This article reviews the main mechanisms of stiffness variation typically found in nature. The temporal changes in stiffness may be fully or partially reversible, or completely irreversible, and can be very slow or fast in time depending on the strategy adopted to alter the mechanical properties. It is also possible to observe changes in the stiffness in order to recover the original mechanical properties in damaged natural materials by means of self-healing mechanisms. In addition to stiffness variations in time, natural materials can also exhibit stiffness changes in space. These variations can be represented by alterations in the spatial distribution of the microscopic constituents across multiple hierarchical scales, from very small physical scales to large macroscopic dimensions. In order to optimise the strength and multifunctionality of these materials, spatial changes can also occur over larger areas at one single scale. In addition, several examples are provided to illustrate how natural materials have been exploited further in order to develop new bio-inspired materials.
AldredN (2007) Tensile and dynamic mechanical analysis of the distal portion of mussel (Mytilus edulis) byssal threads. Journal of the Royal Society Interface4: 1159–1167.
2.
BaiM-YMoranCZhangL. (2012) A facile and general method for the encapsulation of different types of imaging contrast agents within micrometer-sized polymer beads. Advanced Functional Materials22(4): 764–770.
3.
BarbarinoSBilgenOAjajRM. (2011) A review of morphing aircraft. Journal of Intelligent Material Systems and Structures22(9): 823–877.
4.
BarthelatF (2010) Nacre from mollusk shells: a model for high-performance structural materials. Bioinspiration & Biomimetics5(3): 035001.
5.
BarthelatFRabieiR (2011) Toughness amplification in natural composites. Journal of the Mechanics and Physics of Solids59(4): 829–840.
6.
BenjaminMKumaiTMilzS. (2002) The skeletal attachment of tendons–tendon ‘entheses’. Comparative Biochemistry and Physiology A: Molecular & Integrative Physiology133(4): 931–945.
7.
BleaySLoaderCHawyesV. (2001) A smart repair system for polymer matrix composites. Composites Part A: Applied Science and Manufacturing32(12): 1767–1776.
8.
BondererLJStudartARGaucklerLJ (2008) Bioinspired design and assembly of platelet reinforced polymer films. Science319(5866): 1069–1073.
9.
BroedlingNCHartmaierABuehlerMJ. (2008) The strength limit in a bio-inspired metallic nanocomposite. Journal of the Mechanics and Physics of Solids56: 1086–1104.
10.
BuehlerMJ (2010a) Multiscale mechanics of biological and biologically inspired materials and structures. Acta Mechanica Solida Sinica23(6): 471–483.
11.
BuehlerMJ (2010b) Tu(r)ning weakness to strength. Nano Today5: 379–383.
12.
BurgertIFratzlP (2009) Actuation systems in plants as prototypes for bioinspired devices. Philosophical Transactions of the Royal Society A: Mathematical Physical and Engineering Sciences367(1893): 1541–1557.
13.
CapadonaJShanmuganathanKTylerD. (2008) Stimuli-responsive polymer nanocomposites inspired by the sea cucumber dermis. Science319: 1370–1374.
14.
CaveID (1978) Modelling moisture-related mechanical properties of wood, part I: properties of the wood constituents. Wood Science and Technology12(1): 75–86.
15.
ChenXDamMOnoK. (2002) A thermally re-mendable cross-linked polymeric material. Science295(5560): 1698–1702.
16.
CousinWJ (1976) Elastic modulus of lignin as related to moisture content. Wood Science and Technology10(1): 9–17.
17.
CousinWJ (1978) Young’s modulus of hemicellulose as related to moisture content. Wood Science and Technology12(3): 161–167.
18.
DehouxTTsapisNAudoinB (2012) Relaxation dynamics in single polymer microcapsules probed with laser-generated GHz acoustic waves. Soft Matter8(9): 2586–2589.
19.
DryC (1996) Procedures developed for self-repair of polymer matrix composite materials. Composite Structures35(3): 263–269.
20.
DumontER (2010) Bone density and the lightweight skeletons of birds. Proceedings of the Royal Society B: Biological Sciences277(1691): 2193–2198.
21.
DunlopJWCWeinkamerRFratzlP (2011) Artful interfaces within biological materials. Materials Today14(3): 70–78.
22.
ElicesMPlazaGRPérez-RigueiroJ. (2011) The hidden link between supercontraction and mechanical behavior of spider silks. Journal of the Mechanical Behavior of Biomedical Materials4(5): 658–669.
23.
EspinosaHDRimJEBarthelatF. (2009) Merger of structure and material in nacre and bone – perspectives on de novo biomimetic materials. Progress in Materials Science54(8): 1059–1100.
24.
FantnerGEHassenkamTKindtJH. (2005) Sacrificial bonds and hidden length dissipate energy as mineralized fibrils separate during bone fracture. Nature Materials4(8): 612–616.
25.
FantnerGERabinovychOSchitterG. (2006) Hierarchical interconnections in the nanocomposite material bone: fibrillar cross-links resist fracture on several length scales. Composites Science and Technology66(9): 1205–1211.
26.
FratzlP (2003) Cellulose and collagen: from fibres to tissues. Current Opinion in Colloid & Interface Science8(1): 32–39.
27.
FratzlPBarthFG (2009) Biomaterial systems for mechanosensing and actuation. Nature462: 442–448.
28.
FratzlPWeinkamerR (2007) Nature’s hierarchical materials. Progress in Materials Science52(8): 1263–1334.
29.
GaoHJ (2006) Application of fracture mechanics concepts to hierarchical biomechanics of bone and bone-like materials. International Journal of Fracture138: 101–137.
30.
GautieriAVesentiniSRedaelliA. (2011) Hierarchical structure and nanomechanics of collagen microfibrils from the atomistic scale up. Nano Letters11: 757–766.
31.
GriffinC (2007) Pressure deflection behaviour of candidate materials for a morphing wing. Master’s Thesis, Department of Mechanical and Aerospace Engineering, West Virginia University, USA.
32.
GuptaNS (ed.) (2011) Chitin: Formation and Diagenesis (Topics in Geobiology). Springer, New York.
33.
GuptaSZhangQEmrickT. (2006) Entropy-driven segregation of nanoparticles to cracks in multilayered composite polymer structures. Nature Materials5(3): 229–233.
34.
HartJW (ed.) (1990) Plant Tropisms and Other Growth Movements. Chapman & Hall, Great Britain.
35.
HavensESnyderEATongTH (2005) Light-activated shape memory polymers and associated applications. Proceedings of SPIE5762: 48.
36.
HessACapadonaJShanmuganathanK. (2011) Development of a stimuli-responsive polymer nanocomposite toward biologically-optimized MEMS-based neural probes. Journal of Micromechanics and Microengineering21: 054009.
37.
HoSPKuryloMPFongT. (2010) The biomechanical characteristics of the bone-periodontal ligament–cementum complex. Biomaterials31(25): 6635–6646.
38.
HofstetterKHellmichCEberhardsteinerJ (2005) Development and experimental validation of a continuum micromechanics model for the elasticity of wood. European Journal of Mechanics A: Solids24(6): 1030–1053.
39.
HolzapfelG (2000) Computational biomechanics of soft biological tissue. In: SteinEDe BorstRHughesT (eds) Encyclopedia of Computational Mechanics, Solids and Structures, vol. 2. Chichester: Wiley, pp. 605–635.
40.
HookeR (1665) Micrographia: or, Some Physiological Descriptions of Minute Bodies Made by Magnifying Glasses. London: J. Martyn and J. Allestry.
InagakiMUrashimaKToyomasuS. (1985) Work of fracture and crack healing in glass. Journal of the American Ceramic Society68(12): 704–706.
43.
ISO11357-2 (1999) ISO 11357-2: plastics – differential scanning calorimetry (DSC) – part 2: determination of glass transition temperature.
44.
JacksonAPVincentJFVTurnerRM (1988) The mechanical design of nacre. Proceedings of the Royal Society B: Biological Sciences234: 415–440.
45.
JudKKauschHHWilliamsJG (1982) Fracture-mechanics studies of crack healing and welding of polymers. Journal of Materials Science16(1): 204–210.
46.
KalfasI (2001) Principles of bone healing. Neurosurgical Focus10(4): 1–4.
47.
KeckésJBurgertIFrühmannK. (2003) Cell-wall recovery after irreversible deformation of wood. Nature Materials2: 811–814.
48.
KetenSBuehlerMJ (2010) Nanostructure and molecular mechanics of dragline spider silk protein assemblies. Journal of the Royal Society Interface7(53): 1709–1721.
49.
KimKTadokoroS (2007) Electroactive Polymers for Robotic Applications: Artificial Muscles and Sensors. Springer, London.
50.
KulawardanaE (2010) Stimuli-responsive polymers. PhD Thesis, Bowling Green State University, USA.
51.
KumpferJRRowanSJ (2011) Thermo-, photo-, and chemo-responsive shape-memory properties from photo-cross-linked metallo-supramolecular polymers. Journal of the American Chemical Society133(32): 12866–12874.
52.
LakesR (1993) Materials with structural hierarchy. Nature361(6412): 511–515.
53.
LauneyMEBuehlerMJRitchieRO (2010) On the mechanistic origins of toughness in bone. Annual Review of Materials Research40: 25–53.
54.
LawnBRLeeJJ-WChaiH (2010) Teeth: among nature’s most durable biocomposites. Annual Review of Materials Research40(1): 55–75.
55.
LeeJYBuxtonGABalazsAC (2004) Using nanoparticles to create self-healing composites. Journal of Chemical Physics121(11): 5531–5540.
LeondesC (2003) Computational Methods in Biophysics, Biomaterials, Biotechnology and Medical Systems: Algorithm Development, Mathematical Analysis, and Diagnostics. Kluwer Academic Publishers, The Netherlands.
LiXChangWChaoYJ. (2004) Nanoscale structural and mechanical characterization of a natural nanocomposite material: the shell of red abalone. Nano Letters4(4): 613–617.
60.
LuzGMManoJF (2009) Biomimetic design of materials and biomaterials inspired by the structure of nacre. Philosophical Transactions of the Royal Society A. Mathematical, Physical & Engineering Sciences367: 1587–1605.
61.
McGrathKKaplanD (1996) Protein-Based Materials (Bioengineering of Materials). Birkhäuser Boston, United States.
62.
MagalhãesDaCosta AleixoPM (2007) Morphing aircraft structures. Design and testing an experimental UAV. Master’s Thesis, Instituto Superior Técnico, Universidad Técnica de Lisboa, Portugal.
63.
MarkJErmanB (2005) Science and Technology of Rubber. 3rd ed.Elsevier Science & Technology. Elsevier Academic Press, United States.
64.
MartinR (1984) Porosity and specific surface of bone. Critical Reviews in Biomedical Engineering10(3): 179–222.
MeyersMAChenPLinAY. (2008) Biological materials: structure and mechanical properties. Progress in Materials Science53(1): 1–206.
67.
Minary-JolandanMYuM-F (2009) Nanomechanical heterogeneity in the gap and overlap regions of type I collagen fibrils with implications for bone heterogeneity. Biomacromolecules10(9): 2565–2570.
68.
MollicaFPreziosiLRajagopalKR (2007) Modelling of Biological Materials (Modeling and Simulation in Science, Engineering and Technology). Birkhäuser Boston, United States.
69.
MotukuMVaidyaUJanowskiG (1999) Parametric studies on self-repairing approaches for resin infused composites subjected to low velocity impact. Smart Materials and Structures8(5): 623–638.
NallaRKKinneyJHRitchieRO (2003) Mechanistic fracture criteria for the failure of human cortical bone. Nature Materials2(3): 164–168.
72.
NeimanVJVargheseS (2011) Synthetic bio-actuators and their applications in biomedicine. Smart Structures and Systems7(3): 185–198.
73.
PangJBondI (2005a) ‘Bleeding composites’– damage detection and self-repair using a biomimetic approach. Composites Part A: Applied Science and Manufacturing36(2 special issue): 183–188.
74.
PangJBondI (2005b) A hollow fibre reinforced polymer composite encompassing self-healing and enhanced damage visibility. Composites Science and Technology65: 1791–1799.
75.
PelegM (1994) A model of mechanical changes in biomaterials at and around their glass transition. Biotechnology Progress10(4): 385–388.
76.
PlazaGRGuineaGVPérez-RigueiroJ. (2006) Thermo-hygromechanical behavior of spider dragline silk: glassy and rubbery states. Journal of Polymer Science44: 994–999.
77.
RaghavanJWoolR (1999) Interfaces in repair, recycling, joining and manufacturing of polymers and polymer composites. Journal of Applied Polymer Science71(5): 775–785.
78.
RheeHHorstemeyerMHwangY. (2009) A study on the structure and mechanical behavior of the Terrapene carolina carapace: a pathway to design bio-inspired synthetic composites. Materials Science and Engineering: C29(8): 2333–2339.
79.
RüggebergMSpeckTParisO. (2008) Stiffness gradients in vascular bundles of the palmWashingtonia robusta. Proceedings of the Royal Society B: Biological Sciences275(1648): 2221–2229.
80.
RusliRShanmuganathanKRowanS. (2010) Stress-transfer in anisotropic and environmentally adaptive cellulose whisker nanocomposites. Biomacromolecules11: 762–768.
81.
Saavedra FloresEIFriswellMI (2012) Multi-scale finite element model for a new material inspired by the mechanics and structure of wood cell-walls. Journal of the Mechanics and Physics of Solids60(7): 1296–1309.
SinkjaerTToftEAndreassenS. (1988) Muscle stiffness in human ankle dorsiflexors: intrinsic and reflex components. Journal of Neurophysiology60(3): 1110–1121.
90.
SladeLLevineH (1991) Recent advances based on alternative approach to the assessment of food quality and safety. Critical Reviews in Food Science and Nutrition30(2–3): 115–360.
91.
SmithBLSchafferTEVianiM. (1999) Molecular mechanistic origin of the toughness of natural adhesives, fibres and composites. Nature399(6738): 761–763.
92.
SpeirsDCDDe Souza NetoEAPerićD (2008) An approach to the mechanical constitutive modelling of arterial tissue based on homogenization and optimization. Journal of Biomechanics41: 2673–2680.
93.
Stanzl-TscheggSE (2011) Wood as a bioinspiring material. Materials Science and Engineering C31: 1174–1183.
94.
StavrinidisBHollowayDG (1983) Crack healing in glass. Physics and Chemistry of Glasses24(1): 19–25.
95.
TaiKDaoMSureshS. (2007) Nanoscale heterogeneity promotes energy dissipation in bone. Nature Materials6: 454–462.
96.
TakagiSKamitsuboENagaiR (1991) Light-induced changes in the behavior of chloroplasts under centrifugation in vallisneria epidermal cells. Journal of Plant Physiology138(3): 257–262.
97.
TeschWEidelmanNRoschgerP. (2001) Graded microstructure and mechanical properties of human crown dentin. Calcified Tissue International69(3): 147–157.
98.
ThompsonDW (1968) On Growth and Form. 2nd ed.Cambridge University PressUnited Kingdom.
99.
ThompsonJBKindtJHDrakeB. (2001) Bone indentation recovery time correlates with bond reforming time. Nature414(6865): 773–776.
TraskRSBondIP (2010) Bioinspired engineering study of Plantae vascules for self-healing composite structures. Journal of the Royal Society Interface7(47): 921–931.
102.
TuncaboyluDCSariMOppermannW. (2011) Tough and self-healing hydrogels formed via hydrophobic interactions. Macromolecules44: 4997–5005.
103.
Van DoornWGVan MeeterenU (2003) Flower opening and closure: a review. Journal of Experimental Botany54(389): 1801–1812.
104.
VasileCZaikovGE (eds) (2006) New Trends in Natural and Synthetic Polymer Science. Nova Science Publishers, Inc.New York.
105.
WangJChengQTangZ (2011) Layered nanocomposites inspired by the structure and mechanical properties of nacre. Chemical Society Reviews41: 1111–1129.
106.
WangPPLeeSHarmonJP (2003) Ethanol-induced crack healing in poly(methyl methacrylate). Journal of Polymer Science Part B: Polymer Physics32(7): 1217–1227.
107.
WangRHuHLiuW. (2012) The effect of synthesis condition on physical properties of epoxy-containing microcapsules. Journal of Applied Polymer Science124(3): 1866–1879.
108.
WareTHearonKLonneckerA. (2012) Triple-shape memory polymers based on self-complementary hydrogen bonding. Macromolecules45(2): 1062–1069.
109.
WeinkamerRFratzlP (2011) Mechanical adaptation of biological materials the examples of bone and wood. Materials Science and Engineering: C31(6): 1164–1173.
110.
WhiteSRSottosNRGeubellePH. (2001) Autonomic healing of polymer composites. Nature409(6822): 794–797.
111.
WilliamsHTraskRWeaverP. (2008) Minimum mass vascular networks in multifunctional materials. Journal of the Royal Society Interface5(18): 55–65.
112.
WoolRPO’ConnerKM (1982) A theory of crack healing in polymers. Journal of Applied Physics52: 5953–5963.
113.
YangYChenXShaoZ. (2005) Toughness of spider silk at high and low temperatures. Advanced Materials17(1): 84–88.
114.
YaoHGaoH (2007) Multi-scale cohesive laws in hierarchical materials. International Journal of Solids and Structures44(25–26): 8177–8193.
115.
YeniYNFyhrieDP (2001) Collagen-bridged microcrack model for cortical bone tensile strength. In (June27-July1, 2001): Proceedings of the 2001 summer bioengineering conference, vol. 50, American Society of Mechanical Engineers, New York, pp. 293–294.
116.
ZakoMTakanoN (1999) Intelligent material systems using epoxy particles to repair microcracks and delamination damage in GFRP. Journal of Intelligent Material Systems and Structures10(10): 836–841.
117.
ZaslanskyPFriesemAAWeinerS (2006) Structure and mechanical properties of the soft zone separating bulk dentin and enamel in crowns of human teeth: insight into tooth function. Journal of Structural Biology153(2): 188–199.
118.
ZhangZZhangYWGaoH (2010) On optimal hierarchy of load-bearing biological materials. Proceedings of the Royal Society B: Biological Sciences278(1705): 519–525.
119.
ZwaagS (ed.) (2007) Self Healing Materials: An Alternative Approach to 20 Centuries of Materials Science (Series in Materials Science). Springer, The Netherlands.
