Micromechanical properties and structural characterization of modern inarticulated brachiopod shells

Abstract

[1] We investigated micromechanical properties and ultrastructure of the shells of the modern brachiopod species Lingula anatina, Discinisca laevis, and Discradisca stella with scanning electron microscopy (SEM, EDX), transmission electron microscopy (TEM) and Vickers microhardness indentation analyses. The shells are composed of two distinct layers, an outer primary layer and an inner secondary layer. Except for the primary layer in Lingula anatina, which is composed entirely of organic matter, all other shell layers are laminated organic/inorganic composites. The organic matter is built of chitin fibers, which provide the matrix for the incorporation of calcium phosphate. Amorphous calcium phosphate in the outer, primary layer and crystalline apatite is deposited into the inner, secondary layer of the shell. Apatite crystallite sizes in the umbonal region of the shell are about 50 Â 50 nm, while within the valves crystallite sizes are significantly smaller, averanging 10 Â 25 nm. There is great variation in hardness values between shell layers and between the investigated brachiopod species. The microhardness of the investigated shells is significantly lower than that of inorganic hydroxyapatite. This is caused by the predominantly organic material component that in these shells is either developed as purely organic layers or as an organic fibrous matrix reinforced by crystallites. Our results show that this particular fiber composite material is very efficient for the protection and the support of the soft animal tissue. It lowers the probability of crack formation and effectively impedes crack propagation perpendicular to the shell by crack-deviation mechanisms. The high degree of mechanical stability and toughness is achieved by two design features. First, there is the fiber composite material which overcomes some detrimental and enhances some advantageous properties of the single constituents, that is the softness and flexibility of chitin and the hardness and brittleness of apatite. Second, there is a hierarchical structuring from the nanometer to a micrometer level. We could identify at least seven levels of hierarchy within the shells.

Mechanical properties of modern calcite- (Mergerlia truncata) and phosphate-shelled brachiopods (Discradisca stella and Lingula anatina) determined by nanoindentation

“…It contains two distinct materials: an entirely organic and soft primary layer that is followed inward towards the soft tissue of the animal, by a laminated chitinophosphatic secondary layer (Williams et al, 1994;Merkel et al, 2007). The organic primary layer shields the secondary layer from incipient cracks that can occur while the animal burrows itself into and through the sediment.…”

“…Due to their long geologic record in distinct habitats they are of interest for evolutionary systematics (e.g., Williams et al, 1994Williams et al, , 1997Williams et al, , 1998a and for studies of paleoclimatic and paleoenvironment variations (e.g., Veizer et al, 1999;Bruckschen et al, 1999;Brand et al, 2003;Parkinson et al, 2005). The utilization of two distinct shell materials (carbonate and phosphate) with distinct shell design strategies renders them highly appropriate for understanding biomineralization processes and properties of biomaterials (e.g., Cusack et al, 1999;Schmahl et al, 2004aSchmahl et al, , 2006Schmahl et al, , 2008Griesshaber et al, 2005b;Merkel et al, 2007;Perez-Huerta et al, 2007).…”

The effects of environment on <i>Arctica islandica</i> shell formation and architecture

“…The considerable diversity of biomineralizing species contributes to high variability in terms of shape, organization and mineralogy of the structures produced (Lowenstam and Weiner, 1989;Carter et al, 2012). Different architectures at the micrometer and nanometer scale and different biochemical compositions determine material properties that serve specific functions (Weiner and Addadi, 1997;Currey, 1999;Merkel et al, 2007). Besides these differences, all mineralized tissues are hybrid materials consisting in hierarchical arrangements of biomineral units surrounded by organic matrix, also known as "microstructures" (Bøggild, 1930;Carter and Clark, 1985;Rodriguez-Navarro et al, 2006), "ultrastructures" (Blackwell et al, 1977;Olson et al, 2012) or overall "fabrics" (Schöne, 2013;.…”

Species-specific shells: Chitin synthases and cell mechanics in molluscs

“…This fundamental observation from chitin-binding protein complexes would explain, to some extent, how a true 3D preferred orientation of crystals can be present in juvenile shells, while at a later stage of growth, for example in adult Notosaria nigricans (Brachiopoda), the texture looses most of its 3D ordering and becomes a 1D fibre texture [101][102][103][104][105][106]. In some shell regions, the texture becomes bi-or even multimodal as revealed by high-resolution electron backscatter diffraction (EBSD), also known as backscatter Kikuchi diffraction [107].…”