<documentid="9AE42FA18F7CEDA356160FAB09FFB09A"ID-CLB-Dataset="23013"ID-DOI="10.1126/sciadv.aax6250"ID-GBIF-Dataset="60d937e4-d9be-45e7-a532-afd33e2c5283"ID-PMC="PMC6938697"ID-PubMed="31911944"ID-Zenodo-Dep="3749024"IM.bibliography_approvedBy="felipe"IM.metadata_approvedBy="admin"IM.taxonomicNames_approvedBy="admin"IM.treatments_approvedBy="admin"checkinTime="1586697798913"checkinUser="jeremy"docAuthor="Holly N. Woodward, Katie Tremaine, Scott A. Williams, Lindsay E. Zanno, John R. Horner & Nathan Myhrvold"docDate="2020"docId="03E8486CFFE30E52FFBE5400FBC3FE74"docLanguage="en"docName="Woodwardetal2020.pdf"docOrigin="Science Advances (eaax 6250) 6"docStyle="DocumentStyle{}"docTitle="Tyrannosaurus rex Osborn 1905"docType="treatment"docVersion="14"lastPageNumber="7"masterDocId="FFD13014FFE30E54FFDE5763FF88FF89"masterDocTitle="Growing up Tyrannosaurus rex: Osteohistology refutes the pygmy “ Nanotyrannus ” and supports ontogenetic niche partitioning in juvenile Tyrannosaurus"masterLastPageNumber="8"masterPageNumber="1"pageNumber="1"updateTime="1727402517684"updateUser="ExternalLinkService">
<mods:titleid="F132D6AEFB8A9AE0339236ACC5335A77">Growing up Tyrannosaurus rex: Osteohistology refutes the pygmy “ Nanotyrannus ” and supports ontogenetic niche partitioning in juvenile Tyrannosaurus</mods:title>
<mods:namePartid="0553F979604B8A4553C6CF41CF4A3053">Holly N. Woodward</mods:namePart>
<mods:affiliationid="80FFE6EF49B1F74E3066938201F3143A">Department of Anatomy and Cell Biology, Oklahoma State University Center for Health Sciences, 1111 W. 17 th St., Tulsa, OK 74104, USA</mods:affiliation>
<mods:affiliationid="97ECD2340CF329D57332FD952FCB08EC">Department of Earth Science, Montana State University, P. O. Box 173480, Bozeman, MT 59717, USA. Museum of the Rockies, Montana State University, 600 W. Kagy Blvd., Bozeman, MT 59717, USA</mods:affiliation>
<mods:namePartid="DE5AB0F549E0CCBE42485194082A3154">Scott A. Williams</mods:namePart>
<mods:affiliationid="E50151B185F60029B50950016B0F98AD">Museum of the Rockies, Montana State University, 600 W. Kagy Blvd., Bozeman, MT 59717, USA</mods:affiliation>
<mods:namePartid="77A8AAA14334140E0023B8B04AA0BE04">Lindsay E. Zanno</mods:namePart>
<mods:affiliationid="2EC71DE62DCA2A3539CA5256E4D4A36A">Paleontology, North Carolina Museum of Natural Sciences, 11 W. Jones St., Raleigh, NC 27601, USA. Department of Biological Sciences, North Carolina State University, 3510 Thomas Hall, Campus Box 7614, Raleigh, NC 2769, USA</mods:affiliation>
<bibRefCitationid="EFD0848BFFE30E54FFB654FEFFFCFC3C"author="H. F. Osborn"box="[104,116,925,949]"journalOrPublisher="Bull. Am. Mus. Nat. Hist."pageId="0"pageNumber="1"pagination="259 - 265"part="21"refId="ref7084"refString="1. H. F. Osborn, Tyrannosaurus and other Cretaceous carnivorous dinosaurs. Bull. Am. Mus. Nat. Hist. 21, 259 - 265 (1905)."title="Tyrannosaurus and other Cretaceous carnivorous dinosaurs"type="journal article"year="1905">
) was met with intense scientific interest and public popularity, which persists to the present day (
<bibRefCitationid="EFD0848BFFE30E54FEBD54D8FEE7FC5A"author="S. L. Brusatte & M. A. Norell & T. D. Carr & G. M. Erickson & J. R. Hutchinson & A. M. Balanoff & G. S. Bever & J. N. Choiniere & P. J. Makovicky & X. Xu"box="[355,367,955,979]"journalOrPublisher="science"pageId="0"pageNumber="1"pagination="1481 - 1485"part="329"refId="ref7118"refString="2. S. L. Brusatte, M. A. Norell, T. D. Carr, G. M. Erickson, J. R. Hutchinson, A. M. Balanoff, G. S. Bever, J. N. Choiniere, P. J. Makovicky, X. Xu, Tyrannosaur paleobiology: New research on ancient exemplar organisms. science 329, 1481 - 1485 (2010)."title="Tyrannosaur paleobiology: New research on ancient exemplar organisms"type="journal article"year="2010">
biology and behavior result from decades of research primarily focused on skeletal morphology and biomechanics [e.g., (
<bibRefCitationid="EFD0848BFFE30E54FD545496FD1EFB84"author="P. L. Larson & K. Carpenter"box="[650,662,1013,1037]"journalOrPublisher="Indiana Univ. Press, Bloomington"pageId="0"pageNumber="1"refId="ref7198"refString="3. P. L. Larson, K. Carpenter, Tyrannosaurus Rex, the Tyrant King. (Indiana Univ. Press, Bloomington, 2008)."title="Tyrannosaurus Rex, the Tyrant King"type="book"year="2008">
life history inaccessible from gross examinations, addressing questions concerning ontogenetic age, growth rate, skeletal maturity, and sexual maturity. In 2004, two teams independently assessed the growth dynamics of
had an accelerated growth rate compared with other tyrannosaurids and achieved adult size in approximately two decades (
<bibRefCitationid="EFD0848BFFE30E54FE685383FE4AFB71"author="G. M. Erickson & P. J. Makovicky & P. J. Currie & M. A. Norell & S. A. Yerby & C. A. Brochu"box="[438,450,1248,1272]"journalOrPublisher="Nature"pageId="0"pageNumber="1"pagination="772 - 775"part="430"refId="ref7228"refString="4. G. M. Erickson, P. J. Makovicky, P. J. Currie, M. A. Norell, S. A. Yerby, C. A. Brochu, Gigantism and comparative life-history parameters of tyrannosaurid dinosaurs. Nature 430, 772 - 775 (2004)."title="Gigantism and comparative life-history parameters of tyrannosaurid dinosaurs"type="journal article"year="2004">
<bibRefCitationid="EFD0848BFFE30E54FE125383FE50FB7E"author="J. R. Horner & K. Padian"box="[460,472,1248,1271]"journalOrPublisher="Proc. R. soc. Lond. B Biol. sci."pageId="0"pageNumber="1"pagination="1875 - 1880"part="271"refId="ref7285"refString="5. J. R. Horner, K. Padian, Age and growth dynamics of Tyrannosaurus rex. Proc. R. soc. Lond. B Biol. sci. 271, 1875 - 1880 (2004)."title="Age and growth dynamics of Tyrannosaurus rex"type="journal article"year="2004">
). The teams focused on growth curves, rather than on detailed analyses or interpretations of bone tissue microstructures. However, osteohistology is critical for establishing a baseline against which skeletal maturity and growth changes in cortical morphology related to life events in this taxon can be tested. Identifying the timing of growth acceleration and empirically quantifying juvenile
growth rates are of special importance because the juvenile growth record is lost in older individuals because of bone remodeling and resorption (
<bibRefCitationid="EFD0848BFFE30E54FDD152A8FD93FA6A"author="G. M. Erickson & P. J. Makovicky & P. J. Currie & M. A. Norell & S. A. Yerby & C. A. Brochu"box="[527,539,1483,1507]"journalOrPublisher="Nature"pageId="0"pageNumber="1"pagination="772 - 775"part="430"refId="ref7228"refString="4. G. M. Erickson, P. J. Makovicky, P. J. Currie, M. A. Norell, S. A. Yerby, C. A. Brochu, Gigantism and comparative life-history parameters of tyrannosaurid dinosaurs. Nature 430, 772 - 775 (2004)."title="Gigantism and comparative life-history parameters of tyrannosaurid dinosaurs"type="journal article"year="2004">
<bibRefCitationid="EFD0848BFFE30E54FDF952A8FDBBFA6B"author="J. R. Horner & K. Padian"box="[551,563,1483,1506]"journalOrPublisher="Proc. R. soc. Lond. B Biol. sci."pageId="0"pageNumber="1"pagination="1875 - 1880"part="271"refId="ref7285"refString="5. J. R. Horner, K. Padian, Age and growth dynamics of Tyrannosaurus rex. Proc. R. soc. Lond. B Biol. sci. 271, 1875 - 1880 (2004)."title="Age and growth dynamics of Tyrannosaurus rex"type="journal article"year="2004">
Here, we examine the femur and tibia bone microstructure of two tyrannosaur skeletons of controversial taxonomic status recovered from the HCF: BMRP (Burpee Museum of Natural History) 2002.4.1, a largely complete specimen composed of nearly the entire skull and substantial postcranial material, and
, a more fragmentary specimen. Respectively, we estimate these specimens to be 54 and 59% the body length of
<materialsCitationid="3B29F327FFE30E54FBB154FDFBBAFC5A"ID-GBIF-Occurrence="3396425373"collectionCode="FMNH"pageId="0"pageNumber="1"specimenCode="FMNH PR2081">FMNH (Field Museum of Natural History) PR 2081 (“Sue”)</materialsCitation>
(
<bibRefCitationid="EFD0848BFFE30E54FB9D54D8FBC7FC5A"author="J. R. Hutchinson & K. T. Bates & J. Molnar & V. Allen & P. J. Makovicky"box="[1091,1103,955,979]"journalOrPublisher="PLOs ONE"pageId="0"pageNumber="1"pagination="e 26037"part="6"refId="ref7327"refString="6. J. R. Hutchinson, K. T. Bates, J. Molnar, V. Allen, P. J. Makovicky, A computational analysis of limb and body dimensions in Tyrannosaurus rex with implications for locomotion, ontogeny, and growth. PLOs ONE 6, e 26037 (2011)."title="A computational analysis of limb and body dimensions in Tyrannosaurus rex with implications for locomotion, ontogeny, and growth"type="journal article"year="2011">
<bibRefCitationid="EFD0848BFFE30E54FB8354D8FBE1FC5B"author="P. J. Currie"box="[1117,1129,955,978]"journalOrPublisher="Can. J. Earth sci."pageId="0"pageNumber="1"pagination="651 - 665"part="40"refId="ref7386"refString="7. P. J. Currie, Allometric growth in tyrannosaurids (Dinosauria: Theropoda) from the Upper Cretaceous of North America and Asia. Can. J. Earth sci. 40, 651 - 665 (2003)."title="Allometric growth in tyrannosaurids (Dinosauria: Theropoda) from the Upper Cretaceous of North America and Asia"type="journal article"year="2003">
) as 11 years based on fibula osteohistology. However, because the fibula grows more slowly than the weight-bearing femur and tibia, it does not reflect annual increases in body size or relative skeletal maturity as accurately [e.g., (
<bibRefCitationid="EFD0848BFFE30E54FB4C532EFB16FBEC"author="H. N. Woodward & J. R. Horner & J. O. Farlow"box="[1170,1182,1101,1125]"journalOrPublisher="PeerJ"pageId="0"pageNumber="1"pagination="e 422"part="2"refId="ref7460"refString="9. H. N. Woodward, J. R. Horner, J. O. Farlow, Quantification of intraskeletal histovariability in Alligator mississippiensis and implications for vertebrate osteohistology. PeerJ 2, e 422 (2014)."title="Quantification of intraskeletal histovariability in Alligator mississippiensis and implications for vertebrate osteohistology"type="journal article"year="2014">
)]. We use femur and tibia data to (i) provide detailed comparative intra- and interskeletal histological descriptions, (ii) quantify the ontogenetic age and relative skeletal maturity of these specimens, and (iii) allow empirical observation of annual growth rate, with emphasis on variability during the life history of tyrannosaurs (
<bibRefCitationid="EFD0848BFFE30E54FBDB5383FB95FB71"author="K. Padian & E. - T. Lamm"box="[1029,1053,1248,1272]"journalOrPublisher="University of California Press, Berkeley"pageId="0"pageNumber="1"pagination="285"refId="ref7502"refString="10. K. Padian, E. - T. Lamm, Bone Histology of Fossil Tetrapods: Advancing Methods, Analysis, and Interpretation (University of California Press, Berkeley, 2013), p. 285."title="Bone Histology of Fossil Tetrapods: Advancing Methods, Analysis, and Interpretation"type="book chapter"year="2013">
and inferring skeletal maturity, we present new data that can be used to evaluate competing taxonomic hypotheses regarding these and other mid-sized tyrannosaur specimens discovered in the HCF, specifically whether
(and by proxy other specimens) represents an adult “pygmy” genus of tyrannosaurid, “
<taxonomicNameid="4C4182F9FFE30E54FC3652CDFBF1FA4C"authorityName="Bakker, Currie & Williams"authorityYear="1988"box="[1000,1145,1454,1477]"class="Reptilia"family="Tyrannosauridae"genus="Nanotyrannus"higherTaxonomySource="GBIF"kingdom="Animalia"order="Dinosauria"pageId="0"pageNumber="1"phylum="Chordata"rank="genus">
can be classified as a wovenparallel complex. Vascularity and osteocyte lacuna density are uniformly high throughout (
<figureCitationid="137AE5FFFFE30E54FBF751FBFBE4F939"box="[1065,1132,1688,1712]"captionStart="Fig"captionStartId="1.[96,125,1092,1112]"captionTargetBox="[313,1271,161,1076]"captionTargetId="figure@1.[312,1272,160,1077]"captionTargetPageId="1"captionText="Fig. 1. Femur histology of tyrannosaurid specimens BMRP 2002.4.1 and BMRP 2006.4.4. (A) Mid-cortex of the transverse thin section of BMRP 2002.4.1.Plane-polarized light (PPL) emphasizes osteocyte lacuna density and variability in shape within the laminae, as well as longitudinal primary osteons.In CPL, there is a weak preferred fiber arrangement parallel to the transverse plane of section reflected by regional birefringence. Many primary osteons (POs) have uniformly isotropic fibers with rounded osteocyte lacunae. (B) Mid-cortex of the transverse thin section of BMRP 2006.4.4. Osteocyte lacuna density and variability in shape within the laminae are evident in PPL.CPL reveals varying birefringence associated with bone fiber orientation, but there is a weak preferred fiber arrangement parallel to the transverse plane of section reflected by regional birefringence. Many POs are composed of uniformly isotropic fibers with rounded osteocyte lacunae.(C) Longitudinal section of the mid-cortex of BMRP 2006.4.4.Vascular canals appear as near-vertical, thin, dark columns. As in the transverse sectionι the primary laminae between POs contain variably arranged osteocyte lacunae. In CPL, the laminae are weakly isotropic (I), corresponding to the poorly organized parallel orientation of fibers in the transverse plane. The laterally compressed osteocyte lacunae in POs are embedded within a uniformly birefringent [anisotropic (AN)] matrix in CPL, indicating that the PO lamellae are longitudinally oriented parallel-fibered bone (LP). (D) On the posteromedial side of the transverse section of BMRP 2006.4.4, there is a parallel-fibered annulus located at the periosteal surface (thickness indicated with blue line).Photographed in CPL.(E) In the transverse section on the posterolateral side, the annulus shown in (D) (blue lines) is overlain by highly isotropic woven-fibered laminae."figureDoi="http://doi.org/10.5281/zenodo.3749026"httpUri="https://zenodo.org/record/3749026/files/figure.png"pageId="0"pageNumber="1">Figs. 1</figureCitation>
and
<figureCitationid="137AE5FFFFE30E54FB4151FBFB26F939"box="[1183,1198,1688,1712]"captionStart="Fig"captionStartId="2.[96,126,773,793]"captionTargetBox="[313,1271,161,757]"captionTargetId="figure@2.[312,1272,160,758]"captionTargetPageId="2"captionText="Fig. 2. Tibia histology of tyrannosaurid specimens BMRP 2002.4.1 and BMRP 2006.4.4. (A) Transverse mid-cortex thin section of BMRP 2002.4.1. Longitudinal POs are evident, and PPL emphasizes osteocyte lacuna density and variability in shape within laminae. CPL reveals varying birefringence associated with bone fiber orientation, but with a weak arrangement of fibers parallel to the transverse plane of section.Many POs are composed of highly isotropic fibers with rounded osteocyte lacunae. (B) Longitudinal thin section of the mid-cortex of BMRP 2002.4.1.Vascular canals appear as near-vertical, dark columns.Adjacent to the vascular canalsι the POs contain laterally compressed osteocyte lacunae. CPL demonstrates that the laterally compressed osteocyte lacunae of POs are embedded within a uniformly birefringent matrix (anisotropic), indicating that the lamellae of POs are LP.Osteocyte lacunae orientation varies in the thin laminae between POs. In CPL, the laminae are weakly isotropic, corresponding to the weak arrangement of parallel fibers in transverse section. (C) In transverse thin section, the periosteal surface of BMRP 2006.4.4 on the anterior side consists of reticular POs within laminae of highly isotropic, woven tissue.(D) Within the anterior and anteromedial innermost cortex of BMRP 2006.4.4, in transverse thin section, six closely spaced LAGs are visible interstitially.Blue lines highlight the LAG trajectories."figureDoi="http://doi.org/10.5281/zenodo.3749028"httpUri="https://zenodo.org/record/3749028/files/figure.png"pageId="0"pageNumber="1">2</figureCitation>
). In the femora, the primary and secondary osteons surrounding vascular canals are frequently isotropic in the transverse section (
<figureCitationid="137AE5FFFFE30E54FB5551B0FAABF962"box="[1163,1315,1747,1771]"captionStart="Fig"captionStartId="1.[96,125,1092,1112]"captionTargetBox="[313,1271,161,1076]"captionTargetId="figure@1.[312,1272,160,1077]"captionTargetPageId="1"captionText="Fig. 1. Femur histology of tyrannosaurid specimens BMRP 2002.4.1 and BMRP 2006.4.4. (A) Mid-cortex of the transverse thin section of BMRP 2002.4.1.Plane-polarized light (PPL) emphasizes osteocyte lacuna density and variability in shape within the laminae, as well as longitudinal primary osteons.In CPL, there is a weak preferred fiber arrangement parallel to the transverse plane of section reflected by regional birefringence. Many primary osteons (POs) have uniformly isotropic fibers with rounded osteocyte lacunae. (B) Mid-cortex of the transverse thin section of BMRP 2006.4.4. Osteocyte lacuna density and variability in shape within the laminae are evident in PPL.CPL reveals varying birefringence associated with bone fiber orientation, but there is a weak preferred fiber arrangement parallel to the transverse plane of section reflected by regional birefringence. Many POs are composed of uniformly isotropic fibers with rounded osteocyte lacunae.(C) Longitudinal section of the mid-cortex of BMRP 2006.4.4.Vascular canals appear as near-vertical, thin, dark columns. As in the transverse sectionι the primary laminae between POs contain variably arranged osteocyte lacunae. In CPL, the laminae are weakly isotropic (I), corresponding to the poorly organized parallel orientation of fibers in the transverse plane. The laterally compressed osteocyte lacunae in POs are embedded within a uniformly birefringent [anisotropic (AN)] matrix in CPL, indicating that the PO lamellae are longitudinally oriented parallel-fibered bone (LP). (D) On the posteromedial side of the transverse section of BMRP 2006.4.4, there is a parallel-fibered annulus located at the periosteal surface (thickness indicated with blue line).Photographed in CPL.(E) In the transverse section on the posterolateral side, the annulus shown in (D) (blue lines) is overlain by highly isotropic woven-fibered laminae."figureDoi="http://doi.org/10.5281/zenodo.3749026"httpUri="https://zenodo.org/record/3749026/files/figure.png"pageId="0"pageNumber="1">Fig. 1, A and B</figureCitation>
) and anisotropic in the longitudinal section (
<figureCitationid="137AE5FFFFE30E54FB9F5193FB05F881"box="[1089,1165,1776,1800]"captionStart="Fig"captionStartId="1.[96,125,1092,1112]"captionTargetBox="[313,1271,161,1076]"captionTargetId="figure@1.[312,1272,160,1077]"captionTargetPageId="1"captionText="Fig. 1. Femur histology of tyrannosaurid specimens BMRP 2002.4.1 and BMRP 2006.4.4. (A) Mid-cortex of the transverse thin section of BMRP 2002.4.1.Plane-polarized light (PPL) emphasizes osteocyte lacuna density and variability in shape within the laminae, as well as longitudinal primary osteons.In CPL, there is a weak preferred fiber arrangement parallel to the transverse plane of section reflected by regional birefringence. Many primary osteons (POs) have uniformly isotropic fibers with rounded osteocyte lacunae. (B) Mid-cortex of the transverse thin section of BMRP 2006.4.4. Osteocyte lacuna density and variability in shape within the laminae are evident in PPL.CPL reveals varying birefringence associated with bone fiber orientation, but there is a weak preferred fiber arrangement parallel to the transverse plane of section reflected by regional birefringence. Many POs are composed of uniformly isotropic fibers with rounded osteocyte lacunae.(C) Longitudinal section of the mid-cortex of BMRP 2006.4.4.Vascular canals appear as near-vertical, thin, dark columns. As in the transverse sectionι the primary laminae between POs contain variably arranged osteocyte lacunae. In CPL, the laminae are weakly isotropic (I), corresponding to the poorly organized parallel orientation of fibers in the transverse plane. The laterally compressed osteocyte lacunae in POs are embedded within a uniformly birefringent [anisotropic (AN)] matrix in CPL, indicating that the PO lamellae are longitudinally oriented parallel-fibered bone (LP). (D) On the posteromedial side of the transverse section of BMRP 2006.4.4, there is a parallel-fibered annulus located at the periosteal surface (thickness indicated with blue line).Photographed in CPL.(E) In the transverse section on the posterolateral side, the annulus shown in (D) (blue lines) is overlain by highly isotropic woven-fibered laminae."figureDoi="http://doi.org/10.5281/zenodo.3749026"httpUri="https://zenodo.org/record/3749026/files/figure.png"pageId="0"pageNumber="1">Fig. 1C</figureCitation>
). Also in the transverse section, femur primary tissue exhibits moderate anisotropy regionally and weak anisotropy locally, corresponding to a loose arrangement of mineralized fibers in parallel (e.g.,
<figureCitationid="137AE5FFFFE30E54FB85502BFB7BF8D6"box="[1115,1267,1864,1888]"captionStart="Fig"captionStartId="1.[96,125,1092,1112]"captionTargetBox="[313,1271,161,1076]"captionTargetId="figure@1.[312,1272,160,1077]"captionTargetPageId="1"captionText="Fig. 1. Femur histology of tyrannosaurid specimens BMRP 2002.4.1 and BMRP 2006.4.4. (A) Mid-cortex of the transverse thin section of BMRP 2002.4.1.Plane-polarized light (PPL) emphasizes osteocyte lacuna density and variability in shape within the laminae, as well as longitudinal primary osteons.In CPL, there is a weak preferred fiber arrangement parallel to the transverse plane of section reflected by regional birefringence. Many primary osteons (POs) have uniformly isotropic fibers with rounded osteocyte lacunae. (B) Mid-cortex of the transverse thin section of BMRP 2006.4.4. Osteocyte lacuna density and variability in shape within the laminae are evident in PPL.CPL reveals varying birefringence associated with bone fiber orientation, but there is a weak preferred fiber arrangement parallel to the transverse plane of section reflected by regional birefringence. Many POs are composed of uniformly isotropic fibers with rounded osteocyte lacunae.(C) Longitudinal section of the mid-cortex of BMRP 2006.4.4.Vascular canals appear as near-vertical, thin, dark columns. As in the transverse sectionι the primary laminae between POs contain variably arranged osteocyte lacunae. In CPL, the laminae are weakly isotropic (I), corresponding to the poorly organized parallel orientation of fibers in the transverse plane. The laterally compressed osteocyte lacunae in POs are embedded within a uniformly birefringent [anisotropic (AN)] matrix in CPL, indicating that the PO lamellae are longitudinally oriented parallel-fibered bone (LP). (D) On the posteromedial side of the transverse section of BMRP 2006.4.4, there is a parallel-fibered annulus located at the periosteal surface (thickness indicated with blue line).Photographed in CPL.(E) In the transverse section on the posterolateral side, the annulus shown in (D) (blue lines) is overlain by highly isotropic woven-fibered laminae."figureDoi="http://doi.org/10.5281/zenodo.3749026"httpUri="https://zenodo.org/record/3749026/files/figure.png"pageId="0"pageNumber="1">Fig. 1, A and B</figureCitation>
<docAuthorAffiliationid="935E3619FFE30E54FFB95064FDD9F892"box="[103,593,1799,1819]"pageId="0"pageNumber="1">Chapman University, 1 University Dr., Orange, CA 92866, USA</docAuthorAffiliation>
.Plane-polarized light (PPL) emphasizes osteocyte lacuna density and variability in shape within the laminae, as well as longitudinal primary osteons.In CPL, there is a weak preferred fiber arrangement parallel to the transverse plane of section reflected by regional birefringence. Many primary osteons (POs) have uniformly isotropic fibers with rounded osteocyte lacunae. (
. Osteocyte lacuna density and variability in shape within the laminae are evident in PPL.CPL reveals varying birefringence associated with bone fiber orientation, but there is a weak preferred fiber arrangement parallel to the transverse plane of section reflected by regional birefringence. Many POs are composed of uniformly isotropic fibers with rounded osteocyte lacunae.(
.Vascular canals appear as near-vertical, thin, dark columns. As in the transverse section, the primary laminae between POs contain variably arranged osteocyte lacunae. In CPL, the laminae are weakly isotropic (I), corresponding to the poorly organized parallel orientation of fibers in the transverse plane. The laterally compressed osteocyte lacunae in POs are embedded within a uniformly birefringent [anisotropic (AN)] matrix in CPL, indicating that the PO lamellae are longitudinally oriented parallel-fibered bone (LP). (
<figureCitationid="137AE5FFFFE20E55FDB052A9FD30FA6B"box="[622,696,1482,1506]"captionStart="Fig"captionStartId="2.[96,126,773,793]"captionTargetBox="[313,1271,161,757]"captionTargetId="figure@2.[312,1272,160,758]"captionTargetPageId="2"captionText="Fig. 2. Tibia histology of tyrannosaurid specimens BMRP 2002.4.1 and BMRP 2006.4.4. (A) Transverse mid-cortex thin section of BMRP 2002.4.1. Longitudinal POs are evident, and PPL emphasizes osteocyte lacuna density and variability in shape within laminae. CPL reveals varying birefringence associated with bone fiber orientation, but with a weak arrangement of fibers parallel to the transverse plane of section.Many POs are composed of highly isotropic fibers with rounded osteocyte lacunae. (B) Longitudinal thin section of the mid-cortex of BMRP 2002.4.1.Vascular canals appear as near-vertical, dark columns.Adjacent to the vascular canalsι the POs contain laterally compressed osteocyte lacunae. CPL demonstrates that the laterally compressed osteocyte lacunae of POs are embedded within a uniformly birefringent matrix (anisotropic), indicating that the lamellae of POs are LP.Osteocyte lacunae orientation varies in the thin laminae between POs. In CPL, the laminae are weakly isotropic, corresponding to the weak arrangement of parallel fibers in transverse section. (C) In transverse thin section, the periosteal surface of BMRP 2006.4.4 on the anterior side consists of reticular POs within laminae of highly isotropic, woven tissue.(D) Within the anterior and anteromedial innermost cortex of BMRP 2006.4.4, in transverse thin section, six closely spaced LAGs are visible interstitially.Blue lines highlight the LAG trajectories."figureDoi="http://doi.org/10.5281/zenodo.3749028"httpUri="https://zenodo.org/record/3749028/files/figure.png"pageId="1"pageNumber="2">Fig. 2A</figureCitation>
), longitudinal primary osteons are isotropic in circularly polarized light (CPL), but fibers of primary osteons encircling laminar, circular, and plexiform vascular canals are anisotropic. In contrast, primary osteons in the tibia of
and incorporates the fibular crest on the lateral side (
<httpUriid="B5C027D0FFE20E55FD9951D6FF15F963"httpUri="https://advances.sciencemag.org/content/suppl/2019/12/20/6.1.eaax6250.DC1"pageId="1"pageNumber="2">figs. S2D and S8, A and F</httpUri>
). Highly vascularized reticular woven tissue is present on the anterior and anterolateral periosteal surfaces (
<figureCitationid="137AE5FFFFE20E55FDE9518CFD0DF88E"box="[567,645,1775,1799]"captionStart="Fig"captionStartId="2.[96,126,773,793]"captionTargetBox="[313,1271,161,757]"captionTargetId="figure@2.[312,1272,160,758]"captionTargetPageId="2"captionText="Fig. 2. Tibia histology of tyrannosaurid specimens BMRP 2002.4.1 and BMRP 2006.4.4. (A) Transverse mid-cortex thin section of BMRP 2002.4.1. Longitudinal POs are evident, and PPL emphasizes osteocyte lacuna density and variability in shape within laminae. CPL reveals varying birefringence associated with bone fiber orientation, but with a weak arrangement of fibers parallel to the transverse plane of section.Many POs are composed of highly isotropic fibers with rounded osteocyte lacunae. (B) Longitudinal thin section of the mid-cortex of BMRP 2002.4.1.Vascular canals appear as near-vertical, dark columns.Adjacent to the vascular canalsι the POs contain laterally compressed osteocyte lacunae. CPL demonstrates that the laterally compressed osteocyte lacunae of POs are embedded within a uniformly birefringent matrix (anisotropic), indicating that the lamellae of POs are LP.Osteocyte lacunae orientation varies in the thin laminae between POs. In CPL, the laminae are weakly isotropic, corresponding to the weak arrangement of parallel fibers in transverse section. (C) In transverse thin section, the periosteal surface of BMRP 2006.4.4 on the anterior side consists of reticular POs within laminae of highly isotropic, woven tissue.(D) Within the anterior and anteromedial innermost cortex of BMRP 2006.4.4, in transverse thin section, six closely spaced LAGs are visible interstitially.Blue lines highlight the LAG trajectories."figureDoi="http://doi.org/10.5281/zenodo.3749028"httpUri="https://zenodo.org/record/3749028/files/figure.png"pageId="1"pageNumber="2">Fig. 2C</figureCitation>
). In both individuals, the thickest tibial cortex is located anteriorly.
, isotropic, vascularized, primary tissue is separated from the cortex by a lamellar endosteal layer. These features are morphologically consistent with medullary bone (
<bibRefCitationid="EFD0848BFFE20E55FADB5284FA96FA76"author="M. H. Schweitzer & W. Zheng & L. Zanno & S. Werning & T. Sugiyama"box="[1285,1310,1511,1535]"journalOrPublisher="sci. Rep."pageId="1"pageNumber="2"pagination="23099"part="6"refId="ref7543"refString="11. M. H. Schweitzer, W. Zheng, L. Zanno, S. Werning, T. Sugiyama, Chemistry supports the identification of gender-specific reproductive tissue in Tyrannosaurus rex. sci. Rep. 6, 23099 (2016)."title="Chemistry supports the identification of gender-specific reproductive tissue in Tyrannosaurus rex"type="journal article"year="2016">
Cyclical growth marks (CGMs), resembling tree rings in transverse thin section, were observed in the femora and tibiae of both BMRP specimens. Studies on extant vertebrates demonstrate that CGMs result from brief interruptions in osteogenesis, occurring with annual periodicity and typically coinciding with the nadir (
<bibRefCitationid="EFD0848BFFE20E55FAA251B1FA1CF963"author="M. Kohler & N. Marin-Moratalla & X. Jordana & R. Aanes"box="[1404,1428,1746,1770]"journalOrPublisher="Nature"pageId="1"pageNumber="2"pagination="358 - 361"part="487"refId="ref7590"refString="12. M. Kohler, N. Marin-Moratalla, X. Jordana, R. Aanes, Seasonal bone growth and physiology in endotherms shed light on dinosaur physiology. Nature 487, 358 - 361 (2012)."title="Seasonal bone growth and physiology in endotherms shed light on dinosaur physiology"type="journal article"year="2012">
). The annual pauses in bone apposition are recorded as CGMs in cortical microstructure as either pronounced lines of arrested growth (LAGs) or diffuse annulus rings. On the basis of counting CGMs,
was at least 15 years old at death (15 CGMs in the femur and 13 to 18 CGMs in the tibia). Typically, vertebrate long bone cortices will exhibit widely spaced CGMs within the cortex when young, corresponding to high annual osteogenesis. In subadults, CGMs become more closely spaced as osteogenesis decreases approaching adult size [e.g., (
<bibRefCitationid="EFD0848BFFE10E56FDB953A1FDF7FB53"author="K. Padian & E. - T. Lamm"box="[615,639,1218,1242]"journalOrPublisher="University of California Press, Berkeley"pageId="2"pageNumber="3"pagination="285"refId="ref7502"refString="10. K. Padian, E. - T. Lamm, Bone Histology of Fossil Tetrapods: Advancing Methods, Analysis, and Interpretation (University of California Press, Berkeley, 2013), p. 285."title="Bone Histology of Fossil Tetrapods: Advancing Methods, Analysis, and Interpretation"type="book chapter"year="2013">
)]. In contrast to these frequently observed patterns, the spacing of CGMs was unexpectedly variable throughout the femur and tibia cortices of both BMRP specimens.
. Longitudinal POs are evident, and PPL emphasizes osteocyte lacuna density and variability in shape within laminae. CPL reveals varying birefringence associated with bone fiber orientation, but with a weak arrangement of fibers parallel to the transverse plane of section.Many POs are composed of highly isotropic fibers with rounded osteocyte lacunae. (
.Vascular canals appear as near-vertical, dark columns.Adjacent to the vascular canals, the POs contain laterally compressed osteocyte lacunae. CPL demonstrates that the laterally compressed osteocyte lacunae of POs are embedded within a uniformly birefringent matrix (anisotropic), indicating that the lamellae of POs are LP.Osteocyte lacunae orientation varies in the thin laminae between POs. In CPL, the laminae are weakly isotropic, corresponding to the weak arrangement of parallel fibers in transverse section. (
, there is an annulus at the periosteal surface on the medial side (
<figureCitationid="137AE5FFFFE10E56FE695236FD8DFAE4"box="[439,517,1365,1389]"captionStart="Fig"captionStartId="1.[96,125,1092,1112]"captionTargetBox="[313,1271,161,1076]"captionTargetId="figure@1.[312,1272,160,1077]"captionTargetPageId="1"captionText="Fig. 1. Femur histology of tyrannosaurid specimens BMRP 2002.4.1 and BMRP 2006.4.4. (A) Mid-cortex of the transverse thin section of BMRP 2002.4.1.Plane-polarized light (PPL) emphasizes osteocyte lacuna density and variability in shape within the laminae, as well as longitudinal primary osteons.In CPL, there is a weak preferred fiber arrangement parallel to the transverse plane of section reflected by regional birefringence. Many primary osteons (POs) have uniformly isotropic fibers with rounded osteocyte lacunae. (B) Mid-cortex of the transverse thin section of BMRP 2006.4.4. Osteocyte lacuna density and variability in shape within the laminae are evident in PPL.CPL reveals varying birefringence associated with bone fiber orientation, but there is a weak preferred fiber arrangement parallel to the transverse plane of section reflected by regional birefringence. Many POs are composed of uniformly isotropic fibers with rounded osteocyte lacunae.(C) Longitudinal section of the mid-cortex of BMRP 2006.4.4.Vascular canals appear as near-vertical, thin, dark columns. As in the transverse sectionι the primary laminae between POs contain variably arranged osteocyte lacunae. In CPL, the laminae are weakly isotropic (I), corresponding to the poorly organized parallel orientation of fibers in the transverse plane. The laterally compressed osteocyte lacunae in POs are embedded within a uniformly birefringent [anisotropic (AN)] matrix in CPL, indicating that the PO lamellae are longitudinally oriented parallel-fibered bone (LP). (D) On the posteromedial side of the transverse section of BMRP 2006.4.4, there is a parallel-fibered annulus located at the periosteal surface (thickness indicated with blue line).Photographed in CPL.(E) In the transverse section on the posterolateral side, the annulus shown in (D) (blue lines) is overlain by highly isotropic woven-fibered laminae."figureDoi="http://doi.org/10.5281/zenodo.3749026"httpUri="https://zenodo.org/record/3749026/files/figure.png"pageId="2"pageNumber="3">Fig. 1D</figureCitation>
), but when followed posteriorly, the annulus is within the outer cortex, while fibrolamellar tissue makes up the cortex of the periosteal surface (
<figureCitationid="137AE5FFFFE10E56FDBB52F3FD25FA21"box="[613,685,1424,1448]"captionStart="Fig"captionStartId="1.[96,125,1092,1112]"captionTargetBox="[313,1271,161,1076]"captionTargetId="figure@1.[312,1272,160,1077]"captionTargetPageId="1"captionText="Fig. 1. Femur histology of tyrannosaurid specimens BMRP 2002.4.1 and BMRP 2006.4.4. (A) Mid-cortex of the transverse thin section of BMRP 2002.4.1.Plane-polarized light (PPL) emphasizes osteocyte lacuna density and variability in shape within the laminae, as well as longitudinal primary osteons.In CPL, there is a weak preferred fiber arrangement parallel to the transverse plane of section reflected by regional birefringence. Many primary osteons (POs) have uniformly isotropic fibers with rounded osteocyte lacunae. (B) Mid-cortex of the transverse thin section of BMRP 2006.4.4. Osteocyte lacuna density and variability in shape within the laminae are evident in PPL.CPL reveals varying birefringence associated with bone fiber orientation, but there is a weak preferred fiber arrangement parallel to the transverse plane of section reflected by regional birefringence. Many POs are composed of uniformly isotropic fibers with rounded osteocyte lacunae.(C) Longitudinal section of the mid-cortex of BMRP 2006.4.4.Vascular canals appear as near-vertical, thin, dark columns. As in the transverse sectionι the primary laminae between POs contain variably arranged osteocyte lacunae. In CPL, the laminae are weakly isotropic (I), corresponding to the poorly organized parallel orientation of fibers in the transverse plane. The laterally compressed osteocyte lacunae in POs are embedded within a uniformly birefringent [anisotropic (AN)] matrix in CPL, indicating that the PO lamellae are longitudinally oriented parallel-fibered bone (LP). (D) On the posteromedial side of the transverse section of BMRP 2006.4.4, there is a parallel-fibered annulus located at the periosteal surface (thickness indicated with blue line).Photographed in CPL.(E) In the transverse section on the posterolateral side, the annulus shown in (D) (blue lines) is overlain by highly isotropic woven-fibered laminae."figureDoi="http://doi.org/10.5281/zenodo.3749026"httpUri="https://zenodo.org/record/3749026/files/figure.png"pageId="2"pageNumber="3">Fig. 1E</figureCitation>
). Within the innermost cortex on the anterolateral side, six LAGs are closely spaced (
<figureCitationid="137AE5FFFFE10E56FF6A52A9FE8EFA6B"box="[180,262,1482,1506]"captionStart="Fig"captionStartId="2.[96,126,773,793]"captionTargetBox="[313,1271,161,757]"captionTargetId="figure@2.[312,1272,160,758]"captionTargetPageId="2"captionText="Fig. 2. Tibia histology of tyrannosaurid specimens BMRP 2002.4.1 and BMRP 2006.4.4. (A) Transverse mid-cortex thin section of BMRP 2002.4.1. Longitudinal POs are evident, and PPL emphasizes osteocyte lacuna density and variability in shape within laminae. CPL reveals varying birefringence associated with bone fiber orientation, but with a weak arrangement of fibers parallel to the transverse plane of section.Many POs are composed of highly isotropic fibers with rounded osteocyte lacunae. (B) Longitudinal thin section of the mid-cortex of BMRP 2002.4.1.Vascular canals appear as near-vertical, dark columns.Adjacent to the vascular canalsι the POs contain laterally compressed osteocyte lacunae. CPL demonstrates that the laterally compressed osteocyte lacunae of POs are embedded within a uniformly birefringent matrix (anisotropic), indicating that the lamellae of POs are LP.Osteocyte lacunae orientation varies in the thin laminae between POs. In CPL, the laminae are weakly isotropic, corresponding to the weak arrangement of parallel fibers in transverse section. (C) In transverse thin section, the periosteal surface of BMRP 2006.4.4 on the anterior side consists of reticular POs within laminae of highly isotropic, woven tissue.(D) Within the anterior and anteromedial innermost cortex of BMRP 2006.4.4, in transverse thin section, six closely spaced LAGs are visible interstitially.Blue lines highlight the LAG trajectories."figureDoi="http://doi.org/10.5281/zenodo.3749028"httpUri="https://zenodo.org/record/3749028/files/figure.png"pageId="2"pageNumber="3">Fig. 2D</figureCitation>
). Because of resorption from the medullary drift, these LAGs are absent within the innermost cortex of the posterior and lateral sides.
<bibRefCitationid="EFD0848BFFE10E56FEF65140FEC8F9B2"author="E. Prondvai & K. H. W. Stein & A. de Ricqles & J. Cubo"box="[296,320,1571,1595]"journalOrPublisher="Biol. J. Linn. soc."pageId="2"pageNumber="3"pagination="799 - 816"part="112"refId="ref7631"refString="13. E. Prondvai, K. H. W. Stein, A. de Ricqles, J. Cubo, Development-based revision of bone tissue classification: the importance of semantics for science. Biol. J. Linn. soc. 112, 799 - 816 (2014)."title="Development-based revision of bone tissue classification: the importance of semantics for science"type="journal article"year="2014">
) demonstrated that inaccurate bone microstructure interpretations are possible if the mineralized tissue is observed in only a single plane; specifically, the more slowly formed parallel-fibered mineral arrangement could be mistaken for the rapidly deposited woven-fibered mineral arrangement, which has direct bearing on growth rate interpretations. Therefore, the femur of
was sectioned in a medial-lateral plane to accurately assess tissue organization and associated relative growth rates (
<figureCitationid="137AE5FFFFE10E56FF325049FEC8F8CA"box="[236,320,1834,1859]"captionStart="Fig"captionStartId="1.[96,125,1092,1112]"captionTargetBox="[313,1271,161,1076]"captionTargetId="figure@1.[312,1272,160,1077]"captionTargetPageId="1"captionText="Fig. 1. Femur histology of tyrannosaurid specimens BMRP 2002.4.1 and BMRP 2006.4.4. (A) Mid-cortex of the transverse thin section of BMRP 2002.4.1.Plane-polarized light (PPL) emphasizes osteocyte lacuna density and variability in shape within the laminae, as well as longitudinal primary osteons.In CPL, there is a weak preferred fiber arrangement parallel to the transverse plane of section reflected by regional birefringence. Many primary osteons (POs) have uniformly isotropic fibers with rounded osteocyte lacunae. (B) Mid-cortex of the transverse thin section of BMRP 2006.4.4. Osteocyte lacuna density and variability in shape within the laminae are evident in PPL.CPL reveals varying birefringence associated with bone fiber orientation, but there is a weak preferred fiber arrangement parallel to the transverse plane of section reflected by regional birefringence. Many POs are composed of uniformly isotropic fibers with rounded osteocyte lacunae.(C) Longitudinal section of the mid-cortex of BMRP 2006.4.4.Vascular canals appear as near-vertical, thin, dark columns. As in the transverse sectionι the primary laminae between POs contain variably arranged osteocyte lacunae. In CPL, the laminae are weakly isotropic (I), corresponding to the poorly organized parallel orientation of fibers in the transverse plane. The laterally compressed osteocyte lacunae in POs are embedded within a uniformly birefringent [anisotropic (AN)] matrix in CPL, indicating that the PO lamellae are longitudinally oriented parallel-fibered bone (LP). (D) On the posteromedial side of the transverse section of BMRP 2006.4.4, there is a parallel-fibered annulus located at the periosteal surface (thickness indicated with blue line).Photographed in CPL.(E) In the transverse section on the posterolateral side, the annulus shown in (D) (blue lines) is overlain by highly isotropic woven-fibered laminae."figureDoi="http://doi.org/10.5281/zenodo.3749026"httpUri="https://zenodo.org/record/3749026/files/figure.png"pageId="2"pageNumber="3">Figs. 1C</figureCitation>
and
<figureCitationid="137AE5FFFFE10E56FEAC5048FE06F8CA"box="[370,398,1835,1859]"captionStart="Fig"captionStartId="2.[96,126,773,793]"captionTargetBox="[313,1271,161,757]"captionTargetId="figure@2.[312,1272,160,758]"captionTargetPageId="2"captionText="Fig. 2. Tibia histology of tyrannosaurid specimens BMRP 2002.4.1 and BMRP 2006.4.4. (A) Transverse mid-cortex thin section of BMRP 2002.4.1. Longitudinal POs are evident, and PPL emphasizes osteocyte lacuna density and variability in shape within laminae. CPL reveals varying birefringence associated with bone fiber orientation, but with a weak arrangement of fibers parallel to the transverse plane of section.Many POs are composed of highly isotropic fibers with rounded osteocyte lacunae. (B) Longitudinal thin section of the mid-cortex of BMRP 2002.4.1.Vascular canals appear as near-vertical, dark columns.Adjacent to the vascular canalsι the POs contain laterally compressed osteocyte lacunae. CPL demonstrates that the laterally compressed osteocyte lacunae of POs are embedded within a uniformly birefringent matrix (anisotropic), indicating that the lamellae of POs are LP.Osteocyte lacunae orientation varies in the thin laminae between POs. In CPL, the laminae are weakly isotropic, corresponding to the weak arrangement of parallel fibers in transverse section. (C) In transverse thin section, the periosteal surface of BMRP 2006.4.4 on the anterior side consists of reticular POs within laminae of highly isotropic, woven tissue.(D) Within the anterior and anteromedial innermost cortex of BMRP 2006.4.4, in transverse thin section, six closely spaced LAGs are visible interstitially.Blue lines highlight the LAG trajectories."figureDoi="http://doi.org/10.5281/zenodo.3749028"httpUri="https://zenodo.org/record/3749028/files/figure.png"pageId="2"pageNumber="3">2B</figureCitation>
, and
<httpUriid="B5C027D0FFE10E56FE1B5049FD68F8CA"box="[453,736,1834,1859]"httpUri="https://advances.sciencemag.org/content/suppl/2019/12/20/6.1.eaax6250.DC1"pageId="2"pageNumber="3">figs. S2, B and C, S5, and S7</httpUri>
, vascular canals are arranged parallel to the plane of section and to the shaft of the long bone. Adjacent to the vascular canals, bone fibers are highly anisotropic in CPL and contain osteocyte lacunae with long axes arranged parallel to the vascular canals and plane of section. Tissue of the laminae between primary osteons varies locally in degree of isotropy, with corresponding variable shape in osteocyte lacunae. On the medial side of the longitudinal section through the tibia of
). Adjacent to vascular canals, fibers of the primary osteons are anisotropic in CPL with longitudinally flattened osteocyte lacunae. Fibers within the primary laminae vary locally in isotropy and osteocyte lacuna orientation (
<figureCitationid="137AE5FFFFE10E56FB8852CEFB2AFA4C"box="[1110,1186,1453,1477]"captionStart="Fig"captionStartId="2.[96,126,773,793]"captionTargetBox="[313,1271,161,757]"captionTargetId="figure@2.[312,1272,160,758]"captionTargetPageId="2"captionText="Fig. 2. Tibia histology of tyrannosaurid specimens BMRP 2002.4.1 and BMRP 2006.4.4. (A) Transverse mid-cortex thin section of BMRP 2002.4.1. Longitudinal POs are evident, and PPL emphasizes osteocyte lacuna density and variability in shape within laminae. CPL reveals varying birefringence associated with bone fiber orientation, but with a weak arrangement of fibers parallel to the transverse plane of section.Many POs are composed of highly isotropic fibers with rounded osteocyte lacunae. (B) Longitudinal thin section of the mid-cortex of BMRP 2002.4.1.Vascular canals appear as near-vertical, dark columns.Adjacent to the vascular canalsι the POs contain laterally compressed osteocyte lacunae. CPL demonstrates that the laterally compressed osteocyte lacunae of POs are embedded within a uniformly birefringent matrix (anisotropic), indicating that the lamellae of POs are LP.Osteocyte lacunae orientation varies in the thin laminae between POs. In CPL, the laminae are weakly isotropic, corresponding to the weak arrangement of parallel fibers in transverse section. (C) In transverse thin section, the periosteal surface of BMRP 2006.4.4 on the anterior side consists of reticular POs within laminae of highly isotropic, woven tissue.(D) Within the anterior and anteromedial innermost cortex of BMRP 2006.4.4, in transverse thin section, six closely spaced LAGs are visible interstitially.Blue lines highlight the LAG trajectories."figureDoi="http://doi.org/10.5281/zenodo.3749028"httpUri="https://zenodo.org/record/3749028/files/figure.png"pageId="2"pageNumber="3">Fig. 2B</figureCitation>
). The lateral cortex is thinner than the medial cortex, and vascular canals are more closely spaced with fewer communicating canals (
bone fiber organization in the transverse and longitudinal sections using CPL confirms that primary tissue is generally poorly organized parallel fibered to weakly woven. Dense osteocyte lacunae and poor bone fiber organization, in combination with a rich vascular network of reticular, laminar, and plexiform primary osteons, are characteristics that empirically correspond to elevated osteogenesis ranging from 5 to 90 μ m/day (
<bibRefCitationid="EFD0848BFFE00E57FF3C57C0FF72FF32"author="K. Padian & E. - T. Lamm"box="[226,250,163,187]"journalOrPublisher="University of California Press, Berkeley"pageId="3"pageNumber="4"pagination="285"refId="ref7502"refString="10. K. Padian, E. - T. Lamm, Bone Histology of Fossil Tetrapods: Advancing Methods, Analysis, and Interpretation (University of California Press, Berkeley, 2013), p. 285."title="Bone Histology of Fossil Tetrapods: Advancing Methods, Analysis, and Interpretation"type="book chapter"year="2013">
). Nonetheless, the frequency of longitudinal vascularity, as well as regionally prevalent poorly organized parallel fiber bundles within the transverse sections, suggests that annual growth rates were nearer the lower bound (
<bibRefCitationid="EFD0848BFFE00E57FE195798FE57FE9A"author="K. Padian & E. - T. Lamm"box="[455,479,251,275]"journalOrPublisher="University of California Press, Berkeley"pageId="3"pageNumber="4"pagination="285"refId="ref7502"refString="10. K. Padian, E. - T. Lamm, Bone Histology of Fossil Tetrapods: Advancing Methods, Analysis, and Interpretation (University of California Press, Berkeley, 2013), p. 285."title="Bone Histology of Fossil Tetrapods: Advancing Methods, Analysis, and Interpretation"type="book chapter"year="2013">
). The BMRP individuals did, however, experience occasional periods of faster growth indicated by bands of regionally isotropic woven laminae with reticular vascularity (e.g.,
<figureCitationid="137AE5FFFFE00E57FF685631FE8EFEE2"box="[182,262,338,363]"captionStart="Fig"captionStartId="1.[96,125,1092,1112]"captionTargetBox="[313,1271,161,1076]"captionTargetId="figure@1.[312,1272,160,1077]"captionTargetPageId="1"captionText="Fig. 1. Femur histology of tyrannosaurid specimens BMRP 2002.4.1 and BMRP 2006.4.4. (A) Mid-cortex of the transverse thin section of BMRP 2002.4.1.Plane-polarized light (PPL) emphasizes osteocyte lacuna density and variability in shape within the laminae, as well as longitudinal primary osteons.In CPL, there is a weak preferred fiber arrangement parallel to the transverse plane of section reflected by regional birefringence. Many primary osteons (POs) have uniformly isotropic fibers with rounded osteocyte lacunae. (B) Mid-cortex of the transverse thin section of BMRP 2006.4.4. Osteocyte lacuna density and variability in shape within the laminae are evident in PPL.CPL reveals varying birefringence associated with bone fiber orientation, but there is a weak preferred fiber arrangement parallel to the transverse plane of section reflected by regional birefringence. Many POs are composed of uniformly isotropic fibers with rounded osteocyte lacunae.(C) Longitudinal section of the mid-cortex of BMRP 2006.4.4.Vascular canals appear as near-vertical, thin, dark columns. As in the transverse sectionι the primary laminae between POs contain variably arranged osteocyte lacunae. In CPL, the laminae are weakly isotropic (I), corresponding to the poorly organized parallel orientation of fibers in the transverse plane. The laterally compressed osteocyte lacunae in POs are embedded within a uniformly birefringent [anisotropic (AN)] matrix in CPL, indicating that the PO lamellae are longitudinally oriented parallel-fibered bone (LP). (D) On the posteromedial side of the transverse section of BMRP 2006.4.4, there is a parallel-fibered annulus located at the periosteal surface (thickness indicated with blue line).Photographed in CPL.(E) In the transverse section on the posterolateral side, the annulus shown in (D) (blue lines) is overlain by highly isotropic woven-fibered laminae."figureDoi="http://doi.org/10.5281/zenodo.3749026"httpUri="https://zenodo.org/record/3749026/files/figure.png"pageId="3"pageNumber="4">Figs. 1E</figureCitation>
and
<figureCitationid="137AE5FFFFE00E57FEE65630FEDFFEE2"box="[312,343,339,363]"captionStart="Fig"captionStartId="2.[96,126,773,793]"captionTargetBox="[313,1271,161,757]"captionTargetId="figure@2.[312,1272,160,758]"captionTargetPageId="2"captionText="Fig. 2. Tibia histology of tyrannosaurid specimens BMRP 2002.4.1 and BMRP 2006.4.4. (A) Transverse mid-cortex thin section of BMRP 2002.4.1. Longitudinal POs are evident, and PPL emphasizes osteocyte lacuna density and variability in shape within laminae. CPL reveals varying birefringence associated with bone fiber orientation, but with a weak arrangement of fibers parallel to the transverse plane of section.Many POs are composed of highly isotropic fibers with rounded osteocyte lacunae. (B) Longitudinal thin section of the mid-cortex of BMRP 2002.4.1.Vascular canals appear as near-vertical, dark columns.Adjacent to the vascular canalsι the POs contain laterally compressed osteocyte lacunae. CPL demonstrates that the laterally compressed osteocyte lacunae of POs are embedded within a uniformly birefringent matrix (anisotropic), indicating that the lamellae of POs are LP.Osteocyte lacunae orientation varies in the thin laminae between POs. In CPL, the laminae are weakly isotropic, corresponding to the weak arrangement of parallel fibers in transverse section. (C) In transverse thin section, the periosteal surface of BMRP 2006.4.4 on the anterior side consists of reticular POs within laminae of highly isotropic, woven tissue.(D) Within the anterior and anteromedial innermost cortex of BMRP 2006.4.4, in transverse thin section, six closely spaced LAGs are visible interstitially.Blue lines highlight the LAG trajectories."figureDoi="http://doi.org/10.5281/zenodo.3749028"httpUri="https://zenodo.org/record/3749028/files/figure.png"pageId="3"pageNumber="4">2C</figureCitation>
, and
<httpUriid="B5C027D0FFE00E57FE525631FD1AFEE2"box="[396,658,338,363]"httpUri="https://advances.sciencemag.org/content/suppl/2019/12/20/6.1.eaax6250.DC1"pageId="3"pageNumber="4">figs. S6D and S8, C and D</httpUri>
) (
<bibRefCitationid="EFD0848BFFE00E57FD765630FD48FEE2"author="K. Padian & E. - T. Lamm"box="[680,704,339,363]"journalOrPublisher="University of California Press, Berkeley"pageId="3"pageNumber="4"pagination="285"refId="ref7502"refString="10. K. Padian, E. - T. Lamm, Bone Histology of Fossil Tetrapods: Advancing Methods, Analysis, and Interpretation (University of California Press, Berkeley, 2013), p. 285."title="Bone Histology of Fossil Tetrapods: Advancing Methods, Analysis, and Interpretation"type="book chapter"year="2013">
In both BMRP specimens, the majority of primary osteons as well as some secondary osteons were isotropic in the transverse section. Corresponding anisotropy in longitudinal examination confirms that the fiber bundles within osteons are longitudinally arranged (
<figureCitationid="137AE5FFFFE00E57FD0956ABFFF5FE74"captionStart="Fig"captionStartId="1.[96,125,1092,1112]"captionTargetBox="[313,1271,161,1076]"captionTargetId="figure@1.[312,1272,160,1077]"captionTargetPageId="1"captionText="Fig. 1. Femur histology of tyrannosaurid specimens BMRP 2002.4.1 and BMRP 2006.4.4. (A) Mid-cortex of the transverse thin section of BMRP 2002.4.1.Plane-polarized light (PPL) emphasizes osteocyte lacuna density and variability in shape within the laminae, as well as longitudinal primary osteons.In CPL, there is a weak preferred fiber arrangement parallel to the transverse plane of section reflected by regional birefringence. Many primary osteons (POs) have uniformly isotropic fibers with rounded osteocyte lacunae. (B) Mid-cortex of the transverse thin section of BMRP 2006.4.4. Osteocyte lacuna density and variability in shape within the laminae are evident in PPL.CPL reveals varying birefringence associated with bone fiber orientation, but there is a weak preferred fiber arrangement parallel to the transverse plane of section reflected by regional birefringence. Many POs are composed of uniformly isotropic fibers with rounded osteocyte lacunae.(C) Longitudinal section of the mid-cortex of BMRP 2006.4.4.Vascular canals appear as near-vertical, thin, dark columns. As in the transverse sectionι the primary laminae between POs contain variably arranged osteocyte lacunae. In CPL, the laminae are weakly isotropic (I), corresponding to the poorly organized parallel orientation of fibers in the transverse plane. The laterally compressed osteocyte lacunae in POs are embedded within a uniformly birefringent [anisotropic (AN)] matrix in CPL, indicating that the PO lamellae are longitudinally oriented parallel-fibered bone (LP). (D) On the posteromedial side of the transverse section of BMRP 2006.4.4, there is a parallel-fibered annulus located at the periosteal surface (thickness indicated with blue line).Photographed in CPL.(E) In the transverse section on the posterolateral side, the annulus shown in (D) (blue lines) is overlain by highly isotropic woven-fibered laminae."figureDoi="http://doi.org/10.5281/zenodo.3749026"httpUri="https://zenodo.org/record/3749026/files/figure.png"pageId="3"pageNumber="4">Figs. 1C</figureCitation>
and
<figureCitationid="137AE5FFFFE00E57FF6C5686FF47FE74"box="[178,207,485,509]"captionStart="Fig"captionStartId="2.[96,126,773,793]"captionTargetBox="[313,1271,161,757]"captionTargetId="figure@2.[312,1272,160,758]"captionTargetPageId="2"captionText="Fig. 2. Tibia histology of tyrannosaurid specimens BMRP 2002.4.1 and BMRP 2006.4.4. (A) Transverse mid-cortex thin section of BMRP 2002.4.1. Longitudinal POs are evident, and PPL emphasizes osteocyte lacuna density and variability in shape within laminae. CPL reveals varying birefringence associated with bone fiber orientation, but with a weak arrangement of fibers parallel to the transverse plane of section.Many POs are composed of highly isotropic fibers with rounded osteocyte lacunae. (B) Longitudinal thin section of the mid-cortex of BMRP 2002.4.1.Vascular canals appear as near-vertical, dark columns.Adjacent to the vascular canalsι the POs contain laterally compressed osteocyte lacunae. CPL demonstrates that the laterally compressed osteocyte lacunae of POs are embedded within a uniformly birefringent matrix (anisotropic), indicating that the lamellae of POs are LP.Osteocyte lacunae orientation varies in the thin laminae between POs. In CPL, the laminae are weakly isotropic, corresponding to the weak arrangement of parallel fibers in transverse section. (C) In transverse thin section, the periosteal surface of BMRP 2006.4.4 on the anterior side consists of reticular POs within laminae of highly isotropic, woven tissue.(D) Within the anterior and anteromedial innermost cortex of BMRP 2006.4.4, in transverse thin section, six closely spaced LAGs are visible interstitially.Blue lines highlight the LAG trajectories."figureDoi="http://doi.org/10.5281/zenodo.3749028"httpUri="https://zenodo.org/record/3749028/files/figure.png"pageId="3"pageNumber="4">2B</figureCitation>
, and
<httpUriid="B5C027D0FFE00E57FED75686FE15FE74"box="[265,413,485,509]"httpUri="https://advances.sciencemag.org/content/suppl/2019/12/20/6.1.eaax6250.DC1"pageId="3"pageNumber="4">fig. S5, B to D</httpUri>
). Studies on long bone response to loading show that longitudinal collagen fiber orientation within secondary osteons is commonly found in habitually tension-loaded regions (
<bibRefCitationid="EFD0848BFFE00E57FF67555EFF59FDDC"author="J. G. Skedros & S. D. Mendenhall & C. J. Kiser & H. Winet"box="[185,209,573,597]"journalOrPublisher="Bone"pageId="3"pageNumber="4"pagination="392 - 403"part="44"refId="ref7685"refString="14. J. G. Skedros, S. D. Mendenhall, C. J. Kiser, H. Winet, Interpreting cortical bone adaptation and load history by quantifying osteon morphotypes in circularly polarized light images. Bone 44, 392 - 403 (2009)."title="Interpreting cortical bone adaptation and load history by quantifying osteon morphotypes in circularly polarized light images"type="journal article"year="2009">
), which may also apply to primary osteon collagen fiber orientation. As such, future studies on tyrannosaurid locomotion biomechanics may benefit from incorporation of osteohistology.
Rather than exhibiting an external fundamental system (EFS) (
<figureCitationid="137AE5FFFFE00E57FD1D55B3FD73FD61"box="[707,763,720,744]"captionStart="Fig"captionStartId="3.[808,838,1079,1099]"captionTargetBox="[813,1484,161,1063]"captionTargetId="figure@3.[812,1484,160,1064]"captionTargetPageId="3"captionText="Fig. 3. The presence of an EFS at the periosteal surface of a long bone indicates skeletal maturity, while the absence of an EFS indicates that the bone is still growing at the time of death. (A) An EFS composed of tightly stacked birefringent LAGs (between blue arrowheads) at the periosteal surface of an Alligator mississippiensis. (B) The EFS (between blue arrowheads) in an ostrich (struthio camelus) is made of nearly avascular, birefringent parallel-fibered to lamellar primary tissue.(C) No EFS is present at the periosteal surface of the femur of BMRP 2002.4.1, (D) the tibia of BMRP 2002.4.1, (E) the femur of BMRP 2006.4.4, or (F) the tibia of BMRP 2006.4.4.All panels are shown in transverse thin section, with CPL."figureDoi="http://doi.org/10.5281/zenodo.3749030"httpUri="https://zenodo.org/record/3749030/files/figure.png"pageId="3"pageNumber="4">Fig. 3</figureCitation>
), a woven-parallel complex extends to the periosteal surface in both tyrannosaurid specimens. Thus, histology supports morphological observations that
<bibRefCitationid="EFD0848BFFE00E57FE4C5426FE21FCD4"author="K. Padian & E. - T. Lamm"box="[402,425,837,861]"journalOrPublisher="University of California Press, Berkeley"pageId="3"pageNumber="4"pagination="285"refId="ref7502"refString="10. K. Padian, E. - T. Lamm, Bone Histology of Fossil Tetrapods: Advancing Methods, Analysis, and Interpretation (University of California Press, Berkeley, 2013), p. 285."title="Bone Histology of Fossil Tetrapods: Advancing Methods, Analysis, and Interpretation"type="book chapter"year="2013">
). In lieu of epiphyseal fusion, which most reptile taxa lack, an EFS is the only way to conclusively confirm attainment of asymptotic adult body length from the long bones of a vertebrate. When present, the EFS occupies the periosteal surface as either closely spaced LAGs (separated by micrometers) (
<figureCitationid="137AE5FFFFE00E57FD6A54D9FC89FC5A"box="[692,769,954,979]"captionStart="Fig"captionStartId="3.[808,838,1079,1099]"captionTargetBox="[813,1484,161,1063]"captionTargetId="figure@3.[812,1484,160,1064]"captionTargetPageId="3"captionText="Fig. 3. The presence of an EFS at the periosteal surface of a long bone indicates skeletal maturity, while the absence of an EFS indicates that the bone is still growing at the time of death. (A) An EFS composed of tightly stacked birefringent LAGs (between blue arrowheads) at the periosteal surface of an Alligator mississippiensis. (B) The EFS (between blue arrowheads) in an ostrich (struthio camelus) is made of nearly avascular, birefringent parallel-fibered to lamellar primary tissue.(C) No EFS is present at the periosteal surface of the femur of BMRP 2002.4.1, (D) the tibia of BMRP 2002.4.1, (E) the femur of BMRP 2006.4.4, or (F) the tibia of BMRP 2006.4.4.All panels are shown in transverse thin section, with CPL."figureDoi="http://doi.org/10.5281/zenodo.3749030"httpUri="https://zenodo.org/record/3749030/files/figure.png"pageId="3"pageNumber="4">Fig. 3A</figureCitation>
) or as a thick, primarily avascular annulus (
<figureCitationid="137AE5FFFFE00E57FDD854BBFDC6FC79"box="[518,590,984,1008]"captionStart="Fig"captionStartId="3.[808,838,1079,1099]"captionTargetBox="[813,1484,161,1063]"captionTargetId="figure@3.[812,1484,160,1064]"captionTargetPageId="3"captionText="Fig. 3. The presence of an EFS at the periosteal surface of a long bone indicates skeletal maturity, while the absence of an EFS indicates that the bone is still growing at the time of death. (A) An EFS composed of tightly stacked birefringent LAGs (between blue arrowheads) at the periosteal surface of an Alligator mississippiensis. (B) The EFS (between blue arrowheads) in an ostrich (struthio camelus) is made of nearly avascular, birefringent parallel-fibered to lamellar primary tissue.(C) No EFS is present at the periosteal surface of the femur of BMRP 2002.4.1, (D) the tibia of BMRP 2002.4.1, (E) the femur of BMRP 2006.4.4, or (F) the tibia of BMRP 2006.4.4.All panels are shown in transverse thin section, with CPL."figureDoi="http://doi.org/10.5281/zenodo.3749030"httpUri="https://zenodo.org/record/3749030/files/figure.png"pageId="3"pageNumber="4">Fig. 3B</figureCitation>
) (
<bibRefCitationid="EFD0848BFFE00E57FDBD54BBFDF3FC79"author="K. Padian & E. - T. Lamm"box="[611,635,984,1008]"journalOrPublisher="University of California Press, Berkeley"pageId="3"pageNumber="4"pagination="285"refId="ref7502"refString="10. K. Padian, E. - T. Lamm, Bone Histology of Fossil Tetrapods: Advancing Methods, Analysis, and Interpretation (University of California Press, Berkeley, 2013), p. 285."title="Bone Histology of Fossil Tetrapods: Advancing Methods, Analysis, and Interpretation"type="book chapter"year="2013">
, an annulus is present at the periosteal surface of both the femur (
<figureCitationid="137AE5FFFFE00E57FEB65353FE3CFBC1"box="[360,436,1072,1096]"captionStart="Fig"captionStartId="1.[96,125,1092,1112]"captionTargetBox="[313,1271,161,1076]"captionTargetId="figure@1.[312,1272,160,1077]"captionTargetPageId="1"captionText="Fig. 1. Femur histology of tyrannosaurid specimens BMRP 2002.4.1 and BMRP 2006.4.4. (A) Mid-cortex of the transverse thin section of BMRP 2002.4.1.Plane-polarized light (PPL) emphasizes osteocyte lacuna density and variability in shape within the laminae, as well as longitudinal primary osteons.In CPL, there is a weak preferred fiber arrangement parallel to the transverse plane of section reflected by regional birefringence. Many primary osteons (POs) have uniformly isotropic fibers with rounded osteocyte lacunae. (B) Mid-cortex of the transverse thin section of BMRP 2006.4.4. Osteocyte lacuna density and variability in shape within the laminae are evident in PPL.CPL reveals varying birefringence associated with bone fiber orientation, but there is a weak preferred fiber arrangement parallel to the transverse plane of section reflected by regional birefringence. Many POs are composed of uniformly isotropic fibers with rounded osteocyte lacunae.(C) Longitudinal section of the mid-cortex of BMRP 2006.4.4.Vascular canals appear as near-vertical, thin, dark columns. As in the transverse sectionι the primary laminae between POs contain variably arranged osteocyte lacunae. In CPL, the laminae are weakly isotropic (I), corresponding to the poorly organized parallel orientation of fibers in the transverse plane. The laterally compressed osteocyte lacunae in POs are embedded within a uniformly birefringent [anisotropic (AN)] matrix in CPL, indicating that the PO lamellae are longitudinally oriented parallel-fibered bone (LP). (D) On the posteromedial side of the transverse section of BMRP 2006.4.4, there is a parallel-fibered annulus located at the periosteal surface (thickness indicated with blue line).Photographed in CPL.(E) In the transverse section on the posterolateral side, the annulus shown in (D) (blue lines) is overlain by highly isotropic woven-fibered laminae."figureDoi="http://doi.org/10.5281/zenodo.3749026"httpUri="https://zenodo.org/record/3749026/files/figure.png"pageId="3"pageNumber="4">Fig. 1D</figureCitation>
), but when the annulus is followed around the cortex, in both cases it becomes embedded within the outer cortex and superseded by woven primary tissue (
<figureCitationid="137AE5FFFFE00E57FF7C53EBFF67FB29"box="[162,239,1160,1184]"captionStart="Fig"captionStartId="1.[96,125,1092,1112]"captionTargetBox="[313,1271,161,1076]"captionTargetId="figure@1.[312,1272,160,1077]"captionTargetPageId="1"captionText="Fig. 1. Femur histology of tyrannosaurid specimens BMRP 2002.4.1 and BMRP 2006.4.4. (A) Mid-cortex of the transverse thin section of BMRP 2002.4.1.Plane-polarized light (PPL) emphasizes osteocyte lacuna density and variability in shape within the laminae, as well as longitudinal primary osteons.In CPL, there is a weak preferred fiber arrangement parallel to the transverse plane of section reflected by regional birefringence. Many primary osteons (POs) have uniformly isotropic fibers with rounded osteocyte lacunae. (B) Mid-cortex of the transverse thin section of BMRP 2006.4.4. Osteocyte lacuna density and variability in shape within the laminae are evident in PPL.CPL reveals varying birefringence associated with bone fiber orientation, but there is a weak preferred fiber arrangement parallel to the transverse plane of section reflected by regional birefringence. Many POs are composed of uniformly isotropic fibers with rounded osteocyte lacunae.(C) Longitudinal section of the mid-cortex of BMRP 2006.4.4.Vascular canals appear as near-vertical, thin, dark columns. As in the transverse sectionι the primary laminae between POs contain variably arranged osteocyte lacunae. In CPL, the laminae are weakly isotropic (I), corresponding to the poorly organized parallel orientation of fibers in the transverse plane. The laterally compressed osteocyte lacunae in POs are embedded within a uniformly birefringent [anisotropic (AN)] matrix in CPL, indicating that the PO lamellae are longitudinally oriented parallel-fibered bone (LP). (D) On the posteromedial side of the transverse section of BMRP 2006.4.4, there is a parallel-fibered annulus located at the periosteal surface (thickness indicated with blue line).Photographed in CPL.(E) In the transverse section on the posterolateral side, the annulus shown in (D) (blue lines) is overlain by highly isotropic woven-fibered laminae."figureDoi="http://doi.org/10.5281/zenodo.3749026"httpUri="https://zenodo.org/record/3749026/files/figure.png"pageId="3"pageNumber="4">Figs. 1E</figureCitation>
and
<figureCitationid="137AE5FFFFE00E57FEC053EBFEB5FB29"box="[286,317,1160,1184]"captionStart="Fig"captionStartId="2.[96,126,773,793]"captionTargetBox="[313,1271,161,757]"captionTargetId="figure@2.[312,1272,160,758]"captionTargetPageId="2"captionText="Fig. 2. Tibia histology of tyrannosaurid specimens BMRP 2002.4.1 and BMRP 2006.4.4. (A) Transverse mid-cortex thin section of BMRP 2002.4.1. Longitudinal POs are evident, and PPL emphasizes osteocyte lacuna density and variability in shape within laminae. CPL reveals varying birefringence associated with bone fiber orientation, but with a weak arrangement of fibers parallel to the transverse plane of section.Many POs are composed of highly isotropic fibers with rounded osteocyte lacunae. (B) Longitudinal thin section of the mid-cortex of BMRP 2002.4.1.Vascular canals appear as near-vertical, dark columns.Adjacent to the vascular canalsι the POs contain laterally compressed osteocyte lacunae. CPL demonstrates that the laterally compressed osteocyte lacunae of POs are embedded within a uniformly birefringent matrix (anisotropic), indicating that the lamellae of POs are LP.Osteocyte lacunae orientation varies in the thin laminae between POs. In CPL, the laminae are weakly isotropic, corresponding to the weak arrangement of parallel fibers in transverse section. (C) In transverse thin section, the periosteal surface of BMRP 2006.4.4 on the anterior side consists of reticular POs within laminae of highly isotropic, woven tissue.(D) Within the anterior and anteromedial innermost cortex of BMRP 2006.4.4, in transverse thin section, six closely spaced LAGs are visible interstitially.Blue lines highlight the LAG trajectories."figureDoi="http://doi.org/10.5281/zenodo.3749028"httpUri="https://zenodo.org/record/3749028/files/figure.png"pageId="3"pageNumber="4">2C</figureCitation>
). The proximity of the annulus to the periosteal surface instead suggests that
<emphasisid="B9352568FFE00E57FCF65354FBDDFB08"bold="true"pageId="3"pageNumber="4">Fig. 3. The presence of an EFS at the periosteal surface of a long bone indicates skeletal maturity, while the absence of an EFS indicates that the bone is still growing at the time of death.</emphasis>
. Although the number of missing CGMs could be predicted on the basis of innermost zonal thicknesses and a process of retrocalculation [e.g., (
<bibRefCitationid="EFD0848BFFE00E57FE165165FE5CF994"author="J. R. Horner & K. Padian"box="[456,468,1542,1565]"journalOrPublisher="Proc. R. soc. Lond. B Biol. sci."pageId="3"pageNumber="4"pagination="1875 - 1880"part="271"refId="ref7285"refString="5. J. R. Horner, K. Padian, Age and growth dynamics of Tyrannosaurus rex. Proc. R. soc. Lond. B Biol. sci. 271, 1875 - 1880 (2004)."title="Age and growth dynamics of Tyrannosaurus rex"type="journal article"year="2004">
<bibRefCitationid="EFD0848BFFE00E57FE3E5166FE70F994"author="K. Padian & E. - T. Lamm"box="[480,504,1541,1565]"journalOrPublisher="University of California Press, Berkeley"pageId="3"pageNumber="4"pagination="285"refId="ref7502"refString="10. K. Padian, E. - T. Lamm, Bone Histology of Fossil Tetrapods: Advancing Methods, Analysis, and Interpretation (University of California Press, Berkeley, 2013), p. 285."title="Bone Histology of Fossil Tetrapods: Advancing Methods, Analysis, and Interpretation"type="book chapter"year="2013">
<bibRefCitationid="EFD0848BFFE00E57FEF55123FECBF9D1"author="L. E. Zanno & R. T. Tucker & A. Canoville & H. M. Avrahami & T. A. Gates & P. J. Makovicky"box="[299,323,1600,1624]"journalOrPublisher="Commun. Biol."pageId="3"pageNumber="4"pagination="64"part="2"refId="ref7736"refString="15. L. E. Zanno, R. T. Tucker, A. Canoville, H. M. Avrahami, T. A. Gates, P. J. Makovicky, Diminutive fleet-footed tyrannosauroid narrows the 70 - million-year gap in the North American fossil record. Commun. Biol. 2, 64 (2019)."title="Diminutive fleet-footed tyrannosauroid narrows the 70 - million-year gap in the North American fossil record"type="journal article"year="2019">
<figureCitationid="137AE5FFFFE00E57FE9951FBFE1EF939"box="[327,406,1688,1712]"captionStart="Fig"captionStartId="2.[96,126,773,793]"captionTargetBox="[313,1271,161,757]"captionTargetId="figure@2.[312,1272,160,758]"captionTargetPageId="2"captionText="Fig. 2. Tibia histology of tyrannosaurid specimens BMRP 2002.4.1 and BMRP 2006.4.4. (A) Transverse mid-cortex thin section of BMRP 2002.4.1. Longitudinal POs are evident, and PPL emphasizes osteocyte lacuna density and variability in shape within laminae. CPL reveals varying birefringence associated with bone fiber orientation, but with a weak arrangement of fibers parallel to the transverse plane of section.Many POs are composed of highly isotropic fibers with rounded osteocyte lacunae. (B) Longitudinal thin section of the mid-cortex of BMRP 2002.4.1.Vascular canals appear as near-vertical, dark columns.Adjacent to the vascular canalsι the POs contain laterally compressed osteocyte lacunae. CPL demonstrates that the laterally compressed osteocyte lacunae of POs are embedded within a uniformly birefringent matrix (anisotropic), indicating that the lamellae of POs are LP.Osteocyte lacunae orientation varies in the thin laminae between POs. In CPL, the laminae are weakly isotropic, corresponding to the weak arrangement of parallel fibers in transverse section. (C) In transverse thin section, the periosteal surface of BMRP 2006.4.4 on the anterior side consists of reticular POs within laminae of highly isotropic, woven tissue.(D) Within the anterior and anteromedial innermost cortex of BMRP 2006.4.4, in transverse thin section, six closely spaced LAGs are visible interstitially.Blue lines highlight the LAG trajectories."figureDoi="http://doi.org/10.5281/zenodo.3749028"httpUri="https://zenodo.org/record/3749028/files/figure.png"pageId="3"pageNumber="4">Fig. 2D</figureCitation>
). Because the CGMs remain parallel about the cortex and do not merge, they either represent a single hiatus in which growth repeatedly ceased and resumed (totaling 13 years of growth) or up to 6 years where relatively little growth occurred annually (totaling up to 18 years of growth) (
<bibRefCitationid="EFD0848BFFE00E57FDFC506EFDA6F8AC"author="H. N. Woodward & J. R. Horner & J. O. Farlow"box="[546,558,1805,1829]"journalOrPublisher="PeerJ"pageId="3"pageNumber="4"pagination="e 422"part="2"refId="ref7460"refString="9. H. N. Woodward, J. R. Horner, J. O. Farlow, Quantification of intraskeletal histovariability in Alligator mississippiensis and implications for vertebrate osteohistology. PeerJ 2, e 422 (2014)."title="Quantification of intraskeletal histovariability in Alligator mississippiensis and implications for vertebrate osteohistology"type="journal article"year="2014">
<bibRefCitationid="EFD0848BFFE00E57FDE7506EFDD9F8AC"author="M. H. Caetano & J. Castanet"box="[569,593,1805,1829]"journalOrPublisher="Amphibia Reptilia"pageId="3"pageNumber="4"pagination="117 - 129"part="14"refId="ref7799"refString="16. M. H. Caetano, J. Castanet, Variability and microevolutionary patterns in Triturus marmoratus from Portugal: age, size, longevity and individual growth. Amphibia Reptilia 14, 117 - 129 (1993)."title="Variability and microevolutionary patterns in Triturus marmoratus from Portugal: age, size, longevity and individual growth"type="journal article"year="1993">
is questionable because the proximal sampling location away from midshaft incorporates the fibular crest, introducing associated regions of remodeling and directional growth affecting apposition interpretations. Because of this and their absence in the femur, the observed grouping of six CGMs is conservatively interpreted as a single hiatus event. Similar instances of a single hiatus represented by narrowly spaced LAGs are reported in other tyrannosauroids (
<bibRefCitationid="EFD0848BFFE00E57FC545123FC2AF9D1"author="L. E. Zanno & R. T. Tucker & A. Canoville & H. M. Avrahami & T. A. Gates & P. J. Makovicky"box="[906,930,1600,1624]"journalOrPublisher="Commun. Biol."pageId="3"pageNumber="4"pagination="64"part="2"refId="ref7736"refString="15. L. E. Zanno, R. T. Tucker, A. Canoville, H. M. Avrahami, T. A. Gates, P. J. Makovicky, Diminutive fleet-footed tyrannosauroid narrows the 70 - million-year gap in the North American fossil record. Commun. Biol. 2, 64 (2019)."title="Diminutive fleet-footed tyrannosauroid narrows the 70 - million-year gap in the North American fossil record"type="journal article"year="2019">
demonstrates the extent to which these individuals could adjust growth rate based on resource availability, in this case prolonging the ontogenetic duration of
Bone tissue organization was similar across femora and tibiae, suggesting that both bones record annual increases in body size equally well. If the stacked CGMs of
reflect a single hiatus, then each femur preserved more CGMs than the associated tibia. Previous studies demonstrated that intraskeletal inconsistencies in CGM counts are due to variable rates of medullary cavity expansion or cortical drift across elements (
<bibRefCitationid="EFD0848BFFE70E50FE2E57A3FE74FF51"author="H. N. Woodward & J. R. Horner & J. O. Farlow"box="[496,508,192,216]"journalOrPublisher="PeerJ"pageId="4"pageNumber="5"pagination="e 422"part="2"refId="ref7460"refString="9. H. N. Woodward, J. R. Horner, J. O. Farlow, Quantification of intraskeletal histovariability in Alligator mississippiensis and implications for vertebrate osteohistology. PeerJ 2, e 422 (2014)."title="Quantification of intraskeletal histovariability in Alligator mississippiensis and implications for vertebrate osteohistology"type="journal article"year="2014">
<bibRefCitationid="EFD0848BFFE70E50FDD457A3FDAAFF51"author="I. Griffiths"box="[522,546,192,216]"journalOrPublisher="Ann. Mag. Nat. Hist."pageId="4"pageNumber="5"pagination="449 - 465"part="4"refId="ref7841"refString="17. I. Griffiths, Skeletal lamellae as an index of age in Heterothermous Tetrapods. Ann. Mag. Nat. Hist. 4, 449 - 465 (1961)."title="Skeletal lamellae as an index of age in Heterothermous Tetrapods"type="journal article"year="1961">
<bibRefCitationid="EFD0848BFFE70E50FDEE57A3FDC0FF51"author="J. M. Hutton"box="[560,584,192,216]"journalOrPublisher="Copeia"pageId="4"pageNumber="5"pagination="332 - 341"part="2"refId="ref7875"refString="18. J. M. Hutton, Age determination of living Nile crocodiles from the cortical stratification of bone. Copeia 2, 332 - 341 (1986)."title="Age determination of living Nile crocodiles from the cortical stratification of bone"type="journal article"year="1986">
intraskeletal histology suggests that the femur is more informative than the tibia, despite regions of cortical remodeling from tendinous entheses about the cortex. Additional intraskeletal histoanalyses of tyrannosaurid specimens are necessary to test whether the femur is the preferred weight-bearing bone for simultaneous assessments of annual growth rates and skeletochronology.
In addition to ontogenetic zonal thickness variability within the cortex, zonal thickness also changed with respect to cortical orientation. That is, zones were often much thinner relative to one another on one side of the transverse section and much thicker on another side (e.g.,
<httpUriid="B5C027D0FFE70E50FF1D5543FEECFDB1"box="[195,356,544,568]"httpUri="https://advances.sciencemag.org/content/suppl/2019/12/20/6.1.eaax6250.DC1"pageId="4"pageNumber="5">fig. S4, G and H</httpUri>
). This pattern is particularly noticeable in the tibia of
(posteromedial cortical zones are thickest). This observation implies that directional cortical growth occurred over ontogeny and stresses the necessity of complete transverse sections for histological analysis: Obtaining a fragment or core for study from one orientation may result in erroneous interpretations of growth rate and skeletal maturity.
<emphasisid="B9352568FFE70E50FFBE5445FECDFCD4"bold="true"pageId="4"pageNumber="5">Variability in annual growth as a response to resource abundance</emphasis>
Interpretations of relative maturity in nonavian dinosaurs often rely on reported trends in the thickness of cortical zones between CGMs from the inner to the outer cortex (
<bibRefCitationid="EFD0848BFFE70E50FE1354FEFE6DFC3C"author="K. Padian & E. - T. Lamm"box="[461,485,925,949]"journalOrPublisher="University of California Press, Berkeley"pageId="4"pageNumber="5"pagination="285"refId="ref7502"refString="10. K. Padian, E. - T. Lamm, Bone Histology of Fossil Tetrapods: Advancing Methods, Analysis, and Interpretation (University of California Press, Berkeley, 2013), p. 285."title="Bone Histology of Fossil Tetrapods: Advancing Methods, Analysis, and Interpretation"type="book chapter"year="2013">
). Zone thickness is typically greatest within the innermost cortex, corresponding to rapid annual growth early in life. Zones become progressively thinner in the midto the outer cortex of older individuals, as annual growth rate decreases approaching asymptotic body length. These general trends provide the interpretive foundation for the two previous histologybased ontogenetic studies on
<bibRefCitationid="EFD0848BFFE70E50FD7F532EFD25FBEC"author="G. M. Erickson & P. J. Makovicky & P. J. Currie & M. A. Norell & S. A. Yerby & C. A. Brochu"box="[673,685,1101,1125]"journalOrPublisher="Nature"pageId="4"pageNumber="5"pagination="772 - 775"part="430"refId="ref7228"refString="4. G. M. Erickson, P. J. Makovicky, P. J. Currie, M. A. Norell, S. A. Yerby, C. A. Brochu, Gigantism and comparative life-history parameters of tyrannosaurid dinosaurs. Nature 430, 772 - 775 (2004)."title="Gigantism and comparative life-history parameters of tyrannosaurid dinosaurs"type="journal article"year="2004">
<bibRefCitationid="EFD0848BFFE70E50FD65532DFD4FFBEC"author="J. R. Horner & K. Padian"box="[699,711,1102,1125]"journalOrPublisher="Proc. R. soc. Lond. B Biol. sci."pageId="4"pageNumber="5"pagination="1875 - 1880"part="271"refId="ref7285"refString="5. J. R. Horner, K. Padian, Age and growth dynamics of Tyrannosaurus rex. Proc. R. soc. Lond. B Biol. sci. 271, 1875 - 1880 (2004)."title="Age and growth dynamics of Tyrannosaurus rex"type="journal article"year="2004">
<figureCitationid="137AE5FFFFE70E50FEC953EBFEDEFB29"box="[279,342,1160,1184]"captionStart="Fig"captionStartId="4.[808,838,1591,1611]"captionTargetBox="[813,1484,161,1574]"captionTargetId="figure@4.[812,1484,160,1575]"captionTargetPageId="4"captionText="Fig. 4. Examples of variable CGM (blue lines) spacing in tyrannosaurids examined for this study. (A) The variability of CGM spacing in the femur of BMRP 2002.4.1 and (B) the tibia of BMRP 2006.4.4 may imply that these individuals were approaching asymptotic body length. Howeverι CGMs within the innermost cortices of much larger T.rex specimens (C) USNM PAL 555000 and (D) MOR 1128 demonstrate that the CGM spacing is not a reliable indicator of relative maturity status.All panels are shown in transverse thin section."figureDoi="http://doi.org/10.5281/zenodo.3749032"httpUri="https://zenodo.org/record/3749032/files/figure.png"pageId="4"pageNumber="5">Fig. 4</figureCitation>
) is narrower than between some CGMs deeper within the cortices, which suggests that, although not adults, the specimens were approaching a body length asymptote at about one-half the body length of
<figureCitationid="137AE5FFFFE70E50FF1B5278FE9CFABA"box="[197,276,1307,1331]"captionStart="Fig"captionStartId="4.[808,838,1591,1611]"captionTargetBox="[813,1484,161,1574]"captionTargetId="figure@4.[812,1484,160,1575]"captionTargetPageId="4"captionText="Fig. 4. Examples of variable CGM (blue lines) spacing in tyrannosaurids examined for this study. (A) The variability of CGM spacing in the femur of BMRP 2002.4.1 and (B) the tibia of BMRP 2006.4.4 may imply that these individuals were approaching asymptotic body length. Howeverι CGMs within the innermost cortices of much larger T.rex specimens (C) USNM PAL 555000 and (D) MOR 1128 demonstrate that the CGM spacing is not a reliable indicator of relative maturity status.All panels are shown in transverse thin section."figureDoi="http://doi.org/10.5281/zenodo.3749032"httpUri="https://zenodo.org/record/3749032/files/figure.png"pageId="4"pageNumber="5">Fig. 4A</figureCitation>
<figureCitationid="137AE5FFFFE70E50FDDE5278FDC5FABA"box="[512,589,1307,1331]"captionStart="Fig"captionStartId="4.[808,838,1591,1611]"captionTargetBox="[813,1484,161,1574]"captionTargetId="figure@4.[812,1484,160,1575]"captionTargetPageId="4"captionText="Fig. 4. Examples of variable CGM (blue lines) spacing in tyrannosaurids examined for this study. (A) The variability of CGM spacing in the femur of BMRP 2002.4.1 and (B) the tibia of BMRP 2006.4.4 may imply that these individuals were approaching asymptotic body length. Howeverι CGMs within the innermost cortices of much larger T.rex specimens (C) USNM PAL 555000 and (D) MOR 1128 demonstrate that the CGM spacing is not a reliable indicator of relative maturity status.All panels are shown in transverse thin section."figureDoi="http://doi.org/10.5281/zenodo.3749032"httpUri="https://zenodo.org/record/3749032/files/figure.png"pageId="4"pageNumber="5">Fig. 4B</figureCitation>
) are variable, and zones do not consistently progress from widely spaced within the inner cortex to more closely spaced in the outer cortex. Because of unpredictable spacing within the cortex, reduced zonal thickness near the periosteal surface is likely an unreliable indicator of skeletal maturity in
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,
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. In all individuals, variability in annual zonal thicknesses was observed. In particular, compared to zone spacing within the mid-cortex, noticeably thinner zones are present within the innermost cortex of
<materialsCitationid="3B29F327FFE70E50FF2E51D6FE3AF944"ID-GBIF-Occurrence="3396425391"box="[240,434,1717,1742]"collectionCode="USNM"httpUri="http://n2t.net/ark:/65665/381d4ee9c-91b4-4ce0-89eb-9053746a9351"pageId="4"pageNumber="5"specimenCode="USNM PAL 555000">USNM PAL 555000</materialsCitation>
(
<figureCitationid="137AE5FFFFE70E50FE6351D6FD8DF944"box="[445,517,1717,1741]"captionStart="Fig"captionStartId="4.[808,838,1591,1611]"captionTargetBox="[813,1484,161,1574]"captionTargetId="figure@4.[812,1484,160,1575]"captionTargetPageId="4"captionText="Fig. 4. Examples of variable CGM (blue lines) spacing in tyrannosaurids examined for this study. (A) The variability of CGM spacing in the femur of BMRP 2002.4.1 and (B) the tibia of BMRP 2006.4.4 may imply that these individuals were approaching asymptotic body length. Howeverι CGMs within the innermost cortices of much larger T.rex specimens (C) USNM PAL 555000 and (D) MOR 1128 demonstrate that the CGM spacing is not a reliable indicator of relative maturity status.All panels are shown in transverse thin section."figureDoi="http://doi.org/10.5281/zenodo.3749032"httpUri="https://zenodo.org/record/3749032/files/figure.png"pageId="4"pageNumber="5">Fig. 4C</figureCitation>
<figureCitationid="137AE5FFFFE70E50FD6C51D6FD75F944"box="[690,765,1717,1741]"captionStart="Fig"captionStartId="4.[808,838,1591,1611]"captionTargetBox="[813,1484,161,1574]"captionTargetId="figure@4.[812,1484,160,1575]"captionTargetPageId="4"captionText="Fig. 4. Examples of variable CGM (blue lines) spacing in tyrannosaurids examined for this study. (A) The variability of CGM spacing in the femur of BMRP 2002.4.1 and (B) the tibia of BMRP 2006.4.4 may imply that these individuals were approaching asymptotic body length. Howeverι CGMs within the innermost cortices of much larger T.rex specimens (C) USNM PAL 555000 and (D) MOR 1128 demonstrate that the CGM spacing is not a reliable indicator of relative maturity status.All panels are shown in transverse thin section."figureDoi="http://doi.org/10.5281/zenodo.3749032"httpUri="https://zenodo.org/record/3749032/files/figure.png"pageId="4"pageNumber="5">Fig. 4D</figureCitation>
). These results contradict the mathematically predictable zonal spacing in
<bibRefCitationid="EFD0848BFFE70E50FDA85193FD0AF88E"author="J. R. Horner & K. Padian"box="[630,642,1776,1799]"journalOrPublisher="Proc. R. soc. Lond. B Biol. sci."pageId="4"pageNumber="5"pagination="1875 - 1880"part="271"refId="ref7285"refString="5. J. R. Horner, K. Padian, Age and growth dynamics of Tyrannosaurus rex. Proc. R. soc. Lond. B Biol. sci. 271, 1875 - 1880 (2004)."title="Age and growth dynamics of Tyrannosaurus rex"type="journal article"year="2004">
had not yet entered the accelerated growth period proposed for this taxon (
<bibRefCitationid="EFD0848BFFE70E50FCAE506DFCF4F8AF"author="G. M. Erickson & P. J. Makovicky & P. J. Currie & M. A. Norell & S. A. Yerby & C. A. Brochu"box="[880,892,1806,1830]"journalOrPublisher="Nature"pageId="4"pageNumber="5"pagination="772 - 775"part="430"refId="ref7228"refString="4. G. M. Erickson, P. J. Makovicky, P. J. Currie, M. A. Norell, S. A. Yerby, C. A. Brochu, Gigantism and comparative life-history parameters of tyrannosaurid dinosaurs. Nature 430, 772 - 775 (2004)."title="Gigantism and comparative life-history parameters of tyrannosaurid dinosaurs"type="journal article"year="2004">
<bibRefCitationid="EFD0848BFFE70E50FC59506DFC1BF8AC"author="J. R. Horner & K. Padian"box="[903,915,1806,1829]"journalOrPublisher="Proc. R. soc. Lond. B Biol. sci."pageId="4"pageNumber="5"pagination="1875 - 1880"part="271"refId="ref7285"refString="5. J. R. Horner, K. Padian, Age and growth dynamics of Tyrannosaurus rex. Proc. R. soc. Lond. B Biol. sci. 271, 1875 - 1880 (2004)."title="Age and growth dynamics of Tyrannosaurus rex"type="journal article"year="2004">
<bibRefCitationid="EFD0848BFFE70E50FBAC5048FBF6F8CA"author="G. M. Erickson & P. J. Makovicky & P. J. Currie & M. A. Norell & S. A. Yerby & C. A. Brochu"box="[1138,1150,1835,1859]"journalOrPublisher="Nature"pageId="4"pageNumber="5"pagination="772 - 775"part="430"refId="ref7228"refString="4. G. M. Erickson, P. J. Makovicky, P. J. Currie, M. A. Norell, S. A. Yerby, C. A. Brochu, Gigantism and comparative life-history parameters of tyrannosaurid dinosaurs. Nature 430, 772 - 775 (2004)."title="Gigantism and comparative life-history parameters of tyrannosaurid dinosaurs"type="journal article"year="2004">
<emphasisid="B9352568FFE70E50FCF65154FC53F9EC"bold="true"pageId="4"pageNumber="5">Fig. 4. Examples of variable CGM (blue lines) spacing in tyrannosaurids examined for this study.</emphasis>
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Variable LAG spacing is reported in ornithomimids, ornithopods [(
<bibRefCitationid="EFD0848BFFE60E51FFAF57A3FF00FF51"author="T. M. Cullen & D. C. Evans & M. J. Ryan & P. J. Currie & Y. Kobayashi"box="[113,136,192,216]"journalOrPublisher="BMC Evol. Biol."pageId="5"pageNumber="6"pagination="231"part="14"refId="ref7906"refString="19. T. M. Cullen, D. C. Evans, M. J. Ryan, P. J. Currie, Y. Kobayashi, Osteohistological variation in growth marks and osteocyte lacunar density in a theropod dinosaur (Coelurosauria: Ornithomimidae). BMC Evol. Biol. 14, 231 (2014)."title="Osteohistological variation in growth marks and osteocyte lacunar density in a theropod dinosaur (Coelurosauria: Ornithomimidae)"type="journal article"year="2014">
) and references therein], and other tyrannosauroids (
<bibRefCitationid="EFD0848BFFE60E51FD5157A3FD2EFF51"author="L. E. Zanno & R. T. Tucker & A. Canoville & H. M. Avrahami & T. A. Gates & P. J. Makovicky"box="[655,678,192,216]"journalOrPublisher="Commun. Biol."pageId="5"pageNumber="6"pagination="64"part="2"refId="ref7736"refString="15. L. E. Zanno, R. T. Tucker, A. Canoville, H. M. Avrahami, T. A. Gates, P. J. Makovicky, Diminutive fleet-footed tyrannosauroid narrows the 70 - million-year gap in the North American fossil record. Commun. Biol. 2, 64 (2019)."title="Diminutive fleet-footed tyrannosauroid narrows the 70 - million-year gap in the North American fossil record"type="journal article"year="2019">
) and may correlate with annual resource abundance (
<bibRefCitationid="EFD0848BFFE60E51FDCE57BEFDA0FF7C"author="M. Kohler & N. Marin-Moratalla & X. Jordana & R. Aanes"box="[528,552,221,245]"journalOrPublisher="Nature"pageId="5"pageNumber="6"pagination="358 - 361"part="487"refId="ref7590"refString="12. M. Kohler, N. Marin-Moratalla, X. Jordana, R. Aanes, Seasonal bone growth and physiology in endotherms shed light on dinosaur physiology. Nature 487, 358 - 361 (2012)."title="Seasonal bone growth and physiology in endotherms shed light on dinosaur physiology"type="journal article"year="2012">
<bibRefCitationid="EFD0848BFFE60E51FDEA57BEFDC4FF7C"author="T. M. Cullen & D. C. Evans & M. J. Ryan & P. J. Currie & Y. Kobayashi"box="[564,588,221,245]"journalOrPublisher="BMC Evol. Biol."pageId="5"pageNumber="6"pagination="231"part="14"refId="ref7906"refString="19. T. M. Cullen, D. C. Evans, M. J. Ryan, P. J. Currie, Y. Kobayashi, Osteohistological variation in growth marks and osteocyte lacunar density in a theropod dinosaur (Coelurosauria: Ornithomimidae). BMC Evol. Biol. 14, 231 (2014)."title="Osteohistological variation in growth marks and osteocyte lacunar density in a theropod dinosaur (Coelurosauria: Ornithomimidae)"type="journal article"year="2014">
: Because the level of bone tissue organization within zones remained the same from the innermost cortex to the periosteal surface in the BMRP specimens, growth rates were within a similar range from year to year. To produce these extremes in annual bone apposition, the duration of the growth hiatus must have varied annually. On the basis of the larger
specimens examined here for comparison, the adjustment of annual growth hiatus duration in response to resource abundance is a physiological characteristic observed throughout
ontogeny. Regardless of cause, unpredictable CGM spacing observed here and in previous studies stresses caution when inferring relative maturity based on cortical LAG spacing (
<bibRefCitationid="EFD0848BFFE60E51FF2A555EFE84FDDC"author="T. M. Cullen & D. C. Evans & M. J. Ryan & P. J. Currie & Y. Kobayashi"box="[244,268,573,597]"journalOrPublisher="BMC Evol. Biol."pageId="5"pageNumber="6"pagination="231"part="14"refId="ref7906"refString="19. T. M. Cullen, D. C. Evans, M. J. Ryan, P. J. Currie, Y. Kobayashi, Osteohistological variation in growth marks and osteocyte lacunar density in a theropod dinosaur (Coelurosauria: Ornithomimidae). BMC Evol. Biol. 14, 231 (2014)."title="Osteohistological variation in growth marks and osteocyte lacunar density in a theropod dinosaur (Coelurosauria: Ornithomimidae)"type="journal article"year="2014">
<taxonomicNameid="4C4182F9FFE60E51FE9E558EFE55FC8F"authorityName="Bakker, Currie & Williams"authorityYear="1988"box="[320,477,749,774]"class="Reptilia"family="Tyrannosauridae"genus="Nanotyrannus"higherTaxonomySource="GBIF"kingdom="Animalia"order="Dinosauria"pageId="5"pageNumber="6"phylum="Chordata"rank="genus">
ontogeny but also have bearing on discussions concerning
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and
<taxonomicNameid="4C4182F9FFE60E51FFBE5400FF65FCF3"authorityName="Bakker, Currie & Williams"authorityYear="1988"box="[96,237,867,890]"class="Reptilia"family="Tyrannosauridae"genus="Nanotyrannus"higherTaxonomySource="GBIF"kingdom="Animalia"order="Dinosauria"pageId="5"pageNumber="6"phylum="Chordata"rank="genus">
consists of a small isolated skull 572 mm in length (
<bibRefCitationid="EFD0848BFFE60E51FF1754E3FF69FC11"author="T. D. Carr"box="[201,225,896,920]"journalOrPublisher="J. Vertebr. Paleontol."pageId="5"pageNumber="6"pagination="497 - 520"part="19"refId="ref7967"refString="20. T. D. Carr, Craniofacial ontogeny in Tyrannosauridae (Dinosauria, Coelurosauria). J. Vertebr. Paleontol. 19, 497 - 520 (1999)."title="Craniofacial ontogeny in Tyrannosauridae (Dinosauria, Coelurosauria)"type="journal article"year="1999">
<bibRefCitationid="EFD0848BFFE60E51FEA154FEFE1DFC3C"author="C. W. Gilmore"box="[383,405,925,949]"journalOrPublisher="smithson. misc. collect."pageId="5"pageNumber="6"pagination="1 - 19"part="106"refId="ref8000"refString="21. C. W. Gilmore, New carnivorous dinosaur from the Lance formation of Montana. smithson. misc. collect. 106, 1 - 19 (1946)."title="New carnivorous dinosaur from the Lance formation of Montana"type="journal article"year="1946">
<bibRefCitationid="EFD0848BFFE60E51FDA654FEFD06FC3C"author="R. T. Bakker & M. Williams & P. J. Currie"box="[632,654,925,949]"journalOrPublisher="Hunteria"pageId="5"pageNumber="6"pagination="1 - 30"part="1"refId="ref8033"refString="22. R. T. Bakker, M. Williams, P. J. Currie, Nanotyrannus, a new genus of pygmy tyrannosaur, from the latest Cretaceous of Montana. Hunteria 1, 1 - 30 (1988)."title="Nanotyrannus, a new genus of pygmy tyrannosaur, from the latest Cretaceous of Montana"type="journal article"year="1988">
<taxonomicNameid="4C4182F9FFE60E51FDAF54D8FC8AFC5B"authorityName="Bakker, Currie & Williams"authorityYear="1988"box="[625,770,955,978]"class="Reptilia"family="Tyrannosauridae"genus="Nanotyrannus"higherTaxonomySource="GBIF"kingdom="Animalia"order="Dinosauria"pageId="5"pageNumber="6"phylum="Chordata"rank="genus">
. Using an extensive empirical dataset, Carr and Williamson (
<bibRefCitationid="EFD0848BFFE60E51FD4A54BBFD23FC79"author="T. D. Carr & T. E. Williamson"box="[660,683,984,1008]"journalOrPublisher="Zool. J. Linnean soc."pageId="5"pageNumber="6"pagination="419 - 523"part="142"refId="ref8077"refString="23. T. D. Carr, T. E. Williamson, Diversity of Late Maastrichtian Tyrannosauridae (Dinosauria: Theropoda) from western North America. Zool. J. Linnean soc. 142, 419 - 523 (2004)."title="Diversity of Late Maastrichtian Tyrannosauridae (Dinosauria: Theropoda) from western North America"type="journal article"year="2004">
<taxonomicNameid="4C4182F9FFE60E51FF345495FEFFFB84"authorityName="Bakker, Currie & Williams"authorityYear="1988"box="[234,375,1014,1037]"class="Reptilia"family="Tyrannosauridae"genus="Nanotyrannus"higherTaxonomySource="GBIF"kingdom="Animalia"order="Dinosauria"pageId="5"pageNumber="6"phylum="Chordata"rank="genus">
<bibRefCitationid="EFD0848BFFE60E51FE895353FEE6FBC1"author="A. K. Rozhdestvensky"box="[343,366,1072,1096]"journalOrPublisher="Paleontol. Zh."pageId="5"pageNumber="6"pagination="95 - 109"part="3"refId="ref8122"refString="24. A. K. Rozhdestvensky, Growth changes in Asian dinosaurs and some problems of their taxonomy. Paleontol. Zh. 3, 95 - 109 (1965)."title="Growth changes in Asian dinosaurs and some problems of their taxonomy"type="journal article"year="1965">
based on morphological skull features shared with those found in undisputed juvenile individuals of other tyrannosaurid taxa [e.g., (
<bibRefCitationid="EFD0848BFFE60E51FF4053C6FF22FB34"author="S. L. Brusatte & M. A. Norell & T. D. Carr & G. M. Erickson & J. R. Hutchinson & A. M. Balanoff & G. S. Bever & J. N. Choiniere & P. J. Makovicky & X. Xu"box="[158,170,1189,1213]"journalOrPublisher="science"pageId="5"pageNumber="6"pagination="1481 - 1485"part="329"refId="ref7118"refString="2. S. L. Brusatte, M. A. Norell, T. D. Carr, G. M. Erickson, J. R. Hutchinson, A. M. Balanoff, G. S. Bever, J. N. Choiniere, P. J. Makovicky, X. Xu, Tyrannosaur paleobiology: New research on ancient exemplar organisms. science 329, 1481 - 1485 (2010)."title="Tyrannosaur paleobiology: New research on ancient exemplar organisms"type="journal article"year="2010">
<bibRefCitationid="EFD0848BFFE60E51FF6B53C6FF44FB34"author="T. D. Carr"box="[181,204,1189,1213]"journalOrPublisher="J. Vertebr. Paleontol."pageId="5"pageNumber="6"pagination="497 - 520"part="19"refId="ref7967"refString="20. T. D. Carr, Craniofacial ontogeny in Tyrannosauridae (Dinosauria, Coelurosauria). J. Vertebr. Paleontol. 19, 497 - 520 (1999)."title="Craniofacial ontogeny in Tyrannosauridae (Dinosauria, Coelurosauria)"type="journal article"year="1999">
<bibRefCitationid="EFD0848BFFE60E51FF0753C6FF78FB34"author="T. D. Carr & T. E. Williamson"box="[217,240,1189,1213]"journalOrPublisher="Zool. J. Linnean soc."pageId="5"pageNumber="6"pagination="419 - 523"part="142"refId="ref8077"refString="23. T. D. Carr, T. E. Williamson, Diversity of Late Maastrichtian Tyrannosauridae (Dinosauria: Theropoda) from western North America. Zool. J. Linnean soc. 142, 419 - 523 (2004)."title="Diversity of Late Maastrichtian Tyrannosauridae (Dinosauria: Theropoda) from western North America"type="journal article"year="2004">
<bibRefCitationid="EFD0848BFFE60E51FF2253C6FE9BFB34"author="C. A. Brochu"box="[252,275,1189,1213]"journalOrPublisher="J. Vertebr. Paleontol. Memoir"pageId="5"pageNumber="6"pagination="1 - 138"part="22"refId="ref8155"refString="25. C. A. Brochu, Osteology of Tyrannosaurus rex: Insights from a nearly complete skeleton and high-resolution computed tomographic analysis of the skull. J. Vertebr. Paleontol. Memoir 22, 1 - 138 (2003)."title="Osteology of Tyrannosaurus rex: Insights from a nearly complete skeleton and high-resolution computed tomographic analysis of the skull"type="journal article"year="2003">25</bibRefCitation>
–
<bibRefCitationid="EFD0848BFFE60E51FEFF53C6FEB0FB34"author="T. R. Holtz Jr."box="[289,312,1189,1213]"editor="D. Weishampel & P. Dodson & H. Osmolska"journalOrPublisher="University of California Press, Berkeley"pageId="5"pageNumber="6"pagination="111 - 136"refId="ref8336"refString="28. T. R. Holtz Jr., The Dinosauria, D. Weishampel, P. Dodson, H. Osmolska, Eds. (University of California Press, Berkeley, 2004), pp. 111 - 136."title="The Dinosauria"type="book chapter"year="2004">28</bibRefCitation>
</emphasis>
)]. Nonetheless, several publications have since argued for the validity of
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<bibRefCitationid="EFD0848BFFE60E51FF455278FF3AFABA"author="T. Tsuihiji & M. Watabe & K. Tsogtbaatar & T. Tsubamoto & R. Barsbold & S. Suzuki & A. H. Lee & R. C. Ridgely & Y. Kawahara & L. M. Witmer"box="[155,178,1307,1331]"journalOrPublisher="J. Vertebr. Paleontol."pageId="5"pageNumber="6"pagination="497 - 517"part="31"refId="ref8380"refString="29. T. Tsuihiji, M. Watabe, K. Tsogtbaatar, T. Tsubamoto, R. Barsbold, S. Suzuki, A. H. Lee, R. C. Ridgely, Y. Kawahara, L. M. Witmer, Cranial osteology of a juvenile specimen of Tarbosaurus bataar from the Nemegt Formation (Upper Cretaceous) of Bugin Tsav, Mongolia. J. Vertebr. Paleontol. 31, 497 - 517 (2011)."title="Cranial osteology of a juvenile specimen of Tarbosaurus bataar from the Nemegt Formation (Upper Cretaceous) of Bugin Tsav, Mongolia"type="journal article"year="2011">29</bibRefCitation>
–
<bibRefCitationid="EFD0848BFFE60E51FF615278FF5EFABA"author="L. M. Witmer & R. C. Ridgely"box="[191,214,1307,1331]"journalOrPublisher="Kirtlandia"pageId="5"pageNumber="6"pagination="61 - 81"part="57"refId="ref8616"refString="33. L. M. Witmer, R. C. Ridgely, The Cleveland tyrannosaur skull (Nanotyrannus or Tyrannosaurus): new findings based on CT scanning, with special reference to the braincase. Kirtlandia 57, 61 - 81 (2010)."title="The Cleveland tyrannosaur skull (Nanotyrannus or Tyrannosaurus): new findings based on CT scanning, with special reference to the braincase"type="journal article"year="2010">33</bibRefCitation>
</emphasis>
)], which some researchers have assigned to
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<bibRefCitationid="EFD0848BFFE60E51FE7E5236FE30FAE4"author="T. Tsuihiji & M. Watabe & K. Tsogtbaatar & T. Tsubamoto & R. Barsbold & S. Suzuki & A. H. Lee & R. C. Ridgely & Y. Kawahara & L. M. Witmer"box="[416,440,1365,1389]"journalOrPublisher="J. Vertebr. Paleontol."pageId="5"pageNumber="6"pagination="497 - 517"part="31"refId="ref8380"refString="29. T. Tsuihiji, M. Watabe, K. Tsogtbaatar, T. Tsubamoto, R. Barsbold, S. Suzuki, A. H. Lee, R. C. Ridgely, Y. Kawahara, L. M. Witmer, Cranial osteology of a juvenile specimen of Tarbosaurus bataar from the Nemegt Formation (Upper Cretaceous) of Bugin Tsav, Mongolia. J. Vertebr. Paleontol. 31, 497 - 517 (2011)."title="Cranial osteology of a juvenile specimen of Tarbosaurus bataar from the Nemegt Formation (Upper Cretaceous) of Bugin Tsav, Mongolia"type="journal article"year="2011">29</bibRefCitation>
–
<bibRefCitationid="EFD0848BFFE60E51FE185236FE56FAE4"author="L. M. Witmer & R. C. Ridgely"box="[454,478,1365,1389]"journalOrPublisher="Kirtlandia"pageId="5"pageNumber="6"pagination="61 - 81"part="57"refId="ref8616"refString="33. L. M. Witmer, R. C. Ridgely, The Cleveland tyrannosaur skull (Nanotyrannus or Tyrannosaurus): new findings based on CT scanning, with special reference to the braincase. Kirtlandia 57, 61 - 81 (2010)."title="The Cleveland tyrannosaur skull (Nanotyrannus or Tyrannosaurus): new findings based on CT scanning, with special reference to the braincase"type="journal article"year="2010">33</bibRefCitation>
is the only accessioned specimen with postcranial skeletal elements preserved that is specifically argued by proponents of
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<bibRefCitationid="EFD0848BFFE60E51FE7D52CEFE33FA4C"author="T. Tsuihiji & M. Watabe & K. Tsogtbaatar & T. Tsubamoto & R. Barsbold & S. Suzuki & A. H. Lee & R. C. Ridgely & Y. Kawahara & L. M. Witmer"box="[419,443,1453,1477]"journalOrPublisher="J. Vertebr. Paleontol."pageId="5"pageNumber="6"pagination="497 - 517"part="31"refId="ref8380"refString="29. T. Tsuihiji, M. Watabe, K. Tsogtbaatar, T. Tsubamoto, R. Barsbold, S. Suzuki, A. H. Lee, R. C. Ridgely, Y. Kawahara, L. M. Witmer, Cranial osteology of a juvenile specimen of Tarbosaurus bataar from the Nemegt Formation (Upper Cretaceous) of Bugin Tsav, Mongolia. J. Vertebr. Paleontol. 31, 497 - 517 (2011)."title="Cranial osteology of a juvenile specimen of Tarbosaurus bataar from the Nemegt Formation (Upper Cretaceous) of Bugin Tsav, Mongolia"type="journal article"year="2011">29</bibRefCitation>
–
<bibRefCitationid="EFD0848BFFE60E51FE1652CEFE68FA4C"author="N. L. Larson"box="[456,480,1453,1477]"editor="P. Larson & K. Carpenter"journalOrPublisher="Indiana Univ. Press, Bloomington"pageId="5"pageNumber="6"pagination="1 - 56"refId="ref8573"refString="32. N. L. Larson, in Tyrannosaurus rex, the Tyrant King, P. Larson, K. Carpenter, Eds. (Indiana Univ. Press, Bloomington, 2008), pp. 1 - 56."type="book chapter"volumeTitle="Tyrannosaurus rex, the Tyrant King"year="2008">32</bibRefCitation>
<taxonomicNameid="4C4182F9FFE60E51FDDC52A8FD07FA6B"authorityName="Bakker, Currie & Williams"authorityYear="1988"box="[514,655,1483,1506]"class="Reptilia"family="Tyrannosauridae"genus="Nanotyrannus"higherTaxonomySource="GBIF"kingdom="Animalia"order="Dinosauria"pageId="5"pageNumber="6"phylum="Chordata"rank="genus">
Here, we provide histological data that can be used to reject the hypothesis that
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was erected on the basis of a skeletally mature “pygmy” individual, resulting in two remaining alternative hypotheses: (i)
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are the only weight-bearing bones of Upper Cretaceous HCF tyrannosaurids described histologically from complete transverse sections, and these universally demonstrate features characteristic of actively growing juvenile dinosaurs that had not yet entered an exponential phase of growth (as demonstrated by our new data identifying noticeably thinner zones within the innermost cortex of large-bodied
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). On the basis of these data, the latter hypothesis is most parsimonious and is congruent with the morphology-based conclusions of Carr (
<bibRefCitationid="EFD0848BFFE60E51FBDA56EEFB95FE2C"author="T. D. Carr"box="[1028,1053,397,421]"journalOrPublisher="J. Vertebr. Paleontol."pageId="5"pageNumber="6"pagination="497 - 520"part="19"refId="ref7967"refString="20. T. D. Carr, Craniofacial ontogeny in Tyrannosauridae (Dinosauria, Coelurosauria). J. Vertebr. Paleontol. 19, 497 - 520 (1999)."title="Craniofacial ontogeny in Tyrannosauridae (Dinosauria, Coelurosauria)"type="journal article"year="1999">
<bibRefCitationid="EFD0848BFFE60E51FA9B56EEFAD6FE2C"author="T. D. Carr & T. E. Williamson"box="[1349,1374,397,421]"journalOrPublisher="Zool. J. Linnean soc."pageId="5"pageNumber="6"pagination="419 - 523"part="142"refId="ref8077"refString="23. T. D. Carr, T. E. Williamson, Diversity of Late Maastrichtian Tyrannosauridae (Dinosauria: Theropoda) from western North America. Zool. J. Linnean soc. 142, 419 - 523 (2004)."title="Diversity of Late Maastrichtian Tyrannosauridae (Dinosauria: Theropoda) from western North America"type="journal article"year="2004">
). Incorporating additional mid-sized HCF tyrannosaurid specimens into this histology-based relative maturity assessment is necessary to further support or refute the parsimonious hypothesis.
<treatmentCitationid="0AE0DF6BFFE60E51FC34555DFBF0FDDC"authorityName="Bakker et al."authorityYear="1988"box="[1002,1144,574,597]"httpUri="http://treatment.plazi.org/id/03A1879D-FFD0-FFE9-5E7F-F664FEA6A618"pageId="5"pageNumber="6">
<taxonomicNameid="4C4182F9FFE60E51FC34555DFBF0FDDC"authorityName="Bakker, Currie & Williams"authorityYear="1988"baseAuthorityName="Gilmore"baseAuthorityYear="1946"box="[1002,1144,574,597]"class="Reptilia"family="Tyrannosauridae"genus="Nanotyrannus"higherTaxonomySource="GBIF"kingdom="Animalia"order="Dinosauria"pageId="5"pageNumber="6"phylum="Chordata"rank="species"species="lancensis">
occupied the large-sized carnivore niche in the latest Cretaceous HCF ecosystem (
<bibRefCitationid="EFD0848BFFE60E51FB1055D0FB52FD42"author="S. L. Brusatte & M. A. Norell & T. D. Carr & G. M. Erickson & J. R. Hutchinson & A. M. Balanoff & G. S. Bever & J. N. Choiniere & P. J. Makovicky & X. Xu"box="[1230,1242,691,715]"journalOrPublisher="science"pageId="5"pageNumber="6"pagination="1481 - 1485"part="329"refId="ref7118"refString="2. S. L. Brusatte, M. A. Norell, T. D. Carr, G. M. Erickson, J. R. Hutchinson, A. M. Balanoff, G. S. Bever, J. N. Choiniere, P. J. Makovicky, X. Xu, Tyrannosaur paleobiology: New research on ancient exemplar organisms. science 329, 1481 - 1485 (2010)."title="Tyrannosaur paleobiology: New research on ancient exemplar organisms"type="journal article"year="2010">
<bibRefCitationid="EFD0848BFFE60E51FB3955D0FB77FD42"author="J. R. Horner & M. B. Goodwin & N. Myhrvold"box="[1255,1279,691,715]"journalOrPublisher="PLOs ONE"pageId="5"pageNumber="6"pagination="e 16574"part="6"refId="ref8664"refString="34. J. R. Horner, M. B. Goodwin, N. Myhrvold, Dinosaur census reveals abundant Tyrannosaurus and rare ontogenetic stages in the Upper Cretaceous Hell Creek Formation (Maastrichtian), Montana, USA. PLOs ONE 6, e 16574 (2011)."title="Dinosaur census reveals abundant Tyrannosaurus and rare ontogenetic stages in the Upper Cretaceous Hell Creek Formation (Maastrichtian), Montana, USA"type="journal article"year="2011">
), achieving an average adult body mass of ~9502 kg (
<bibRefCitationid="EFD0848BFFE60E51FB5755B3FB1DFD61"author="J. R. Hutchinson & K. T. Bates & J. Molnar & V. Allen & P. J. Makovicky"box="[1161,1173,720,744]"journalOrPublisher="PLOs ONE"pageId="5"pageNumber="6"pagination="e 26037"part="6"refId="ref7327"refString="6. J. R. Hutchinson, K. T. Bates, J. Molnar, V. Allen, P. J. Makovicky, A computational analysis of limb and body dimensions in Tyrannosaurus rex with implications for locomotion, ontogeny, and growth. PLOs ONE 6, e 26037 (2011)."title="A computational analysis of limb and body dimensions in Tyrannosaurus rex with implications for locomotion, ontogeny, and growth"type="journal article"year="2011">
<bibRefCitationid="EFD0848BFFE60E51FAB555B3FAFFFD61"author="G. M. Erickson & P. J. Makovicky & P. J. Currie & M. A. Norell & S. A. Yerby & C. A. Brochu"box="[1387,1399,720,744]"journalOrPublisher="Nature"pageId="5"pageNumber="6"pagination="772 - 775"part="430"refId="ref7228"refString="4. G. M. Erickson, P. J. Makovicky, P. J. Currie, M. A. Norell, S. A. Yerby, C. A. Brochu, Gigantism and comparative life-history parameters of tyrannosaurid dinosaurs. Nature 430, 772 - 775 (2004)."title="Gigantism and comparative life-history parameters of tyrannosaurid dinosaurs"type="journal article"year="2004">
<bibRefCitationid="EFD0848BFFE60E51FB395468FB7BFCAA"author="J. R. Hutchinson & K. T. Bates & J. Molnar & V. Allen & P. J. Makovicky"box="[1255,1267,779,803]"journalOrPublisher="PLOs ONE"pageId="5"pageNumber="6"pagination="e 26037"part="6"refId="ref7327"refString="6. J. R. Hutchinson, K. T. Bates, J. Molnar, V. Allen, P. J. Makovicky, A computational analysis of limb and body dimensions in Tyrannosaurus rex with implications for locomotion, ontogeny, and growth. PLOs ONE 6, e 26037 (2011)."title="A computational analysis of limb and body dimensions in Tyrannosaurus rex with implications for locomotion, ontogeny, and growth"type="journal article"year="2011">
<bibRefCitationid="EFD0848BFFE60E51FB215468FA83FCAB"author="P. J. Currie"box="[1279,1291,779,802]"journalOrPublisher="Can. J. Earth sci."pageId="5"pageNumber="6"pagination="651 - 665"part="40"refId="ref7386"refString="7. P. J. Currie, Allometric growth in tyrannosaurids (Dinosauria: Theropoda) from the Upper Cretaceous of North America and Asia. Can. J. Earth sci. 40, 651 - 665 (2003)."title="Allometric growth in tyrannosaurids (Dinosauria: Theropoda) from the Upper Cretaceous of North America and Asia"type="journal article"year="2003">
<bibRefCitationid="EFD0848BFFE60E51FCEF544BFCB5FCC9"author="J. R. Hutchinson & K. T. Bates & J. Molnar & V. Allen & P. J. Makovicky"box="[817,829,808,832]"journalOrPublisher="PLOs ONE"pageId="5"pageNumber="6"pagination="e 26037"part="6"refId="ref7327"refString="6. J. R. Hutchinson, K. T. Bates, J. Molnar, V. Allen, P. J. Makovicky, A computational analysis of limb and body dimensions in Tyrannosaurus rex with implications for locomotion, ontogeny, and growth. PLOs ONE 6, e 26037 (2011)."title="A computational analysis of limb and body dimensions in Tyrannosaurus rex with implications for locomotion, ontogeny, and growth"type="journal article"year="2011">
, which falls within the mid-sized dinosaur body mass range defined by Holtz (
<bibRefCitationid="EFD0848BFFE60E51FC055400FC7BFCF2"author="T. R. Holtz Jr."box="[987,1011,867,891]"journalOrPublisher="J. Vertebr. Paleontol."pageId="5"pageNumber="6"pagination="72 A"part="24"refId="ref8716"refString="35. T. R. Holtz Jr., Taxonomic diversity, morphological disparity, and guild structure in theropod carnivore communities: implications for paleoecology and life history strategies in tyrant dinosaurs. J. Vertebr. Paleontol. 24, 72 A (2004)."title="Taxonomic diversity, morphological disparity, and guild structure in theropod carnivore communities: implications for paleoecology and life history strategies in tyrant dinosaurs"type="journal article"year="2004">
relative to the ontogenetic timing of exponential growth in other tyrannosaurids (
<bibRefCitationid="EFD0848BFFE60E51FBD754BBFB9DFC79"author="G. M. Erickson & P. J. Makovicky & P. J. Currie & M. A. Norell & S. A. Yerby & C. A. Brochu"box="[1033,1045,984,1008]"journalOrPublisher="Nature"pageId="5"pageNumber="6"pagination="772 - 775"part="430"refId="ref7228"refString="4. G. M. Erickson, P. J. Makovicky, P. J. Currie, M. A. Norell, S. A. Yerby, C. A. Brochu, Gigantism and comparative life-history parameters of tyrannosaurid dinosaurs. Nature 430, 772 - 775 (2004)."title="Gigantism and comparative life-history parameters of tyrannosaurid dinosaurs"type="journal article"year="2004">
<bibRefCitationid="EFD0848BFFE60E51FC515495FC12FB87"author="G. M. Erickson & P. J. Makovicky & P. J. Currie & M. A. Norell & S. A. Yerby & C. A. Brochu"box="[911,922,1014,1038]"journalOrPublisher="Nature"pageId="5"pageNumber="6"pagination="772 - 775"part="430"refId="ref7228"refString="4. G. M. Erickson, P. J. Makovicky, P. J. Currie, M. A. Norell, S. A. Yerby, C. A. Brochu, Gigantism and comparative life-history parameters of tyrannosaurid dinosaurs. Nature 430, 772 - 775 (2004)."title="Gigantism and comparative life-history parameters of tyrannosaurid dinosaurs"type="journal article"year="2004">
), many aspects of its biology likely differed between juvenile and adult individuals, leading to hypotheses that it used ontogenetic niche partitioning (
<bibRefCitationid="EFD0848BFFE60E51FC3A5353FC78FBC1"author="S. L. Brusatte & M. A. Norell & T. D. Carr & G. M. Erickson & J. R. Hutchinson & A. M. Balanoff & G. S. Bever & J. N. Choiniere & P. J. Makovicky & X. Xu"box="[996,1008,1072,1096]"journalOrPublisher="science"pageId="5"pageNumber="6"pagination="1481 - 1485"part="329"refId="ref7118"refString="2. S. L. Brusatte, M. A. Norell, T. D. Carr, G. M. Erickson, J. R. Hutchinson, A. M. Balanoff, G. S. Bever, J. N. Choiniere, P. J. Makovicky, X. Xu, Tyrannosaur paleobiology: New research on ancient exemplar organisms. science 329, 1481 - 1485 (2010)."title="Tyrannosaur paleobiology: New research on ancient exemplar organisms"type="journal article"year="2010">
<bibRefCitationid="EFD0848BFFE60E51FC245353FB99FBC1"author="T. R. Holtz Jr."box="[1018,1041,1072,1096]"editor="P. Larson & K. Carpenter"journalOrPublisher="Indiana Univ. Press, Bloomington"pageId="5"pageNumber="6"pagination="371 - 396"part="chap. 20"refId="ref8765"refString="36. T. R. Holtz Jr., Tyrannosaurus rex, the Tyrant King, P. Larson, K. Carpenter, Eds. (Indiana Univ. Press, Bloomington, 2008), chap. 20, pp. 371 - 396."title="Tyrannosaurus rex, the Tyrant King"type="journal article"year="2008">
<bibRefCitationid="EFD0848BFFE60E51FBC25353FBBBFBC1"author="A. Kane & K. Healy & G. D. Ruxton & A. L. Jackson"box="[1052,1075,1072,1096]"journalOrPublisher="Am. Nat."pageId="5"pageNumber="6"pagination="706 - 716"part="187"refId="ref8813"refString="37. A. Kane, K. Healy, G. D. Ruxton, A. L. Jackson, Body size as a driver of scavenging in theropod dinosaurs. Am. Nat. 187, 706 - 716 (2016)."title="Body size as a driver of scavenging in theropod dinosaurs"type="journal article"year="2016">
<bibRefCitationid="EFD0848BFFE60E51FCEE532DFCB4FBEF"author="S. L. Brusatte & M. A. Norell & T. D. Carr & G. M. Erickson & J. R. Hutchinson & A. M. Balanoff & G. S. Bever & J. N. Choiniere & P. J. Makovicky & X. Xu"box="[816,828,1102,1126]"journalOrPublisher="science"pageId="5"pageNumber="6"pagination="1481 - 1485"part="329"refId="ref7118"refString="2. S. L. Brusatte, M. A. Norell, T. D. Carr, G. M. Erickson, J. R. Hutchinson, A. M. Balanoff, G. S. Bever, J. N. Choiniere, P. J. Makovicky, X. Xu, Tyrannosaur paleobiology: New research on ancient exemplar organisms. science 329, 1481 - 1485 (2010)."title="Tyrannosaur paleobiology: New research on ancient exemplar organisms"type="journal article"year="2010">
<bibRefCitationid="EFD0848BFFE60E51FC99532EFCD6FBEC"author="T. R. Holtz Jr."box="[839,862,1101,1125]"editor="P. Larson & K. Carpenter"journalOrPublisher="Indiana Univ. Press, Bloomington"pageId="5"pageNumber="6"pagination="371 - 396"part="chap. 20"refId="ref8765"refString="36. T. R. Holtz Jr., Tyrannosaurus rex, the Tyrant King, P. Larson, K. Carpenter, Eds. (Indiana Univ. Press, Bloomington, 2008), chap. 20, pp. 371 - 396."title="Tyrannosaurus rex, the Tyrant King"type="journal article"year="2008">
<bibRefCitationid="EFD0848BFFE60E51FCB7532DFC08FBEF"author="D. A. Russell"box="[873,896,1102,1126]"journalOrPublisher="National Museum of Natural sciences, Publications, in Paleontology"pageId="5"pageNumber="6"pagination="1 - 34"part="1"refId="ref8859"refString="38. D. A. Russell, Tyrannosaurs from the Late Cretaceous of western Canada. National Museum of Natural sciences, Publications, in Paleontology 1, 1 - 34 (1970)."title="Tyrannosaurs from the Late Cretaceous of western Canada"type="journal article"year="1970">
, because it occupies different carnivore niches before and after achieving skeletal maturity (
<bibRefCitationid="EFD0848BFFE60E51FB4B53EBFB24FB29"author="P. Dodson"box="[1173,1196,1160,1184]"journalOrPublisher="J. Zool."pageId="5"pageNumber="6"pagination="315 - 355"part="175"refId="ref8895"refString="39. P. Dodson, Functional and ecological significance of relative growth in Alligator. J. Zool. 175, 315 - 355 (1975)."title="Functional and ecological significance of relative growth in Alligator"type="journal article"year="1975">
<bibRefCitationid="EFD0848BFFE60E51FCB253C5FC0CFB37"author="J. E. Peterson & K. N. Daus"box="[876,900,1190,1214]"journalOrPublisher="PeerJ"pageId="5"pageNumber="6"pagination="e 6573"part="7"refId="ref8924"refString="40. J. E. Peterson, K. N. Daus, Feeding traces attributable to juvenile Tyrannosaurus rex offer insight into ontogenetic dietary trends. PeerJ 7, e 6573 (2019)."title="Feeding traces attributable to juvenile Tyrannosaurus rex offer insight into ontogenetic dietary trends"type="journal article"year="2019">
biology and ecology, and additional evidence that there were no sympatric tyrannosaurids in the HCF. Furthermore, we hypothesize that ontogenetic niche partitioning, coupled with an ability to adjust annual growth hiatus duration to track resource abundance, made
consists of a nearly complete skull with associated postcrania, including a partial femur [estimated length, 68.8 cm; (
<bibRefCitationid="EFD0848BFFE60E51FB7C5118FB26F91B"author="P. J. Currie"box="[1186,1198,1659,1682]"journalOrPublisher="Can. J. Earth sci."pageId="5"pageNumber="6"pagination="651 - 665"part="40"refId="ref7386"refString="7. P. J. Currie, Allometric growth in tyrannosaurids (Dinosauria: Theropoda) from the Upper Cretaceous of North America and Asia. Can. J. Earth sci. 40, 651 - 665 (2003)."title="Allometric growth in tyrannosaurids (Dinosauria: Theropoda) from the Upper Cretaceous of North America and Asia"type="journal article"year="2003">
were histologically processed by the MOR for an earlier project, and the resulting thin section slides were made available on loan to the senior author. Additional thin sections were produced for the current study to directly compare histological features across bones of
were produced following the methodology of Padian and Lamm (
<bibRefCitationid="EFD0848BFFE50E52FF6C5630FF42FEE2"author="K. Padian & E. - T. Lamm"box="[178,202,339,363]"journalOrPublisher="University of California Press, Berkeley"pageId="6"pageNumber="7"pagination="285"refId="ref7502"refString="10. K. Padian, E. - T. Lamm, Bone Histology of Fossil Tetrapods: Advancing Methods, Analysis, and Interpretation (University of California Press, Berkeley, 2013), p. 285."title="Bone Histology of Fossil Tetrapods: Advancing Methods, Analysis, and Interpretation"type="book chapter"year="2013">
<bibRefCitationid="EFD0848BFFE50E52FE07555EFE78FDDC"author="E. Prondvai & K. H. W. Stein & A. de Ricqles & J. Cubo"box="[473,496,573,597]"journalOrPublisher="Biol. J. Linn. soc."pageId="6"pageNumber="7"pagination="799 - 816"part="112"refId="ref7631"refString="13. E. Prondvai, K. H. W. Stein, A. de Ricqles, J. Cubo, Development-based revision of bone tissue classification: the importance of semantics for science. Biol. J. Linn. soc. 112, 799 - 816 (2014)."title="Development-based revision of bone tissue classification: the importance of semantics for science"type="journal article"year="2014">
), modern bone is composed of integrated hydroxyapatite crystals and collagen fibrils, with long axes arranged in parallel. Thus, the orientation of inorganic hydroxyapatite minerals implies collagen fiber arrangement in fossil bone, and this orientation can be inferred visually by the intensity of birefringence associated with anisotropy in polarized light: If the fiber bundles are cut across their longitudinal axis, they will appear bright (anisotropic), whereas if cut transversely, they will remain dark (isotropic). Bone fiber orientation is typically diagnosed from a thin section of bone cut transverse to the long axis of a diaphysis. Bone tissue was classified as parallel fibered or lamellar if uniformly anisotropic with flattened osteocyte lacunae (i.e., lacuna long axis parallel to fiber orientation) and woven if uniformly isotropic with rounded lacunae. Without examining bone tissue in the longitudinal as well as transverse planes, it is impossible to distinguish woven tissue, which should remain isotropic in both orientations, from longitudinally oriented parallel-fibered or lamellar tissue, which is isotropic in the transverse section and can therefore be mistaken for woven tissue. This distinction is critical, because ranges of daily apposition rates are frequently assigned on the basis of fiber orientation [see (
<bibRefCitationid="EFD0848BFFE50E52FD4A5308FD24FB0A"author="E. Prondvai & K. H. W. Stein & A. de Ricqles & J. Cubo"box="[660,684,1131,1155]"journalOrPublisher="Biol. J. Linn. soc."pageId="6"pageNumber="7"pagination="799 - 816"part="112"refId="ref7631"refString="13. E. Prondvai, K. H. W. Stein, A. de Ricqles, J. Cubo, Development-based revision of bone tissue classification: the importance of semantics for science. Biol. J. Linn. soc. 112, 799 - 816 (2014)."title="Development-based revision of bone tissue classification: the importance of semantics for science"type="journal article"year="2014">
) for discussion]. For this reason, when thin sections were produced for this study, each specimen was sectioned both longitudinally and transversely to more accurately assess bone fiber orientation.
were removed from the bones using a circular saw with a continuous rim diamond blade. The samples removed were molded and cast, and the cast replicas were restored to the fossil bones. The samples removed were then embedded in Silmar polyester resin, and transverse wafers were cut (~3 to 4 mm thick) to either side of the line of minimum circumference with a circular saw and continuous rim diamond blade. These wafers were glued to frosted glass slides and polished on a variable speed grinder to mirror finish using a series of 60, 120, 180, 320, 600, 800, and 1200 silicon carbide grit papers and 5- and 1-μ m hand-polish slurries. Final slide thicknesses were between 97 and 177 μ m. Longitudinal sections were made from the embedded diaphysis samples, along a lateral-medial plane in the tibia of
Thin sections were analyzed using a Nikon Eclipse Ni-U polarizing microscope and plane-polarized light (i.e., only the polarizer in position), CPL, and cross-polarized light with 540-nm lambda filter. Photomicrographs were taken using a Nikon Fi2 microscope camera. Composite images of each full thin section at ×20 total magnification were obtained through the use of an automated Applied Scientific Instrumentation microscope stage and Nikon Elements: Documentation software. Annually formed CGMs, including LAGs and annuli, were identified and digitally traced using Adobe Photoshop CC. Comparisons of annual zonal thicknesses between CGMs were made along a transect, and measurements were taken in Adobe Photoshop CC. Histological descriptions were made from observations using CPL and follow the terminology of Padian and Lamm (
<bibRefCitationid="EFD0848BFFE50E52FA5B5630FA14FEE2"author="K. Padian & E. - T. Lamm"box="[1413,1436,339,363]"journalOrPublisher="University of California Press, Berkeley"pageId="6"pageNumber="7"pagination="285"refId="ref7502"refString="10. K. Padian, E. - T. Lamm, Bone Histology of Fossil Tetrapods: Advancing Methods, Analysis, and Interpretation (University of California Press, Berkeley, 2013), p. 285."title="Bone Histology of Fossil Tetrapods: Advancing Methods, Analysis, and Interpretation"type="book chapter"year="2013">
<bibRefCitationid="EFD0848BFFE50E52FC125613FC6CFE01"author="E. Prondvai & K. H. W. Stein & A. de Ricqles & J. Cubo"box="[972,996,368,392]"journalOrPublisher="Biol. J. Linn. soc."pageId="6"pageNumber="7"pagination="799 - 816"part="112"refId="ref7631"refString="13. E. Prondvai, K. H. W. Stein, A. de Ricqles, J. Cubo, Development-based revision of bone tissue classification: the importance of semantics for science. Biol. J. Linn. soc. 112, 799 - 816 (2014)."title="Development-based revision of bone tissue classification: the importance of semantics for science"type="journal article"year="2014">
). A CGM was identified as an annulus if it consisted of a diffuse band of parallel-fibered bone and interpreted as a period of considerably decreased osteogenesis. A LAG was identified as a thin hypermineralized ring, indicating a period when osteogenesis ceased altogether.
