Abstract
Millions of years of evolution have adapted spider silks to achieve a range of functions, including the well-known capture of prey, with efficient use of material. From a materials perspective, the exceptional mechanical properties of self-assembling silk biopolymers have been extensively explored, both experimentally and in computational investigations. Yet few studies account for the structural function of silk within the web itself. Recently, a series of investigations have been conducted to examine structure-function relationships across different length scales in silk, ranging from atomistic models of protein constituents to the spider web architecture. Here, through theoretical and computational models, we attempt to reconcile the unique mechanical behavior of spider silk (i.e., material) with the performance of the web itself (i.e., structure), and elucidate the intimate and synergistic relationship between the two – the ultimate merging of material and structure. Particularly, we review recent analyses that considered an entire web structure subject to load, as well as the critical anchorage that secures the web to its (uncertain) environment. Beyond assessment of simple performance, we derive the theoretical basis for the underlying mechanics (through quantized fracture mechanics and the theory of multiple peeling, respectively). As such, the results can be translated to engineered structures in general, beyond the particular case of spider silks and webs. Interestingly, in both cases (web fracture and anchorage failure), the extreme hyperelasticity – i.e. elastic stiffening under large extension – benefits structural performance, in contrast to typical engineering practice (wherein large deformation is typically avoided). The spider web is a highly adapted system where both material and hierarchical structure across all length-scales is critical for its functional properties.
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References
Agnarsson I, Blackledge TA (2009) Can a spider web be too sticky? Tensile mechanics constrains the evolution of capture spiral stickiness in orb-weaving spiders. J Zool 278(2):134–140
Agnarsson I et al (2009) Supercontraction forces in spider dragline silk depend on hydration rate. Zoology 112(5):325–331
Agnarsson I, Kuntner M, Blackledge TA (2010) Bioprospecting finds the toughest biological material: extraordinary silk from a giant riverine orb spider. PLoS One 5(9):e11234
Aizenberg J, Fratzl P (2009) Biological and biomimetic materials. Adv Mater 21(4):387–388
Aizenberg J et al (2005) Skeleton of Euplectella sp.: structural hierarchy from the nanoscale to the macroscale. Science 309(5732):275–278
Alam MS, Jenkins CH (2005) Damage tolerance in naturally compliant structures. Int J Damage Mech 14(4):365–384
Alam MS, Wahab MA, Jenkins CH (2007) Mechanics in naturally compliant structures. Mech Mater 39(2):145–160
Aoyanagi Y, Okumura K (2010) Simple model for the mechanics of spider webs. Phys Rev Lett 104(3):038102
Arzt E, Gorb S, Spolenak R (2003) From micro to nano contacts in biological attachment devices. Proc Natl Acad Sci USA 100(19):10603–10606
Autumn K et al (2000) Adhesive force of a single gecko foot-hair. Nature 405(6787):681–685
Blackledge TA et al (2009) Reconstructing web evolution and spider diversification in the molecular era. Proc Natl Acad Sci USA 106(13):5229–5234
Blamires SJ, Wu CL, Tso IM (2012) Variation in protein intake induces variation in spider silk expression. PLoS One 7(2):e31626
Blasingame E et al (2009) Pyriform Spidroin 1, a novel member of the silk gene family that anchors dragline silk fibers in attachment discs of the black widow spider, Latrodectus hesperus. J Biol Chem 284(42):29097–29108
Bosia F, Buehler MJ, Pugno NM (2010) Hierarchical simulations for the design of supertough nanofibers inspired by spider silk. Phys Rev E 82(5):056103
Boutry C, Blackledge TA (2009) Biomechanical variation of silk links spinning plasticity to spider web function. Zoology 112(6):451–460
Bratzel G, Buehler MJ (2012) Molecular mechanics of silk nanostructures under varied mechanical loading. Biopolymers 97(6):408–417
Brown CP et al (2012) Rough fibrils provide a toughening mechanism in biological fibers. ACS Nano 6(3):1961–1969
Buehler MJ (2010) Tu(r)ning weakness to strength. Nano Today 5(5):379–383
Buehler MJ, Yung YC (2009) Deformation and failure of protein materials in physiologically extreme conditions and disease. Nat Mater 8(3):175–188
Carpinteri A, Pugno N (2005) Fracture instability and limit strength condition in structures with re-entrant corners. Eng Fract Mech 72(8):1254–1267
Carpinteri A, Pugno NM (2008) Super-bridges suspended over carbon nanotube cables. J Phys Condens Matter 20(47):474213
Cetinkaya M et al (2011) Silk fiber mechanics from multiscale force distribution analysis. Biophys J 100(5):1298–1305
Craig CL (1987) The ecological and evolutionary interdependence between web architecture and web silk spun by orb web weaving spiders. Biol J Linn Soc 30(2):135–162
Craig CL et al (1999) A comparison of the composition of silk proteins produced by spiders and insects. Int J Biol Macromol 24(2–3):109–118
Cranford SW, Buehler MJ (2012) Biomateriomics, 1st edn. Springer, New York
Cranford SW et al (2012) Nonlinear material behaviour of spider silk yields robust webs. Nature 482(7383):72–76
Du N et al (2006) Design of superior spider silk: from nanostructure to mechanical properties. Biophys J 91(12):4528–4535
Elices M et al (2009) Mechanical behavior of silk during the evolution of orb-web spinning spiders. Biomacromolecules 10(7):1904–1910
Elices M et al (2011) The hidden link between supercontraction and mechanical behavior of spider silks. J Mech Behav Biomed Mater 4(5):658–669
Espinosa HD et al (2009) Merger of structure and material in nacre and bone – perspectives on de novo biomimetic materials. Prog Mater Sci 54(8):1059–1100
Federle W (2006) Why are so many adhesive pads hairy? J Exp Biol 209(14):2611–2621
Feig M, Karanicolas J, Brooks CL (2004) MMTSB tool set: enhanced sampling and multiscale modeling methods for applications in structural biology. J Mol Graph Model 22:377–395
Filippov A, Popov VL, Gorb SN (2011) Shear induced adhesion: contact mechanics of biological spatula-like attachment devices. J Theor Biol 276(1):126–131
Foelix RF (1996) Biology of spiders, 2nd edn. Oxford University Press/Georg Thieme Verlag, New York/Stuttgart, 330 p
Fratzl P (2007) Biomimetic materials research: what can we really learn from nature’s structural materials? J R Soc Interface 4(15):637–642
Fratzl P (2008) Collagen: structure and mechanics. Springer, New York
Fratzl P, Barth FG (2009) Biomaterial systems for mechanosensing and actuation. Nature 462(7272):442–448
Frische S, Maunsbach AB, Vollrath F (1998) Elongate cavities and skin-core structure in Nephila spider silk observed by electron microscopy. J Microsc 189:64–70
Gao HJ, Yao HM (2004) Shape insensitive optimal adhesion of nanoscale fibrillar structures. Proc Natl Acad Sci USA 101(21):7851–7856
Gao H et al (2003) Materials become insensitive to flaws at nanoscale: lessons from nature. Proc Natl Acad Sci USA 100(10):5597–5600
Gay C, Leibler L (1999) Theory of tackiness. Phys Rev Lett 82(5):936–939
Geurts P et al (2010) Synthetic spider silk fibers spun from Pyriform Spidroin 2, a glue silk protein discovered in orb-weaving spider attachment discs. Biomacromolecules 11(12):3495–3503
Giesa T et al (2011) Nanoconfinement of spider silk fibrils begets superior strength, extensibility, and toughness. Nano Lett 11(11):5038–5046
Gosline JM, Demont ME, Denny MW (1986) The structure and properties of spider silk. Endeavour 10(1):37–43
Gosline JM et al (1999) The mechanical design of spider silks: from fibroin sequence to mechanical function. J Exp Biol 202(23):3295–3303
Guinea GV et al (2003) Self-tightening of spider silk fibers induced by moisture. Polymer 44(19):5785–5788
Hansell MH (2005) Animinal architecture, 1st edn. Oxford University Press, New York
Heim M, Romer L, Scheibel T (2010) Hierarchical structures made of proteins. The complex architecture of spider webs and their constituent silk proteins. Chem Soc Rev 39(1):156–164
Holland GP et al (2008) Determining secondary structure in spider dragline silk by carbon-carbon correlation solid-state NMR spectroscopy. J Am Chem Soc 130:9871–9877
Jelinski LW (1998) Establishing the relationship between structure and molecular function in silks. Curr Opin Solid State Mater Sci 3:237–245
Jenkins JE et al (2010) Quantitative correlation between the protein primary sequences and secondary structures in spider dragline silks. Biomacromolecules 11(1):192–200
Kamat S et al (2000) Structural basis for the fracture toughness of the shell of the conch Strombus gigas. Nature 405(6790):1036–1040
Kendall K (1975) Thin-film peeling – elastic term. J Phys D: Appl Phys 8(13):1449–1452
Keten S, Buehler MJ (2010a) Nanostructure and molecular mechanics of spider dragline silk protein assemblies. J R Soc Interface 7(53):1709–1721
Keten S, Buehler MJ (2010b) Atomistic model of the spider silk nanostructure. Appl Phys Lett 96(15):153701
Keten S et al (2010) Nanoconfinement controls stiffness, strength and mechanical toughness of beta-sheet crystals in silk. Nat Mater 9(4):359–367
Knippers J, Speck T (2012) Design and construction principles in nature and architecture. Bioinspir Biomim 7(1):015002
Ko FK, Jovicic J (2004) Modeling of mechanical properties and structural design of spider web. Biomacromolecules 5(3):780–785
Ko KK et al (2002) Engineering properties of spider silk. Adv Fiber Plast Laminate Compos 702:17–23
Kohler T, Vollrath F (1995) Thread biomechanics in the 2 orb-weaving spiders Araneus-diadematus (Araneae, Araneidae) and Uloborus-walckenaerius (Araneae, Uloboridae). J Exp Zool 271(1):1–17
Kummerlen J et al (1996) Local structure in spider dragline silk investigated by two-dimensional spin-diffusion nuclear magnetic resonance. Macromolecules 29:2920
Lazaris A et al (2002) Spider silk fibers spun from soluble recombinant silk produced in mammalian cells. Science 295(5554):472–476
Lefevre T, Rousseau ME, Pezolet M (2007) Protein secondary structure and orientation in silk as revealed by Raman spectromicroscopy. Biophys J 92(8):2885–2895
Lewis RV (2006) Spider silk: ancient ideas for new biomaterials. Chem Rev 106(9):3762–3774
Li SFY, Mcghie AJ, Tang SL (1994) New internal structure of spider dragline silk revealed by atomic-force microscopy. Biophys J 66(4):1209–1212
Lin LH, Sobek W (1998) Structural hierarchy in spider webs and spiderweb-type system. Struct Eng 76(4):59–64
Liu Y, Shao ZZ, Vollrath F (2005) Relationships between supercontraction and mechanical properties of spider silk. Nat Mater 4(12):901–905
Ma B, Nussinov R (2002) Molecular dynamics simulations of alanine rich beta-sheet oligomers: insight into amyloid formation. Protein Sci 11(10):2335–2350
Nova A et al (2010) Molecular and nanostructural mechanisms of deformation, strength and toughness of spider silk fibrils. Nano Lett 10(7):2626–2634
O’Brien JP et al (1998) Nylons from nature: synthetic analogs to spider silk. Adv Mater 10(15):1185
Omenetto FG, Kaplan DL (2010) New opportunities for an ancient material. Science 329(5991):528–531
Opell BD (1998) Economics of spider orb-webs: the benefits of producing adhesive capture thread and of recycling silk. Funct Ecol 12(4):613–624
Opell BD, Bond JE (2001) Changes in the mechanical properties of capture threads and the evolution of modern orb-weaving spiders. Evol Ecol Res 3(5):567–581
Papadopoulos P, Solter J, Kremer F (2009) Hierarchies in the structural organization of spider silk-a quantitative model. Colloid Polym Sci 287(2):231–236
Porter D, Vollrath F (2007) Nanoscale toughness of spider silk. Nano Today 2(3):6
Porter D, Vollrath F (2009) Silk as a biomimetic ideal for structural polymers. Adv Mater 21(4):487–492
Porter D, Vollrath F, Shao Z (2005) Predicting the mechanical properties of spider silk as a model nanostructured polymer. Eur Phys J E Soft Matter 16(2):199–206
Poulin S, Larsen A (2007) Drag loading of circular cylinders inclined in the along-wind direction. J Wind Eng Ind Aerodyn 95(9–11):1350–1363
Poza P et al (2002) Fractographic analysis of silkworm and spider silk. Eng Fract Mech 69(9):1035–1048
Pugno NM (2007) Towards a Spiderman suit: large invisible cables and self-cleaning releasable superadhesive materials. J Phys Condens Matter 19(39):395001
Pugno N (2011) The theory of multiple peeling. Int J Fract 171(2):185–193
Pugno NM, Lepore E (2008) Observation of optimal gecko’s adhesion on nanorough surfaces. Biosystems 94(3):218–222
Pugno N et al (2008) Atomistic fracture: QFM vs. MD. Eng Fract Mech 75(7):1794–1803
Pugno N, Cranford SW, Buehler MJ (2013) Synergetic material and structure optimization yields robust spider web anchorages. Small. doi:10.1002/smll.201201343
Rammensee S et al (2008) Assembly mechanism of recombinant spider silk proteins. Proc Natl Acad Sci USA 105(18):6590–6595
Rice JR, Rosengre GF (1968) Plane strain deformation near a crack tip in a power-law hardening material. J Mech Phys Solid 16(1):1
Sahni V et al (2012) Cobweb-weaving spiders produce different attachment discs for locomotion and prey capture. Nat Commun 3(1106):1–7
Sen D, Buehler MJ (2011) Structural hierarchies define toughness and defect-tolerance despite simple and mechanically inferior brittle building blocks. Sci Rep 1(1):35
Sensenig A, Agnarsson I, Blackledge TA (2010) Behavioural and biomaterial coevolution in spider orb webs. J Evol Biol 23(9):1839–1856
Shao ZZ, Vollrath F (1999) The effect of solvents on the contraction and mechanical properties of spider silk. Polymer 40(7):1799–1806
Shao ZZ, Vollrath F (2002) Materials: surprising strength of silkworm silk. Nature 418(6899):741
Spivak D et al (2011) Category theoretic analysis of hierarchical protein materials and social networks. PLoS ONE 6. http://dx.plos.org/10.1371/journal.pone.0023911
Sugita Y, Okamoto Y (1999) Replica exchange molecular dynamics method for protein folding. Chem Phys Lett 314:141–151
Swanson BO et al (2006) Variation in the material properties of spider dragline silk across species. Appl Phys A Mater Sci Process 82(2):213–218
Swanson BO, Blackledge TA, Hayashi CY (2007) Spider capture silk: performance implications of variation in an exceptional biomaterial. J Exp Zool A Ecol Genet Physiol 307A(11):654–666
Swanson BO et al (2009) The evolution of complex biomaterial performance: the case of spider silk. Integr Comp Biol 49(1):21–31
Tang ZY et al (2003) Nanostructured artificial nacre. Nat Mater 2(6):413–418
Tarakanova A, Buehler MJ (2012a) A materiomics approach to spider silk: protein molecules to webs. JOM 64(2):214–225
Tarakanova A, Buehler MJ (2012b) The role of capture spiral silk properties in the diversification of orb webs. J R Soc Interface 9(77):3240–3248
Termonia Y (1994) Molecular modeling of spider silk elasticity. Macromolecules 27(25):7378–7381
Tian Y et al (2006) Adhesion and friction in gecko toe attachment and detachment. Proc Natl Acad Sci USA 103(51):19320–19325
van Beek JD et al (2002) The molecular structure of spider dragline silk: folding and orientation of the protein backbone. Proc Natl Acad Sci USA 99(16):10266–10271
Varenberg M, Pugno NM, Gorb SN (2010) Spatulate structures in biological fibrillar adhesion. Soft Matter 6(14):3269–3272
Vepari C, Kaplan DL (2007) Silk as a biomaterial. Prog Polym Sci 32(8–9):991–1007
Vincent JFV (2001) Stealing ideas from nature. In: Deployable structures. Springer, Vienna, pp 51–58
Vollrath F (1992) Spider webs and silks. Sci Am 266(3):70–76
Vollrath F (1999) Biology of spider silk. Int J Biol Macromol 24:81–88
Vollrath F (2000) Strength and structure of spiders’ silks. Rev Mol Biotechnol 74:67–83
Vollrath F (2010) Spider silk: evolution and 400 million years of spinning, waiting, snagging, and mating. Nature 466(7304):319
Vollrath F, Knight DP (2001) Liquid crystalline spinning of spider silk. Nature 410(6828):541–548
Vollrath F, Mohren W (1985) Spiral geometry in the garden spider’s orb web. Naturwissenschaften 72(12):666–667
Vollrath F, Porter D (2006) Spider silk as archetypal protein elastomer. Soft Matter 2(5):377–385
Vollrath F, Porter D (2009) Silks as ancient models for modern polymers. Polymer 50(24):5623–5632
Vollrath F, Selden P (2007) The role of behavior in the evolution of spiders, silks, and webs. Annu Rev Ecol Evol Syst 38:819–846
Vollrath F et al (1996) Structural organization of spider silk. Proc R Soc Lond B Biol Sci 263(1367):147–151
Vollrath F, Porter D, Holland C (2011) There are many more lessons still to be learned from spider silks. Soft Matter 7(20):9595–9600
Zschokke S, Vollrath F (1995) Web construction patterns in a range of orb-weaving spiders (Araneae). Eur J Entomol 92(3):523–541
Acknowledgements
NMP is supported by the European Research Council under the European Union’s Seventh Framework Programme (FP7/2007-2013)/ERC Grant agreement n° 279985 (Ideas Starting Grant BIHSNAM, 2012–2016). NMP and MJB acknowledge the support from the MIT-Italy program MITOR. MJB and SWC acknowledge support from a NSF-MRSEC grant with additional support from ONR, AFOSR and ARO. SWC acknowledges additional support from Northeastern University, Department of Civil and Environmental Engineering.
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Cranford, S.W., Pugno, N.M., Buehler, M.J. (2014). Silk and Web Synergy: The Merging of Material and Structural Performance. In: Asakura, T., Miller, T. (eds) Biotechnology of Silk. Biologically-Inspired Systems, vol 5. Springer, Dordrecht. https://doi.org/10.1007/978-94-007-7119-2_12
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