A Fracture Resisting Molecular Interaction in Trabecular Bone: Sacrificial Bonds and Hidden Length Dissipate Energy as Mineralized Fibrils Separate*

A molecular energy dissipation mechanism in the form of sacrificial bonds and hidden length was previously found in bone constituent molecules of which the efficiency increased with the presence of Ca$^{2}$+ ions in the experimental solution. Here we present evidence for how this sacrificial bond-hidden length mechanism contributes to the mechanical properties of the bone composite. From investigations into the nanoscale arrangement of the bone constituents in combination with pico-Newton adhesion force measurements between mineralized collagen fibrils, based on single molecule force spectroscopy, we find evidence that bone consists of mineralized collagen fibrils and a non fibrillar organic matrix which acts as a ``glue'' that holds the mineralized fibrils together. We propose that this ``glue'' resists the separation of mineralized collagen fibrils. Like in the case of the sacrificial bonds in single molecules, the effectiveness of this ``glue'' increases with the presence of Ca$^{2+}$ ions. We further investigate how this molecular scale strengthening mechanism increases the fracture toughness of the macroscopic material.