Formation and fracture mechanics of tough apatite structures in the stomatopod hammer

Abstract

The stomatopod dactyl club is one of many materials showing Nature’s prowess and ingenuity in creating materials with superior properties using intrinsically weak building blocks. Moreover, they are synthesized under mild environmental conditions compared to the energy-intensive conditions required for many manmade materials. Previous research has shown that the club is a multi-layered structure consisting of a hard and highly mineralized outer region consisting of Fluorapatite (FAP) and a softer inner region made primarily of chitin and CaCO3. The hard-outer region can be further divided into the impact surface which starts at the surface and is followed by the impact region. Recent studies focused on understanding and imitating the toughening mechanisms in the club, while little emphasis has been placed on the growth and development of the club. Only a single study has been conducted to date, which found that that the club develops from the surface in by a “diecast” method and identified a major protein regulating the biomineralization of apatite. In this thesis, the spatial temporal composition and apatite crystallography are explored in greater detail using primarily synchrotron X-rays. Apatite was found in the club as early as 2 hours after molting. The crystals have different textures in the impact surface and impact region of the club. Results also suggest that the apatite crystals undergo compositional changes throughout its development.

To date, most studies of the mechanical properties of the stomatopod dactyl club were conducted using nanoindentation because the size of the club precludes other commonly used methods. However, properties like fracture toughness are only semi-quantitatively determined using contact mechanics. The reliability of indentation fracture measurements, in particular, is a subject of much debate among the scientific community. Hence, in this project chevron-notched micro-cantilevers were prepared and tested to determine fracture toughness values using linear elastic and elastic plastic fracture mechanics. The fracture behavior in the impact region of the dactyl club was shown to be dominated by plastic dissipation. Using the microcantilevers, fracture toughness in the impact region was also shown to be isotropic and not dependent on the direction of measurement.

Previous studies have shown that the impact region consists of FAP crystals aligned with their strongest c-axis toward the surface. SEM images showed that the crystals were misaligned from the surface directly beneath a damaged zone. This is a new toughening mechanism observed in Nature. To verify that this mechanism exists, synchrotron μXRD mapping was used with monotonically and cyclically loaded samples. The results were inconclusive likely because of the averaging of the X-ray data. The first 3D imaging of the impact region and periodic region was achieved using Ptychographic X-ray Computed Tomography. The 3D reconstruction showed the microchannels present in both layers and a bone osteon-like structure was observed at the impact region, which suggests yet another toughening mechanism employed in the club. Overall, this thesis contributes to understanding the biomineralization of apatite biotools in the marine environment and extends micro-fracture methods to hard biological materials. Future work can focus on expanding the micro-fracture toughness method used in this thesis to other hard mineralized tissues. Many questions remained from the time study of apatite biomineralized in the dactyl club and should be addressed in future studies as well. A physical model capable of predicting the nanocrystal rotation and high-resolution elemental and crystallographic 3D imaging can be another area for further research.