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Long bone histology and growth patterns in ankylosaurs: implications for life history and evolution.

Stein M, Hayashi S, Sander PM - PLoS ONE (2013)

Bottom Line: In contrast to other taxa, ankylosaurs substitute large amounts of their primary tissue early in ontogeny.Metabolically driven remodeling processes must have liberated calcium to ossify the protective osteodermal structures in juveniles to subadult stages, which led to further remodeling due to increased mechanical loading.Abundant structural fibers observed in the primary bone and even in remodeled bone may have improved the mechanical properties of the Haversian bone.

View Article: PubMed Central - PubMed

Affiliation: Steinmann Institut für Geologie, Mineralogie und Paläontologie, Universität Bonn, Bonn, Germany.

ABSTRACT
The ankylosaurs are one of the major dinosaur groups and are characterized by unique body armor. Previous studies on other dinosaur taxa have revealed growth patterns, life history and evolutionary mechanisms based on their long bone histology. However, to date nothing is known about long bone histology in the Ankylosauria. This study is the first description of ankylosaurian long bone histology based on several limb elements, which were sampled from different individuals from the Ankylosauridae and Nodosauridae. The histology is compared to that of other dinosaur groups, including other Thyreophora and Sauropodomorpha. Ankylosaur long bone histology is characterized by a fibrolamellar bone architecture. The bone matrix type in ankylosaurs is closest to that of Stegosaurus. A distinctive mixture of woven and parallel-fibered bone together with overall poor vascularization indicates slow growth rates compared to other dinosaurian taxa. Another peculiar characteristic of ankylosaur bone histology is the extensive remodeling in derived North American taxa. In contrast to other taxa, ankylosaurs substitute large amounts of their primary tissue early in ontogeny. This anomaly may be linked to the late ossification of the ankylosaurian body armor. Metabolically driven remodeling processes must have liberated calcium to ossify the protective osteodermal structures in juveniles to subadult stages, which led to further remodeling due to increased mechanical loading. Abundant structural fibers observed in the primary bone and even in remodeled bone may have improved the mechanical properties of the Haversian bone.

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Long bone histology of Ankylosauridae indet.A, Inner cortex of the humerus (ROM 47655) showing secondary osteons of different shapes and stages of infilling. B, Same view in cross-polarized light. C, Heavily remodeled outer cortex of the radius (TMP 1997.12.220). D, Same view in cross-polarized light. E, Anterior outer cortex of the ulna (TMP 1982.16.264) displaying obliquely oriented unmineralized Sharpey’s fibers in primary bone tissue with primary osteons. F, Middle and outer posterior cortex of the ulna (TMP 1982.16.264) showing transition from dense Haversian tissue to predominantly primary bone with black arrows marking “bright lines” in outer cortex; Vascular canals opening to the surface indicate an actively growing individual. G, Same view in cross-polarized light. H, Anterior cortex of the ulna (TMP 1982.16.264) with active resorption cavities in outer cortex showing a generally stronger remodeling than the histology of the posterior cortex.
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pone-0068590-g002: Long bone histology of Ankylosauridae indet.A, Inner cortex of the humerus (ROM 47655) showing secondary osteons of different shapes and stages of infilling. B, Same view in cross-polarized light. C, Heavily remodeled outer cortex of the radius (TMP 1997.12.220). D, Same view in cross-polarized light. E, Anterior outer cortex of the ulna (TMP 1982.16.264) displaying obliquely oriented unmineralized Sharpey’s fibers in primary bone tissue with primary osteons. F, Middle and outer posterior cortex of the ulna (TMP 1982.16.264) showing transition from dense Haversian tissue to predominantly primary bone with black arrows marking “bright lines” in outer cortex; Vascular canals opening to the surface indicate an actively growing individual. G, Same view in cross-polarized light. H, Anterior cortex of the ulna (TMP 1982.16.264) with active resorption cavities in outer cortex showing a generally stronger remodeling than the histology of the posterior cortex.

Mentions: The only sampled ankylosaurid humerus, ROM 47655, is from a large individual (92% maximum size; Table 1). The core comprises the posterior cortex and large parts of the medullary region. The preserved trabeculae, which are generally uncrushed, build up a massive network of trabecular bone, producing a comparatively compact medullary region, and grade into the compact bone of the inner cortex. Dense Haversian bone dominates the cortical region with at least three generations of secondary osteons present in the inner and two generations in the outer parts. Resorption cavities without infill, representing actively proceeding cutting cones, are abundant in the perimedullary to inner cortex. The new Haversian canals, as well as the more mature secondary osteons, are variable in shape and size (Figure 2A–B). Therefore, the secondary bone develops a heterogeneous appearance. Canals are linked or fused, and in places secondary osteons appear as one large structure and can have multiple canals, creating a reticular vascular pattern. A remarkable feature is the presence of diffusely oriented structural fibers (sensu[16]) within the dense Haversian bone of the cortex. They tend to occur in bundles, imprinting and blurring the original texture of the bone. Osteocyte lacunae are generally round and flattened along the lamellae of the secondary osteons. In the outermost cortex a belt of primary bone is present. It includes woven-fibered bone tissue with primary osteons. The vascular canals are oriented longitudinally and their diameter is small (30–40 µm). The cortical bone tissue is composed of fibrolamellar tissue, made up of a matrix showing a mixture of woven and parallel-fibered tissue. Common features observed in all thin sections of the Dinosaur Provincial Park material are radial cracks in the periphery of secondary osteons, which are caused by early diagenetic desiccation [46].


Long bone histology and growth patterns in ankylosaurs: implications for life history and evolution.

Stein M, Hayashi S, Sander PM - PLoS ONE (2013)

Long bone histology of Ankylosauridae indet.A, Inner cortex of the humerus (ROM 47655) showing secondary osteons of different shapes and stages of infilling. B, Same view in cross-polarized light. C, Heavily remodeled outer cortex of the radius (TMP 1997.12.220). D, Same view in cross-polarized light. E, Anterior outer cortex of the ulna (TMP 1982.16.264) displaying obliquely oriented unmineralized Sharpey’s fibers in primary bone tissue with primary osteons. F, Middle and outer posterior cortex of the ulna (TMP 1982.16.264) showing transition from dense Haversian tissue to predominantly primary bone with black arrows marking “bright lines” in outer cortex; Vascular canals opening to the surface indicate an actively growing individual. G, Same view in cross-polarized light. H, Anterior cortex of the ulna (TMP 1982.16.264) with active resorption cavities in outer cortex showing a generally stronger remodeling than the histology of the posterior cortex.
© Copyright Policy
Related In: Results  -  Collection

Show All Figures
getmorefigures.php?uid=PMC3722194&req=5

pone-0068590-g002: Long bone histology of Ankylosauridae indet.A, Inner cortex of the humerus (ROM 47655) showing secondary osteons of different shapes and stages of infilling. B, Same view in cross-polarized light. C, Heavily remodeled outer cortex of the radius (TMP 1997.12.220). D, Same view in cross-polarized light. E, Anterior outer cortex of the ulna (TMP 1982.16.264) displaying obliquely oriented unmineralized Sharpey’s fibers in primary bone tissue with primary osteons. F, Middle and outer posterior cortex of the ulna (TMP 1982.16.264) showing transition from dense Haversian tissue to predominantly primary bone with black arrows marking “bright lines” in outer cortex; Vascular canals opening to the surface indicate an actively growing individual. G, Same view in cross-polarized light. H, Anterior cortex of the ulna (TMP 1982.16.264) with active resorption cavities in outer cortex showing a generally stronger remodeling than the histology of the posterior cortex.
Mentions: The only sampled ankylosaurid humerus, ROM 47655, is from a large individual (92% maximum size; Table 1). The core comprises the posterior cortex and large parts of the medullary region. The preserved trabeculae, which are generally uncrushed, build up a massive network of trabecular bone, producing a comparatively compact medullary region, and grade into the compact bone of the inner cortex. Dense Haversian bone dominates the cortical region with at least three generations of secondary osteons present in the inner and two generations in the outer parts. Resorption cavities without infill, representing actively proceeding cutting cones, are abundant in the perimedullary to inner cortex. The new Haversian canals, as well as the more mature secondary osteons, are variable in shape and size (Figure 2A–B). Therefore, the secondary bone develops a heterogeneous appearance. Canals are linked or fused, and in places secondary osteons appear as one large structure and can have multiple canals, creating a reticular vascular pattern. A remarkable feature is the presence of diffusely oriented structural fibers (sensu[16]) within the dense Haversian bone of the cortex. They tend to occur in bundles, imprinting and blurring the original texture of the bone. Osteocyte lacunae are generally round and flattened along the lamellae of the secondary osteons. In the outermost cortex a belt of primary bone is present. It includes woven-fibered bone tissue with primary osteons. The vascular canals are oriented longitudinally and their diameter is small (30–40 µm). The cortical bone tissue is composed of fibrolamellar tissue, made up of a matrix showing a mixture of woven and parallel-fibered tissue. Common features observed in all thin sections of the Dinosaur Provincial Park material are radial cracks in the periphery of secondary osteons, which are caused by early diagenetic desiccation [46].

Bottom Line: In contrast to other taxa, ankylosaurs substitute large amounts of their primary tissue early in ontogeny.Metabolically driven remodeling processes must have liberated calcium to ossify the protective osteodermal structures in juveniles to subadult stages, which led to further remodeling due to increased mechanical loading.Abundant structural fibers observed in the primary bone and even in remodeled bone may have improved the mechanical properties of the Haversian bone.

View Article: PubMed Central - PubMed

Affiliation: Steinmann Institut für Geologie, Mineralogie und Paläontologie, Universität Bonn, Bonn, Germany.

ABSTRACT
The ankylosaurs are one of the major dinosaur groups and are characterized by unique body armor. Previous studies on other dinosaur taxa have revealed growth patterns, life history and evolutionary mechanisms based on their long bone histology. However, to date nothing is known about long bone histology in the Ankylosauria. This study is the first description of ankylosaurian long bone histology based on several limb elements, which were sampled from different individuals from the Ankylosauridae and Nodosauridae. The histology is compared to that of other dinosaur groups, including other Thyreophora and Sauropodomorpha. Ankylosaur long bone histology is characterized by a fibrolamellar bone architecture. The bone matrix type in ankylosaurs is closest to that of Stegosaurus. A distinctive mixture of woven and parallel-fibered bone together with overall poor vascularization indicates slow growth rates compared to other dinosaurian taxa. Another peculiar characteristic of ankylosaur bone histology is the extensive remodeling in derived North American taxa. In contrast to other taxa, ankylosaurs substitute large amounts of their primary tissue early in ontogeny. This anomaly may be linked to the late ossification of the ankylosaurian body armor. Metabolically driven remodeling processes must have liberated calcium to ossify the protective osteodermal structures in juveniles to subadult stages, which led to further remodeling due to increased mechanical loading. Abundant structural fibers observed in the primary bone and even in remodeled bone may have improved the mechanical properties of the Haversian bone.

Show MeSH
Related in: MedlinePlus