Life History of Rhamphorhynchus Inferred from Bone Histology and the Diversity of Pterosaurian Growth Strategies
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{"title"=>"Life history of rhamphorhynchus inferred from bone histology and the diversity of pterosaurian growth strategies", "type"=>"journal", "authors"=>[{"first_name"=>"Edina", "last_name"=>"Prondvai", "scopus_author_id"=>"35100672300"}, {"first_name"=>"Koen", "last_name"=>"Stein", "scopus_author_id"=>"24477600400"}, {"first_name"=>"Attila", "last_name"=>"Osi", "scopus_author_id"=>"8367528300"}, {"first_name"=>"Martin P.", "last_name"=>"Sander", "scopus_author_id"=>"16639641300"}], "year"=>2012, "source"=>"PLoS ONE", "identifiers"=>{"scopus"=>"2-s2.0-84857098085", "doi"=>"10.1371/journal.pone.0031392", "pui"=>"364268128", "issn"=>"19326203", "pmid"=>"22355361", "isbn"=>"1932-6203 (Electronic)\\n1932-6203 (Linking)", "sgr"=>"84857098085"}, "id"=>"0850afdb-2947-301d-bf58-19dbc8283ea2", "abstract"=>"BACKGROUND: Rhamphorhynchus from the Solnhofen Limestones is the most prevalent long tailed pterosaur with a debated life history. Whereas morphological studies suggested a slow crocodile-like growth strategy and superprecocial volant hatchlings, the only histological study hitherto conducted on Rhamphorhynchus concluded a relatively high growth rate for the genus. These controversial conclusions can be tested by a bone histological survey of an ontogenetic series of Rhamphorhynchus. METHODOLOGY/PRINCIPAL FINDINGS: Our results suggest that Bennett's second size category does not reflect real ontogenetic stage. Significant body size differences of histologically as well as morphologically adult specimens suggest developmental plasticity. Contrasting the 'superprecocial hatchling' hypothesis, the dominance of fibrolamellar bone in early juveniles implies that hatchlings sustained high growth rate, however only up to the attainment of 30-50% and 7-20% of adult wingspan and body mass, respectively. The early fast growth phase was followed by a prolonged, slow-growth phase indicated by parallel-fibred bone deposition and lines of arrested growth in the cortex, a transition which has also been observed in Pterodaustro. An external fundamental system is absent in all investigated specimens, but due to the restricted sample size, neither determinate nor indeterminate growth could be confirmed in Rhamphorhynchus. CONCLUSIONS/SIGNIFICANCE: The initial rapid growth phase early in Rhamphorhynchus ontogeny supports the non-volant nature of its hatchlings, and refutes the widely accepted 'superprecocial hatchling' hypothesis. We suggest the onset of powered flight, and not of reproduction as the cause of the transition from the fast growth phase to a prolonged slower growth phase. Rapidly growing early juveniles may have been attended by their parents, or could have been independent precocial, but non-volant arboreal creatures until attaining a certain somatic maturity to get airborne. This study adds to the understanding on the diversity of pterosaurian growth strategies.", "link"=>"http://www.mendeley.com/research/life-history-rhamphorhynchus-inferred-bone-histology-diversity-pterosaurian-growth-strategies", "reader_count"=>47, "reader_count_by_academic_status"=>{"Professor > Associate Professor"=>2, "Librarian"=>1, "Researcher"=>11, "Student > Doctoral Student"=>2, "Student > Ph. D. Student"=>6, "Student > Postgraduate"=>1, "Other"=>3, "Student > Master"=>6, "Student > Bachelor"=>13, "Lecturer"=>1, "Professor"=>1}, "reader_count_by_user_role"=>{"Professor > Associate Professor"=>2, "Librarian"=>1, "Researcher"=>11, "Student > Doctoral Student"=>2, "Student > Ph. D. Student"=>6, "Student > Postgraduate"=>1, "Other"=>3, "Student > Master"=>6, "Student > Bachelor"=>13, "Lecturer"=>1, "Professor"=>1}, "reader_count_by_subject_area"=>{"Unspecified"=>3, "Environmental Science"=>3, "Biochemistry, Genetics and Molecular Biology"=>1, "Agricultural and Biological Sciences"=>20, "Medicine and Dentistry"=>2, "Arts and Humanities"=>1, "Physics and Astronomy"=>1, "Computer Science"=>1, "Earth and Planetary Sciences"=>15}, "reader_count_by_subdiscipline"=>{"Medicine and Dentistry"=>{"Medicine and Dentistry"=>2}, "Physics and Astronomy"=>{"Physics and Astronomy"=>1}, "Earth and Planetary Sciences"=>{"Earth and Planetary Sciences"=>15}, "Agricultural and Biological Sciences"=>{"Agricultural and Biological Sciences"=>20}, "Computer Science"=>{"Computer Science"=>1}, "Biochemistry, Genetics and Molecular Biology"=>{"Biochemistry, Genetics and Molecular Biology"=>1}, "Unspecified"=>{"Unspecified"=>3}, "Environmental Science"=>{"Environmental Science"=>3}, "Arts and Humanities"=>{"Arts and Humanities"=>1}}, "reader_count_by_country"=>{"Argentina"=>1, "United States"=>1, "Chile"=>1, "Switzerland"=>1, "Spain"=>1}, "group_count"=>3}

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Figshare

  • {"files"=>["https://ndownloader.figshare.com/files/348457", "https://ndownloader.figshare.com/files/348485", "https://ndownloader.figshare.com/files/348539", "https://ndownloader.figshare.com/files/348570", "https://ndownloader.figshare.com/files/348625"], "description"=>"<div><h3>Background</h3><p><em>Rhamphorhynchus</em> from the Solnhofen Limestones is the most prevalent long tailed pterosaur with a debated life history. Whereas morphological studies suggested a slow crocodile-like growth strategy and superprecocial volant hatchlings, the only histological study hitherto conducted on <em>Rhamphorhynchus</em> concluded a relatively high growth rate for the genus. These controversial conclusions can be tested by a bone histological survey of an ontogenetic series of <em>Rhamphorhynchus</em>.</p> <h3>Methodology/Principal Findings</h3><p>Our results suggest that Bennett's second size category does not reflect real ontogenetic stage. Significant body size differences of histologically as well as morphologically adult specimens suggest developmental plasticity. Contrasting the ‘superprecocial hatchling’ hypothesis, the dominance of fibrolamellar bone in early juveniles implies that hatchlings sustained high growth rate, however only up to the attainment of 30–50% and 7–20% of adult wingspan and body mass, respectively. The early fast growth phase was followed by a prolonged, slow-growth phase indicated by parallel-fibred bone deposition and lines of arrested growth in the cortex, a transition which has also been observed in <em>Pterodaustro</em>. An external fundamental system is absent in all investigated specimens, but due to the restricted sample size, neither determinate nor indeterminate growth could be confirmed in <em>Rhamphorhynchus</em>.</p> <h3>Conclusions/Significance</h3><p>The initial rapid growth phase early in <em>Rhamphorhynchus</em> ontogeny supports the non-volant nature of its hatchlings, and refutes the widely accepted ‘superprecocial hatchling’ hypothesis. We suggest the onset of powered flight, and not of reproduction as the cause of the transition from the fast growth phase to a prolonged slower growth phase. Rapidly growing early juveniles may have been attended by their parents, or could have been independent precocial, but non-volant arboreal creatures until attaining a certain somatic maturity to get airborne. This study adds to the understanding on the diversity of pterosaurian growth strategies.</p> </div>", "links"=>[], "tags"=>["inferred", "histology", "pterosaurian", "strategies"], "article_id"=>128902, "categories"=>["Physiology", "Evolutionary Biology"], "users"=>["Edina Prondvai", "Koen Stein", "Attila Ősi", "Martin P. Sander"], "doi"=>["https://dx.doi.org/10.1371/journal.pone.0031392.s001", "https://dx.doi.org/10.1371/journal.pone.0031392.s002", "https://dx.doi.org/10.1371/journal.pone.0031392.s003", "https://dx.doi.org/10.1371/journal.pone.0031392.s004", "https://dx.doi.org/10.1371/journal.pone.0031392.s005"], "stats"=>{"downloads"=>0, "page_views"=>0, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/Life_History_of_Rhamphorhynchus_Inferred_from_Bone_Histology_and_the_Diversity_of_Pterosaurian_Growth_Strategies/128902", "title"=>"Life History of <em>Rhamphorhynchus</em> Inferred from Bone Histology and the Diversity of Pterosaurian Growth Strategies", "pos_in_sequence"=>0, "defined_type"=>4, "published_date"=>"2012-02-15 02:28:22"}
  • {"files"=>["https://ndownloader.figshare.com/files/682719"], "description"=>"<p>(A) The cortex of the tibia in the smallest studied specimen BSPG 1960 I 470a is dominated by immature fibrolamellar bone. It is noteworthy that already in this early ontogenetic stage endosteal bone rims the medullar cavity. (B) The femoral cortex of BSPG 1877 X I reveals more mature fibrolamellar bone with numerous longitudinal vascular canals resulting in high degree of porosity. Both specimens exhibit large, plump osteocyte lacunae.</p>", "links"=>[], "tags"=>["histological", "sections", "crossed", "corresponding", "interpretative", "drawings", "juvenile", "bones"], "article_id"=>353198, "categories"=>["Physiology", "Evolutionary Biology"], "users"=>["Edina Prondvai", "Koen Stein", "Attila Ősi", "Martin P. Sander"], "doi"=>["https://dx.doi.org/10.1371/journal.pone.0031392.g001"], "stats"=>{"downloads"=>0, "page_views"=>0, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Transverse_histological_sections_under_crossed_polarizers_and_corresponding_interpretative_drawings_of_early_juvenile_long_bones_of_Rhamphorhynchus_muensteri_/353198", "title"=>"Transverse histological sections under crossed polarizers, and corresponding interpretative drawings of early juvenile long bones of <i>Rhamphorhynchus muensteri</i>.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2012-02-15 00:53:18"}
  • {"files"=>["https://ndownloader.figshare.com/files/682916"], "description"=>"<p>(A) The femoral cortex shows three periosteal layers of different tissue types. Only a small portion of the oldest, innermost parallel-fibred layer with high vascularization degree is retained. The middle layer is a thick annulus formed of circumferential lamellae and numerous LAGs. The outer periosteal layer is parallel-fibred with moderately large osteocyte lacunae arranged in circular rows. The vascularity is locally different and some vascular canals open onto the periosteal surface. (B) Almost avascular, woven bone with a few deep intracortical LAGs makes up the bulk of the cortex of the tibia which is locally invaded by Sharpey's fibres.</p>", "links"=>[], "tags"=>["sections", "bones", "ipb", "179", "viewed", "polarized"], "article_id"=>353397, "categories"=>["Physiology", "Evolutionary Biology"], "users"=>["Edina Prondvai", "Koen Stein", "Attila Ősi", "Martin P. Sander"], "doi"=>["https://dx.doi.org/10.1371/journal.pone.0031392.g002"], "stats"=>{"downloads"=>0, "page_views"=>0, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Histological_sections_of_long_bones_of_IPB_179_viewed_with_polarized_microscopy_/353397", "title"=>"Histological sections of long bones of IPB 179 viewed with polarized microscopy.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2012-02-15 00:56:37"}
  • {"files"=>["https://ndownloader.figshare.com/files/683126"], "description"=>"<p>Peripheral to the thick endosteal layer, extensive compacted coarse cancellous bone forms the middle layer of the cortex. Locally, the middle cortical layer consists of loose Haversian bone. The outer periosteal layer is composed of a strongly asymmetrical OCL.</p>", "links"=>[], "tags"=>["histology", "mtm", "crossed"], "article_id"=>353621, "categories"=>["Physiology", "Evolutionary Biology"], "users"=>["Edina Prondvai", "Koen Stein", "Attila Ősi", "Martin P. Sander"], "doi"=>["https://dx.doi.org/10.1371/journal.pone.0031392.g003"], "stats"=>{"downloads"=>0, "page_views"=>0, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Ulnar_histology_of_MTM_2008_33_1_under_crossed_polarizers_/353621", "title"=>"Ulnar histology of MTM 2008.33.1. under crossed polarizers.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2012-02-15 01:00:21"}
  • {"files"=>["https://ndownloader.figshare.com/files/683372"], "description"=>"<p>The medullary cavity is lined by a narrow layer of endosteal bone. The middle cortical layer is composed of loose Haversian bone. The outermost, primary layer is formed of sparsely vascularized fibrolamellar bone with one peripheral LAG.</p>", "links"=>[], "tags"=>["phalanx", "wingfinger", "mtm", "polarized", "crossed"], "article_id"=>353855, "categories"=>["Physiology", "Evolutionary Biology"], "users"=>["Edina Prondvai", "Koen Stein", "Attila Ősi", "Martin P. Sander"], "doi"=>["https://dx.doi.org/10.1371/journal.pone.0031392.g004"], "stats"=>{"downloads"=>0, "page_views"=>0, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Histology_of_the_III_phalanx_of_the_wingfinger_in_MTM_2008_33_1_under_normal_polarized_light_and_crossed_nicols_/353855", "title"=>"Histology of the III. phalanx of the wingfinger in MTM 2008.33.1. under normal polarized light and crossed nicols.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2012-02-15 01:04:15"}
  • {"files"=>["https://ndownloader.figshare.com/files/683576"], "description"=>"<p>Thick endosteal layer merges into compacted coarse cancellous bone which forms the majority of the cortex. The periosteal outer layer is parallel-fibred, almost avascular with a few scattered secondary osteons and dense network of Sharpey's fibres.</p>", "links"=>[], "tags"=>["histology", "mtm", "polarized", "crossed"], "article_id"=>354065, "categories"=>["Physiology", "Evolutionary Biology"], "users"=>["Edina Prondvai", "Koen Stein", "Attila Ősi", "Martin P. Sander"], "doi"=>["https://dx.doi.org/10.1371/journal.pone.0031392.g005"], "stats"=>{"downloads"=>0, "page_views"=>0, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Femoral_histology_of_MTM_2008_33_1_under_normal_polarized_light_and_crossed_nicols_/354065", "title"=>"Femoral histology of MTM 2008.33.1. under normal polarized light and crossed nicols.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2012-02-15 01:07:45"}
  • {"files"=>["https://ndownloader.figshare.com/files/683770"], "description"=>"<p>(A) The femoral cortex has a very thick layer of endosteal lamellae. The parallel-fibred periosteal bone is moderately well vascularized by mostly longitudinal channels. Deep intracortical LAGs within three to four thin, lamellar-fibred annuli are present. (B) The medullar cavity of the tibia is lined by endosteal bone. The bulk of its cortex is composed of an almost avascular, parallel-fibred primary bone tissue with a few, widely spaced LAGs.</p>", "links"=>[], "tags"=>["sections", "bones", "bspg", "1929", "69", "viewed", "polarized"], "article_id"=>354247, "categories"=>["Physiology", "Evolutionary Biology"], "users"=>["Edina Prondvai", "Koen Stein", "Attila Ősi", "Martin P. Sander"], "doi"=>["https://dx.doi.org/10.1371/journal.pone.0031392.g006"], "stats"=>{"downloads"=>0, "page_views"=>0, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Histological_sections_of_long_bones_of_BSPG_1929_I_69_viewed_with_polarized_microscopy_/354247", "title"=>"Histological sections of long bones of BSPG 1929 I 69 viewed with polarized microscopy.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2012-02-15 01:10:47"}
  • {"files"=>["https://ndownloader.figshare.com/files/683926"], "description"=>"<p>Changes in the relation between these two traits during ontogeny can best be described by a power function in which high r<sup>2</sup> value (p = 0.000) guarantees the reliability of the equation making wingspan estimations of specimens with missing wing bones possible.</p>", "links"=>[], "tags"=>["regression", "femoral", "wingspan", "17"], "article_id"=>354408, "categories"=>["Physiology", "Evolutionary Biology"], "users"=>["Edina Prondvai", "Koen Stein", "Attila Ősi", "Martin P. Sander"], "doi"=>["https://dx.doi.org/10.1371/journal.pone.0031392.g007"], "stats"=>{"downloads"=>0, "page_views"=>0, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Plot_and_regression_of_femoral_length_vs_estimated_wingspan_of_17_Rhamphorhynchus_specimens_/354408", "title"=>"Plot and regression of femoral length vs. estimated wingspan of 17 <i>Rhamphorhynchus</i> specimens.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2012-02-15 01:13:28"}
  • {"files"=>["https://ndownloader.figshare.com/files/684022"], "description"=>"<p>Taxa are specified at generic or family level. Taxa that have been histologically investigated so far are framed in rectangles. Those framed by rectangles of solid line have predominantly fibrolamellar bone of varying vascularity degree in the majority of the cortex, occasionally with LAGs and EFS indicating dramatic slowing down of growth in late ontogenetic stages, in which the onset of flight may have occurred. The two genera distinguished by frames of broken lines, <i>Rhamphorhynchus</i> and the ctenochasmatid <i>Pterodaustro</i> differ from the latter in revealing fibrolamellar bone only in juvenile stages and parallel-fibred bone with LAGs in later stages of development. We hypothesize that the early slowing down of growth in these genera is due to the relatively early onset of powered flight. Phylogenetic interrelationships without implications for divergence times are modified after <a href=\"http://www.plosone.org/article/info:doi/10.1371/journal.pone.0031392#pone.0031392-DallaVecchia1\" target=\"_blank\">[15]</a> for non-pterodactyloids, and after <a href=\"http://www.plosone.org/article/info:doi/10.1371/journal.pone.0031392#pone.0031392-Padian3\" target=\"_blank\">[66]</a> for Pterodactyloidea. Temporal ranges and chart are modified after <a href=\"http://www.plosone.org/article/info:doi/10.1371/journal.pone.0031392#pone.0031392-Andres1\" target=\"_blank\">[68]</a>–<a href=\"http://www.plosone.org/article/info:doi/10.1371/journal.pone.0031392#pone.0031392-si2\" target=\"_blank\">[70]</a>.</p>", "links"=>[], "tags"=>["temporal", "ranges", "histological", "characters", "members"], "article_id"=>354506, "categories"=>["Physiology", "Evolutionary Biology"], "users"=>["Edina Prondvai", "Koen Stein", "Attila Ősi", "Martin P. Sander"], "doi"=>["https://dx.doi.org/10.1371/journal.pone.0031392.g008"], "stats"=>{"downloads"=>0, "page_views"=>0, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Phylogenetic_interrelationships_temporal_ranges_and_general_bone_histological_characters_of_different_members_of_Pterosauria_/354506", "title"=>"Phylogenetic interrelationships, temporal ranges and general bone histological characters of different members of Pterosauria.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2012-02-15 01:15:06"}
  • {"files"=>["https://ndownloader.figshare.com/files/684175"], "description"=>"<p>Asterisk indicates that wingspan was deduced from the regression equation describing the relationship between femur length and wingspan.</p>", "links"=>[], "tags"=>["wingspan", "investigated"], "article_id"=>354661, "categories"=>["Physiology", "Evolutionary Biology"], "users"=>["Edina Prondvai", "Koen Stein", "Attila Ősi", "Martin P. Sander"], "doi"=>["https://dx.doi.org/10.1371/journal.pone.0031392.t002"], "stats"=>{"downloads"=>0, "page_views"=>0, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Estimated_wingspan_and_body_mass_of_the_five_investigated_specimens_/354661", "title"=>"Estimated wingspan and body mass of the five investigated specimens.", "pos_in_sequence"=>0, "defined_type"=>3, "published_date"=>"2012-02-15 01:17:41"}
  • {"files"=>["https://ndownloader.figshare.com/files/684207"], "description"=>"<p>Tabulation of specimens studied, selected elements, femoral length, and some particulars of specimens.</p>", "links"=>[], "tags"=>["specimens", "femoral", "particulars"], "article_id"=>354695, "categories"=>["Physiology", "Evolutionary Biology"], "users"=>["Edina Prondvai", "Koen Stein", "Attila Ősi", "Martin P. Sander"], "doi"=>["https://dx.doi.org/10.1371/journal.pone.0031392.t001"], "stats"=>{"downloads"=>0, "page_views"=>0, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Tabulation_of_specimens_studied_selected_elements_femoral_length_and_some_particulars_of_specimens_/354695", "title"=>"Tabulation of specimens studied, selected elements, femoral length, and some particulars of specimens.", "pos_in_sequence"=>0, "defined_type"=>3, "published_date"=>"2012-02-15 01:18:15"}

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Relative Metric

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