Sucking the Oil: Adsorption Ability of Three-Dimensional Epicuticular Wax Coverages in Plants As a Possible Mechanism Reducing Insect Wet Adhesion

  • Elena V. Gorb
  • Philipp Hofmann
  • Alexander E. Filippov
  • Stanislav N. Gorb
Chapter
Part of the Biologically-Inspired Systems book series (BISY, volume 10)

Abstract

Primary aerial surfaces of terrestrial plants are very often covered with three-dimensional epicuticular waxes. Such wax coverages play an important role in insect-plant interactions. Wax blooms have been experimentally shown in numerous previous studies to be impeding locomotion and reducing attachment of insects. Among the mechanisms responsible for these effects, a possible adsorption of insect adhesive fluid by highly porous wax coverage has been proposed (adsorption hypothesis). Recently, a great decrease in insect attachment force on artificial adsorbing materials was revealed in a few studies. However, adsorption ability of plant wax blooms was still not tested. Using a cryo scanning electron microscopy approach and high-speed video recordings of fluid drops behavior, followed by numerical analysis of experimental data, we show here that the three-dimensional epicuticular wax coverage in the waxy zone of Nepenthes alata pitcher adsorbs oil: we detected changes in the base, height, and volume of the oil drops. The wax layer thickness, differing in samples with untreated two-layered wax coverage and treated one-layered wax, did not significantly affect the drop behavior. These results provide strong evidence that three-dimensional plant wax coverages due to their adsorption capability are in general anti-adhesive for insects, which rely on wet adhesion.

Notes

Acknowledgements

This book chapter is adapted from the publication Gorb, E.V. et al. Oil adsorption ability of three-dimensional epicuticular wax coverages in plants, Sci. Rep. 7, 45483; doi: 10.1038/srep45483 (2017). This work was partly supported by the CARBTRIB Project of The Leverhulme Trust (U. K.) to S. N. G. and E. V. G. and the Georg Forster Research Award (Alexander von Humboldt Foundation, Germany) to A. E. F. The authors acknowledge Alexander Kovalev (Kiel University, Germany) for his help in improving the MatLab program for the numerical analysis of experimental data and Lars Heepe (Kiel University, Germany) for useful discussions on adsorption phenomenon and for comments on the early version of the manuscript.

References

  1. Attygalle, A. B., Aneshansley, D. J., Meinwald, J., & Eisner, T. (2000). Defense by foot adhesion in a chrysomelid beetle (Hemisphaerota cyanea): Characterization of the adhesive oil. Zoology, 103, 1–6.Google Scholar
  2. Bargel, H., Koch, K., Cerman, Z., & Neinhuis, C. (2006). Structure–function relationships of the plant cuticle and cuticular waxes—A smart material? Functional Plant Biology, 33, 893–910.CrossRefGoogle Scholar
  3. Barthlott, W., Neinhuis, C., Cutler, D., Ditsch, F., Meusel, I., Theisen, I., & Wilhelmi, H. (1998). Classification and terminology of plant epicuticular waxes. Botanical Journal of the Linnean Society, 126, 237–260.CrossRefGoogle Scholar
  4. Benz, M. J., Gorb, E. V., & Gorb, S. N. (2012). Diversity of the slippery zone microstructure in pitchers of nine carnivorous Nepenthes taxa. Arthropod-Plant Interactions, 6, 147–158.CrossRefGoogle Scholar
  5. Betz, O., Verheyden, A. N., Maurer, A., Schmitt, C., Braun, J., Kowalik, T., Grunwald, I., Hartwig, A., & Neuenfeldt, M. (2016). Peptide mass analyses of the tarsal adhesive secretion in the desert locust Schistocerca gregaria and the Madagascar hissing cockroach Gromphadorhina portentosa. Insect Molecular Biology, 25, 541–549.CrossRefPubMedGoogle Scholar
  6. Bullock, J. M., & Federle, W. (2009). Division of labour and sex differences between fibrillar, tarsal adhesive pads in beetles: Effective elastic modulus and attachment performance. The Journal of Experimental Biology, 212, 1876–1888.CrossRefPubMedGoogle Scholar
  7. Busscher, H. J., Vanpert, A. W. J., Deboer, P., & Arends, J. (1984). The effect of the surface roughening of polymers on measured contact angle of liquids. Colloids and Surfaces, 9, 319–331.CrossRefGoogle Scholar
  8. Dirks, J.-H., & Federle, W. (2011). Fluid-based adhesion in insects—Principles and challenges. Soft Matter, 7, 11047–11053.CrossRefGoogle Scholar
  9. Dirks, J.-H., Clemente, C. J., & Federle, W. (2010). Insect tricks: Two-phasic foot pad secretion prevents slipping. Journal of the Royal Society Interface, 7, 587–593.CrossRefGoogle Scholar
  10. Dixon, A. F. G., Croghan, P. C., & Gowing, R. P. (1990). The mechanism by which aphids adhere to smooth surfaces. The Journal of Experimental Biology, 152, 243–253.Google Scholar
  11. Drechsler, P., & Federle, W. (2006). Biomechanics of smooth adhesive pads in insects: Influence of tarsal secretion on attachment performance. Journal of Comparative Physiology A, 192, 1213–1222.CrossRefGoogle Scholar
  12. Edwards, J. S., & Tarkanian, M. (1970). The adhesive pads of Heteroptera: A re-examination. Proceedings of the Royal Entomological Society of London. Series A, General Entomology, 45, 1–5.CrossRefGoogle Scholar
  13. Eigenbrode, S. D. (1996). Plant surface waxes and insect behavior. In G. Kerstiens (Ed.), Plant cuticles—An integrated functional approach (pp. 201–222). Oxford: BIOS Scientific Publishers.Google Scholar
  14. Eigenbrode, S. D., Castognola, T., Roux, M. B., & Steljes, L. (1999). Mobility of three generalist predators is greater on cabbage with glossy leaf wax than on cabbage with a wax bloom. Entomologia Experimentalis et Applicata, 81, 335–343.CrossRefGoogle Scholar
  15. Eisner, T., & Aneshansley, D. J. (2000). Defense by foot adhesion in a beetle (Hemisphaerota cyanea). Proceedings of the National Academy of Sciences of the United States of America, 97, 6568–6573.CrossRefPubMedPubMedCentralGoogle Scholar
  16. Gaume, L., Gorb, S., & Rowe, N. (2002). Function of epidermal surfaces in the trapping efficiency of Nepenthes alata pitchers. The New Phytologist, 156, 479–489.CrossRefGoogle Scholar
  17. Gaume, L., Perret, P., Gorb, E., Gorb, S., Labat, J.-J., & Rowe, N. (2004). How do plant waxes cause flies to slide? Experimental tests of wax-based trapping mechanisms in three pitfall carnivorous plants. Arthropod Structure & Development, 33, 103–111.CrossRefGoogle Scholar
  18. Geiselhardt, S. F., Geiselhardt, S., & Peschke, K. (2009). Comparison of tarsal and cuticular chemistry in the leaf beetle Gastrophysa viridula (Coleoptera: Chrysomelidae) and an evaluation of solid-phase microextraction and solvent extraction techniques. Chemoecology, 19, 185–193.CrossRefGoogle Scholar
  19. Gerhardt, H., Schmitt, C., Betz, O., Albert, K., & Lämmerhofer, M. (2015). Contact solid-phase microextraction with uncoated glass and polydimethylsiloxane-coated fibers versus solvent sampling for the determination of hydrocarbons in adhesion secretions of Madagascar hissing cockroaches Gromphadorrhina portentosa (Blattodea) by gas chromatography-mass spectrometry. Journal of Chromatography A, 1388, 24–35.CrossRefPubMedGoogle Scholar
  20. Gerhardt, H., Betz, O., Albert, K., & Lämmerhofer, M. (2016). Similarities, dissimilarities and classification of molecular (hydrocarbon) profiles of insect secretions in dependence of species, sex, and sampled body region. Journal of Chemical Ecology, 42, 725–738.CrossRefPubMedGoogle Scholar
  21. Gorb, S. N. (2001). Attachment devices of insect cuticle. Dordrecht/Boston/London: Kluwer Academic Publishers.Google Scholar
  22. Gorb, S. N. (2007). Visualisation of native surfaces by two-step molding. Microscopy Today, 15, 44–46.CrossRefGoogle Scholar
  23. Gorb, E. V., & Gorb, S. N. (2002). Attachment ability of the beetle Chrysolina fastuosa on various plant surfaces. Entomologia Experimentalis et Applicata, 105, 13–28.CrossRefGoogle Scholar
  24. Gorb, E. V., & Gorb, S. N. (2006a). Do plant waxes make insect attachment structures dirty? Experimental evidence for the contamination hypothesis. In A. Herrel, T. Speck, & N. P. Rowe (Eds.), Ecology and biomechanics—A mechanical approach to the ecology of animals and plants (pp. 147–162). Boca Raton: CRC Press.CrossRefGoogle Scholar
  25. Gorb, E. V., & Gorb, S. N. (2006b). Physicochemical properties of functional surfaces in pitchers of the carnivorous plant Nepenthes alata Blanco (Nepenthaceae). Plant Biology, 8, 841–848.CrossRefPubMedGoogle Scholar
  26. Gorb, E., & Gorb, S. (2009). Functional surfaces in the pitcher of the carnivorous plant Nepenthes alata: A cryo-SEM approach. In S. N. Gorb (Ed.), Functional surfaces in biology: Adhesion related effects (pp. 205–238). Dordrecht/Heidelberg/London/New York: Springer.CrossRefGoogle Scholar
  27. Gorb, E. V., & Gorb, S. N. (2013). Anti-adhesive surfaces in plants and their biomimetic potential. In P. Fratzl, J. W. C. Dunlop, & R. Weinkamer (Eds.), Materials design inspired by nature: Function through inner architecture (pp. 282–309). Cambridge: RSC Publishing.CrossRefGoogle Scholar
  28. Gorb, E., Haas, K., Henrich, A., Enders, S., Barbakadze, N., & Gorb, S. (2005). Composite structure of the crystalline epicuticular wax layer of the slippery zone in the pitchers of the carnivorous plant Nepenthes alata and its effect on insect attachement. The Journal of Experimental Biology, 208, 4651–4662.CrossRefPubMedGoogle Scholar
  29. Gorb, E., Voigt, D., Eigenbrode, S. D., & Gorb, S. (2008). Attachment force of the beetle Cryptolaemus montrouzieri (Coleoptera, Coccinellidae) on leaf surfaces of mutants of the pea Pisum sativum (Fabaceae) with regular and reduced wax coverage. Arthropod-Plant Interactions 2, 247–259.Google Scholar
  30. Gorb, E. V., Hosoda, N., Miksch, C., & Gorb, S. N. (2010). Slippery pores: Anti-adhesive effect of nanoporous substrates on the beetle attachment system. Journal of the Royal Society Interface, 7, 1571–1579.CrossRefPubMedCentralGoogle Scholar
  31. Gorb, E. V., Baum, M. J., & Gorb, S. N. (2013). Development and regeneration ability of the wax coverage in Nepenthes alata pitchers: A cryo-SEM approach. Scientific Reports, 3, 3078.CrossRefPubMedPubMedCentralGoogle Scholar
  32. Gorb, E. V., Purtov, J., & Gorb, S. N. (2014a). Adhesion force measurements on the two wax layers of the waxy zone in Nepenthes alata pitchers. Scientific Reports, 4, 5154.CrossRefPubMedPubMedCentralGoogle Scholar
  33. Gorb, E. V., Böhm, S., Jacky, N., Maier, L.-P., Dening, K., Pechook, S., Pokroy, B., & Gorb, S. N. (2014b). Insect attachment on crystalline bioinspired wax surfaces formed by alkanes of varying chain lengths. Beilstein Journal of Nanotechnology, 5, 1031–1041.CrossRefPubMedPubMedCentralGoogle Scholar
  34. Ishii, S. (1987). Adhesion of a leaf feeding ladybird Epilachna vigintioctomaculta (Coleoptera: Coccinellidae) on a vertically smooth surface. Applied Entomology and Zoology, 22, 222–228.CrossRefGoogle Scholar
  35. Jeffree, C. F. (1986). The cuticle, epicuticular waxes and trichomes of plants, with reference to their structure, function and evolution. In B. Juniper & R. Southwood (Eds.), Insects and the plant surface (pp. 23–64). London: Edward Arnold Publishers.Google Scholar
  36. Jeffree, C. E. (2006). The fine structure of the plant cuticle. In M. Riederer & C. Müller (Eds.), Biology of the plant cuticle (pp. 11–125). Oxford: Blackwell.CrossRefGoogle Scholar
  37. Jeffree, C. E., Baker, E. A., & Holloway, P. J. (1975). Ultrastructure and recrystallisation of plant epicuticular waxes. The New Phytologist, 75, 539–449.CrossRefGoogle Scholar
  38. Jetter, R., & Riederer, M. (1994). Epicuticular crystals of nanocosan-10 ol: In vitro reconstitution and factors influencing crystal habits. Planta, 195, 257–270.CrossRefGoogle Scholar
  39. Jetter, R., & Riederer, M. (1995). In vitro reconstitution of epicuticular wax crystals: Formation of tubular aggregates by long chain secondary alkanediols. Botanica Acta: Journal of the German Botanical Society, 108, 111–120.CrossRefGoogle Scholar
  40. Jetter, R., Kunst, L., & Samuels, A. L. (2006). Composition of plant epicuticular waxes. In M. Riederer & C. Müller (Eds.), Biology of the plant cuticle (pp. 145–181). Oxford: Blackwell.CrossRefGoogle Scholar
  41. Juniper, B. E., & Burras, J. K. (1962). How pitcher plants trap insects. New Scientist (1971), 269, 75–77.Google Scholar
  42. Koch, K., & Ensikat, H. J. (2008). The hydrophobic coatings of plant surfaces: Epicuticular wax crystals and their morphologies, crystallinity and molecular self-assembly. Micron, 39, 759–772.CrossRefPubMedGoogle Scholar
  43. Koch, K., Bhushan, B., & Barthlott, W. (2010). Multifunctional plant surfaces and smart materials. In B. Bhushan (Ed.), Handbook of nanotechnology (pp. 1399–1436). Heidelberg: Springer.CrossRefGoogle Scholar
  44. Kosaki, A., & Yamaoka, R. (1996). Chemical composition of footprints and cuticula lipids of three species of lady beetles. Japanese Journal of Applied Entomology and Zoology, 40, 47–53.CrossRefGoogle Scholar
  45. McPherson, S. (2009). Pitcher plants of the old world. Poole: Redfern Natural History Productions.Google Scholar
  46. Meusel, I., Neinhuis, C., Markstadter, C., & Barthlott, W. (2000). Chemical composition and recrystallization of epicuticular waxes: Coiled rodlets and tubules. Plant Biology, 2, 462–470.CrossRefGoogle Scholar
  47. Müller, C. (2006). Plant-insect interactions on cuticular surfaces. In M. Riederer & C. Müller (Eds.), Biology of the plant cuticle (pp. 398–422). Oxford: Blackwell.CrossRefGoogle Scholar
  48. Peisker, H., & Gorb, S. N. (2012). Evaporation dynamics of tarsal liquid footprints in flies (Calliphora vicina) and beetles (Coccinella septempunctata). The Journal of Experimental Biology, 215, 1266–1271.CrossRefPubMedGoogle Scholar
  49. Peisker, H., Heepe, L., Kovalev, A., & Gorb, S. N. (2014). Comparative study of the fluid viscosity in tarsal hairy attachment systems of flies and beetles. Journal of the Royal Society Interface, 11, 1–7.CrossRefGoogle Scholar
  50. Peressadko, A., & Gorb, S. (2004). Surface profile and friction force generated by insects. In I. Boblan & R. Bannasch (Eds.), Proceedings of the first international industrial conference bionik (pp. 257–263). Düsseldorf: VDI Verlag.Google Scholar
  51. Reitz, M., Gerhardt, H., Schmitt, C., Betz, O., Albert, K., & Laemmerhofer, M. (2015). Analysis of chemical profiles of insect adhesion secretions by gas chromatography-mass spectrometry. Analytica Chimica Acta, 854, 47–60.CrossRefPubMedGoogle Scholar
  52. Scholz, I., Bückins, M., Dolge, L., Erlinghagen, T., Weth, A., Hischen, F., Mayer, J., Hoffmann, S., Riederer, M., Riedel, M., & Baumgartner, W. (2010). Slippery surfaces of pitcher plants: Nepenthes wax crystals minimize insect attachment via microscopic surface roughness. The Journal of Experimental Biology, 213, 115–1125.CrossRefGoogle Scholar
  53. Starov, V. M., Zhdanov, S. A., Kosvintsev, S. R., Sobolev, V. D., & Velarde, M. G. (2003). Spreading of liquid drops over porous substrates. Advances in Colloid and Interface Science, 104, 123–158.CrossRefPubMedGoogle Scholar
  54. Stork, N. E. (1980). Role of waxblooms in preventing attachment to brassicas by the mustard beetle, Phaedon cochleariae. Entomologia Experimentalis et Applicata, 26, 100–107.CrossRefGoogle Scholar
  55. Voigt, D., Schuppert, J. M., Dattinger, S., & Gorb, S. N. (2008). Sexual dimorphism in the attachment ability of the Colorado potato beetle Leptinotarsa decemlineata (Coleoptera: Chrysomelidae) to rough substrates. Journal of Insect Physiology, 54, 765–776.CrossRefPubMedGoogle Scholar
  56. Vötsch, W., Nicholson, G., Müller, R., Stierhof, Y.-D., Gorb, S. N., & Schwarz, U. (2002). Chemical composition of the attachment pad secretion of the locust Locusta migratoria. Insect Biochemistry and Molecular Biology, 32, 1605–1613.CrossRefPubMedGoogle Scholar

Copyright information

© Springer International Publishing AG, part of Springer Nature 2017

Authors and Affiliations

  • Elena V. Gorb
    • 1
  • Philipp Hofmann
    • 1
  • Alexander E. Filippov
    • 1
    • 2
  • Stanislav N. Gorb
    • 1
  1. 1.Department of Functional Morphology and BiomechanicsZoological Institute, Kiel UniversityKielGermany
  2. 2.Department N5Donetsk Institute for Physics and EngineeringDonetskUkraine

Personalised recommendations