  Natural hard composites like human bone possess a combination of strength and
toughness that exceeds that of their constituents and of many engineered
composites. This augmentation is attributed to their complex hierarchical
structure, spanning multiple length scales; in bone, characteristic dimensions
range from nanoscale fibrils to microscale lamellae to mesoscale osteons and
macroscale organs. The mechanical properties of bone have been studied, with
the understanding that the isolated microstructure at micro- and nano-scales
gives rise to superior strength compared to that of whole tissue, and the
tissue possesses an amplified toughness relative to that of its nanoscale
constituents. Nanoscale toughening mechanisms of bone are not adequately
understood at sample dimensions that allow for isolating salient
microstructural features, because of the challenge of performing fracture
experiments on small-sized samples. We developed an in-situ three-point bend
experimental methodology that probes site-specific fracture behavior of
micron-sized specimens of hard material. Using this, we quantify crack
initiation and growth toughness of human trabecular bone with sharp fatigue
pre-cracks and blunt notches. Our findings indicate that bone with fatigue
cracks is two times tougher than that with blunt cracks. In-situ
data-correlated electron microscopy videos reveal this behavior arises from
crack-bridging by nanoscale fibril structure. The results reveal a transition
between fibril-bridging (~1 $\mu$m) and crack deflection/twist (~500 $\mu$m) as
a function of length-scale, and quantitatively demonstrate hierarchy-induced
toughening in a complex material. This versatile approach enables quantifying
the relationship between toughness and microstructure in various complex
material systems and provides direct insight for designing biomimetic
composites.
