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, 12 (6), e0179707
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Novel Insight Into the Origin of the Growth Dynamics of Sauropod Dinosaurs

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Novel Insight Into the Origin of the Growth Dynamics of Sauropod Dinosaurs

Ignacio Alejandro Cerda et al. PLoS One.

Abstract

Sauropod dinosaurs include the largest terrestrial animals and are considered to have uninterrupted rapid rates of growth, which differs from their more basal relatives, which have a slower cyclical growth. Here we examine the bone microstructure of several sauropodomorph dinosaurs, including basal taxa, as well as the more derived sauropods. Although our results agree that the plesiomorphic condition for Sauropodomorpha is cyclical growth dynamics, we found that the hypothesized dichotomy between the growth patterns of basal and more derived sauropodomorphs is not supported. Here, we show that sauropod-like growth dynamics of uninterrupted rapid growth also occurred in some basal sauropodomorphs, and that some basal sauropods retained the plesiomorphic cyclical growth patterns. Among the sauropodomorpha it appears that the basal taxa exploited different growth strategies, but the more derived Eusauropoda successfully utilized rapid, uninterrupted growth strategies.

Conflict of interest statement

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

Figures

Fig 1
Fig 1. Phylogenetic relationships of basal sauropodomorpha showing the taxa included in this study (red lettering).
The tree corresponds with the reduced strict consensus tree from the modified matrix of Otero et al. [40]. Taxa employed for comparison are in magenta lettering. Distinction between stem and node based taxa is not included in the tree.
Fig 2
Fig 2. Femur histology of Riojasaurus incertus PVL 3526.
(A, B) General view of the external cortex in normal transmitted (A) and polarized light (B). Note the predominance of well organized intrinsic fibers in the unaltered portions of the sample (bright areas of the outer cortex in B). Arrowheads indicate the presence of LAGs. (C) Detail of the primary bone tissue showing well organized intrinsic fibers and flattened osteocyte lacunae. A growth line (arrowhead) and several Sharpey’s fibers are also observed. Polarized light. (D) Enlarged view of the outer cortex showing a distinctive variation in the vascularization pattern in the compact bone. Such variation starts just above the last preserved LAG (arrowhead). Polarized light with lambda compensator. (E) LAGs (arrowheads) formed in the outer cortex. Normal transmitted light. (F) detailed view of the last six LAGs (arrowheads) formed in the outer cortex. Note the scarce vascularization of the outermost region. Polarized light with lambda compensator. Abbreviations: Sf: Sharpey’s fibers.
Fig 3
Fig 3. Femur histology of Riojasaurus incertus PVL 3669.
(A) General view of the cortical bone. Growth marks (arrowheads) are formed from the inner to the outer region of the compacta. Normal transmitted light. (B) Detail of the primary bone, which is composed of parallel fibered bone (see mass birefringence). Arrowheads indicate a double LAG. Polarized light. (C) Highly vascularized woven fibered bone in the inner cortex. Note the variation of the vascularization pattern from the inner to the outer area. Polarized light with lambda compensator. (D) General view of the inner cortex showing the variation of the vascular canals arrangement (plexiform in the inner region, reticular in the middle and plexiform again in the outer region). Normal transmitted light. (E, F) General (E) and detailed (F) view of the anterior portion of the cortex showing the irregular arrangement of the vascular canals. Normal transmitted (E) and polarized light with a lambda compensator (F). (G) Detail of Sharpey’s fibers. A single LAG accompanied by an annulus is also observed in the figure. (H, I) Detailed view of LAGs (arrowheads) and annuli in the cortical bone viewed under normal transmitted (H) and polarized light (I). Abbreviations: an: annulus; lag: line of arrested growth; pb: plexiform bone; Sf: Sharpey’s fibers; rb: reticular bone; rv: radially oriented vascular canal; rc: resorption cavity.
Fig 4
Fig 4. Femur histology of Coloradisaurus brevis PVL 5904.
(A) General view of the cortex, which is composed almost entirely of well vascularized primary bone tissue. Normal light. (B) General view of the cortical bone showing the predominance of parallel fibered bone in the compacta. Polarized light. (C) Enlarged view of the primary bone. Note the flattened appearance of the osteocyte lacunae and its circumferential arrangement. Normal transmitted light. (D) Primary bone tissue in which circumferential vascular canals predominate, and are often anastomosed by large radial canals. Normal transmitted light. (E) Primary bone tissue in which longitudinally oriented vascular canals predominate, with some anastomosing oblique canals. Normal transmitted light. (F, G) General view of the cortex showing a stratified pattern in the primary bone tissue caused by the presence of poorly vascularized annuli (arrowheads). Normal transmitted light. (H) Detailed view of a LAG in mid cortex. Polarized light. Abbreviations: an: annulus; cv: circumferentially oriented vascular canal; lv: longitudinally oriented vascular canal; rv: radially oriented vascular canal.
Fig 5
Fig 5. Femur histology of Massospondylus carinatus BP/1/4934.
(A) General view of the compact bone. Note the extensive secondary remodeling in the inner half of the compacta. Several LAGs are observed in the primary bone tissue (arrowheads). Normal light. (B) Primary bone tissue at the outer cortex. Some degree of birefringence is evident in the matrix. Polarized light. (C) Detailed view of the primary bone tissue showing primary osteons and strongly flattened osteocyte lacunae. Normal light. (D) Detail of the mid cortex showing predominance of fibrolamellar bone tissue. Polarized light with lambda compensator. (E) Enlarged view of the primary bone showing variation in the shape of the osteocyte lacunae shape and their arrangement. The bone matrix is interrupted by a single LAG. Normal light. (F) Detail of secondary osteons and Sharpey’s fibers. Normal light. (G) Primary bone at outer cortex interrupted by LAGs. Normal light. (H) Detailed view of the inner cortex showing abundant secondary osteons. Normal light. Abbreviations: pfb: parallel fibered bone; po: primary osteons; Sf: Sharpey’s fibers; so: secondary osteons; wfb: woven fibered bone.
Fig 6
Fig 6. Femur histology of Adeopapposaurus mognai PVSJ 569.
(A, B) General view of the cortex in normal transmitted (A) and polarized light (B). Note that intrinsic fibers exhibit a moderate to high degree of organization. (C) Detailed view of the outer cortex showing the high degree of birefringence at the subperiosteal region of the compacta. Polarized light. (D, E) General view (D) and detail (E) of the primary bone tissue. Note the Sharpey’s fibers embedded in the tissue. Normal light. (F) General view of the cortical bone showing the predominance of circumferentially arranged vascular canals. Polarized light. (G) Detailed view of the cortex showing the predominance of longitudinally oriented vascular canals in this area. Normal light. (H) Poorly defined annulus and LAG in the inner cortex (arrowhead). Polarized light with lambda compensator. (I) Detail of the outer cortex showing three LAGs (arrowheads). Normal light. Abbreviations: an: annulus; Sf: Sharpey’s fibers.
Fig 7
Fig 7. Femur histology of Leyesaurus marayensis PVSJ 1079.
(A, B) General view (A) and detail (B) of the cortical bone. Note the mass birefringence of the primary bone tissue. Polarized light (A) and polarized light with lambda compensator (B). (C) Detailed view of the primary bone tissue showing flattened osteocyte lacunae. Double and single LAGs are also observed. Normal transmitted light. (D, E) General view (D) and detail (E) of the cortex showing the arrangement of vascular canals and the relative distribution of LAGs. Normal transmitted light. (F) Enlarged view of the outer cortex. Note that the spacing between successive LAGs is reduced toward the periosteal surface. Normal transmitted light. (G) Highly remodeled portion of the cortex showing different generations of secondary osteons. Despite the relative abundance of the secondary osteons, interstitial primary bone is preserved. Polarized light with lambda compensator. (H) General view of the compact bone showing abundant secondary osteons, which are arranged in concentric rows in some areas. Polarized light with lambda compensator. Abbreviations: cv: circumferentially oriented vascular canal; nrp: non remodeled primary bone tissue; lv: longitudinally oriented vascular canal; mc: medullary cavity; ol: osteocyte lacunae; pfb: parallel fibered bone; rv: radially oriented vascular canal; so: secondary osteons.
Fig 8
Fig 8. Femur histology of Mussaurus patagonicus MLP 61-III-20-22.
(A) General view of the compact bone. Arrowheads indicate the presence of LAGs in the outer third of the compacta. Normal light. (B) Detailed view of the fibrolamellar bone tissue. Primary bone is interrupted by some secondary osteons. Polarized light with lambda compensator. (C) Detail of the cortical bone showing predominance of parallel fibered bone tissue. Polarized light. (D) Detail of the highly vascualrized primary bone. Vascular canals are exhibits a plexiform pattern. Normal light. (E) Detailed view of the outer cortex showing several LAGs (arrowheads). Note that some secondary osteons are organized in concentric rows. Normal light. (F) Detailed view of the primary bone showing closely spaced LAGs and secondary osteons. (G) Closely spaced LAGs at the outer lateral region. Note the presence of some bundles of Sharpey’s fibers. Normal light. (H) Enlarged view of the cortex showing the presence of abundant secondary osteons developed only in the anterolateral region of the cortex (right half of the image). Normal light. (I) Detail of the most remodeled area of the compacta. Note that interstitial primary bone tissue is still preserved. Polarized light with lambda compensator. Abbreviations: cv: circumferentially oriented vascular canal; mc: medullary cavity; nrp: non remodeled primary bone tissue; po: primary osteon; rc: resorption cavity; rv: radially oriented vascular canal; Sf: Sharpey’s fibers; so: secondary osteon.
Fig 9
Fig 9. Femur histology of Mussaurus patagonicus MPM-PV 1815.
(A) General view of the compact bone. Arrowheads indicate the presence of LAGs in the outer third of the compacta. Normal transmitted light. (B) Detailed view of the outer cortex showing predominance of parallel fibered bone tissue. Polarized light. (C) Detail of the fibrolamellar bone tissue in the mid cortex. Polarized light with lambda compensator. (D) Primary bone tissue showing a plexiform pattern of vascularization, with a predominance of circumferential canals. Normal transmitted light. (E) Detail of the anteromedial cortex showing abundant longitudinally oriented vascular canals, which are anastomosed by oblique canals. Note the presence of several secondary osteons. Normal transmitted light. (F) Closely spaced LAGs in the outer cortex. Normal transmitted light. (G) Detail of the inner cortex showing abundant large resorption cavities. Normal transmitted light. (H) Detail of the inner cortex showing abundant resorption cavities. Note the presence of a distinctive layer of primary bone in the innermost region. Polarized light with lambda compensator. (I) Detailed view of the outer cortex showing abundant secondary osteons. Polarized light. Abbreviations: cv: circumferentially oriented vascular canal; lv: longitudinally oriented vascular canal; mc: medullary cavity; nrp: non remodeled primary bone tissue; rc: resorption cavity; rv: radially oriented vascular canal; so: secondary osteons; wfb: woven fibered bone.
Fig 10
Fig 10. Femur histology of Leonerasaurus taquetrensis MPEF 1663.
(A, B) General view (A) and detail (B) of the primary bone tissue, which is mostly composed of parallel fibered bone. Polarized light with lambda compensator (A) and polarized light (B). (CE) General view (C) and detail (D, E) of coarse woven fibered bone tissue. Polarized (E) and polarized light with lambda compensator (C, D). (F) Primary bone tissue in which longitudinally oriented vascular canals predominate. Normal transmitted light. (G) General view of the compact bone showing relative abundance of radial vascular canals. Normal transmitted light. (H) General view of the cortex in which two poorly defined annuli occur (arrowheads). Note that each annulus exhibits a higher degree of birefringence. Polarized light. (IK) General view (I) and detail (J, K) of a single annulus formed in the inner cortex. Note the presence of a single LAG (arrowhead). The broken surface corresponds to a second LAG. Polarized light with lambda compensator (I), polarized light (J) and normal light (K). (L) Cancellous bone in the perimedullary region. Bony trabeculae are composed of lamellar bone deposited during different episodes of secondary remodeling. Polarized light with lambda compensator. Abbreviations: an: annulus; cv: circumferentially oriented vascular canal; lv: longitudinally oriented vascular canal; mc: medullary cavity; po: primary osteon; rv: radially oriented vascular canal; wfb: woven fibered bone.
Fig 11
Fig 11. Femur histology of Lessemsaurus sauropoides PVL 4822/64.
(A) General view of the compact bone. Arrowheads indicate LAGs. Normal transmitted light. (B) Detail of fibrolamellar bone tissue. Polarized light with lambda compensator. (C) Detail of parallel fibered bone tissue. Polarized light with lambda compensator. (D) Detailed view of the fibrolamellar complex showing the shape and relative abundance of osteocyte lacunae. Note the presence of a single LAG (arrowhead). Normal transmitted light. (E, F) General views of the compact bone showing the local variation of the vascularization pattern. Note the transition between plexiform and reticular bone. Normal transmitted light. (G) Cortical bone at the anteromedial region of the compacta, in which longitudinally vascular canals predominate. A detailed view of the Sharpey’s fibers is showed in the insert box. Normal transmitted light. (H) Detail of the cortical bone at the anteromedial region of the compacta. Note the presence of a large reconstructed erosion cavity lined with lamellar bone. Polarized light with lambda compensator. (I) Detail of the primary bone at the mid cortex showing three LAGs (arrowheads). Note the birefringence of the bone tissue accompanying each LAG (box inset). Polarized light with lambda compensator. (J) Detailed view of the inner cortex showing a well preserved LAG (arrowhead). Normal transmitted light. Abbreviations: lb: lamellar bone; mc: medullary cavity; pb: plexiform bone; rb: reticular bone; rc: resorption cavity; Sf: Sharpey’s fibers; so: secondary osteon.
Fig 12
Fig 12. Femur histology of Volkheimeria chubutensis PVL 4077.
(A) General view of the compact bone. Normal transmitted light. (B, C) General view (B) and detail (C) of fibrolamellar bone tissue. Polarized light with lambda compensator. (DF) General view (D) and detail (E, F) of the outer cortex. Note the striking variation of the vascularization pattern evident in the subperiosteal region. A line of arrested growth is present in the sample (arrowhead). Polarized light with lambda compensator (D, E) and normal transmitted light (F). (G) Abrupt transition of the vascularization pattern and bone matrix in the anterolateral portion of the cortex. Normal transmitted light. (HJ) General view (H) and detail (I, J) of the cortical bone showing a distinct LAG (arrowhead). Normal transmitted light (H, I) and polarized light (J). (K) Resorption cavities at the perimedullary region of the cortex. Normal transmitted light. Abbreviations: cv: circumferentially oriented vascular canal; lv: longitudinally oriented vascular canal; mc: medullary cavity; rc: resorption cavity; so: secondary osteon.
Fig 13
Fig 13. Femur histology of Patagosaurus fariasi PVL 4075.
(A) General view of the compact bone. Note the stratified pattern of the primary bone. Normal transmitted light. (B, C) Details of the fibrolamellar complex. Note the high density of osteocyte lacunae. Normal transmitted light. (D) Detail of laminar bone tissue. The primary bone is interrupted by a single LAG. Normal transmitted light. (E, F) General view (E) and detail (F) of the cortical bone at the anterolateral region of the bone. Note the abrupt variation in the vascularization pattern and the relative abundance of secondary osteons. Normal transmitted light. (G, H) General view (G) and detail (H) of the annuli in the cortical bone. Note the variation in the density, shape and arrangement of the osteocyte lacunae. Normal transmitted light. (I) Haversian bone tissue at the anterolateral portion of the compacta. Normal transmitted light. (J) Transition between the trabecular and compact bone in the perimedullary region. Normal transmitted light. Abbreviations: cb: compact bone: an: annulus; its: intertrabecular space; po: primary osteons; so: secondary osteons; tb: trabecular; wfb: woven fibered bone; zo: zone.
Fig 14
Fig 14. Optimization of the histological characters in the phylogeny of basal sauropodomorpha.
(A) Optimization of the character “predominant bone tissue in the compact bone”. This character refers to the relative proportions of woven fibered (WFB) and parallel fibered bone (PFB). (B) Optimization of the character “growth marks (GM) in the femoral cortex”. The characters have been optimized for the reduced strict consensus tree from the modified matrix of Otero et al. [40]. Except for those taxa studied here (red lettering), the data for the histological scoring (magenta lettering) were obtained from the following sources: Saturnalia [, M. Sander com. pers.], Plateosaurus engelhardti [, M. Sander com. pers.], Isanosaurus [3], and Neosauropoda [2, 34]. Distinction between stem and node based taxa were not indicated.

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Grant support

This work was supported by National Geographic Society, Ministerio de Ciencia, Tecnología e Innovación Productiva of the República Argentina and the National Research Foundation (NRF), South Africa, Agencia Nacional de Promoción Científica y Técnica, African Origins platform.
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