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Surface protection in bio-shields via a functional soft skin layer: Lessons from the turtle shell
Journal of the mechanical behavior of biomedical materials (xxxx) xxxx–xxxx
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Surface protection in bio-shields via a functional soft skin layer: Lessons from the turtle shell ⁎
Yaniv Shelef, Benny Bar-On
Department of Mechanical Engineering, Ben-Gurion University of the Negev, Beer Sheva 84105, Israel
A R T I C L E I N F O
A BS T RAC T
Keywords: Bio-shields Indentation resistance Bio-composites
The turtle shell is a functional bio-shielding element, which has evolved naturally to provide protection against predator attacks that involve biting and clawing. The near-surface architecture of the turtle shell includes a soft bi-layer skin coating – rather than a hard exterior – which functions as a first line of defense against surface damage. This architecture represents a novel type of bio-shielding configuration, namely, an inverse structural– mechanical design, rather than the hard-coated bio-shielding elements identified so far. In the current study, we used experimentally based structural modeling and FE simulations to analyze the mechanical significance of this unconventional protection architecture in terms of resistance to surface damage upon extensive indentations. We found that the functional bi-layer skin of the turtle shell, which provides graded (soft-softer-hard) mechanical characteristics to the bio-shield exterior, serves as a bumper–buffer mechanism. This material-level adaptation protects the inner core from the highly localized indentation loads via stress delocalization and extensive near-surface plasticity. The newly revealed functional bi-layer coating architecture can potentially be adapted, using synthetic materials, to considerably enhance the surface load-bearing capabilities of various engineering configurations.
1. Introduction
reinforcing elements (nano-fibrils, nano-platelets, etc.) and bio-polymers (Barth, 1973; Vincent and Wegst, 2004; Chen et al., 2008a, 2008b; Dunlop and Fratzl, 2010; Dunlop et al., 2011; Bar-On and Wagner, 2013; Meyers et al., 2013; Moussian, 2013; Barthelat et al., 2016; Naleway et al., 2016). In recent years, intensive research has addressed the structure and the mechanical behavior of various shielding materials, most notably seashells, teeth, fish scales, arthropod exoskeletons, and the armored osteoderms of the armadillo, alligator, and the shell of the turtle. Seashells, for example, possess an external hard prismatic layer, which serves as a first line of defense against predator attacks; this layer is underlaid with a high-toughness nacreous layer, which resists crack propagation and reduces the risk of catastrophic damage to the shell (Meyers, 2008). Similarly, teeth possess a highly mineralized hard-but-brittle enamel coating, which serves as a grinding surface for food and is underlaid with a more compliant and less mineralized dentin region (Chen et al., 2008a, 2008b; Bar-On and Wagner, 2012). The enamel and dentin are linked by an interfacial dentin–enamel junction, which has a lower degree of hardness and stiffness than either dentin or enamel, thus providing crack-arresting capabilities and preventing enamel cracks from propagating toward the inner part of the tooth (Chai et al., 2009; Imbeni et al., 2005; Shimizu and Macho, 2007). The protective exoskeleton of various arthropods,
Being the product of natural selection over millions of years of evolution, bio-shielding elements have evolved to provide mechanical protection against a variety of load-bearing conditions. As such, they can both resist structural loads (e.g., bending moments and torsion) that tend to macroscopically deform the shield shape (e.g., (Vincent, 2005; Chen et al., 2008a, 2008b; Krauss et al., 2009; Damiens et al., 2012; Magwene and Socha, 2013; Fish and Stayton, 2014)), and they can sustain localized surface tractions, which are typically associated with predator biting attacks, which tend to crack the shield (e.g., (Bruet et al., 2008; Wang et al., 2009; Yao et al., 2010; Song et al., 2011; Amini et al., 2014, 2015)). The two functions are achieved through the complex hierarchical structure of bio-shields; while resistance to structural loads is associated with the macro-structural–mechanical characteristics of the shield as a whole, the ability to sustain localized surface tractions is related to the near-surface characteristics and, in particular, to the mechanical rigidity and hardness of the shield exterior. Natural bio-shielding elements are fundamentally structured as hierarchical bio-composites that comprise several micro-scale layers, each of which is structured as an integrated array of small-scale
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Corresponding author. E-mail address: [email protected] (B. Bar-On).
http://dx.doi.org/10.1016/j.jmbbm.2017.01.019 Received 7 August 2016; Received in revised form 5 January 2017; Accepted 11 January 2017 1751-6161/ © 2017 Elsevier Ltd. All rights reserved.
Please cite this article as: Shelef, Y., Journal of the mechanical behavior of biomedical materials (2017), http://dx.doi.org/10.1016/j.jmbbm.2017.01.019
Journal of the mechanical behavior of biomedical materials (xxxx) xxxx–xxxx
Y. Shelef, B. Bar-On
(Wang et al., 2009; Yao et al., 2010; Amini et al., 2014, 2015; Chintapalli et al., 2014; Rudykh et al., 2015)). Whereas the surface protection capabilities of the hard-coat bioshielding architectures are straightforward, it is less intuitive to understand how soft-coat architectures promote surface protection, if, indeed, they do. Nevertheless, several studies on synthetic materials have implied that a soft skin coating overlaid on a rigid substrate may protect against surface damage (Jayachandran et al., 1995; Suresh, 2001; Choi et al., 2008) and even detain near-surface crack propagation (Kolednik, 2000; Simha et al., 2003). In line with these studies, experimental evidence from impact tests on the turtle shell, which is overlaid with two layers of soft skin, indicate that the skin plays a critical role in shielding against impact damage (Achrai et al., 2015). In the current investigation, we focused on the turtle shell as a specific case study, representative of the large family of soft-coated bioshielding elements, and analyzed its resistance to surface damage upon extensive indentations. First, we used experimental measurements to establish a numerical structural–mechanical model for the turtle shell. Then, we investigated the role of each individual skin layer in protecting the turtle shell against extensive indentations. Finally, we studied the effect of the difference in the mechanical properties of the two layers comprising the turtle-shell skin and analyzed the effect of indenter sharpness and physiological hydration conditions on the resultant damage patterns.
including insects (Barth, 1973; Vincent and Wegst, 2004; Moussian, 2013; Barbakadze et al., 2006), spiders (Politi et al., 2012; Bar-On et al., 2014), lobsters (Raabe et al., 2005), and crabs (Chen et al., 2008a, 2008b), typically includes a lamellar architecture of chitin nanofibrils arranged in helical lamellar patterns (twisted plywood). These lamellae form external and internal layers (exocuticle and endocuticle, respectively) of increasing densities, and, thereby, enhance the mechanical properties of the cuticle toward its exterior. In addition, the near-surface region of the arthropod exoskeleton is commonly associated with an increase in the mineralization and sclerotization levels and with the presence of metal ions, which stiffen and harden the exoskeleton (Amini et al., 2014; Politi et al., 2012; Degtyar et al., 2014). Surprisingly, despite the obvious distinctive evolutionary origin of the various natural shielding elements across taxa, all these elements share the same generic structural–mechanical design: a hard exterior underlaid with a softer interior. In contrast, the osteoderms of the armadillo and alligator and the shell of the turtle demonstrate an alternative structural strategy (Krauss et al., 2009; Damiens et al., 2012; Magwene and Socha, 2013; Fish and Stayton, 2014; Rhee et al., 2009; Balani et al., 2011; Chen et al., 2011, 2014, 2015; Achrai and Wagner, 2013, 2015 Achrai et al., 2014, 2015, 2015; Sun and Chen, 2013 and see the review on turtle shells by Achrai and Wagner in this issue), which incorporates a soft skin coating (namely, a keratin–collagen bi-layer) overlaid with a harder boney core (Fig. 1). The skin coating is mechanically inferior to the underlying boney core, and, obviously, induces a negligible effect on the macro-structural rigidity of the shield (Achrai et al., 2014). However, it appears to play a significant role in adsorbing impact energy, and thereby to increases the damage resilience of the bio-shield against sudden mechanical loads (Achrai et al., 2015). In the past few years, the resilience of hard-coated bio-shields to surface damage was extensively analyzed in a wide range of biological systems, among which are fish scales, which typically comprise a highly mineralized hard-and-brittle exterior, underlaid by a less mineralized softer layer (Bruet et al., 2008; Song et al., 2014; Zhu et al., 2012; Dastjerdi and Barthelat 2015). Experimental and numerical studies of fish scales demonstrated that low-force indentations (i.e., indentations that do not cause coating failure) produce shallow penetrations, which only damage the hard surface layer. Higher indentation forces, i.e., beyond the coating failure point, severely fracture the hard surface layer and damage the softer underlying material. Finite-Element (FE) simulations indicate that the hard coating functions as a load barrier by confining the high-stress fields to the scale exterior and screening the indentation effects from the inner regions. Other hard-coated biological and bio-inspired shielding elements demonstrated similar effects (e.g.
2. Materials and methods 2.1. Experimental Two carapaces from red-eared slider turtles (Trachemys scripta elegans) were used for the mechanical testing. The samples were kept frozen (−70 °C) and were allowed to defrost and dry under ambient conditions for 24 h prior to measurement; no further treatment was conducted to the samples. Micro-indentation experiments were conducted by using a Hysitron TI 950 TriboIndenter, equipped with a high-load cell (3D OmniProb) allowing extensive indentations of a few tens of micrometers in depth and a few Newtons in load. A conical diamond probe tip (tip radius: 5.26 µm; angle: 57.03°) was used for the experiments. The experiments included a 5-s loading-up stage (linear ramp) up to a maximal load, which was kept steady for 20 s to exclude creep effects, followed by a 5-s unloading stage (linear ramp). The indentation locations were carefully selected to avoid natural roughness problems of the native (unpolished and untreated) carapace surface.
Fig. 1. Schematic description and a SEM image of the near-surface architecture of the turtle shell (adapted from (Achrai and Wagner, 2013; Achrai et al., 2015)). The shell is viewed as a layered composite material with a thick boney bulk (porous boney interior enclosed by dense boney layers) overlaid with a thin keratin–collagen bi-layer skin. The near-surface region of the shell is modeled as a tri-layered segment, composed of a boney core of thickness hb , coated by keratin and collagen layers of thickness hk and hc , respectively. Young's modulus (E) and the hardness (H) of the keratin, collagen, and bone layers are indicated by Ek , Ec and Eb , and Hk , Hc and Hb , respectively. Note that, typically,(Ec,Hc ) < (Ek ,Hk ) < (Eb,Hb ) .
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Table 1 Typical literature values for Young's modulus and yield strength for keratin, collagen and bone. Region
E [GPa]
Surface Layer (Keratin)
2–5 1.5, 1.4,1.3 2.7 3.8 0.7–2.5 3.26 1.9–2.4 14–20, 13, 6–10 17.5
Interface (Collagen)
Underlying Layer (Bone)
a
σY [MPa] Carapace, Turtle (Achrai and Wagner, 2013) Beak, Toucan (Seki et al., 2006; McKittrick et al., 2012) Claw, Ostrich (McKittrick et al., 2012; Wang et al., 2016) Quill, Hedgehog (McKittrick et al., 2012) Carapace, Turtle (Achrai and Wagner, 2013) Micro-fibril (Gautieri et al., 2011) Bone tissue, Antler (Hang and Barber, 2011) Carapace, Turtle (Achrai and Wagner, 2013; Achrai et al., 2014; Rhee et al., 2009) Antler, Deer (Currey et al., 2009)
20–90a 30 90 – 4–36a – 81–156 160–270a, 300a,130–290 352.2
The σY was estimated based on hardness measurements via ~H/3 (Bruet et al., 2008).
obtained for the entire range of indentation depths (10, 15…50 µm) in the two shells tested (Fig. 2b-c). The FE results fall within the experimental range for extensive indentations (i.e., beyond ~25 µm depth); however, for shallower indentations, the FE results provide less compatible predictions (Fig. 2d), possibly because the refined micromechanical characteristics of the keratin layer were not accounted for. After confirming the suitability of the FE model, the same numerical platform was employed to analyze the mechanical role of the turtle shell skin as a protective medium against extensive indentations. The analysis focused on the stress distribution and residual plastic damage in the vicinity of the indentation zone. To isolate the mechanical functionality of the individual keratin and collagen skin layers, three simulation models were employed (Fig. 3): (a) a bulk bone without a skin layer (for reference), (b) a single-layer keratin skin, superimposed on the bulk bone, and (c) a keratin–collagen bi-layer skin, superimposed on the bulk bone. Two criteria were considered to investigate the mechanical response to indentations: (1) the equivalent Von-Mises stress field (VM) for a gradual indentation loading up to 1 N, and (2) the resultant plastic strain field (P) after complete unloading. For the bulk bone without skin layers (reference model, Fig. 3a), the maximal indentation load of 1 N is associated with a penetration depth of a few micrometers and the emergence of a classical indentation-induced VM stress field in the order of a few hundred of megapascals in the close vicinity of the indentation tip (Johnson and Johnson, 1987). Fig. 3b and c show the FE results for the keratin and keratin–collagen skin models, with the VM stress field built-up for increasing indentation loads (0.1 N, 0.5 N, and 1 N loads) and the residual plastic deformation. Note the color scale differences between Fig. 3a and b-c. The effect of the indent sharpness on the resultant damage morphology is shown in Fig. 4. To further investigate the damage resistance of the turtle shell, the effects of variations in the mechanical properties of the bi-layer skin on the residual plastic deformations were characterized (Fig. 5). Fig. 5a demonstrates the damage morphology resulting from increasing Young's modulus and the hardness values of the keratin while maintaining the mechanical characteristics of the collagen and bulk regions as in Figs. 3 and 4 (Table 2). Fig. 5b demonstrates the complementary effect of increasing Young's modulus and the hardness of the collagen layer. To assess the effect of physiological hydration conditions on the mechanical behavior of the bi-layer skin, the VM stress fields and the plastic damage of a 50 µm indentation depth were studied for various indent sharpness in dry and wet states (Figs. 6 and 7). The mechanical properties of the keratin, collagen, and bone layers at the dry and wet
2.2. Finite element analysis Commercial FE software (ABAQUS/explicit 6.12) was used for the numerical simulations. The indenter was modeled as a perfectly rigid conical element with a geometry equivalent to that of the experimental setup. The turtle shell was modelled as layered isotropic material with an elastic–perfectly plastic constitutive behavior (realized via 3-D, 8node, reduced integration hexahedral elements; C3D8R in ABAQUS element library). The mechanical properties and thickness of the individual model layers were selected according to the typical geometrical and mechanical characteristics obtained from the literature, as follows. Perfect binding conditions were assumed between the adjacent layers. The bottom face of the layered model was fixed and the lateral faces were kept free from mechanical loads. The model dimensions were chosen to be sufficiently large so as to avoid undesired effects by the boundary conditions. Frictionless contact between the conical indenter and the layered model were considered. Non-uniform segmentation, with a finer mesh in the vicinity of the indentation regime, was used to increase the solution accuracy at the region of interest. Convergence pre-analysis was conducted to estimate the required mesh parameters. The performed extensive indentation simulations, which naturally incorporate a large deformation and plasticity, were associated with adaptive meshing (ALE method) to reduce element distortion effects.
3. Results To investigate the indentation resistance of the turtle shell by FE simulations, a structural model of the shell was first formulated according to the literature data and validated by micro-indentation experiments. The simulation model considered the near-surface architecture of the turtle shell and included a thin keratin–collagen bi-layer skin underlaid by a thick bulk boney core (Fig. 1). The thickness of the keratin and collagen skin layers and their mechanical properties were selected based on previous structural observations (Achrai and Wagner, 2013) and typical literature values (Table 1). Young's modulus (E), yield strengths (σY ), and thicknesses (h) of the individual layers used for the FE simulations are listed in Table 2. Due to the lack of experimental data, the micro-structure of the individual layers and their mechanical anisotropic characteristics were not accounted for by the current FE modeling; such an approximated treatment, however, is customary in indentation simulations of bio-shielding materials (Bruet et al., 2008; Yao et al., 2010; Song et al., 2011; Wang et al., 2009). As a preliminary validation stage for the model parameters, a series of micro-indentation experiments with increasing penetration depths were conducted on two native turtle shells, and a set of equivalent – but independent – indentation simulations were conducted by the FE model (Fig. 2). Both methods yielded similar functional trends and a good agreement in the maximal force values (Fmax ), suggesting that the FE model parameters are compatible for describing the mechanical behavior (Fig. 2a). Similar experimental–FE compatibilities were
Table 2 Model parameters for the FE simulations (see Fig. 1).
3
Region
Young's modulus [GPa]
Yield stress [MPa]
thickness [μm]
Keratin layer Collagen layer Boney core
Ek =2 Ec=1.5 Eb=14
(σY )k =20 (σY )c =7 (σY )b =160
hk =50 hc=50 hb=900
Journal of the mechanical behavior of biomedical materials (xxxx) xxxx–xxxx
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Fig. 2. (a) Representative force-displacement curves for a 50-µm indentation depth, obtained by a micro-indentation experiment on the native turtle shell (red) and by the FE simulation model (black). The indentation loading and unloading stages and the maximal indentation force (Fmax ) are indicated. (b-c) Force-displacement curves for 10, 20, 30, 40, and 50 µm indentation depths, as obtained by (b) micro-indentation experiments, and (c) FE simulations. (d) Fmax values for increasing indentation depths. Marked regions represent the range of experimental results (20 experiments per depth, on two different shells). Symbols indicate the FE simulation results. The connecting dashed lines pronounce the trends of the experimental and simulation results. The input parameters for the FE simulation are indicated in Table 2.
Fig. 3. Results of the FE simulations of the von-Mises stress field and residual plastic deformations for indentation loads up to 1N in (a) a boney core without a skin layer (reference configuration), (b) keratin skin on a boney core (without the intermediate collagen), and (c) keratin–collagen skin on a boney core. The yield strength of the keratin and collagen layers is indicated in the scale bar; note scale differences between (a) and (b-c).
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Fig. 4. Results of the FE simulations of the residual plastic deformations for indentation of a 50 µm depth for models with increasing indent angle (left-to-right: 45°, 57.03°, and 70.3° ). The input parameters for the simulation are indicated in Table 2.
Fig. 5. (a) Results of the FE simulations of the residual plastic deformations for indentation of a 50 µm depth for models with increasing keratin modulus and yield strength (left-toright: E [GPa]={2,4,5}, σY [MPa]=[20,50,90]). The input parameters for the collagen and bone are the same as those indicated in Table 2. (b) Results of FE simulation of the residual plastic deformations for indentation of a 50 µm depth in models with increasing collagen modulus and yield strengths (left-to-right: E [GPa]={1,1.5,2.5}, σY [MPa]={4,7,15}). The input parameters for the keratin are E =4 GPa , σY =50
MPa , and for the bone: E =14 GPa , σY =160 MPa .
Fig. 6. Results of the FE simulations of the reaction force and the Von-Mises stress field for indentation of a 50 µm depth in dry and wet conditions. The input parameters for the simulation are indicated in Table 3.
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Fig. 7. Results of FE simulations of the von-Mises stress field for indentation of 50 µm in depth in dry and wet conditions (keratin–collagen skin on a boney core) with increasing indent tip angle (decreasing tip sharpness). The input parameters for the simulation are indicated in Table 3.
collagen layer between the keratin and the bulk bone, the indentation stresses are further distributed over a greater region – a “buffering” interface that further blunts the indentation effects and significantly decreases the bulk bone stresses by ~50%. While the VM stress morphology and its magnitude are largely affected by the presence of the collagen interface, the resulting penetration depth for a given load is almost unaffected (less than 5%). After full unloading, both the keratin and the keratin–collagen skin models exhibit considerable plastic damage in the near-surface region, which includes stamping the keratin surface (bumper) and squeezing the collagen interface (buffering). This dual bumper–buffer effect confines the indentation damage to the bi-layer skin region of the shell and thereby protects the underlying bulk bone. The resulting damage profiles to the bi-layer skin vary with the sharpness of the indents; for sharper indents, a greater stamping damage is generated at the keratin layer, which may even be pronounced by a pile-up of the surface (i.e., raised upward at the edge of the indentation region), whereas for blunter indents, greater collagen squeezing damage emerges and less of the keratin stamping. Upon decreasing Young's modulus or the hardness of the keratin surface layer or increasing of the Young's modulus and hardness of the collagen interface, a greater keratin stamping and less collagen squeezing damage is generated. This effect is effectively equivalent to that of tip sharpening. The complementary damage effect, i.e., greater collagen squeezing and less keratin stamping, is obtained by decreasing Young's modulus or the hardness of the collagen (or by increasing those of the keratin), which is equivalent to the effect of tip blunting. Significantly, the buffer–bumper mechanism, which protects the brittle boney region from indentation damage, was found throughout the entire range of keratin and collagen properties and for all indent shapes tested. As expected, the result of the simulations for different hydration conditions indicate that, for a given indentation depth, the reaction force at the dry state is higher than that at the wet state due to the greater stiffness and hardness of the keratin and collagen in dry states, as compared with their wet state. Nevertheless, VM stress morphology in both hydration states is very similar, and the
states were selected according to typical literature values (Achrai and Wagner, 2013), and are summarized in Table 3. 4. Discussion and conclusions While the exterior layer of most bio-shields is hard (Chen et al., 2008a, 2008b; Bruet et al., 2008; Wang et al., 2009; Yao et al., 2010; Song et al., 2011; Meyers et al., 2008; Chai et al., 2009; Barbakadze et al., 2006; Raabe et al., 2005; Zhu et al., 2012; Dastjerdi and Barthelat, 2015), some bio-shields have an overlaying soft, functional skin layer that protects the harder inner core (Krauss et al., 2009; Damiens et al., 2012; Magwene and Socha 2013; Fish and Stayton, 2014; Rhee et al., 2009; Balani et al., 2011; Chen et al., 2011, 2014, 2015; Achrai and Wagner, 2013, 2015; Sun and Chen, 2013; Achrai et al., 2014, 2015). Using the turtle shell as a case study of such inverse near-surface shielding architecture, we found that the skin stresses reach the keratin yielding strength in the vicinity of the indentation region, even at very shallow penetration depths with mild indentation loads. The emerging localized plasticity – which is effectively analogous to a “bumper” – blunts the penetration effect and diminishes the resulting stress concentrations. Consequently, this plasticity significantly reduces the stresses in the underlying bone, as compared with the skinned model. By including an additional softer intermediate Table 3 FE model parameters used for the dry and wet simulations in Figs. 6–7 (Achrai and Wagner, 2013). Region Keratin layer Collagen layer Boney core
Dry Wet Dry Wet Dry Wet
Young's modulus [GPa]
Yield stress [MPa]
Ek =4 Ek =1.3 Ec=1.5 Ec=0.2 Eb=14 Eb=11
(σY )k =50 (σY )k =13 (σY )c =15 (σY )c =2.5 (σY )b =160 (σY )b =93
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differences emerged mostly at the absolute magnitude of the stress field. The same trend was found for various indent geometries. These findings suggest that the bumper–buffer mechanism is an invariant structure–functional characteristic of the bi-layer skin of the turtle shell, regardless of the specific hydration conditions and the sharpness of the indenting elements. In conclusion, the mechanically inferior bi-layer skin coating of the turtle shell appears to play a major role in confining indentation effects to the near-surface region, thereby reducing the risk for potential damage in the hard-but-brittle bulk boney core. The turtle shell skin, which effectively functions as an integrated bumper–buffer mechanism, significantly enhances the damage resilience of the bio-shield to surface indentations by reducing the localized stress intensification and promoting energy dissipation via plasticity. While previous studies on synthetic soft-coating configurations (Jayachandran et al., 1995; Suresh, 2001; Choi et al., 2008) focused on gradual mechanical softening effects toward the surface, the turtle shell exhibits a rather novel architectural concept of a soft–softer–hard protective design strategy, which promotes significant resistance capabilities to the bioshield. Such an innovative functional bi-layer near-surface shielding concept can be adapted via synthetic materials to improve the resilience of engineering elements to various surface damage effects. Acknowledgements We acknowledge Prof. Daniel Wagner from the Weizmann Institute of Science (Israel) and Prof. Ron Shahar from the Hebrew University (Israel) for providing the samples, and acknowledge Dr. Ben Achrai from the Weizmann Institute of Science (Israel) and Mrs. Noga KalishAchrai from the Hebrew University (Israel) for their guidance and support with the sample preparations. This research was supported by the Israel Science Foundation (Grant no. 1429/16). References Achrai, B., Wagner, H.D., 2013. Micro-structure and mechanical properties of the turtle carapace as a biological composite shield. Acta Biomater. 9 (4), 5890–5902. Achrai, B., Wagner, H.D., 2015. The red-eared slider turtle carapace under fatigue loading: the effect of rib–suture arrangement. Mater. Sci. Eng.: C 53, 128–133. Achrai, B., Bar-On, B., Wagner, H.D., 2014. Bending mechanics of the red-eared slider turtle carapace. J. Mech. Behav. Biomed. Mater. 30, 223–233. Achrai, B., Bar-On, B., Wagner, H.D., 2015. Biological armors under impact—effect of keratin coating, and synthetic bio-inspired analogues. Bioinspir. Biomim. 10 (1), 016009. Amini, S., Tadayon, M., Idapalapati, S., Miserez, A., 2015. The role of quasi-plasticity in the extreme contact damage tolerance of the stomatopod dactyl club. Nat. Mater. 14, 943–950. Amini, S., Masic, A., Bertinetti, L., Teguh, J.S., Herrin, J.S., Zhu, X., Miserez, A., 2014. Textured fluorapatite bonded to calcium sulphate strengthen stomatopod raptorial appendages. Nat. Commun., 5. Balani, K., Patel, R.R., Keshri, A.K., Lahiri, D., Agarwal, A., 2011. Multi-scale hierarchy of Chelydra serpentina: microstructure and mechanical properties of turtle shell. J. Mech. Behav. Biomed. Mater. 4 (7), 1440–1451. Barbakadze, N., Enders, S., Gorb, S., Arzt, E., 2006. Local mechanical properties of the head articulation cuticle in the beetle Pachnoda marginata (Coleoptera, Scarabaeidae). J. Exp. Biol. 209 (4), 722–730. Bar-On, B., Wagner, H.D., 2012. Enamel and dentin as multi-scale bio-composites. J. Mech. Behav. Biomed. Mater. 12, 174–183. Bar-On, B., Wagner, H.D., 2013. Structural motifs and elastic properties of hierarchical biological tissues – a review. J. Struct. Biol. 183 (2), 149–164. Bar-On, B., Barth, F.G., Fratzl, P., Politi, Y., 2014. Multiscale structural gradients enhance the biomechanical functionality of the spider fang. Nat. Commun., 5. Barth, F.G., 1973. Microfiber reinforcement of an arthropod cuticle. Z. Zellforsch. Mikrosk. Anat. 144 (3), 409–433. Barthelat, F., Yin, Z., Buehler, M.J., 2016. Structure and mechanics of interfaces in biological materials. Nat. Rev. Mater. 1, 16007. Bruet, B.J., Song, J., Boyce, M.C., Ortiz, C., 2008. Materials design principles of ancient fish armour. Nat. Mater. 7 (9), 748–756. Chai, H., Lee, J.J.W., Constantino, P.J., Lucas, P.W., Lawn, B.R., 2009. Remarkable resilience of teeth. Proc. Natl. Acad. Sci. USA 106 (18), 7289–7293. Chen, I.H., Yang, W., Meyers, M.A., 2014. Alligator osteoderms: mechanical behavior and hierarchical structure. Mater. Sci. Eng.: C 35, 441–448. Chen, I.H., Yang, W., Meyers, M.A., 2015. Leatherback sea turtle shell: a tough and flexible biological design. Acta Biomater. 28, 2–12. Chen, I.H., Kiang, J.H., Correa, V., Lopez, M.I., Chen, P.Y., McKittrick, J., Meyers, M.A.,
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Yao, H., Dao, M., Imholt, T., Huang, J., Wheeler, K., Bonilla, A., Ortiz, C., 2010. Protection mechanisms of the iron-plated armor of a deep-sea hydrothermal vent gastropod. Proc. Natl. Acad. Sci. USA 107 (3), 987–992. Zhu, D., Ortega, C.F., Motamedi, R., Szewciw, L., Vernerey, F., Barthelat, F., 2012. Structure and mechanical performance of a “modern” fish scale. Adv. Eng. Mater. 14 (4), B185–B194.
Vincent, J.F.V., 2005. Defense and Attack Strategies and Mechanisms in Biology. Biomimetics-Biologically Inspired Technologies. Wang, B., Yang, W., McKittrick, J., Meyers, M.A., 2016. Keratin: structure, mechanical properties, occurrence in biological organisms, and efforts at bioinspiration. Prog. Mater. Sci. 76, 229–318. Wang, L., Song, J., Ortiz, C., Boyce, M.C., 2009. Anisotropic design of a multilayered biological exoskeleton. J. Mater. Res. 24 (12), 3477–3494.
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Contents lists available at ScienceDirect
Journal of the Mechanical Behavior of Biomedical Materials journal homepage: www.elsevier.com/locate/jmbbm
Surface protection in bio-shields via a functional soft skin layer: Lessons from the turtle shell ⁎
Yaniv Shelef, Benny Bar-On
Department of Mechanical Engineering, Ben-Gurion University of the Negev, Beer Sheva 84105, Israel
A R T I C L E I N F O
A BS T RAC T
Keywords: Bio-shields Indentation resistance Bio-composites
The turtle shell is a functional bio-shielding element, which has evolved naturally to provide protection against predator attacks that involve biting and clawing. The near-surface architecture of the turtle shell includes a soft bi-layer skin coating – rather than a hard exterior – which functions as a first line of defense against surface damage. This architecture represents a novel type of bio-shielding configuration, namely, an inverse structural– mechanical design, rather than the hard-coated bio-shielding elements identified so far. In the current study, we used experimentally based structural modeling and FE simulations to analyze the mechanical significance of this unconventional protection architecture in terms of resistance to surface damage upon extensive indentations. We found that the functional bi-layer skin of the turtle shell, which provides graded (soft-softer-hard) mechanical characteristics to the bio-shield exterior, serves as a bumper–buffer mechanism. This material-level adaptation protects the inner core from the highly localized indentation loads via stress delocalization and extensive near-surface plasticity. The newly revealed functional bi-layer coating architecture can potentially be adapted, using synthetic materials, to considerably enhance the surface load-bearing capabilities of various engineering configurations.
1. Introduction
reinforcing elements (nano-fibrils, nano-platelets, etc.) and bio-polymers (Barth, 1973; Vincent and Wegst, 2004; Chen et al., 2008a, 2008b; Dunlop and Fratzl, 2010; Dunlop et al., 2011; Bar-On and Wagner, 2013; Meyers et al., 2013; Moussian, 2013; Barthelat et al., 2016; Naleway et al., 2016). In recent years, intensive research has addressed the structure and the mechanical behavior of various shielding materials, most notably seashells, teeth, fish scales, arthropod exoskeletons, and the armored osteoderms of the armadillo, alligator, and the shell of the turtle. Seashells, for example, possess an external hard prismatic layer, which serves as a first line of defense against predator attacks; this layer is underlaid with a high-toughness nacreous layer, which resists crack propagation and reduces the risk of catastrophic damage to the shell (Meyers, 2008). Similarly, teeth possess a highly mineralized hard-but-brittle enamel coating, which serves as a grinding surface for food and is underlaid with a more compliant and less mineralized dentin region (Chen et al., 2008a, 2008b; Bar-On and Wagner, 2012). The enamel and dentin are linked by an interfacial dentin–enamel junction, which has a lower degree of hardness and stiffness than either dentin or enamel, thus providing crack-arresting capabilities and preventing enamel cracks from propagating toward the inner part of the tooth (Chai et al., 2009; Imbeni et al., 2005; Shimizu and Macho, 2007). The protective exoskeleton of various arthropods,
Being the product of natural selection over millions of years of evolution, bio-shielding elements have evolved to provide mechanical protection against a variety of load-bearing conditions. As such, they can both resist structural loads (e.g., bending moments and torsion) that tend to macroscopically deform the shield shape (e.g., (Vincent, 2005; Chen et al., 2008a, 2008b; Krauss et al., 2009; Damiens et al., 2012; Magwene and Socha, 2013; Fish and Stayton, 2014)), and they can sustain localized surface tractions, which are typically associated with predator biting attacks, which tend to crack the shield (e.g., (Bruet et al., 2008; Wang et al., 2009; Yao et al., 2010; Song et al., 2011; Amini et al., 2014, 2015)). The two functions are achieved through the complex hierarchical structure of bio-shields; while resistance to structural loads is associated with the macro-structural–mechanical characteristics of the shield as a whole, the ability to sustain localized surface tractions is related to the near-surface characteristics and, in particular, to the mechanical rigidity and hardness of the shield exterior. Natural bio-shielding elements are fundamentally structured as hierarchical bio-composites that comprise several micro-scale layers, each of which is structured as an integrated array of small-scale
⁎
Corresponding author. E-mail address: [email protected] (B. Bar-On).
http://dx.doi.org/10.1016/j.jmbbm.2017.01.019 Received 7 August 2016; Received in revised form 5 January 2017; Accepted 11 January 2017 1751-6161/ © 2017 Elsevier Ltd. All rights reserved.
Please cite this article as: Shelef, Y., Journal of the mechanical behavior of biomedical materials (2017), http://dx.doi.org/10.1016/j.jmbbm.2017.01.019
Journal of the mechanical behavior of biomedical materials (xxxx) xxxx–xxxx
Y. Shelef, B. Bar-On
(Wang et al., 2009; Yao et al., 2010; Amini et al., 2014, 2015; Chintapalli et al., 2014; Rudykh et al., 2015)). Whereas the surface protection capabilities of the hard-coat bioshielding architectures are straightforward, it is less intuitive to understand how soft-coat architectures promote surface protection, if, indeed, they do. Nevertheless, several studies on synthetic materials have implied that a soft skin coating overlaid on a rigid substrate may protect against surface damage (Jayachandran et al., 1995; Suresh, 2001; Choi et al., 2008) and even detain near-surface crack propagation (Kolednik, 2000; Simha et al., 2003). In line with these studies, experimental evidence from impact tests on the turtle shell, which is overlaid with two layers of soft skin, indicate that the skin plays a critical role in shielding against impact damage (Achrai et al., 2015). In the current investigation, we focused on the turtle shell as a specific case study, representative of the large family of soft-coated bioshielding elements, and analyzed its resistance to surface damage upon extensive indentations. First, we used experimental measurements to establish a numerical structural–mechanical model for the turtle shell. Then, we investigated the role of each individual skin layer in protecting the turtle shell against extensive indentations. Finally, we studied the effect of the difference in the mechanical properties of the two layers comprising the turtle-shell skin and analyzed the effect of indenter sharpness and physiological hydration conditions on the resultant damage patterns.
including insects (Barth, 1973; Vincent and Wegst, 2004; Moussian, 2013; Barbakadze et al., 2006), spiders (Politi et al., 2012; Bar-On et al., 2014), lobsters (Raabe et al., 2005), and crabs (Chen et al., 2008a, 2008b), typically includes a lamellar architecture of chitin nanofibrils arranged in helical lamellar patterns (twisted plywood). These lamellae form external and internal layers (exocuticle and endocuticle, respectively) of increasing densities, and, thereby, enhance the mechanical properties of the cuticle toward its exterior. In addition, the near-surface region of the arthropod exoskeleton is commonly associated with an increase in the mineralization and sclerotization levels and with the presence of metal ions, which stiffen and harden the exoskeleton (Amini et al., 2014; Politi et al., 2012; Degtyar et al., 2014). Surprisingly, despite the obvious distinctive evolutionary origin of the various natural shielding elements across taxa, all these elements share the same generic structural–mechanical design: a hard exterior underlaid with a softer interior. In contrast, the osteoderms of the armadillo and alligator and the shell of the turtle demonstrate an alternative structural strategy (Krauss et al., 2009; Damiens et al., 2012; Magwene and Socha, 2013; Fish and Stayton, 2014; Rhee et al., 2009; Balani et al., 2011; Chen et al., 2011, 2014, 2015; Achrai and Wagner, 2013, 2015 Achrai et al., 2014, 2015, 2015; Sun and Chen, 2013 and see the review on turtle shells by Achrai and Wagner in this issue), which incorporates a soft skin coating (namely, a keratin–collagen bi-layer) overlaid with a harder boney core (Fig. 1). The skin coating is mechanically inferior to the underlying boney core, and, obviously, induces a negligible effect on the macro-structural rigidity of the shield (Achrai et al., 2014). However, it appears to play a significant role in adsorbing impact energy, and thereby to increases the damage resilience of the bio-shield against sudden mechanical loads (Achrai et al., 2015). In the past few years, the resilience of hard-coated bio-shields to surface damage was extensively analyzed in a wide range of biological systems, among which are fish scales, which typically comprise a highly mineralized hard-and-brittle exterior, underlaid by a less mineralized softer layer (Bruet et al., 2008; Song et al., 2014; Zhu et al., 2012; Dastjerdi and Barthelat 2015). Experimental and numerical studies of fish scales demonstrated that low-force indentations (i.e., indentations that do not cause coating failure) produce shallow penetrations, which only damage the hard surface layer. Higher indentation forces, i.e., beyond the coating failure point, severely fracture the hard surface layer and damage the softer underlying material. Finite-Element (FE) simulations indicate that the hard coating functions as a load barrier by confining the high-stress fields to the scale exterior and screening the indentation effects from the inner regions. Other hard-coated biological and bio-inspired shielding elements demonstrated similar effects (e.g.
2. Materials and methods 2.1. Experimental Two carapaces from red-eared slider turtles (Trachemys scripta elegans) were used for the mechanical testing. The samples were kept frozen (−70 °C) and were allowed to defrost and dry under ambient conditions for 24 h prior to measurement; no further treatment was conducted to the samples. Micro-indentation experiments were conducted by using a Hysitron TI 950 TriboIndenter, equipped with a high-load cell (3D OmniProb) allowing extensive indentations of a few tens of micrometers in depth and a few Newtons in load. A conical diamond probe tip (tip radius: 5.26 µm; angle: 57.03°) was used for the experiments. The experiments included a 5-s loading-up stage (linear ramp) up to a maximal load, which was kept steady for 20 s to exclude creep effects, followed by a 5-s unloading stage (linear ramp). The indentation locations were carefully selected to avoid natural roughness problems of the native (unpolished and untreated) carapace surface.
Fig. 1. Schematic description and a SEM image of the near-surface architecture of the turtle shell (adapted from (Achrai and Wagner, 2013; Achrai et al., 2015)). The shell is viewed as a layered composite material with a thick boney bulk (porous boney interior enclosed by dense boney layers) overlaid with a thin keratin–collagen bi-layer skin. The near-surface region of the shell is modeled as a tri-layered segment, composed of a boney core of thickness hb , coated by keratin and collagen layers of thickness hk and hc , respectively. Young's modulus (E) and the hardness (H) of the keratin, collagen, and bone layers are indicated by Ek , Ec and Eb , and Hk , Hc and Hb , respectively. Note that, typically,(Ec,Hc ) < (Ek ,Hk ) < (Eb,Hb ) .
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Table 1 Typical literature values for Young's modulus and yield strength for keratin, collagen and bone. Region
E [GPa]
Surface Layer (Keratin)
2–5 1.5, 1.4,1.3 2.7 3.8 0.7–2.5 3.26 1.9–2.4 14–20, 13, 6–10 17.5
Interface (Collagen)
Underlying Layer (Bone)
a
σY [MPa] Carapace, Turtle (Achrai and Wagner, 2013) Beak, Toucan (Seki et al., 2006; McKittrick et al., 2012) Claw, Ostrich (McKittrick et al., 2012; Wang et al., 2016) Quill, Hedgehog (McKittrick et al., 2012) Carapace, Turtle (Achrai and Wagner, 2013) Micro-fibril (Gautieri et al., 2011) Bone tissue, Antler (Hang and Barber, 2011) Carapace, Turtle (Achrai and Wagner, 2013; Achrai et al., 2014; Rhee et al., 2009) Antler, Deer (Currey et al., 2009)
20–90a 30 90 – 4–36a – 81–156 160–270a, 300a,130–290 352.2
The σY was estimated based on hardness measurements via ~H/3 (Bruet et al., 2008).
obtained for the entire range of indentation depths (10, 15…50 µm) in the two shells tested (Fig. 2b-c). The FE results fall within the experimental range for extensive indentations (i.e., beyond ~25 µm depth); however, for shallower indentations, the FE results provide less compatible predictions (Fig. 2d), possibly because the refined micromechanical characteristics of the keratin layer were not accounted for. After confirming the suitability of the FE model, the same numerical platform was employed to analyze the mechanical role of the turtle shell skin as a protective medium against extensive indentations. The analysis focused on the stress distribution and residual plastic damage in the vicinity of the indentation zone. To isolate the mechanical functionality of the individual keratin and collagen skin layers, three simulation models were employed (Fig. 3): (a) a bulk bone without a skin layer (for reference), (b) a single-layer keratin skin, superimposed on the bulk bone, and (c) a keratin–collagen bi-layer skin, superimposed on the bulk bone. Two criteria were considered to investigate the mechanical response to indentations: (1) the equivalent Von-Mises stress field (VM) for a gradual indentation loading up to 1 N, and (2) the resultant plastic strain field (P) after complete unloading. For the bulk bone without skin layers (reference model, Fig. 3a), the maximal indentation load of 1 N is associated with a penetration depth of a few micrometers and the emergence of a classical indentation-induced VM stress field in the order of a few hundred of megapascals in the close vicinity of the indentation tip (Johnson and Johnson, 1987). Fig. 3b and c show the FE results for the keratin and keratin–collagen skin models, with the VM stress field built-up for increasing indentation loads (0.1 N, 0.5 N, and 1 N loads) and the residual plastic deformation. Note the color scale differences between Fig. 3a and b-c. The effect of the indent sharpness on the resultant damage morphology is shown in Fig. 4. To further investigate the damage resistance of the turtle shell, the effects of variations in the mechanical properties of the bi-layer skin on the residual plastic deformations were characterized (Fig. 5). Fig. 5a demonstrates the damage morphology resulting from increasing Young's modulus and the hardness values of the keratin while maintaining the mechanical characteristics of the collagen and bulk regions as in Figs. 3 and 4 (Table 2). Fig. 5b demonstrates the complementary effect of increasing Young's modulus and the hardness of the collagen layer. To assess the effect of physiological hydration conditions on the mechanical behavior of the bi-layer skin, the VM stress fields and the plastic damage of a 50 µm indentation depth were studied for various indent sharpness in dry and wet states (Figs. 6 and 7). The mechanical properties of the keratin, collagen, and bone layers at the dry and wet
2.2. Finite element analysis Commercial FE software (ABAQUS/explicit 6.12) was used for the numerical simulations. The indenter was modeled as a perfectly rigid conical element with a geometry equivalent to that of the experimental setup. The turtle shell was modelled as layered isotropic material with an elastic–perfectly plastic constitutive behavior (realized via 3-D, 8node, reduced integration hexahedral elements; C3D8R in ABAQUS element library). The mechanical properties and thickness of the individual model layers were selected according to the typical geometrical and mechanical characteristics obtained from the literature, as follows. Perfect binding conditions were assumed between the adjacent layers. The bottom face of the layered model was fixed and the lateral faces were kept free from mechanical loads. The model dimensions were chosen to be sufficiently large so as to avoid undesired effects by the boundary conditions. Frictionless contact between the conical indenter and the layered model were considered. Non-uniform segmentation, with a finer mesh in the vicinity of the indentation regime, was used to increase the solution accuracy at the region of interest. Convergence pre-analysis was conducted to estimate the required mesh parameters. The performed extensive indentation simulations, which naturally incorporate a large deformation and plasticity, were associated with adaptive meshing (ALE method) to reduce element distortion effects.
3. Results To investigate the indentation resistance of the turtle shell by FE simulations, a structural model of the shell was first formulated according to the literature data and validated by micro-indentation experiments. The simulation model considered the near-surface architecture of the turtle shell and included a thin keratin–collagen bi-layer skin underlaid by a thick bulk boney core (Fig. 1). The thickness of the keratin and collagen skin layers and their mechanical properties were selected based on previous structural observations (Achrai and Wagner, 2013) and typical literature values (Table 1). Young's modulus (E), yield strengths (σY ), and thicknesses (h) of the individual layers used for the FE simulations are listed in Table 2. Due to the lack of experimental data, the micro-structure of the individual layers and their mechanical anisotropic characteristics were not accounted for by the current FE modeling; such an approximated treatment, however, is customary in indentation simulations of bio-shielding materials (Bruet et al., 2008; Yao et al., 2010; Song et al., 2011; Wang et al., 2009). As a preliminary validation stage for the model parameters, a series of micro-indentation experiments with increasing penetration depths were conducted on two native turtle shells, and a set of equivalent – but independent – indentation simulations were conducted by the FE model (Fig. 2). Both methods yielded similar functional trends and a good agreement in the maximal force values (Fmax ), suggesting that the FE model parameters are compatible for describing the mechanical behavior (Fig. 2a). Similar experimental–FE compatibilities were
Table 2 Model parameters for the FE simulations (see Fig. 1).
3
Region
Young's modulus [GPa]
Yield stress [MPa]
thickness [μm]
Keratin layer Collagen layer Boney core
Ek =2 Ec=1.5 Eb=14
(σY )k =20 (σY )c =7 (σY )b =160
hk =50 hc=50 hb=900
Journal of the mechanical behavior of biomedical materials (xxxx) xxxx–xxxx
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Fig. 2. (a) Representative force-displacement curves for a 50-µm indentation depth, obtained by a micro-indentation experiment on the native turtle shell (red) and by the FE simulation model (black). The indentation loading and unloading stages and the maximal indentation force (Fmax ) are indicated. (b-c) Force-displacement curves for 10, 20, 30, 40, and 50 µm indentation depths, as obtained by (b) micro-indentation experiments, and (c) FE simulations. (d) Fmax values for increasing indentation depths. Marked regions represent the range of experimental results (20 experiments per depth, on two different shells). Symbols indicate the FE simulation results. The connecting dashed lines pronounce the trends of the experimental and simulation results. The input parameters for the FE simulation are indicated in Table 2.
Fig. 3. Results of the FE simulations of the von-Mises stress field and residual plastic deformations for indentation loads up to 1N in (a) a boney core without a skin layer (reference configuration), (b) keratin skin on a boney core (without the intermediate collagen), and (c) keratin–collagen skin on a boney core. The yield strength of the keratin and collagen layers is indicated in the scale bar; note scale differences between (a) and (b-c).
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Fig. 4. Results of the FE simulations of the residual plastic deformations for indentation of a 50 µm depth for models with increasing indent angle (left-to-right: 45°, 57.03°, and 70.3° ). The input parameters for the simulation are indicated in Table 2.
Fig. 5. (a) Results of the FE simulations of the residual plastic deformations for indentation of a 50 µm depth for models with increasing keratin modulus and yield strength (left-toright: E [GPa]={2,4,5}, σY [MPa]=[20,50,90]). The input parameters for the collagen and bone are the same as those indicated in Table 2. (b) Results of FE simulation of the residual plastic deformations for indentation of a 50 µm depth in models with increasing collagen modulus and yield strengths (left-to-right: E [GPa]={1,1.5,2.5}, σY [MPa]={4,7,15}). The input parameters for the keratin are E =4 GPa , σY =50
MPa , and for the bone: E =14 GPa , σY =160 MPa .
Fig. 6. Results of the FE simulations of the reaction force and the Von-Mises stress field for indentation of a 50 µm depth in dry and wet conditions. The input parameters for the simulation are indicated in Table 3.
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Fig. 7. Results of FE simulations of the von-Mises stress field for indentation of 50 µm in depth in dry and wet conditions (keratin–collagen skin on a boney core) with increasing indent tip angle (decreasing tip sharpness). The input parameters for the simulation are indicated in Table 3.
collagen layer between the keratin and the bulk bone, the indentation stresses are further distributed over a greater region – a “buffering” interface that further blunts the indentation effects and significantly decreases the bulk bone stresses by ~50%. While the VM stress morphology and its magnitude are largely affected by the presence of the collagen interface, the resulting penetration depth for a given load is almost unaffected (less than 5%). After full unloading, both the keratin and the keratin–collagen skin models exhibit considerable plastic damage in the near-surface region, which includes stamping the keratin surface (bumper) and squeezing the collagen interface (buffering). This dual bumper–buffer effect confines the indentation damage to the bi-layer skin region of the shell and thereby protects the underlying bulk bone. The resulting damage profiles to the bi-layer skin vary with the sharpness of the indents; for sharper indents, a greater stamping damage is generated at the keratin layer, which may even be pronounced by a pile-up of the surface (i.e., raised upward at the edge of the indentation region), whereas for blunter indents, greater collagen squeezing damage emerges and less of the keratin stamping. Upon decreasing Young's modulus or the hardness of the keratin surface layer or increasing of the Young's modulus and hardness of the collagen interface, a greater keratin stamping and less collagen squeezing damage is generated. This effect is effectively equivalent to that of tip sharpening. The complementary damage effect, i.e., greater collagen squeezing and less keratin stamping, is obtained by decreasing Young's modulus or the hardness of the collagen (or by increasing those of the keratin), which is equivalent to the effect of tip blunting. Significantly, the buffer–bumper mechanism, which protects the brittle boney region from indentation damage, was found throughout the entire range of keratin and collagen properties and for all indent shapes tested. As expected, the result of the simulations for different hydration conditions indicate that, for a given indentation depth, the reaction force at the dry state is higher than that at the wet state due to the greater stiffness and hardness of the keratin and collagen in dry states, as compared with their wet state. Nevertheless, VM stress morphology in both hydration states is very similar, and the
states were selected according to typical literature values (Achrai and Wagner, 2013), and are summarized in Table 3. 4. Discussion and conclusions While the exterior layer of most bio-shields is hard (Chen et al., 2008a, 2008b; Bruet et al., 2008; Wang et al., 2009; Yao et al., 2010; Song et al., 2011; Meyers et al., 2008; Chai et al., 2009; Barbakadze et al., 2006; Raabe et al., 2005; Zhu et al., 2012; Dastjerdi and Barthelat, 2015), some bio-shields have an overlaying soft, functional skin layer that protects the harder inner core (Krauss et al., 2009; Damiens et al., 2012; Magwene and Socha 2013; Fish and Stayton, 2014; Rhee et al., 2009; Balani et al., 2011; Chen et al., 2011, 2014, 2015; Achrai and Wagner, 2013, 2015; Sun and Chen, 2013; Achrai et al., 2014, 2015). Using the turtle shell as a case study of such inverse near-surface shielding architecture, we found that the skin stresses reach the keratin yielding strength in the vicinity of the indentation region, even at very shallow penetration depths with mild indentation loads. The emerging localized plasticity – which is effectively analogous to a “bumper” – blunts the penetration effect and diminishes the resulting stress concentrations. Consequently, this plasticity significantly reduces the stresses in the underlying bone, as compared with the skinned model. By including an additional softer intermediate Table 3 FE model parameters used for the dry and wet simulations in Figs. 6–7 (Achrai and Wagner, 2013). Region Keratin layer Collagen layer Boney core
Dry Wet Dry Wet Dry Wet
Young's modulus [GPa]
Yield stress [MPa]
Ek =4 Ek =1.3 Ec=1.5 Ec=0.2 Eb=14 Eb=11
(σY )k =50 (σY )k =13 (σY )c =15 (σY )c =2.5 (σY )b =160 (σY )b =93
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differences emerged mostly at the absolute magnitude of the stress field. The same trend was found for various indent geometries. These findings suggest that the bumper–buffer mechanism is an invariant structure–functional characteristic of the bi-layer skin of the turtle shell, regardless of the specific hydration conditions and the sharpness of the indenting elements. In conclusion, the mechanically inferior bi-layer skin coating of the turtle shell appears to play a major role in confining indentation effects to the near-surface region, thereby reducing the risk for potential damage in the hard-but-brittle bulk boney core. The turtle shell skin, which effectively functions as an integrated bumper–buffer mechanism, significantly enhances the damage resilience of the bio-shield to surface indentations by reducing the localized stress intensification and promoting energy dissipation via plasticity. While previous studies on synthetic soft-coating configurations (Jayachandran et al., 1995; Suresh, 2001; Choi et al., 2008) focused on gradual mechanical softening effects toward the surface, the turtle shell exhibits a rather novel architectural concept of a soft–softer–hard protective design strategy, which promotes significant resistance capabilities to the bioshield. Such an innovative functional bi-layer near-surface shielding concept can be adapted via synthetic materials to improve the resilience of engineering elements to various surface damage effects. Acknowledgements We acknowledge Prof. Daniel Wagner from the Weizmann Institute of Science (Israel) and Prof. Ron Shahar from the Hebrew University (Israel) for providing the samples, and acknowledge Dr. Ben Achrai from the Weizmann Institute of Science (Israel) and Mrs. Noga KalishAchrai from the Hebrew University (Israel) for their guidance and support with the sample preparations. This research was supported by the Israel Science Foundation (Grant no. 1429/16). References Achrai, B., Wagner, H.D., 2013. Micro-structure and mechanical properties of the turtle carapace as a biological composite shield. Acta Biomater. 9 (4), 5890–5902. Achrai, B., Wagner, H.D., 2015. The red-eared slider turtle carapace under fatigue loading: the effect of rib–suture arrangement. Mater. Sci. Eng.: C 53, 128–133. Achrai, B., Bar-On, B., Wagner, H.D., 2014. Bending mechanics of the red-eared slider turtle carapace. J. Mech. Behav. Biomed. Mater. 30, 223–233. Achrai, B., Bar-On, B., Wagner, H.D., 2015. Biological armors under impact—effect of keratin coating, and synthetic bio-inspired analogues. Bioinspir. Biomim. 10 (1), 016009. Amini, S., Tadayon, M., Idapalapati, S., Miserez, A., 2015. The role of quasi-plasticity in the extreme contact damage tolerance of the stomatopod dactyl club. Nat. Mater. 14, 943–950. Amini, S., Masic, A., Bertinetti, L., Teguh, J.S., Herrin, J.S., Zhu, X., Miserez, A., 2014. Textured fluorapatite bonded to calcium sulphate strengthen stomatopod raptorial appendages. Nat. Commun., 5. Balani, K., Patel, R.R., Keshri, A.K., Lahiri, D., Agarwal, A., 2011. Multi-scale hierarchy of Chelydra serpentina: microstructure and mechanical properties of turtle shell. J. Mech. Behav. Biomed. Mater. 4 (7), 1440–1451. Barbakadze, N., Enders, S., Gorb, S., Arzt, E., 2006. Local mechanical properties of the head articulation cuticle in the beetle Pachnoda marginata (Coleoptera, Scarabaeidae). J. Exp. Biol. 209 (4), 722–730. Bar-On, B., Wagner, H.D., 2012. Enamel and dentin as multi-scale bio-composites. J. Mech. Behav. Biomed. Mater. 12, 174–183. Bar-On, B., Wagner, H.D., 2013. Structural motifs and elastic properties of hierarchical biological tissues – a review. J. Struct. Biol. 183 (2), 149–164. Bar-On, B., Barth, F.G., Fratzl, P., Politi, Y., 2014. Multiscale structural gradients enhance the biomechanical functionality of the spider fang. Nat. Commun., 5. Barth, F.G., 1973. Microfiber reinforcement of an arthropod cuticle. Z. Zellforsch. Mikrosk. Anat. 144 (3), 409–433. Barthelat, F., Yin, Z., Buehler, M.J., 2016. Structure and mechanics of interfaces in biological materials. Nat. Rev. Mater. 1, 16007. Bruet, B.J., Song, J., Boyce, M.C., Ortiz, C., 2008. Materials design principles of ancient fish armour. Nat. Mater. 7 (9), 748–756. Chai, H., Lee, J.J.W., Constantino, P.J., Lucas, P.W., Lawn, B.R., 2009. Remarkable resilience of teeth. Proc. Natl. Acad. Sci. USA 106 (18), 7289–7293. Chen, I.H., Yang, W., Meyers, M.A., 2014. Alligator osteoderms: mechanical behavior and hierarchical structure. Mater. Sci. Eng.: C 35, 441–448. Chen, I.H., Yang, W., Meyers, M.A., 2015. Leatherback sea turtle shell: a tough and flexible biological design. Acta Biomater. 28, 2–12. Chen, I.H., Kiang, J.H., Correa, V., Lopez, M.I., Chen, P.Y., McKittrick, J., Meyers, M.A.,
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Journal of the mechanical behavior of biomedical materials (xxxx) xxxx–xxxx
Y. Shelef, B. Bar-On
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