Abstract
Simple SummaryBirds have existed on Earth for over one hundred million years, and the eggshell is one of the main factors in them having survived for such a long period of time. The avian eggshell is a multifunctional thin-shelled structure that protects the developing embryo from damage and excessive water loss, provides the embryo with calcium for its skeleton, and sustains the weight of incubating birds. It must also be breakable for the hatchling to emerge. Elastic modulus (Young’s modulus) is the most fundamental mechanical property for such a load-bearing structure. Despite extensive studies on avian eggs, our understanding of the elastic moduli and structure–function relationship of avian eggshells remains incomplete—most previous works have focused on chicken or only a few species. One challenge is the availability and collection of freshly-laid egg samples. The present study is based on 700 freshly-laid eggs collected over a period of seven years from 2015 to 2021, covering a wide taxonomic scale and egg mass (from 1 g to 1459 g). With this large dataset, we may obtain a bird’s-eye view of the elasticity and structure–function relationships of the avian eggshell.We analyze 700 freshly-laid eggs from 58 species (22 families and 13 orders) across three orders of magnitude in egg mass. We study the elastic moduli using three metrics: (i) effective Young’s modulus, EFEM, by a combined experimental and numerical method; (ii) elastic modulus, Enano, by nanoindentation, and (iii) theoretical Young’s modulus, Etheory. We measure the mineral content by acid-base titration, and crystallographic characteristics by electron backscatter diffraction (EBSD), on representative species. We find that the mineral content ranges between 83.1% (Zebra finch) and 96.5% (ostrich) and is positively correlated with EFEM—23.28 GPa (Zebra finch) and 47.76 GPa (ostrich). The EBSD shows that eggshell is anisotropic and non-homogeneous, and different species have different degrees of crystal orientation and texture. Ostrich eggshell exhibits strong texture in the thickness direction, whereas chicken eggshell has little. Such anisotropy and inhomogeneity are consistent with the nanoindentation tests. However, the crystal characteristics do not appear to correlate with EFEM, as EFEM represents an overall “average” elasticity of the entire shell. The experimental results are consistent with the theoretical prediction of linear elasticity. Our comprehensive investigation into the elastic moduli of avian eggshell over broad taxonomic scales provides a useful dataset for those who work on avian reproduction.
Highlights
Nature is filled with various biological materials, each having a unique design to survive in different environments
Avian eggshell is a highly ordered multilayer porous material largely made of calcite crystals, embedded in an organic matrix, and is mainly composed of four layers from the inner to the outer surface: (i) the shell membrane, (ii) the inner mammillary cone layer adhered to the shell membrane, (iii) the columnar palisade layer, known as the spongy layer and the squamatic ultrastructure [29], which makes up most of the shell, and (iv) a thin cuticle [30,31]
Comparing EFEM with the crystal orientations of six avian species (Table 2 and Figure S2), we found that the orientation of calcite crystals appears to have no effect on EFEM
Summary
Nature is filled with various biological materials, each having a unique design to survive in different environments. Thin-shelled structures are ubiquitous in nature, e.g., eggshells and conch shells, as they have the merit of using minimum material to construct a secure protective structure. While eggshells and conch shells are both mostly composed of calcium carbonate (CaCO3 ) with fractions of organic constituents (proteins), they have distinct microstructures in their formation. The conch shell has a crossed laminar structure whose major function is to protect the mollusk [1]. The avian eggshell is multifunctional—it allows gas and water exchange [2,3], prevents microbial contamination [4,5,6], and provides calcium for the developing embryo [7,8,9]. Most birds practice bird–egg contact incubation and “egg turning” to maintain a proper condition for embryonic development [10]. Eggs must sustain the weight of the incubating bird (even the massive extinct elephant birds [11]) and resist possible impact between the egg and its surroundings
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