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doi: 10.1371/journal.pone.0036907. Epub 2012 May 16.

Modified laminar bone in Ampelosaurus atacis and other Titanosaurs (Sauropoda): implications for life history and physiology

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Modified laminar bone in Ampelosaurus atacis and other Titanosaurs (Sauropoda): implications for life history and physiology

Nicole Klein et al. PLoS One.2012.

Abstract

Background: Long bone histology of the most derived Sauropoda, the Titanosauria suggests that titanosaurian long bone histology differs from the uniform bone histology of basal Sauropoda. Here we describe the long bone histology of the titanosaur Ampelosaurus atacis and compare it to that of basal neosauropods and other titanosaurs to clarify if a special titanosaur bone histology exists.

Methodology/principal findings: Ampelosaurus retains the laminar vascular organization of basal Sauropoda, but throughout most of cortical growth, the scaffolding of the fibrolamellar bone, which usually is laid down as matrix of woven bone, is laid down as parallel-fibered or lamellar bone matrix instead. The remodeling process by secondary osteons is very extensive and overruns the periosteal bone deposition before skeletal maturity is reached. Thus, no EFS is identifiable. Compared to the atypical bone histology of Ampelosaurus, the large titanosaur Alamosaurus shows typical laminar fibrolamellar bone. The titanosaurs Phuwiangosaurus, Lirainosaurus, and Magyarosaurus, although differing in certain features, all show this same low amount or absence of woven bone from the scaffolding of the fibrolamellar bone, indicating a clear reduction in growth rate resulting in a higher bone tissue organization. To describe the peculiar primary cortical bone tissue of Phuwiangosaurus, Ampelosaurus, Lirainosaurus, and Magyarosaurus, we here introduce a new term, "modified laminar bone" (MLB).

Conclusions/significance: Importantly, MLB is as yet not known from extant animals. At least in Lirainosaurus and Magyarosaurus the reduction of growth rate indicated by MLB is coupled with a drastic body size reduction and maybe also a reduction in metabolic rate, interpreted as a result of dwarfing on the European islands during the Late Cretaceous. Phuwiangosaurus and Ampelosaurus both show a similar reduction in growth rate but not in body size, possibly indicating also a reduced metabolic rate. The large titanosaur Alamosaurus, on the other hand, retained the plesiomorphic bone histology of basal neosauropods.

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Conflict of interest statement

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

Figures

Figure 1
Figure 1. Phylogenetic relationships of the sampled titanosaur taxa (underlined in red) and outgroup taxa (black box) and body size evolution in Titanosauria.
For the reconstruction of body size evolution, we used femur length as a proxy for body size and optimized it on the only phylogeny that includes all the taxa discussed in this study .Europasaurus was inserted into this phylogeny as a basal macronarian .Magyarosaurus,Lirainosaurus, andEuropasaurus show autapomorphic size decrease, i.e., dwarfing.Phuwiangosaurus also has a slightly reduced body size compared to the stem line, whileAmpelosaurus shows a slight phylogenetic size increase. Character optimization analysis was performed in TNT .
Figure 2
Figure 2. Circumference at midshaft (cam) plotted versus bone length (in millimeter) of humeri and femora ofAmpelosaurus atacis from the locality of Bellevue from the Upper Aude Valley.
A) Femora. B) Humeri. The plot suggests that there are two morphotypes, because humeri and femora of a similar length form two groups in terms of circumference. A gracile and a more robust type is thus suggested by differences around 100 mm in circumference at midshaft. This graph also includes bones which were not sampled.
Figure 3
Figure 3. Histological details of the humeral cortex of a growth series of the derived titanosaurAlamosaurus sanjuanensis from the Upper Cretaceous Javelina Formation, Texas, USA.
The bones tissues in this growth series of the large titanosaurAlamosaurus are identical to those of large diplodocoid and basal macronarian sauropods. The plane of sectioning is perpendicular to bone long axis, and the direction of bone apposition is towards the top of the images.A) Typical laminar fibrolamellar bone tissue of a young individual (HOS 4; TMM 45600-1; 460 mm long, 31% max. size) in normal light. Note the absence of LAGs but the subtle modulations in vascularization (arrows).B) Same view in polarized light. Note the dominance of the scaffolding of woven bone in the fibrolamellar complex.C) Typical laminar fibrolamellar bone tissue of a young adult individual (HOS 7; TMM 43600-2; 915 mm long, 61% max. size). Note the strictly circumferential arrangement of the vascular canals.D) Same view in polarized light. Note the primary osteons in the scaffolding of woven bone.E) IncipientEFS in the outermost cortex and scattered secondary osteons in laminar fibrolamellar bone of a fully grown individual (HOS 12; TMM uncat.; 1350 mm long, 90% max. size).F) Same view in polarized light. Note the highly birefringent parallel-fibered bone of the EFS and the woven to parallel-fibered scaffolding of the fibrolamellar bone in the deeper cortex, between the secondary osteons. The high amount of parallel-fibered bone in the scaffolding of the fibrolamellar bone is typical in late ontogenetic stages in diplodocoid and basal macronarian dinosaurs as well as forAlamosaurus but occurs already in early ontogenetic stages inAmpelosaurus.
Figure 4
Figure 4. Histological details of humerus bone tissue ofAmpelosaurus atacis from Bellevue locality (MDE C3) and from a titanosaur north of Narbonne (Cru), all from the Maastrichian of South France.
A) Modified laminar bone at the anterior bone side of humerus C3-270 (cam 170 mm). The vascular canals are wide open, and primary osteons had not yet developed. The scaffolding of the fibrolamellar bone consists largely of parallel-fibered and lamellar bone matrix. This bone tissue represents HOS 7.B) Modified laminar bone at the posterior bone side of humerus C3-270 (cam 170 mm). The vascular canals are still distinctly open. Laminar organization is greater when compared to the anterior bone side. Primary osteons had partially developed. The scaffolding of the fibrolamellar bone consists of parallel-fibered and lamellar bone matrix. This bone tissue represents HOS 9.C) Modified laminar bone at the anterior bone side of humerus C3-1506 (cam 195 mm, humerus length is 620 mm). Primary bone tissue is visible in the upper third of the cortex, whereas the inner part is remodeled by secondary osteons. The scaffolding of the fibrolamellar bone consists of parallel-fibered and lamellar bone matrix. Primary osteons are nearly filled in. This bone tissue represents HOS 11.D) Modified laminar bone of humerus Cru-1723 (cam 250 mm). The scaffolding of the fibrolamellar bone consists largely of lamellar bone matrix. The vascular density in this sample is still moderate with still open primary osteons. Most of the cortex is completely remodeled by secondary osteons. The outer cortex shows dense secondary osteons. This bone tissue represents HOS 12.E) The posterior bone side of humerus C3-602 (cam 250 mm) is completely remodeled by secondary osteons representing HOS 13.F) The anterior bone side of humerus C3-1189 (cam 310 mm) is completely remodeled by secondary osteons representing HOS 13.
Figure 5
Figure 5. Histological details of femur bone tissue ofAmpelosaurus atacis from Bellevue locality (MDE C3) from the Maastrichian of South France.
A) Modified laminar bone at the anterior side of femur C3-1182 (cam is 255 mm, femur length is 695 mm). The scaffolding of the fibrolamellar bone consists largely of parallel-fibered bone matrix. The vascular canals are still open. Primary osteons had partially developed. Dense remodeling occurs up to the middle cortex, and there are scattered secondary osteons in the outer cortex. This bone tissue represents HOS 11.B) Modified laminar bone on the anterior side of femur C3-203 (cam 270 mm, femur length is 780 mm). The scaffolding of the fibrolamellar bone consists largely of lamellar bone matrix. The vascular canals are still open, and primary osteons had partially developed. Dense remodeling occurs up to the outer cortex. This bone tissue represents HOS 12.C) Modified laminar bone on the anterior side of femur C3-527 (cam 280 mm, femur length is 680 mm). The primary cortex is completely remodeled by secondary osteons. This bone tissue represents HOS 13.D) Modified laminar bone on the anterior bone side of femur C3-261 (cam 288 mm, femur length is 840 mm). The vascular canals are nearly filled in. Primary osteons had only poorly developed. The scaffolding of the fibrolamellar bone consists largely of parallel-fibered bone matrix. This bone tissue represents HOS 12.E) Modified laminar bone on the anterior side of femur C3-1239 (cam 350 mm). The vascular canals are still open. Primary osteons are well developed. The scaffolding of the fibrolamellar bone consists of parallel-fibered and lamellar bone matrix. This bone tissue represents HOS 11.F) Modified laminar bone on the anterior side of femur C3-78 (cam 465 mm). The vascular canals are still open. Primary osteons are well developed. The scaffolding of the fibrolamellar bone consists laregly of lamellar bone matrix. Secondary osteons are only scattered throughout the cortex. This bone tissue represents HOS 11.
Figure 6
Figure 6. Overview (A) and enlargements (B, C) of a cross section of anAmpelosaurus atacis humerus (MDE C3-328, cam 270 mm) from Bellevue locality.
On the posterior side (B), the humerus shows an “older” bone tissue (HOS 13) than at the anterior side (C) (HOS 12). Scale bars in B and C equals 0.5 mm.
Figure 7
Figure 7. HOS ofAmpelosaurus atacis from Bellevue locality (MDE C3) and from titanosaurs north of Narbonne (Cru) plotted against bone circumference at midshaft.
Circumference at midshaft (mm) versus histological ontogenetic stage (HOS) from the posterior and the anterior bone side. Note that the posterior side in the humerus is a later stage than the anterior one (the standard sampling location) and that the anterior side of femur is older than the posterior side (the standard sampling location). Red arrows connect the anterior and posterior side of the same bone (from old to young). The rectangles mark the samples formA. atacis from Bellevue locality. The triangles mark the samples from titanosaurs north of Narbonne (Cru).
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