Microstructure and texture contributing to damage resistance of the anosteocytic hinge-bone in the cleithrum of Esox lucius

Abstract

Bones are nanocomposites of protein, mineral and water that form mineralized collagen fibrils arranged in a variety of layered lamellae. Bone material has a long evolutionary record and specific bones attain shapes and microstructures that have well stood the test of time such that they can be considered optimized to match their function. Further, most bones typically contain entombed living cells, osteocytes responsible for adaptation, healing and biochemical signaling. The bones of pike fish (Esox lucius) are different because, as with other advanced teleost species, they evolved to eliminate osteocytes from the microstructure. This suggests that these cells are not needed because these bones are more damage resistant than mammalian bones. Here we explore details of this biologically-grown structure, using a combination of light and X-ray based characterization methods. We report the three-dimensional arrangement and composition of the heavily cyclically-loaded pivot of the cleithrum bone in the pectoral girdle of pike. By combining absorption and phase contrast-enhanced micro-computed tomography, electron microscopy, polarized light microscopy and second harmonic generation multi-photon confocal laser scanning microscopy we reveal the principle layout of the bone of this predator which we determine at the millimeter, micrometer and nanometer lengthscales.