement in the sauropod dinosaurs <i>Camarasaurus</i> and <i>Diplodocus</i>.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2013-07-17 02:24:41"}
  • {"files"=>["https://ndownloader.figshare.com/files/1121308"], "description"=>"<p>The light gray field indicates taxa that have at least three replacement teeth at each tooth position; dark gray field encapsulates taxa that have narrow tooth crowns. Silhouettes along the top of the cladogram show the number and size of replacement teeth in one tooth position. These include (from left to right): <i>Patagosaurus</i> (MPEF-PV 1670), <i>Mamenchisaurus </i><a href=\"http://www.plosone.org/article/info:doi/10.1371/journal.pone.0069235#pone.0069235-Ouyang1\" target=\"_blank\">[47]</a>, <i>Diplodocus</i> (this study), <i>Nigersaurus</i> [Sereno, Wilson, Witmer, Whitlock, Maga, Ide and Rowe, unpublished data], <i>Camarasaurus</i> (this study), and the Río Negro titanosaur (MPCA-79) <a href=\"http://www.plosone.org/article/info:doi/10.1371/journal.pone.0069235#pone.0069235-Coria1\" target=\"_blank\">[48]</a>. Number of replacement teeth is unknown in Brachiosauridae, but the taxon is optimized to have had at least three. Cladogram based on <a href=\"http://www.plosone.org/article/info:doi/10.1371/journal.pone.0069235#pone.0069235-Wilson2\" target=\"_blank\">[30]</a> with the addition of <i>Tazoudasaurus </i><a href=\"http://www.plosone.org/article/info:doi/10.1371/journal.pone.0069235#pone.0069235-Allain1\" target=\"_blank\">[49]</a> and <i>Bonitasaura </i><a href=\"http://www.plosone.org/article/info:doi/10.1371/journal.pone.0069235#pone.0069235-Gallina1\" target=\"_blank\">[50]</a>. [planned for column width].</p>", "links"=>[], "tags"=>["Evolutionary biology", "Paleontology", "paleobiology", "paleoecology", "Vertebrate paleontology", "Evolutionary ecology", "histology", "Zoology", "Comparative anatomy", "sauropodomorphs", "optimization", "elevated"], "article_id"=>747398, "categories"=>["Biological Sciences", "Earth and Environmental Sciences"], "users"=>["Michael D. D’Emic", "John A. Whitlock", "Kathlyn M. Smith", "Daniel C. Fisher", "Jeffrey A. Wilson"], "doi"=>["https://dx.doi.org/10.1371/journal.pone.0069235.g003"], "stats"=>{"downloads"=>0, "page_views"=>0, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Cladogram_of_sauropodomorphs_showing_the_optimization_of_key_features_related_to_elevated_tooth_replacement_rates_/747398", "title"=>"Cladogram of sauropodomorphs showing the optimization of key features related to elevated tooth replacement rates.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2013-07-17 02:24:41"}
  • {"files"=>["https://ndownloader.figshare.com/files/1121310"], "description"=>"<p>Abbreviations: UMNH, Utah Museum of Natural History, Salt Lake City, USA; YPM, Yale Peabody Museum, New Haven, USA.</p>", "links"=>[], "tags"=>["Evolutionary biology", "Paleontology", "paleobiology", "paleoecology", "Vertebrate paleontology", "Evolutionary ecology", "histology", "Zoology", "Comparative anatomy"], "article_id"=>747399, "categories"=>["Biological Sciences", "Earth and Environmental Sciences"], "users"=>["Michael D. D’Emic", "John A. Whitlock", "Kathlyn M. Smith", "Daniel C. Fisher", "Jeffrey A. Wilson"], "doi"=>["https://dx.doi.org/10.1371/journal.pone.0069235.t001"], "stats"=>{"downloads"=>0, "page_views"=>0, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Tooth_formation_time_days_and_replacement_rate_1_tooth_X_days_in_Diplodocus_YPM_4677_and_Camarasaurus_UMNH_5527_/747399", "title"=>"Tooth formation time (days) and replacement rate (1 tooth/X days) in <i>Diplodocus</i> (YPM 4677) and <i>Camarasaurus</i> (UMNH 5527).", "pos_in_sequence"=>0, "defined_type"=>3, "published_date"=>"2013-07-17 02:24:41"}
  • {"files"=>["https://ndownloader.figshare.com/files/1121311"], "description"=>"<p>Each value shown is an average of teeth from more than one alveolus at similar stages of development (e.g., ‘ii’ is an average of values for tooth position 2ii, 3ii, 4ii, etc.). See <a href=\"http://www.plosone.org/article/info:doi/10.1371/journal.pone.0069235#pone.0069235.s001\" target=\"_blank\">Raw Data S1</a>.</p>", "links"=>[], "tags"=>["Evolutionary biology", "Paleontology", "paleobiology", "paleoecology", "Vertebrate paleontology", "Evolutionary ecology", "histology", "Zoology", "Comparative anatomy", "enamel", "thickness", "stages"], "article_id"=>747400, "categories"=>["Biological Sciences", "Earth and Environmental Sciences"], "users"=>["Michael D. D’Emic", "John A. Whitlock", "Kathlyn M. Smith", "Daniel C. Fisher", "Jeffrey A. Wilson"], "doi"=>["https://dx.doi.org/10.1371/journal.pone.0069235.t003"], "stats"=>{"downloads"=>0, "page_views"=>0, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Summary_of_enamel_thickness_mm_in_Diplodocus_YPM_4677_and_Camarasaurus_UMNH_5527_at_different_tooth_developmental_stages_i_v_/747400", "title"=>"Summary of enamel thickness (mm) in <i>Diplodocus</i> (YPM 4677) and <i>Camarasaurus</i> (UMNH 5527) at different tooth developmental stages (i–v).", "pos_in_sequence"=>0, "defined_type"=>3, "published_date"=>"2013-07-17 02:24:41"}
  • {"files"=>["https://ndownloader.figshare.com/files/1121312"], "description"=>"<p>There is a range for <i>Massospondylus</i> tooth replacement rate because estimates were made both using the narrow-crowned and broad-crowned equations. Note the similarity of estimated replacement rates for <i>Camarasaurus</i> and <i>Diplodocus</i> with histologically obtained rates of 62 and 35 days for these taxa, respectively.</p><p>Abbreviations: MNN, Musée National du Niger, Niamey, Niger; MPCA, Museo Provincial Carlos Ameghino, Cipolletti, Argentina; SAM, South African Museum, Ikizo Museums, Cape Town, South Africa; UMNH, Utah Museum of Natural History, Salt Lake City, USA; YPM, Yale Peabody Museum, New Haven, USA; ZDM, Zigong Dinosaur Museum, Zigong, China.</p>", "links"=>[], "tags"=>["Evolutionary biology", "Paleontology", "paleobiology", "paleoecology", "Vertebrate paleontology", "Evolutionary ecology", "histology", "Zoology", "Comparative anatomy", "times", "rates"], "article_id"=>747401, "categories"=>["Biological Sciences", "Earth and Environmental Sciences"], "users"=>["Michael D. D’Emic", "John A. Whitlock", "Kathlyn M. Smith", "Daniel C. Fisher", "Jeffrey A. Wilson"], "doi"=>["https://dx.doi.org/10.1371/journal.pone.0069235.t002"], "stats"=>{"downloads"=>0, "page_views"=>0, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Estimated_tooth_formation_times_ages_and_replacement_rates_in_several_sauropodomorphs_/747401", "title"=>"Estimated tooth formation times (ages) and replacement rates in several sauropodomorphs.", "pos_in_sequence"=>0, "defined_type"=>3, "published_date"=>"2013-07-17 02:24:41"}
  • {"files"=>["https://ndownloader.figshare.com/files/1121314"], "description"=>"<p>Data for sauropods are from this study; other data are from <a href=\"http://www.plosone.org/article/info:doi/10.1371/journal.pone.0069235#pone.0069235-Sereno2\" target=\"_blank\">[6]</a>, <a href=\"http://www.plosone.org/article/info:doi/10.1371/journal.pone.0069235#pone.0069235-Erickson2\" target=\"_blank\">[12]</a>.</p>", "links"=>[], "tags"=>["Evolutionary biology", "Paleontology", "paleobiology", "paleoecology", "Vertebrate paleontology", "Evolutionary ecology", "histology", "Zoology", "Comparative anatomy", "rates"], "article_id"=>747402, "categories"=>["Biological Sciences", "Earth and Environmental Sciences"], "users"=>["Michael D. D’Emic", "John A. Whitlock", "Kathlyn M. Smith", "Daniel C. Fisher", "Jeffrey A. Wilson"], "doi"=>["https://dx.doi.org/10.1371/journal.pone.0069235.t004"], "stats"=>{"downloads"=>0, "page_views"=>0, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Tooth_replacement_rates_days_for_archosaurs_/747402", "title"=>"Tooth replacement rates (days) for archosaurs.", "pos_in_sequence"=>0, "defined_type"=>3, "published_date"=>"2013-07-17 02:24:41"}
  • {"files"=>["https://ndownloader.figshare.com/files/1121319", "https://ndownloader.figshare.com/files/1121320", "https://ndownloader.figshare.com/files/1121322", "https://ndownloader.figshare.com/files/1121323"], "description"=>"<div><p>Background</p><p>Tooth replacement rate can be calculated in extinct animals by counting incremental lines of deposition in tooth dentin. Calculating this rate in several taxa allows for the study of the evolution of tooth replacement rate. Sauropod dinosaurs, the largest terrestrial animals that ever evolved, exhibited a diversity of tooth sizes and shapes, but little is known about their tooth replacement rates.</p><p>Methodology/Principal Findings</p><p>We present tooth replacement rate, formation time, crown volume, total dentition volume, and enamel thickness for two coexisting but distantly related and morphologically disparate sauropod dinosaurs <i>Camarasaurus</i> and <i>Diplodocus</i>. Individual tooth formation time was determined by counting daily incremental lines in dentin. Tooth replacement rate is calculated as the difference between the number of days recorded in successive replacement teeth. Each tooth family in <i>Camarasaurus</i> has a maximum of three replacement teeth, whereas each <i>Diplodocus</i> tooth family has up to five. Tooth formation times are about 1.7 times longer in <i>Camarasaurus</i> than in <i>Diplodocus</i> (315 vs. 185 days). Average tooth replacement rate in <i>Camarasaurus</i> is about one tooth every 62 days versus about one tooth every 35 days in <i>Diplodocus</i>. Despite slower tooth replacement rates in <i>Camarasaurus</i>, the volumetric rate of <i>Camarasaurus</i> tooth replacement is 10 times faster than in <i>Diplodocus</i> because of its substantially greater tooth volumes. A novel method to estimate replacement rate was developed and applied to several other sauropodomorphs that we were not able to thin section.</p><p>Conclusions/Significance</p><p>Differences in tooth replacement rate among sauropodomorphs likely reflect disparate feeding strategies and/or food choices, which would have facilitated the coexistence of these gigantic herbivores in one ecosystem. Early neosauropods are characterized by high tooth replacement rates (despite their large tooth size), and derived titanosaurs and diplodocoids independently evolved the highest known tooth replacement rates among archosaurs.</p></div>", "links"=>[], "tags"=>["Evolutionary biology", "Paleontology", "paleobiology", "paleoecology", "Vertebrate paleontology", "Evolutionary ecology", "histology", "Zoology", "Comparative anatomy", "rates", "sauropod"], "article_id"=>747405, "categories"=>["Biological Sciences", "Earth and Environmental Sciences"], "users"=>["Michael D. D’Emic", "John A. Whitlock", "Kathlyn M. Smith", "Daniel C. Fisher", "Jeffrey A. Wilson"], "doi"=>["https://dx.doi.org/10.1371/journal.pone.0069235.s001", "https://dx.doi.org/10.1371/journal.pone.0069235.s002", "https://dx.doi.org/10.1371/journal.pone.0069235.s003", "https://dx.doi.org/10.1371/journal.pone.0069235.s004"], "stats"=>{"downloads"=>0, "page_views"=>0, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Evolution_of_High_Tooth_Replacement_Rates_in_Sauropod_Dinosaurs_/747405", "title"=>"Evolution of High Tooth Replacement Rates in Sauropod Dinosaurs", "pos_in_sequence"=>0, "defined_type"=>4, "published_date"=>"2013-07-17 02:24:41"}

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Relative Metric

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