Nanocrystal Residual Strains and Density Fluctuations Entail Cyclic Load Failure Resistance in a High Aspect Ratio Bone of Evolutionary Advanced Anosteocytic Fish

Abstract

Failure-resistant designs are particularly crucial for bones subjected to rapid loading, such as during acceleration of the northern pike (Esox lucius). These fish have slim and low-density osteocyte-lacking bones that effectively provide impressive strength and damage resistance, essential for the repetitive ambush gape-and-suck hunting demands that involve rapid loading. The thin wing-shaped structures comprise anisotropic layers of periodic 10% variations in mineral density on mm and micrometer length-scales. Wavy collagen fibrils create or interconnect these layers establishing twofold anisotropy. Hydrated cleithra exhibit Young's moduli spanning 3-9 GPa where the yield stress of ~40 MPa increases markedly to exceed ~180 MPa upon drying. This 5x strengthening corresponds to a change in fracture patterns and the emergence of residual strains of ~0.15% induced within the mineral crystals due to compressive forces from the shrinking collagen layers. The strengthening mechanisms on the nanoscale, combined with the layered anisotropic microstructure, jointly confer structural stability in the slender and lightweight bones. By employing a range of physical imaging and mechanical characterization techniques, we reveal the natural nano-composite strengthening strategies making the anosteocytic cleithra bones an evolutionarily advanced smart material.

Keywords: Anosteocytic bone, transverse isotropy, toughness, residual strain