Sauer, K.; Silveira, A.; Schoeppler, V.; Rack, A.; Zizak, I.; Pacureanu, A.; Nassif, N.; Mantouvalou, I.; de Nolf, W.; Fleck, C.; Shahar, R.; Zaslansky, P.: Nanocrystal residual strains and density layers enhance failure resistance in the cleithrum bone of evolutionary advanced pike fish. Acta Biomaterialia 179 (2024), p. 164-179
10.1016/j.actbio.2024.03.017
Open Access Version
Abstract:
Failure-resistant designs are particularly crucial for bones subjected to rapid loading, as is the case for the ambush-hunting northern pike (Esox lucius). These fish have slim and low-density osteocyte-lacking bones. As part of the swallowing mechanism, the cleithrum bone opens and closes the jaw. The cleithrum needs sufficient strength and damage tolerance, to withstand years of repetitive rapid gape-and-suck cycles of feeding. The thin wing-shaped bone comprises anisotropic layers of mineralized collagen fibers that exhibit periodic variations in mineral density on the mm and micrometer length scales. Wavy collagen fibrils interconnect these layers yielding a highly anisotropic structure. 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 observation of increased strength corresponds to a change to brittle fracture patterns. It matches the emergence of compressive residual strains of ∼0.15% within the mineral crystals due to forces from shrinking collagen layers. Compressive stresses on the nanoscale, combined with the layered anisotropic microstructure on the mm length scale, jointly confer structural stability in the slender and lightweight bones. By employing a range of X-ray, electron and optical imaging and mechanical characterization techniques, we reveal the structure and properties that make the cleithra impressively damage resistant composites.