journal article·2013-03

Non-invasive determination of the complete elastic moduli of spider silks

Kristie J. Koski, Paul Akhenblit, Keri McKiernan, Jeffery L. Yarger

Nature Materials· Volume 12· Issue 3
Publisher page

Abstract

Spider silks possess nature's most exceptional mechanical properties, with unrivalled extensibility and high tensile strength. Unfortunately, our understanding of silks is limited because the complete elastic response has never been measured-leaving a stark lack of essential fundamental information. Using non-invasive, non-destructive Brillouin light scattering, we obtain the entire stiffness tensors (revealing negative Poisson's ratios), refractive indices, and longitudinal and transverse sound velocities for major and minor ampullate spider silks: Argiope aurantia, Latrodectus hesperus, Nephila clavipes, Peucetia viridans. These results completely quantify the linear elastic response for all possible deformation modes, information unobtainable with traditional stress-strain tests. For completeness, we apply the principles of Brillouin imaging to spatially map the elastic stiffnesses on a spider web without deforming or disrupting the web in a non-invasive, non-contact measurement, finding variation among discrete fibres, junctions and glue spots. Finally, we provide the stiffness changes that occur with supercontraction.
Source: europepmc · Quality: candidate unverified · Source record ↗

Research context

OpenAlex topics: Silk-based biomaterials and applications · Neurobiology and Insect Physiology Research · Insect and Arachnid Ecology and Behavior

SciVX discovery tags are terminology-based. OpenAlex topics are source-provided classifications.

References (50)

Show source-provided references
1. Cranford, S. W., Tarakanova, A., Pugno, N. M. & Buehler, M. J. Nonlinear material behavior of spider silk yields robust webs. Nature 482, 72–76 (2012).10.1038/nature10739 ↗
2. Keten, S., Xu, Z., Ihle, B. & Buehler, M. J. Nanoconfinement controls stiffness, strength and mechanical toughness of β-sheet crystals in silk. Nature Mater. 9, 359–367 (2010).10.1038/nmat2704 ↗
3. Vollrath, F. Silk evolution untangled. Nature 466, 319 (2010).10.1038/466319a ↗
4. Vollrath, F. Spider webs and silks. Sci. Am. 266, 70–76 (1992).10.1038/scientificamerican0392-70 ↗
5. Work, R. W. Viscoelastic behaviour and wet supercontraction of major ampullate silk fibres of certain orb-web-building spiders (Araneae). J. Exp. Biol. 118, 379–404 (1985).10.1242/jeb.118.1.379 ↗
6. Blackledge, T. A., Swindeman, J. E. & Hayashi, C. Y. Quasistatic and continuous dynamic characterization of the mechanical properties of silk from the cobweb of the black widow spider Latrodectus hesperus. J. Exp. Biol. 208, 1937–1949 (2005).10.1242/jeb.01597 ↗
7. Gosline, J. M., Guerette, P. A., Ortlepp, C. S. & Savage, K. N. The mechanical design of spider silks: from fibroin sequence to mechanical function. J. Exp. Biol. 202, 3295–3303 (1999).10.1242/jeb.202.23.3295 ↗
8. Blackledge, T. A., Cardullo, R. A. & Hayashi, C. Y. Polarized light microscopy, variability in spider silk diameters, and the mechanical characterization of spider silk. Invertebr. Biol. 124, 165–173 (2005).10.1111/j.1744-7410.2005.00016.x ↗
9. Liu, Y., Shao, Z. & Vollrath, F. Relationships between supercontraction and mechanical properties of spider silk. Nature Mater. 4, 901–905 (2005).10.1038/nmat1534 ↗
10. Emile, O., Le Floch, A. & Vollrath, F. Biopolymers: Shape memory in spider draglines. Nature 440, 621 (2006).10.1038/440621a ↗
11. Eisoldt, L., Smith, A. & Scheibel, T. Decoding the secrets of spider silk. Mater. Today 14, 80–86 (March, 2011).10.1016/S1369-7021(11)70057-8 ↗
12. Omenetto, F. G. & Kaplan, D. L. New opportunities for an ancient material. Science 329, 528–531 (2010).10.1126/science.1188936 ↗
13. Speziale, S. et al. Sound velocity and elasticity of tetragonal lysozyme crystals by Brillouin spectroscopy. Biophys. J. 85, 3202–3213 (2003).10.1016/S0006-3495(03)74738-9 ↗
14. Randall, S. J. & Vaughan, J. M. Brillouin scattering in systems of biological significance [and discussion]. Phil. Trans. R. Soc. Lond. A 293, 341–348 (1979).10.1098/rsta.1979.0101 ↗
15. Cusack, S. & Miller, A. Determination of the elastic constants of collagen by Brillouin light scattering. J. Mol. Biol. 135, 39–51 (1979).10.1016/0022-2836(79)90339-5 ↗
16. Harley, R., James, D., Miller, A. & White, J. W. Phonons and the elastic moduli of collagen and muscle. Nature 267, 285–287 (1977).10.1038/267285a0 ↗
17. Berovic, N., Thomas, N., Thornhill, R. A. & Vaughan, J. M. Observation of Brillouin scattering from single muscle fibres. Eur. Biophys. J. 17, 69–74 (1989).10.1007/BF00257104 ↗
18. Koski, K. J. & Yarger, J. L. Brillouin imaging. Appl. Phys. Lett. 87, 061903 (2005).10.1063/1.1999857 ↗
19. Arecchi, F. T. et al. Laser Handbook (North-Holland, 1972).
20. Saravanan, D. Spider silk—structure, properties and spinning. J. Text. Apparel Technol. Manage. 5, 1–20 (2006).
21. Work, R. W. Dimensions, birefringences, and force-elongation behavior of major and minor ampullate silk fibers from orb-web-spinning spiders—the effects of wetting on these properties. Tex. Res. J. 47, 650–662 (1977).10.1177/004051757704701003 ↗
22. Zemlin, J. C. Technical Report 69-29-CM: A Study of the Mechanical Behavior of Spider Silks (Collaborative Research, 1968).
23. Vincent, J. F. V. Structural Materials 1–378 (Macmillan, 1982).
24. Fossey, S. A. & Kaplan, D. L. in Polymer Data Handbook (ed. Mark, J. E.) (Oxford Univ. Press, 1999).
25. Little, D. J. & Kane, D. M. Hybrid immersion-polarization method for measuring birefringence applied to spider silks. Opt. Lett. 36, 4098–4100 (2011).10.1364/OL.36.004098 ↗
26. Ko, F. K. & Jovicic, J. Modeling of mechanical properties and structural design of spider web. Biomacromolecules 5, 780–785 (2004).10.1021/bm0345099 ↗
27. Boutry, C., Rezac, M. & Blackledge, T. A. Plasticity in major ampullate silk production in relation to spider phylogeny and ecology. PLOS ONE 6, e22467 (2011).10.1371/journal.pone.0022467 ↗
28. Heim, M., Keerl, D. & Scheibel, T. Spider silk: From soluble protein to extraordinary fiber. Angew. Chem. Int. Ed. 48, 3584–3596 (2009).10.1002/anie.200803341 ↗
29. Moore, A. M. F. & Tran, K. Material properties of cobweb silk from the black widow spider Latrodectus hesperus. Int. J. Biol. Macromol. 24, 277–282 (1999).10.1016/S0141-8130(98)00090-7 ↗
30. Nova, A., Keten, S., Pugno, N. M., Redaelli, A. & Buehler, M. J. Molecular and nanostructural mechanisms of deformation, strength, and toughness of spider silk fibrils. Nano Lett. 10, 2626–2634 (2010).10.1021/nl101341w ↗
31. Denny, M. The physical properties of spider’s silk and their role in the design of orb-webs. J. Exp. Biol. 65, 483–506 (1976).10.1242/jeb.65.2.483 ↗
32. Gosline, J. M., Demont, M. E. & Denny, M. W. The structure and properties of spider silk. Endeavour 10, 37–43 (1986).10.1016/0160-9327(86)90049-9 ↗
33. Vollrath, F. Biology of spider silk. Int. J. Biol. Macromol. 24, 81–88 (1999).10.1016/S0141-8130(98)00076-2 ↗
34. Sahni, V., Blackledge, T. A. & Dhinojwala, A. Viscoelastic solids explain spider web stickiness. Nature Commun. 1, 1–4 (2010).10.1038/ncomms1019 ↗
35. Blackledge, T. A., Summers, A. P. & Hayashi, C. Y. Gumfooted lines in black widow cobwebs and the mechanical properties of spider capture silk. Zoology 108, 41–46 (2005).10.1016/j.zool.2004.11.001 ↗
36. Sahni, V., Blackledge, T. A. & Dhinojwala, A. Changes in the adhesive properties of spider aggregate glue during the evolution of cobwebs. Sci. Rep. 1, 1–41 (2011).10.1038/srep00041 ↗
37. Xu, M. & Lewis, R. M. Structure of a protein superfiber: Spider dragline silk. Proc. Natl Acad. Sci. USA 87, 7120–7124 (1990).10.1073/pnas.87.18.7120 ↗
38. Bell, F. I., McEwen, I. J. & Viney, C. Fibre science: Supercontraction stress in wet spider dragline. Nature 416, 37 (2002).10.1038/416037a ↗
39. Blackledge, T. A. et al. How super is supercontraction? Persistent versus cyclic responses to humidity in spider dragline silk. J. Exp. Biol. 212, 1981–1989 (2009).10.1242/jeb.028944 ↗
40. Van Beek, J. D., Hess, S., Vollrath, F. & Meier, B. H. The molecular structure of spider dragline silk: Folding and orientation of the protein backbone. Proc. Natl Acad. Sci. USA 99, 10266–10271 (2002).10.1073/pnas.152162299 ↗
41. Simmons, A. H., Michal, C. A. & Jelinski, L. W. Molecular orientation and two-component nature of the crystalline fraction of spider dragline silk. Science 271, 84–87 (1996).10.1126/science.271.5245.84 ↗
42. Eles, P.T. & Michal, C. A. Strain dependent local phase transitions observed during controlled supercontraction reveal mechanisms in spider silk. Macromolecules 37, 1342–1345 (2004).10.1021/ma035567p ↗
43. Boutry, C. & Blackledge, T. A. Evolution of supercontraction in spider silk: structure function relationship from tarantulas to orb-weavers. J. Exp. Biol. 213, 3505–3514 (2010).10.1242/jeb.046110 ↗
44. Guinea, G. V., Elices, M., Prez-Rigueiro, J. & Plaza, G. R. Stretching of supercontracted fibers: A link between spinning and the variability of spider silk. J. Exp. Biol. 208, 25–30 (2005).10.1242/jeb.01344 ↗
45. Savage, K. N., Guerette, P. A. & Gosline, J. M. Supercontraction stress in spider webs. Biomacromolecules 5, 675–679 (2004).10.1021/bm034270w ↗
46. Work, R. W. A comparative study of the supercontraction of major ampullate silk fibers of orb-web-building spiders (Araneae). J. Arachnol. 9, 299–308 (1981).
47. Fossey, S. A. & Kaplan, D. L. Polymer Data Handbook 970–974 (Oxford Univ. Press, 1999).
48. Work, R. W. & Emerson, P. D. J. An apparatus and technique for the forcible silking of spiders. J. Arachnol. 10, 1–10 (1982).
49. Fedorov, F. I. Theory of Elastic Waves in Crystals (Plenum, 1958).
50. Nye, J. F. Physical Properties of Crystals 144–145 (Clarendon, 1957).