Investigating the Remarkable Deformability of Intermuscular Bones in Teleost Fish: Insights from Porous Networks and Mineralization Patterns

Abstract Intermuscular bones (IB) are exclusively found in the skeleton of bony fish. This type of mineralized tissue is considered as ossified tendon and has recently been depicted with a unique combination of mechanical strength akin to mammalian bones and ability for large deformation observed in mammalian tendons. Here, we aim to further investigate the intriguing nature of IB by employing thermogravimetric analysis, synchrotron small‐angle X‐ray scattering with in situ uniaxial tensile testing, and synchrotron phase‐contrast nano‐computed tomography (nanoCT) on two groups of herring fish: small and large fish as proxies for younger and older fish, respectively. IB from large fish exhibited a 50% higher strain‐to‐failure (up to 4.5%) compared to IB of small fish ( p = 0.015). Hereby, the applied tissue strain was almost entirely transmitted to the collagen fibrils. While IB of larger fish showed higher mineral maturity than smaller fish, their overall mass density was similar. NanoCT revealed patterns of hypo‐ and hyper‐mineralized regions organized in concentric layers within the cross‐sections of both groups, yet more pronounced in larger IB. Additionally, IB from larger fish showed an extensive porous network with 180% higher tissue porosity compared to IB of smaller fish ( p = 0.036). Extending the previous work, these data suggest that tissue heterogeneity due to layers of varying mineral density, along with high fibril stretching, and potential cellular (re‐)modeling processes contribute to the pronounced deformation abilities in IB. Given the particular combination of strength, stretching capability, heterogeneous microstructure, and mineralization patterns, intermuscular bones can inspire composite biomaterials with specific structure‐function relationships.