Impact resistant structures and materials have been evolved in nature during millions of years of evolution. Some examples of energy absorbent biological materials have been recently reported; however, a better comprehensive understanding of impact-resistant biological materials is still required to compare their unique features: a degree of mineralization, specific mechanical behavior and/or loading condition of tissue/animal, and intentional (active) or indirect (passive) modification of the innate structure/material. The woodpecker head was chosen as a representative impact-resistant material/structure found in nature because woodpeckers avoid brain injury while they peck at trees up to 20 Hz with speeds up to 7 m/s, undergoing decelerations up to 1,200 g.
The brain is one of the most important and complicated organs, but it is delicate and therefore needs to be protected from external forces. This makes the pecking behavior of the woodpecker so impressive, as they are not known to sustain any brain injury due to their anatomical adaptations (e.g., a specialized beak, skull bone, and hyoid bone). However, the relationship between the morphology of the woodpecker head and its mechanical function against damage from daily pecking habits remain an open question. The shape of the hyoid apparatus is unusual in woodpeckers and its structure and mechanical properties have not been reported in detail. Moreover, the shape and mechanical properties of the skull bone of woodpeckers is different from other non-pecking birds. Therefore, the research works throughout this dissertation aim to examine the anatomical structure, composition, and mechanical properties of the hyoid bone and the skull bone, and to find an interspecies variation of the skull bone morphology in woodpeckers eventually in order to determine its potential role in energy absorption and dissipation as an efficient protection of the brain. Aided by recent technical advancements, such as multiscale imaging tools (micro-computed tomography, optical and scanning electron microscopy), 3D printing, high-precision, miniaturized sensors, and computational simulation, these questions can be explored by applying new materials science concepts of bioinspiration and bioexploration to identify adapted structures/materials in a design that results from millions of years of evolution.
The hyoid apparatus has four distinct bone sections, with three joints between these sections. Nanoindentation results on cross-sectional regions of each bone reveal a previously unreported structure consisting of a stiff core and outer, more compliant shell with moduli of up to 27.4 GPa and 8.5 GPa, respectively. The bending resistance is low at the posterior section of the hyoid bones, indicating that this region has a high degree of flexibility to absorb impact. In the skull bone of woodpeckers compared to the chicken skull, two different strategies are found: the skull bone of the woodpecker shows a relatively small but uniform level of closed porosity, a higher degree of mineralization, and a higher cortical to skull bone ratio. From the 3D printing and computational simulation approach, two main features, including the beam-like bar structure of the jugal bone acting as the main stress deflector and the high natural frequency of the skull bone of woodpeckers can teach two lessons for potential materials development as well as engineering applications: 1) protection of a delicate internal organ occurs by redirection of the main stress pathway and 2) a large mismatch of the natural frequencies between the skull and brain avoids resonance and reduces the overall load experienced by the brain.
Lastly, bioinspired designs and engineering applications will be discussed using some case studies in biological materials for the development of protective devices or robots. This novel approach will provide a new insight to many researchers and engineers in materials science and mechanical engineering disciplines to teach how the natural materials have evolved to adapt its impact-resistant ability against different environments.
|1970||Hirsch AE, Ommaya AK, Mahone RH. Tolerance of subhuman primate brain to cerebral concussion. In: Gurdjian ES, Lange WA, Patrick LM, Thomas LM, eds. Impact Injury and Crash Protection. Springfield, IL: Charles C. Thomas; 1970:352-369.|
|1999||Rho J-Y, Pharr GM. Effects of drying on the mechanical properties of bovine femur measured by nanoindentation. J Mater Sci Mater Med. 1999;10(8):485-488.|
|2008||Ritchie RO, Koester KJ, Ionova S, Yao W, Lane NE, Ager JW III. Measurement of the toughness of bone: a tutorial with special reference to small animal studies. Bone. November 2008;43(5):798-812.|
|2009||McKee AC, Cantu RC, Nowinski CJ, Hedley-Whyte ET, Gavett BE, Budson AE, Santini VE, Lee H-S, Kubilus CA, Stern RA. Chronic traumatic encephalopathy in athletes: progressive tauopathy after repetitive head injury. J Neuropathol & Exp Neurol. July 2009;68(7):709-735.|
|2005||Nalla RK, Kruzic JJ, Kinney JH, Ritchie RO. Mechanistic aspects of fracture and R-curve behavior in human cortical bone. Biomaterials. January 2005;26(2):217-231.|
|2003||Nalla RK, Kinney JH, Ritchie RO. Effect of orientation on the in vitro fracture toughness of dentin: the role of toughening mechanisms. Biomaterials. October 2003;24(22):3955-3968.|
|2004||Nalla RK, Kruzic JJ, Kinney JH, Ritchie RO. Effect of aging on the toughness of human cortical bone: evaluation by R-curves. Bone. December 2004;35(6):1240-1246.|
|2003||Nalla RK, Kinney JH, Ritchie RO. Mechanistic fracture criteria for the failure of human cortical bone. Nat Mater. 2003;2(3):164-168.|
|2004||Wegst UGK, Ashby MF. The mechanical efficiency of natural materials. Philos Mag. July 21, 2004;84(21):2167-2181.|
|2001||Evans AG, Suo Z, Wang RZ, Aksay IA, He MY, Hutchinson JW. Model for the robust mechanical behavior of nacre. J Mater Res. September 2001;16(9):2475-2484.|
|2010||Doube M, Kłosowski MM, Arganda-Carreras I, Cordelières FP, Dougherty RP, Jackson JS, Schmid B, Hutchinson JR, Shefelbine SJ. BoneJ: free and extensible bone image analysis in ImageJ. Bone. December 2010;47(6):1076-1079.|
|2010||Launey ME, Buehler MJ, Ritchi RO. On the mechanistic origins of toughness in bone. Ann Rev Mater Sci. 2010;40:25-53.|
|2002||Wang X, Shen X, Li X, Agrawal CM. Age-related changes in the collagen network and toughness of bone [published correction appears in Bone. 2003;32(1):107]. Bone. 2002;31(1):1-7.|
|2011||Ritchie RO. The conflicts between strength and toughness. Nat Mater. November 2011;10(11):817-822.|
|2011||Wang L, Cheung JT-M, Pu F, Li D, Zhang M, Fan Y. Why do woodpeckers resist head impact injury: a biomechanical investigation. PLoS One. 2011;6(10):e26490.|
|2010||Bouxsein ML, Boyd SK, Christiansen BA, Guldberg RE, Jepsen KJ, Müller R. Guidelines for assessment of bone microstructure in rodents using micro-computed tomography. J Bone Miner Res. July 2010;25(7):1468-1486.|
|1987||Parfitt AM, Drezner MK, Glorieux FH, Kanis JA, Malluche H, Meunier PJ, Ott SM, Recker RR. Bone histomorphometry: standardization of nomenclature, symbols, and units: report of the ASBMR histomorphometry nomenclature committee. J Bone Miner Res. 1987;2(6):595-610.|
|2001||Wang RZ, Suo Z, Evans AG, Yao N, Aksay IA. Deformation mechanisms in nacre. J Mater Res. September 2001;16(9):2485-2493.|
|2006||Bembey AK, Oyen ML, Bushby AJ, Boyde A. Viscoelastic properties of bone as a function of hydration state determined by nanoindentation. Philos Mag. November 21–December 11, 2006;86(33-35):5691-5703.|
|1992||Oliver WC, Pharr GM. An improved technique for determining hardness and elastic modulus using load and displacement sensing indentation experiments. J Mater Res. 1992;7(6):1564-1583.|
|2006||Adharapurapu RR, Jiang F, Vecchio KS. Dynamic fracture of bovine bone. Mater Sci Eng C Mater Biol Appl. September 2006;26(8):1325-1332.|
|2006||Barthelat F, Li C-M, Comi C, Espinosa HD. Mechanical properties of nacre constituents and their impact on mechanical performance. J Mater Sci. 2006;21(8):1977-1986.|
|2015||Wegst UGK, Bai H, Saiz E, Tomsia AP, Ritchie RO. Bioinspired structural materials. Nat Mater. January 2015;14(1):23-36.|
|2008||Koester KJ, Ager JW III, Ritchie RO. The true toughness of human cortical bone measured with realistically short cracks. Nat Mater. August 2008;7(8):672-677.|
|1993||Odgaard A, Gundersen HJG. Quantification of connectivity in cancellous bone, with special emphasis on 3-D reconstructions. Bone. March–April 1993;14(2):173-182.|
|2012||Zhu ZD, Ma GJ, Wu CW, Chen Z. Numerical study of the impact response of woodpecker’s head. AIP Advances. 2012;2(4):042173.|
|1997||Rho J-Y, Tsui TY, Pharr GM. Elastic properties of human cortical and trabecular lamellar bone measured by nanoindentation. Biomaterials. 1997;18(20):1325-1330.|
|1998||Rho J-Y, Kuhn-Spearing L, Zioupos P. Mechanical properties and the hierarchical structure of bone. Med Eng Phys. 1998;20(2):92-102.|