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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 Nodosauridae indet.A, Heavily remodeled outer cortex of the humerus of TMP 1981.19.15 with little amounts of parallel-fibered primary tissue. B, Same view in cross-polarized light. C, Outer cortex of the radius of TMP 1982.19.267 showing comparatively moderate remodeling. D, Same view in cross-polarized light. E, Heavily remodeled cortex of the ulna of TMP 2007.20.57. F, Same view in cross-polarized light. G, The rib of TMP 1981.16.434 with high amounts of structural fibers. H, Heavily remodeled cortex of the rib of ROM 1215 in cross-polarized light.
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pone-0068590-g006: Long bone histology of Nodosauridae indet.A, Heavily remodeled outer cortex of the humerus of TMP 1981.19.15 with little amounts of parallel-fibered primary tissue. B, Same view in cross-polarized light. C, Outer cortex of the radius of TMP 1982.19.267 showing comparatively moderate remodeling. D, Same view in cross-polarized light. E, Heavily remodeled cortex of the ulna of TMP 2007.20.57. F, Same view in cross-polarized light. G, The rib of TMP 1981.16.434 with high amounts of structural fibers. H, Heavily remodeled cortex of the rib of ROM 1215 in cross-polarized light.

Mentions: TMP 1981.19.15 is a fragmentary humerus that could not be assigned to species (Table 1). The core sample includes the posterior and anterior cortex plus the medullary region. The isolated secondary osteons with structural fibers are overlain by osteons of a younger generation. There is an increase in density of structural fibers in the middle and outer cortex. The secondary osteons are of varying shapes and sizes. Generally, they are fused into radially oriented structures with multiple canals in the center. The whole cortex is remodeled, the outermost cortex exhibiting two generations of secondary osteons. The primary tissue retained in the outer cortex (Figure 6A–B) is of the parallel-fibered type with round, randomly distributed osteocyte lacunae. The inner cortex of TMP 1981.19.15 is similar to TMP 1998.98.1. There is an accumulation of unmineralized structural fibers. Towards the outer cortex the amount of primary bone tissue gradually increases, revealing poorly vascularized tissue intermediate between parallel-fibered and fibrolamellar bone.


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 Nodosauridae indet.A, Heavily remodeled outer cortex of the humerus of TMP 1981.19.15 with little amounts of parallel-fibered primary tissue. B, Same view in cross-polarized light. C, Outer cortex of the radius of TMP 1982.19.267 showing comparatively moderate remodeling. D, Same view in cross-polarized light. E, Heavily remodeled cortex of the ulna of TMP 2007.20.57. F, Same view in cross-polarized light. G, The rib of TMP 1981.16.434 with high amounts of structural fibers. H, Heavily remodeled cortex of the rib of ROM 1215 in cross-polarized light.
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Related In: Results  -  Collection

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

pone-0068590-g006: Long bone histology of Nodosauridae indet.A, Heavily remodeled outer cortex of the humerus of TMP 1981.19.15 with little amounts of parallel-fibered primary tissue. B, Same view in cross-polarized light. C, Outer cortex of the radius of TMP 1982.19.267 showing comparatively moderate remodeling. D, Same view in cross-polarized light. E, Heavily remodeled cortex of the ulna of TMP 2007.20.57. F, Same view in cross-polarized light. G, The rib of TMP 1981.16.434 with high amounts of structural fibers. H, Heavily remodeled cortex of the rib of ROM 1215 in cross-polarized light.
Mentions: TMP 1981.19.15 is a fragmentary humerus that could not be assigned to species (Table 1). The core sample includes the posterior and anterior cortex plus the medullary region. The isolated secondary osteons with structural fibers are overlain by osteons of a younger generation. There is an increase in density of structural fibers in the middle and outer cortex. The secondary osteons are of varying shapes and sizes. Generally, they are fused into radially oriented structures with multiple canals in the center. The whole cortex is remodeled, the outermost cortex exhibiting two generations of secondary osteons. The primary tissue retained in the outer cortex (Figure 6A–B) is of the parallel-fibered type with round, randomly distributed osteocyte lacunae. The inner cortex of TMP 1981.19.15 is similar to TMP 1998.98.1. There is an accumulation of unmineralized structural fibers. Towards the outer cortex the amount of primary bone tissue gradually increases, revealing poorly vascularized tissue intermediate between parallel-fibered and fibrolamellar bone.

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