Hierarchical structure is a hallmark of many biological materials that naturally originate from their growth process, which starts with the biosynthesis of molecular building blocks that self-assemble into larger units. Compartmentalization is used to locally control the synthesis and self-assembly and, thus bridge multiple length scales between the atomistic and macroscopic worlds. Multiscalar structures have the advantage that different physical properties may be adjusted at various structural levels. In particular, when these properties are conflicting, the result can lead to exceptional multifunctional materials. The fiber is a ubiquitous structural motif of biological materials, although its biochemical basis can be diverse. While fibers perform well under tension, they do not under compression. Biological materials are also adaptive and possess self-repair capabilities—properties that require the transport of matter and information. This requires networks of transport and communication that are also hierarchically organized to conciliate the conflicting goals of maximum accessibility and minimal perforation of the material volume. Several examples are discussed in this article.

An important determinant of mechanical properties of bone is Young’s modulus and its variation in individual osteons of cortical bone tissue. Its mechanical behavior also depends on deformation rate owing to its visco- or poroelastic properties. We developed a method to measure dynamical mechanical properties of bulk bone tissue at osteonal level based on scanning acoustic microscopy (SAM) using time-of-flight (TOF) measurements in combination with quantitative backscattered electron imaging (qBEI). SAM-TOF yields local sound velocities and qBEI corresponding material densities together providing elastic properties. Osteons (n=55) were measured in three human femoral diaphyseal ground bone sections (∼30 µm in thickness). In addition, subchondral bone and mineralized articular cartilage were investigated. The mean mineral contents, the mean sound velocities, and the mean elastic modulus of the osteons ranged from 20 to 26 wt%, from 3,819 to 5,260 m/s, and from 21 to 44 GPa, respectively. There was a strong positive correlation between material density and sound velocity (Pearson’s r=0.701; p<0.0001) of the osteons. Sound velocities between cartilage and bone was similar, though material density was higher in cartilage (+4.46%, p<0.0001). These results demonstrate the power of SAM-TOF to estimate dynamic mechanical properties of the bone materials at the osteonal level.

Modulus mapping using nanoDMA (Dynamic Mechanical Analysis) is a recently developed technique based on a nanoindentation instrument equipped with an AFM-like piezoscanner and dynamic force modulation system. The surface properties, storage and loss moduli are quantified based on the Hertz model for the contact mechanics of the sample-tip configuration. In this approach, the applied load, topography features, and their size may have a pronounced effect on the obtained results. In order to demonstrate that, internal interfaces of deep sea sponge (Monorhaphis chuni), which comprises alternating layers of relatively thick (4 μm in average) biosilica and thin (60 nm) organic material, were characterized using the nanoDMA modulus mapping technique. Experimental data were analyzed in tight interrelation with finite element simulations. This combination allowed us to evaluate elastic modulus of a 60 nm wide organic layers in M. chuni.

Natural materials display a wealth of structures and fulfill a variety of functions. Hierarchical structuring is one of the keys to providing multifunctionality and to adapting to varying needs of an organism. As a consequence, the natural environment represents not only a direct and renewable source of useful materials, such as wood, plant fibers, or even proteins of pharmaceutical importance, but also an enormous “database” of structures with exceptional mechanical, optical, or magnetic properties. Rather than focusing on the direct use of natural materials, this article discusses the use of structures that appeared in evolution and have been implemented in artificial materials of an entirely different type and chemical composition. This may be done either by directly copying the structure (biotemplating) or by extracting the design principles encoded in them for the fabrication of novel bioinspired materials.

Irreversible or plastic deformation in bone is associated with both permanent plastic strain as well as localized microdamage. Whereas mechanisms at the molecular and mesoscopic level have been proposed to explain aspects of irreversible deformation, a quantitative correlation of mechanical yielding, microstructural deformation, and macroscopic plastic strain does not exist. To address this issue, we developed and applied a two-dimensional image correlation technique to the tensile deformation of bovine fibrolamellar bone, to determine the spatial distribution of strain fields at the length scale of 10 μm to 1 mm in bone during irreversible tensile deformation. We find that tensile deformation is relatively homogeneous in the elastic regime and starts at the yield point, showing regions of locally higher strain. Multiple regions of high deformation can exist at the same time over a length scale of 1 to 10 mm. Macroscopic fracture always occurs at one of the locally highly deformed regions, but the selection of which region cannot be predicted. Locally, strain rates can be enhanced by a factor of 3 to 10 over global strain rates in the highly deformed zones and are lower but always positive in all other regions. Light microscopic imaging shows the onset of structural “banding” in the regions of high deformation, which is most likely correlated to microstructural damage at the inter- and intrafibrillar level.

Certain design strategies appear repeatedly in a variety of biological structures. One such motif consists of a soft and pliable interface joining much larger and stiffer elements. Examples include the craniofacial sutures between the bones of the skull, the sutures between the bony plates in shell of turtles and the periodontal ligament between teeth and their sockets. Yet the detailed mechanics of these systems are not fully understood.

Turtles are believed to have existed already in the early Triassic, about 200 million years ago. They are thus one of the oldest non-extinct vertebrates. Their shell is therefore a particularly attractive subject for investigation since it has developed and conserved through such an extremely long evolutionary process and has achieved a highly optimized structure.

The turtle shell has a ‘sandwich’ structure typical of flat bones like the skull of vertebrates. It consists of two external, relatively thin sheets of dense bone (internal endocortical and external exocortical bone plates) which contain very few voids, and between them a thick and very porous spongy bone layer. At the mid-distance between adjacent ribs the dermal bones are separated by soft sutures which have a unique and complex 3-D shape.

The primary function of the shell is to protect the turtle from external trauma, and therefore it has to be stiff. However excessive stiffness may result in microdamage accumulation as a result of everyday activities like minor impact, and decrease the efficiency of respiration and locomotion. We speculate that the structure and architecture of the sutures allow easy deformation of the shell at small loads but cause it to become considerably more rigid at larger loads, reminiscent of composite materials with interlocking elements. We hypothesize that this mechanical property is related to the putative function of the suture in the turtle shell.

In order to examine this hypothesis we studied samples obtained from shells of the red eared slider turtle (Chrysemys scripta elegans). We used several imaging techniques (micro-computed tomography, scanning electron microscopy and light microscopy), histology and mechanical testing. Based on these observations we present a concept of the structure-mechanics relationship of the shell, and present a simple mathematical model of the deformation pattern of the suture-containing samples in 3-point bending tests and compare its predictions to our experimental results.

The silica skeleton of the deep-sea sponge Euplectella aspergillum was recently shown to be structured over at least six levels of hierarchy with a clear mechanical functionality. In particular, the skeleton is built of laminated spicules that consist of alternating layers of silica and organic material. In the present work, we investigated the micromechanical properties of the composite material in spicules of Euplectella aspergillum and the giant anchor spicule of Monorhaphis chuni. Organic layers were visualized by backscattered electron imaging in the environmental scanning electron microscope. Raman spectroscopic imaging showed that the organic layers are protein-rich and that there is an OH-enrichment in silica near the central organic filament of the spicule. Small-angle x-ray scattering revealed the presence of nanospheres with a diameter of only 2.8 nm as the basic units of silica. Nanoindentation showed a considerably reduced stiffness of the spicule silica compared to technical quartz glass with different degrees of hydration. Moreover, stiffness and hardness were shown to oscillate as a result of the laminate structure of the spicules. In summary, biogenic silica from deep-sea sponges has reduced stiffness but an architecture providing substantial toughening over that of technical glass, both by structuring at the nanometer and at the micrometer level.

Using a stochastic lattice model we have studied the architectural changes of trabecular bone occurring while the structure is remodeled. Our model considers the mechanical feedback loop, which control the remodeling process. A fast algorithm was employed to solve approximately the mechanical problem. A general feature of the model is that a networklike structure emerges, which further coarsens while the bone volume fraction remains unchanged. Decreasing the mechanical response of the system by either lowering the external load or the internal mechano-sensitivity leads not only to a reduction of the bone volume fraction, but results in topological changes of the trabecular bone architecture, where the loss of horizontal trabeculae is the most obvious effect.

The material bone consists of a biopolymer matrix (collagen) reinforced with mineral nanoparticles (carbonated hydroxylapatite), forming a natural composite which builds up a dense shell on the exterior and a network of struts with a mean diameter of 200μm in the core of many bones. The architecture of the foamy inner part of bones (spongiosa) is determined by loading conditions. The architecture strongly influences the mechanical properties of cellular solids together with the apparent density and the material it consists of. In addition, the ingrowth of bone cells into porous implants depends on pore size, size distribution and interconnectivity. From this it is clear that the possibility to design the architecture of a bone replacement material is beneficial from a biological as well as a mechanical point of view. Our approach uses rapid prototyping methods, ceramic gelcasting and sintering to produce cellular structures with designed architecture from hydroxylapatite and other bioceramics.

The influence of sintering temperature and atmosphere on the physical properties of these scaffolds was investigated with x-ray diffraction and scanning electron microscopy. Furthermore, the cell ingrowth behaviour was determined in cell culture experiments, using the praeosteoblastic cell line MC3T3-E1, derived from mouse calvariae. The cell ingrowth behaviour was evaluated during a culture period of two and three weeks, by light microscopy and afterwards by histology after embedding and Giemsa-staining.

The phase composition of the material was found to change with increasing sintering temperature and its surface characteristics was influenced by the sintering atmosphere. These changes also affected the cell ingrowth behaviour. In some experiments, the osteoblasts-like cells were found to cover the whole external and internal surface of the scaffold. The cells produced extracellular matrix consisting of collagen, which eventually filled nearly all the pores. In particular, the cells had the tendency to fill any crack or opening in the scaffolds, and to generally smooth the surfaces.

In conclusion, rapid prototyping and ceramic gelcasting allows the freeform fabrication of porous bioceramics with controlled architecture. Such structures made of hydroxylapatit were found to support the growth of mouse osteoblasts.

3D Small Angle X-ray scattering (3D – SAXS) was applied to study the microstructure and the deformation mechanism in PVDF – foils (polyvinyhdene fluoride). SAXS is a powerful tool to investigate structural changes in deformed polymers to reveal morphology at the nanometer scale. When PVDF is strained the structure changes from spherohtic isotropie to a highly anisotropie fiber bundle structure, which requires a full three-dimensional analysis of the SAXS signal.

Inorganic-organic hybrid polymers were prepared by radical polymerization of methacrylic acid or methyl methacrylate with the (meth) acrylate-substituted oxozirconium and oxotitanium clusters Zr6(OH)4O4(OMc)12(OMc = methacrylate), Zr4O2(OMc)12, Ti6O4(OEt)8(OMc)8 and Ti4O2(OPri)6(OAcr)6(OAcr = acrylate). A few mol% of cluster is sufficient for an efficient cross-linking of the polymer chains. Small-angle X-ray scattering data indicate that the cluster size is retained in the polymers and that the microstructure of the cluster cross-linked samples can be described by a dispersion of identical spherical or disk-shaped clusters in the polymer. The obtained hybrid polymers exhibit a higher thermal stability because depolymerization reactions are inhibited. Contrary to undoped poly (methyl methacrylate), the cluster cross-linked polymers are insoluble but swell in organic solvents. The solvent uptake upon swelling decreases with an increasing amount of polymerized cluster.