The bone microstructure of living and fossil birds: high-resolution 3D imaging for enhanced avian palaeobiology

Abstract

Accurately estimating developmental age and life history traits in fossils is crucial for identifying and classifying extinct species and understanding how biological attributes evolved. The evolution of life history traits such as growth pattern is far from clear in birds, and development has been studied in only a handful of modern species. The exceptionally rapid growth of modern birds means ageing methods based on annual incremental growth lines, used in other vertebrates, are inapplicable to birds and robust alternative methods remain to be established. Analysis of avian intracortical bone microstructure, which varies both with age and tissue deposition rate, is a promising approach already used in palaeobiology. However, current thin section-based histological methods are destructive. Moreover, to date, most microstructural studies in avian bone are qualitative, 2D, and involve a limited range of extant species. The objective of this study was to investigate cortical bone microstructure and developmental age and life history traits in living birds, to identify phenotypes which can then be applied to examination of the fossil record, using minimally-destructive high-resolution 3D imaging. First, the necessity of 3D measurement was tested: a combination of idealised, simulated datasets and real synchrotron-based computed tomography (SR CT) datasets were used to compare published methods for measuring key microstructural traits based on 2D sections and 3D volumes. Next, SR CT imaging and quantitative measurements were used to characterise age-related changes in bone microstructure in a range of extant bird species: growth series ducks and pheasants, and a smaller sample size in starlings, rock doves, partridges, and ostrich. The methods tested in modern material were applied to fossils as a proof-of concept. It was found that 3D quantification methods are required for measuring vascular canal orientation and osteocyte lacunar shape and volume, though 2D sections could be used to measure traits such as bone volume fraction (BV/TV) and osteocyte lacunar volume. In all species studied, juvenile, subadult, and adult species could be distinguished by their values of BV/TV, and further information could be added using measured values of vascular canal diameter as well as qualitative assessment. Using a synchrotron-based CT system, high-resolution 3D datasets comparable to modern bone samples were obtained from fossils, and preliminary estimates of developmental age can be made. Further work may reveal more changes within juvenile age stages, and better characterise the variation within extant birds, allowing more accurate interpretation of the fossil record. Therefore developmental studies in a greater number of extant bird species are required using larger sample sizes, to support and add to the results presented in this thesis.

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Identifiers

ORCID for Katherine Anne Williams: orcid.org/0000-0001-6827-9261

ORCID for Philipp Schneider: orcid.org/0000-0001-7499-3576

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