Structure and Mechanical Properties
The multiscale structure, materials properties, and mechanical responses of the turtle shell (Terrapene carolina) were studied to understand the fundamental knowledge of naturally occurring biological penetrator-armor systems. The structure observation and chemical analysis results revealed that the turtle shell carapace comprises a multiphase sandwich composite structure of functionally graded material having exterior bone layers and a foam-like bony network of closed-cells between the two exterior bone layers. Although the morphology was quite different, the exterior bone layers and interior bony network possessed comparable hardness and elastic modulus values of ~1 GPa and ~20 GPa, respectively. Compression and flexure test results showed a typical nonlinear deformation behavior recognizant of man-made foams. The mechanical test results revealed that the interior closed-cell foam layer plays a significant role on the overall deformation behavior of the turtle shell. The finite element analysis simulation results showed comparable agreement with the actual experimental test data. This systematic study could provide fundamental understanding for structure-property phenomena and biological pathways to design bio-inspired synthetic composite materials
Structure observations on the turtle shell revealed a multiphase composite material that is arranged by a multiscale hierarchy. Such a multiscale hierarchical structure of the turtle shell carapace is depicted in Fig. 1. The turtle shell comprises a series of connected individual plates covered with a layer of horny keratinized scutes (Fig. 1a–b). The scutes are made up of a fibrous protein called keratin that also comprises the scales of other reptiles . These scutes overlap the seams between the shell bones and serve to reinforce the overall protection to the shell. The carapace is made of a sandwich composite structure of functionally graded material (FGM) having relatively denser exterior layers and an interior fibrous foam-like layer (Fig. 1c–d). SEM micrographs clearly revealed such fibrous structure inside of the cell (Fig. 1e–f).
The internal structure of the turtle shell was nondestructively observed by using an X-ray computed tomography (CT) and obtained images are provided in Fig. 2. The X-ray CT was carried out by using a v|tome|x by phoenix|x-ray. The X-ray CT images clearly showed that the pores within the interior foam-like layer of the turtle shell carapace were closed-cell type and randomly distributed. In addition, the results obtained from the in-house image analyzer software revealed that the porosity levels of the relatively denser exterior, interior foamlike layer, and whole turtle shell carapace including all three layers were 6.86%, 65.5%, and 48.9%, respectively.
Figs. 3 and 4 show the microstructure observation and chemical analysis results obtained from various surfaces of the turtle shell. Three different layers of the outermost keratin layer, right underneath the keratin layer, and the inside surface of the turtle shell carapace were observed and analyzed by using an SEM and an energy dispersive X-ray (EDX) spectroscopy technique, respectively. These layers have different surface microstructures and chemical compositions. The EDX analysis showed that the outermost keratin layer mainly consists of carbon (C), oxygen (O), nitrogen (N), and sulfur (S) that are main constituents of the protein. The result is not surprising since the keratins are a family of fibrous structural proteins, also called scleroproteins. Unlike the outermost keratin layer, right underneath the keratin layer and the inside surface of the turtle shell carapace contained abundant additional minerals as indicated by the presence of calcium (Ca, 15–20 wt.%), phosphorous (P, 7–10 wt.%), sodium (Na), chlorine (Cl), and magnesium (Mg) that are known to be main components of the bone.
The microstructures and chemical analysis results obtained from different locations of the fracture surfaces of the turtle shell carapace are provided in Figs. 5 and 6. The chemical compositions obtained from the exterior layers and the network (e.g. closed-cell wall) region within the foam-like interior layer were quite similar to those can be found in Fig. 4b–c. The fibers inside of the closedcell also showed an accordant chemical composition (Fig. 6b), which implies that they include “bony” fibers. The microstructure observation and chemical analysis results obtained from various locations of the turtle shell clearly revealed that the turtle shell carapace is made of a sandwich composite structure having exterior lamellar bone layers and an interior bony network of closedcell fibrous foam layer.