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.2022 Aug;241(2):518-526.
doi: 10.1111/joa.13665. Epub 2022 Apr 12.

Osteohistological description of ostrich and emu long bones, with comments on markers of growth

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Osteohistological description of ostrich and emu long bones, with comments on markers of growth

Nathan Ong et al. J Anat.2022 Aug.

Abstract

Ostriches and emus are among the largest extant birds and are frequently used as modern analogs for the growth dynamics of non-avian theropod dinosaurs. These ratites quickly reach adult size in under 1 year, and as such do not typically exhibit annually deposited growth marks. Growth marks, commonly classified as annuli or lines of arrested growth (LAGs), represent reduced or halted osteogenesis, respectively, and their presence demonstrates varying degrees of developmental plasticity. Growth marks have not yet been reported from ostriches and emus, prompting authors to suggest that they have lost the plasticity required to deposit them. Here we observe the hind limb bone histology of three captive juvenile emus and one captive adult ostrich. Two of the three juvenile emus exhibit typical bone histology but the third emu, a 4.5-month-old juvenile, exhibits a regional arc of avascular tissue, which we interpret as a growth mark. As this mark is not present in the other two emus from the same cohort and it co-occurs with a contralateral broken fibula, we suggest variable biomechanical load as a potential cause. The ostrich exhibits a complete ring of avascular, hypermineralized bone with sparse, flattened osteocyte lacunae. We identify this as an annulus and interpret it as slowing of growth. In the absence of other growth marks and lacking the animal's life history, the timing and cause of this ostrich's reduced growth are unclear. Even so, these findings demonstrate that both taxa retain the ancestral developmental plasticity required to temporarily slow growth. We also discuss the potential challenges of identifying growth marks using incomplete population data sets and partial cortical sampling.

Keywords: annuli; emu; growth marks; lines of arrested growth; osteohistology; ostrich.

© 2022 Anatomical Society.

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Figures

FIGURE 1
FIGURE 1
Mid‐diaphyseal section of 4.5‐month‐old emu tibia, imaged under multiple light conditions, showing various structures discussed in “Results” section. (a) Photomosaic scan imaged under 20x magnification with anatomic directions. (b) Photomosaic of endosteal surface imaged under 20x magnification and cross‐polarized light, (c) CCCB/cortex interface imaged under 50x magnification and full‐wave plate light, (d) CCCB/cortex interface imaged under 50x magnification and full‐wave plate light, (e) CCCB imaged under 10x magnification and full‐wave plate light, (f) photomosaic of reticular to sublaminar vascularization imaged under 20x magnification and cross‐polarized light, (g) bright lines imaged under 100x magnification and cross‐polarized light, and (h) photomosaic of periosteal surface imaged under 20x magnification and polarized light
FIGURE 2
FIGURE 2
Mid‐diaphyseal section of 4.5‐month‐old emu tibia, imaged under multiple light conditions. (a) Photomosaic with anatomic directions. Black region is a preparation artifact caused by partial delamination of specimen from the slide. Red box indicates region enlarged in b–d. (b–d) photomosaic of the growth mark imaged under 20x magnification and imaged under (b) plane‐polarized, (c) full‐wave plate, and (d) cross‐polarized light. (e) Osteocyte lacunae at the growth mark, imaged under 100x magnification and polarized light and (f) osteocyte lacunae at the growth mark, imaged under 100x magnification and cross‐polarized light.
FIGURE 3
FIGURE 3
Mid‐diaphyseal section of femur from 3‐year‐old ostrich, imaged under multiple light conditions, showing various structures discussed in “Results” section. (a) Photomosaic scan imaged under 20x magnification and plane‐polarized light, with anatomic directions. (b) ICL/cortex interface, imaged under 20x magnification and cross‐polarized light. (c) Photomosaic scan of toluidine‐blue stained slide, imaged under 20x magnification and plane‐polarized light, note sublaminar to laminar vascularization throughout the cortex. (d) Photomosaic was taken at 20x magnification under cross‐polarized light to illuminate hypermineralized vascular laminae. (e) Sublaminar vascularization with sparse woven matrix, imaged under 50x magnification and waveplate retardation. (f) Photomosaic scan of toluidine‐blue stained slide, imaged under 20x magnification and polarized light. Note reticular vascularization deep to trochanter minor. (g) Outer circumferential layer (OCL) imaged under 50x magnification and cross‐polarized light
FIGURE 4
FIGURE 4
Mid‐diaphyseal section of MOR 1707, a femur from 3‐year‐old ostrich. Photomosaic shows the growth mark imaged under multiple light conditions and magnifications. (a) Photomosaic scan of entire specimen, with region in red box expanded to see the potential mark. Imaged under 20x magnification and plane‐polarized light. Red box in the expanded region indicates regions imaged by b‐d. red arrows indicate mark. (b‐d) growth mark imaged at 100x magnification and various light conditions. Red arrows indicate the mark. (b) Mark imaged under polarized light. Note flattened osteocyte lacunae and canaliculi. (c) Mark imaged under cross‐polarized light. Note inconsistent hypermineralization of the region. (d) Mark imaged under cross‐polarized light and wave‐plate retardation. Note distinct fiber orientation
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