Nanoscale Pattern Formation in Biological Surfaces

  • Alexander E. Filippov
  • Stanislav N. Gorb
Part of the Biologically-Inspired Systems book series (BISY, volume 16)


In the present chapter, three problems of nanoscale pattern formation will be discussed. (1) The particular symmetry violation in the dimple-like nano-pattern on the belly scales of the pythonid snake Morelia viridis is analyzed using correlation analysis of the distances between individual nanostructures. (2) Pattern formation in the multi-component colloidal secretion of whip-spiders (cerotegument) is numerically simulated and discussed. (3) Pattern formation of the springtail cuticle nanostructures.

Dimple-like nano-pattern on the belly scales of the snake skin is supposed to reduce both friction and abrasion. On the real snake skin surface, the pattern analysis revealed non-random, but very specific symmetry violation. The results of the analysis, performed on the snake were compared with nano-nipple pattern on the eye of the sphingid moth being well known reference of highly-ordered biological nanopatterns. In the case of the moth eye, the nano-nipple arrangement forms a set of domains, while, in the case of the snake skin, the nano-dimples arrangement resembles an ordering of molecules in amorphous state, which might provide friction isotropy to the skin. A simple model of such pattern formation is suggested, which almost perfectly reproduces the experimental results. Some other biological surfaces gain their super-hydrophobic properties by nano-structures on the surface. Some arachnids, such as the cryptic, large whip-spiders and some mites, exhibit a crust of dried secretion containing globular micro-structures covered with regularly arranged nano-particles built from a multi-phasic secretion. In order to gain a better understanding of the process of self-assembly of nanostructures on spherical microstructures, in the present chapter, we studied it from a theoretical point of view. It is demonstrated that slight changes of simple parameters lead to a variety of morphologies highly similar to the ones observed in the species specific cerotegument structures. Also springtails have a complex hierarchically structured cuticle surface with even stronger repelling properties against water, low-surface-tension liquids, and sticky secrets of predatory insects. Non-wetting property of the collembolan cuticle is mainly based on the cuticle topography rather than on the surface chemistry. In material science, analogous surface coatings have been produced by colloidal lithography utilizing the self-assembly of nanoparticles on a substrate. We introduce here a numerical model to study the effect of different interactions between the substances on the morphology of the desired structure. In general the study of biological self-organising nanopatterns and their evolution seems to be a promising approach for generating new solutions for future industrial applications.

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  1. Alberti G, Storch V, Renner H (1981) Über den feinstrukturellen Aufbau der Milbencuticula (Acari, Arachnida). Zool Jb Anat 105:183–236Google Scholar
  2. Badge I, Bhawalkar SP, Jia L, Dhinojwala A (2013) Tuning surface wettability using single layered and hierarchically ordered arrays of spherical colloidal particles. Soft Matter 9:3032–3040Google Scholar
  3. Barthlott W, Neinhuis C (1997) Purity of the sacred lotus, or escape from contamination in biological surfaces. Planta 202:1–8Google Scholar
  4. Barthlott W, Mail M, Neinhuis C (2016) Superhydrophobic hierarchically structured surfaces in biology: evolution, structural principles and biomimetic applications. Phil Trans R Soc A 374:20160191PubMedGoogle Scholar
  5. Baum M, Heepe L, Gorb SN (2014) Friction behavior of a microstructured polymer surface inspired by snake skin. Beilstein J Nanotechnol 5:83–97PubMedPubMedCentralGoogle Scholar
  6. Bernhard CG, Miller WH (1962) A corneal nipple pattern in insect compound eyes. Acta Physiol Scand 56:385–386PubMedGoogle Scholar
  7. Berthé RA, Westhoff G, Bleckmann H, Gorb SN (2009) Surface structure and frictional properties of the skin of the Amazon tree boa Corallus hortulanus (Squamata, Boidae). J Comp Physiol A 195:311–318Google Scholar
  8. Blagodatski A, Sergeev A, Kryuchkova M, Lopatinad Y, Katanaev VL (2015) Diverse set of Turing nanopatterns coat corneae across insect lineages. Proc Natl Acad Sci U S A 112:10750–10755PubMedPubMedCentralGoogle Scholar
  9. Dennell RA (1946) Study of an insect cuticle: the larval cuticle of Sarcophaga faculata Pand. (Diptera). Proc R Soc B 133:348–373Google Scholar
  10. Erber T, Hockney GM (1991) Equilibrium configurations of N equal charges on a sphere. J Phys A Math Gen 24:L1369–L1377Google Scholar
  11. Filippov AE (1997) Kinetics of vortex structure formation in magnetic materials. J Exp Theor Phys 84:971–977Google Scholar
  12. Filippov AE (1998) Two-component model for the growth of porous subsurface layers. J Exp Theor Phys 87:814–822Google Scholar
  13. Filippov AE, Wolff JO, Seiter M, Gorb SN (2017) Numerical simulation of colloidal self-assembly of super-hydrophobic arachnid cerotegument structures. J Theor Biol 430:1–8PubMedGoogle Scholar
  14. Filippov AE, Kovalev A, Gorb SN (2018) Numerical simulation of the pattern formation of the springtail cuticle nanostructures. J R Soc Interface 15:20180217PubMedPubMedCentralGoogle Scholar
  15. Geim AK, Grigorieva IV, Dubonos SV, Lok JGS, Maan JC, Filippov AE, Peeters FM (1997) Phase transitions in individual sub-micrometre superconductors. Nature 390:259–262Google Scholar
  16. Gorb SN (1997) Porous channels in the cuticle of the head-arrester system in dragon/damselflies (Insecta: Odonata). Microsc Res Tech 37:583–591PubMedGoogle Scholar
  17. Hale WG, Smith AL (1966) Scanning electron microscope studies of cuticular structures in the genus Onychiurus (Collembola). Rev Ecol Biol Sol 3:343–354Google Scholar
  18. Helbig R, Nickerl J, Neinhuis C, Werner C (2011) Smart skin patterns protect springtails. PLoS One 6:e25105PubMedPubMedCentralGoogle Scholar
  19. Hensel R, Helbig R, Aland S, Braun H-G, Voigt A, Neinhuis C, Werner C (2013a) Wetting resistance at its topographical limit: the benefit of mushroom and serif T structures. Langmuir 29:1100–1112PubMedGoogle Scholar
  20. Hensel R, Helbig R, Aland S, Voigt A, Neinhuis C, Werner C (2013b) Tunable nano-replication to explore the omniphobic characteristics of springtail skin. NPG Asia Mater 5:e37Google Scholar
  21. Hensel R, Finn A, Helbig R, Braun H-G, Neinhuis C, Fischer W-J, Werner C (2014) Biologically inspired omniphobic surfaces by reverse imprint lithography. Adv Mater 26:2029–2033PubMedGoogle Scholar
  22. Klein M-CG, Gorb SN (2012) Epidermis architecture and material properties of the skin of four snake species. J R Soc Interface 9:3140–3155PubMedPubMedCentralGoogle Scholar
  23. Klein M-CG, Gorb SN (2014) Ultrastructure and wear patterns of the ventral epidermis of four snake species (Squamata, Serpentes). Zoology 117:295–314PubMedGoogle Scholar
  24. Klein M-CG, Deuschle JK, Gorb SN (2010) Material properties of the skin of the Kenyan sand boa Gongylophis colubrinus (Squamata, Boidae). J Comp Physiol A 196:659–668Google Scholar
  25. Koerner L, Gorb SN, Betz O (2012) Adhesive performance of the stick-capture apparatus of rove beetles of the genus Stenus (Coleoptera, Staphylinidae) toward various surfaces. J Insect Physiol 58:155–163PubMedGoogle Scholar
  26. Kosterlitz JM, Thouless DJ (1973) Ordering, metastability and phase transitions in two-dimensional systems. J Physics C: Solid State Physics 6:1181–1203Google Scholar
  27. Kovalev A, Filippov AE, Gorb SN (2016) Correlation analysis of symmetry breaking in the surface nanostructure ordering: case study of the ventral scale of the snake Morelia viridis. Applied Physics A 122:1–6Google Scholar
  28. Krzysztofowicz A, Klag J, Komorowska B (1972) The fine structure of the cuticle in Tetrodontophora bielanensis (Waga), Collembola. Acta Biol Cracoviensia Ser Zool 15:113–119Google Scholar
  29. Lee KC, Erb U (2015) Remarkable crystal and defect structures in butterfly eye nano-nipple arrays. Arthropod Struct Dev 44:587–594PubMedGoogle Scholar
  30. Li R, Bowerman B (2010) Symmetry breaking in biology. Cold Spring Harb Perspect Biol 2:a003475PubMedPubMedCentralGoogle Scholar
  31. Locke M (1961) Pore canals and related structures in insect cuticle. J Biophys Biochem Cytol 10:589–618PubMedPubMedCentralGoogle Scholar
  32. Miskimen GW, Rodriguez NL (1981) Structure and functional aspects of the Scotopic compound eye of the sugarcane borer moth. J Morphol 168:73–84PubMedGoogle Scholar
  33. Mityushev V (2016) Pattern formations and optimal packing. Math Biosci 274: 12–16 and Chapter 9 of Bressloff PC 2014 Stochastic processes in cell biology. Springer, ChamGoogle Scholar
  34. Nickerl J, Helbig R, Schulz H-J, Werner C, Neinhuis C (2013) Diversity and potential correlations to the function of Collembola cuticle structures. Zoomorphology 132:183–195Google Scholar
  35. Nickerl J, Tsurkan M, Hensel R, Neinhuis C, Werner C (2014) The multilayered protective cuticle of Collembola: a chemical analysis. J R Soc Interface 11:20140619PubMedPubMedCentralGoogle Scholar
  36. Peisker H, Gorb SN (2010) Always on the bright side of life: anti-adhesive properties of insect ommatidia grating. J Exp Biol 213:3457–3462PubMedGoogle Scholar
  37. Prum RO, Torres RH (2003) Structural colouration of avian skin: convergent evolution of coherently scattering dermal collagen arrays. J Exp Biol 206:2409–2429PubMedGoogle Scholar
  38. Rakitov R, Gorb SN (2013) Brochosomal coats turn leafhopper (Insecta, Hemiptera, Cicadellidae) integument to superhydrophobic state. Proc R Soc Lond B 280:20122391Google Scholar
  39. Raspotnig G, Matischek T (2010) Anti-wetting strategies of soil-dwelling Oribatida (Acari). Acta Soc Zool Bohem 74:91–96Google Scholar
  40. Richards AG (1951) The integument of arthropods. The chemical composition and their properties, the anatomy and development, and the permeability. University of Minnnesota Press, Minneapolis, London, Geoffrey Cumberlege, Oxford University PressGoogle Scholar
  41. Rusek J (1998) Biodiversity of Collembola and their functional role in the ecosystem. Biodivers Conserv 7:1207–1219Google Scholar
  42. Schmidt CV, Gorb SN (2012) Snake scale microstructure: phylogenetic significance and functional adaptations. Zoologica 157:1–106Google Scholar
  43. Sergeev A, Timchenko AA, Kryuchkov M, Blagodatski A, Enin GA, Katanaev VL (2015) Origin of order in bionanostructures. RSC Adv 5:63521–63527Google Scholar
  44. Stalleicken J, Labhart T, Mouritsen H (2006) Physiological characterization of the compound eye in monarch butterflies with focus on the dorsal rim area. J Comp Physiol A 192:321–331Google Scholar
  45. Stavenga DG, Foletti S, Palasantzas G, Arikawa K (2006) Light on the moth-eye corneal nipple array of butterflies. Proc R Soc Lond B Biol Sci 273:661–667Google Scholar
  46. Tammes PML (1930) On the origin of number and arrangement of the places of exit on pollen grains. Recl Trav Bot Néerl 27:1–84Google Scholar
  47. Tarnai T, Gáspár Z (1987) Multi-symmetric close packings of equal spheres on the spherical surface. Acta Crystallogr 43:612–616Google Scholar
  48. Thompson CV (2000) Structure evolution during processing of polycrystalline films. Ann Rev Mater Sci 30:159–190Google Scholar
  49. Varenberg M, Halperin G, Etsion I (2002) Different aspects of the role of wear debris in fretting wear. Wear 252:902–910Google Scholar
  50. Weygoldt P (2000) Whip spiders, (Chelicerata, Amblypygi), their biology, morphology and systematics. Apollo Books, Stenstrup, p 163Google Scholar
  51. Wiggelsworth VB (1947) The epicuticle in an insect, Rhodnius prolixus. Proc R Ent Soc L B 134:163–181Google Scholar
  52. Wiggelsworth VB (1976) The distribution of lipid in cuticle of Rhodnius. In: Hepburn HR (ed) The insect integument. Elsevier, Amsterdam, pp 89–106Google Scholar
  53. Wolff JO, Schwaha T, Seiter M, Gorb SN (2016) Whip spiders (Amblypygi) become water-repellent by a colloidal secretion that self-assembles into hierarchical microstructures. Zool Letters 2(N23):1–10Google Scholar
  54. Wolff JO, Seiter M, Gorb SN (2017) The water-repellent cerotegument of whip-spiders (Arachnida: Amblypygi). Arthropod Struct Dev 46:116–129PubMedGoogle Scholar
  55. Yang SM, Jang SG, Choi DG, Kim S, Yu HK (2006) Nanomachining by colloidal lithography. Small 2:458–475PubMedGoogle Scholar

Copyright information

© Springer Nature Switzerland AG 2020

Authors and Affiliations

  • Alexander E. Filippov
    • 1
  • Stanislav N. Gorb
    • 2
  1. 1.Donetsk Institute for Physics and EngineeringDonetskUkraine
  2. 2.Zoological InstituteKiel UniversityKielGermany

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