Plant Surfaces: Structures and Functions for Biomimetic Innovations

Abstract

An overview of plant surface structures and their evolution is presented. It combines surface chemistry and architecture with their functions and refers to possible biomimetic applications. Within some 3.5 billion years biological species evolved highly complex multifunctional surfaces for interacting with their environments: some 10 million living prototypes (i.e., estimated number of existing plants and animals) for engineers. The complexity of the hierarchical structures and their functionality in biological organisms surpasses all abiotic natural surfaces: even superhydrophobicity is restricted in nature to living organisms and was probably a key evolutionary step with the invasion of terrestrial habitats some 350–450 million years ago in plants and insects. Special attention should be paid to the fact that global environmental change implies a dramatic loss of species and with it the biological role models. Plants, the dominating group of organisms on our planet, are sessile organisms with large multifunctional surfaces and thus exhibit particular intriguing features. Superhydrophilicity and superhydrophobicity are focal points in this work. We estimate that superhydrophobic plant leaves (e.g., grasses) comprise in total an area of around 250 million km2, which is about 50% of the total surface of our planet. A survey of structures and functions based on own examinations of almost 20,000 species is provided, for further references we refer to Barthlott et al. (Philos. Trans. R. Soc. A 374: 20160191, 1). A basic difference exists between aquatic non-vascular and land-living vascular plants; the latter exhibit a particular intriguing surface chemistry and architecture. The diversity of features is described in detail according to their hierarchical structural order. The first underlying and essential feature is the polymer cuticle superimposed by epicuticular wax and the curvature of single cells up to complex multicellular structures. A descriptive terminology for this diversity is provided. Simplified, the functions of plant surface characteristics may be grouped into six categories: (1) mechanical properties, (2) influence on reflection and absorption of spectral radiation, (3) reduction of water loss or increase of water uptake, moisture harvesting, (4) adhesion and non-adhesion (lotus effect, insect trapping), (5) drag and turbulence increase, or (6) air retention under water for drag reduction or gas exchange (Salvinia effect). This list is far from complete. A short overview of the history of bionics and the impressive spectrum of existing and anticipated biomimetic applications are provided. The major challenge for engineers and materials scientists, the durability of the fragile nanocoatings, is also discussed.

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     Mundo C, Sommerfeld M, Tropea C. Droplet-wall collisions: experimental studies of the deformation and breakup process. Int. J. Multiph. Flow. 1995;21:151-173.

     Not in our library10.1016/0301-9322(94)00069-v

117. 117.

     Mao T, Kuhn D, Tran H. Spread and rebound of liquid droplets upon impact on flat surfaces. AIChE J. 1997;43:2169-2179.

     Not in our library10.1002/aic.690430903

118. 118.

     Xu L, Barcos L, Nagel SR. Splashing of liquids: interplay of surface roughness with surrounding gas. Phys. Rev. E. 2007;76:066311.

     Not in our library10.1103/physreve.76.066311

119. 119.

     Rioboo R, Tropea C, Marengo M. Outcomes from a drop impact on solid surfaces. At. Sprays. 2001;11:155-165.

     Not in our library

120. 120.

     Motzkus C, Gensdarmes F, Géhin E. Study of the coalescence/splash threshold of droplet impact on liquid films and its relevance in assessing airborne particle release. J. Colloid Interface Sci. 2011;362:540-552.

     Not in our library10.1016/j.jcis.2011.06.031

121. 121.

     Gilet T, Bourouiba L. Rain-induced ejection of pathogens from leaves: revisiting the hypothesis of splash-on-film using high-speed visualization. Integr. Comp. Biol. 2014;54(6):974-984.

     Not in our library10.1093/icb/icu116

122. 122.

     Koch K, Grichnik R. Influence of surface structure and chemistry on water droplet splashing. Philos. Trans. R. Soc. A. 2016;374:20160183.

     Not in our library10.1098/rsta.2016.0183

123. 123.

     Liu Y, Moevius L, Xu X, Qian T, Yeomans JM, Wang Z. Pancake bouncing on superhydrophobic surfaces. Nat. Phys. 2014;10(7):515-519.

     Not in our library10.1038/nphys2980

124. 124.

     Koch K, Bennemann M, Bohn HF, Albach DC, Barthlott W. Surface microstructures of daisy florets (Asteraceae) and characterization of their anisotropic wetting. Bioinspir. Biomim. 2013;8:036005.

     Not in our library10.1088/1748-3182/8/3/036005

125. 125.

     Otten A, Herminghaus S. How plants keep dry: a physicist’s point of view. Langmuir. 2004;20:2405-2408.

     Not in our library10.1021/la034961d

126. 126.
     Superhydrophobicity in perfection: the outstanding properties of the lotus leaf · 2011

     No notice
127. 127.

     Barthlott W, Riede K, Wolter M. Mimicry and ultrastructural analogy between the semi-aquatic grasshopper Paulinia acuminata (Orthoptera: Pauliniidae) and its foodplant, the water-fern Salvinia auriculata (Filicateae: Salviniaceae). Amazoniana. 1994;13:47-58.

     Not in our library

128. 128.

     Bargel H, Barthlott W, Koch K, Schreiber L, Neinhuis C, Hemsley AR, Poole I. Plant Cuticles: Multifunctional Interfaces Between Plant and Environment. The Evolution of Plant Physiology. 2003;171-194.

     Not in our library

129. 129.

     Schreiber L, Schonherr J. Water and Solute Permeability of Plant Cuticles. 2009.

     Not in our library

130. 130.

     Koch K, Barthlott W. Superhydrophobic and superhydrophilic plant surfaces: an inspiration for biomimetic materials. Philos. Trans. R. Soc. A. 2009;367:1487-1509.

     Not in our library10.1098/rsta.2009.0022

131. 131.

     Barthlott W. Epidermal and seed surface characters of plants: systematic applicability and some evolutionary aspects. Nordic J. Bot. 1981;1:345-355.

     Not in our library10.1111/j.1756-1051.1981.tb00704.x

132. 132.

     Kevan PG, Lanet MA. Flower petal microtexture is a tactile cue for bees. Proc. Nat. Acad. Sci. USA. 1985;82:4750-4752.

     Not in our library10.1073/pnas.82.14.4750

133. 133.

     Gorb SN. Functional surfaces in biology: adhesion related phenomena. 2009.

     Not in our library

134. 134.

     Exner F, Exner S. Die physikalischen Grundlagen der Blütenfärbungen. Sitzungsber. Kais. Akad. Wiss. Wien, Math.-nat. Kl. 1910;119:191-245.

     Not in our library

135. 135.

     Toda Y. Physiological studies on Schistostega osmundacea (Dicks.) Mohr. J. Coll. Sci. Imp. Univ. Tokyo. 1918;40(5):1-30.

     Not in our library

136. 136.

     Kay Q, Daoud H, Stirton C. Pigment distribution, light reflection and cell structure in petals. Bot. J. Linnean Soc. 1981;83:57-84.

     Not in our library10.1111/j.1095-8339.1981.tb00129.x

137. 137.

     Whitney HM, Kolle M, Andrew P, Chittka L, Steiner U, Glover B. Floral iridescence, produced by diffractive optics, acts as cue for animal pollinators. Science. 2009;323:130-133.

     Not in our library10.1126/science.1166256

138. 138.

     Lloyd DG, Barret SCH. Floral Biology-Studies on Floral Evolution in Animal-pollinated Plants. 1995.

     Not in our library

139. 139.

     B. Burr, D. Rosen, W. Barthlott, Untersuchungen zur Ultraviolettreflexion von Angiospermenblüten. III. Dilleniidae und Asteridae S. I. Trop. Subtrop. Pflanzenwelt 93 (Akad. Wiss. Lit. Mainz, F. Steiner Verlag, Stuttgart, 1995), 186 pp

     Not in our library

140. 140.

     B. Burr, W. Barthlott, Untersuchungen zur Ultraviolettreflexion von Angiospermenblüten. II. Magnoliidae, Ranunculidae, Hamamelididae, Caryophyllidae, Rosidae. Trop. subtrop. Pflanzenwelt 87 (Akad. Wiss. Lit. Mainz, F. Steiner Verlag, Stuttgart, 1993), 193 pp

     Not in our library

141. 141.

     N. Biedinger, W. Barthlott, Untersuchungen zur Ultraviolettreflexion von Angiospermenblüten. I. Monocotyledoneae. Trop. Subtrop. Pflanzenwelt 86 (Akad. Wiss. Lit. Mainz, F. Steiner Verlag, Stuttgart, 1993), 122 pp

     Not in our library

142. 142.

     Whitney H, Kolle M, Alvarez-Fernandez R, Steiner U, Glover B. Contributions of iridescence to floral patterning. Commun. Integr. Biol. 2009;2(3):230-232.

     Not in our library10.4161/cib.2.3.8084

143. 143.

     Robinson S, Lovelock CE, Osmond CB. Wax as a mechanism for protection against photoinhibition: a study of Cotyledon orbiculata. Bot. Acta. 1993;106:307-312.

     Not in our library10.1111/j.1438-8677.1993.tb00753.x

144. 144.

     Müller C, Riederer M. Plant surface properties in chemical ecology. Chem. Ecol. 2005;3:2621-2651.

     Not in our library10.1007/s10886-005-7617-7

145. 145.

     Ehleringer JR, Björkman O. Pubescence and leaf spectral characteristics in a desert shrub Encelia farinosa. Oecologia. 1978;36:151-162.

     Not in our library10.1007/bf00349805

146. 146.

     Holmes MG, Keiller DR. Effects of pubescence and waxes on the reflectance of leaves in the ultraviolet and photosynthetic wavebands: a comparison of a range of species. Plant Cell Environ. 2002;25:85-93.

     Not in our library10.1046/j.1365-3040.2002.00779.x

147. 147.

     Gates DM, Lange OL, Kappen L, Schulze ED. Energy Exchange and Transpiration. Water and Plant Life. 1976;137-147.

     Not in our library

148. 148.

     Schuepp PH. Model experiments on free convection heat and mass transfer of leaves and plant elements. Boundary-Layer Meteorol. 1973;3:454-457.

     Not in our library10.1007/bf01034988

149. 149.

     Schuepp PH. Leaf boundary layers. New Phytol. 1993;125:477-507.

     Not in our library10.1111/j.1469-8137.1993.tb03898.x

150. 150.

     Jones HG, Rotenberg E, Hetherington AM. Radiation and Temperature Regulation in Plants. Encyclopedia of Life Science. 2001;1-8.

     Not in our library

151. 151.

     Barthlott W, Schultze-Motel W. Zur feinstruktur der blattoberflächen und systematischen stellung der laubmoosgattung rhacocarpus und anderer hedwigiaceae. Willdenowia. 1981;11:3-11.

     Not in our library

152. 152.

     Edelmann HG, Neinhuis C, Jarvis M, Evans B, Fischer E, Barthlott W. Ultrastructure and chemistry of the cell wall of the moss Rhacocarpus purpurascens (Rhacocarpaceae): a puzzling architecture among plants. Planta. 1998;206:315-321.

     Not in our library10.1007/s004250050406

153. 153.

     Malik FT, Clement RM, Gethin DT, Krawszik W, Parker AR. Nature’s moisture harvesters: a comparative review. Bioinspir. Biomim. 2014;9:031002.

     Not in our library10.1088/1748-3182/9/3/031002

154. 154.

     Azad MAK, Ellerbrok D, Barthlott W, Koch K. Fog collecting biomimetic surfaces: influence of microstructure and wettability. Bioinspir. Biomim. 2015;10:016004.

     Not in our library10.1088/1748-3190/10/1/016004

155. 155.

     Azad MAK, Barthlott W, Koch K. Hierarchical surface architecture of plants as an inspiration for biomimetic fog collectors. Langmuir. 2015;31(48):13172-13179.

     Not in our library10.1021/acs.langmuir.5b02430

156. 156.

     Martone PT, Kost L, Boller M. Drag reduction in wave-swept macroalgae: alternative stratgies and new predictions. Am. J. Bot. 2012;99(5):806-815.

     Not in our library10.3732/ajb.1100541

157. 157.

     Barthlott W, Koch H. Die Selbstreinigungsfähigkeit Pflanzlicher Oberflächen Durch Epicuticularwachse. Klima- und Umweltforschung an der Universität Bonn. 1992;117-120.

     Not in our library

158. 158.

     Extrand CW, Moon SI. Repellency of the lotus leaf: contact angles, drop retention, and sliding angles. Langmuir. 2014;30:8791-8797.

     Not in our library10.1021/la5019482

159. 159.

     Balmert A, Bohn HF, Ditsche-Kuru P, Barthlott W. Dry under water: comparative morphology and functional aspects of air-retaining insect surfaces. J. Morphol. 2011;272:442-451.

     Not in our library10.1002/jmor.10921

160. 160.

     Seymour RS, Matthews PGD. Physical gills in diving insects and spiders: theory and experiment. J. Exp. Biol. 2013;216:164-170.

     Not in our library10.1242/jeb.070276

161. 161.

     Koch K, Bohn HF, Barthlott W. Hierarchical sculpturing of plant surfaces and superhydrophobicity. Part of the ‘Langmuir 25th year: wetting and superhydrophobicity’ special issue’. Langmuir. 2009;25:14116-14120.

     Not in our library10.1021/la9017322

162. 162.

     Amabili M, Giacomello A, Meloni S, Casciola CM. Unraveling the Salvinia paradox: design principles for submerged superhydrophobicity. Adv. Mater. Interfaces. 2015;2:1500248.

     Not in our library10.1002/admi.201500248

163. 163.

     Ditsche P, Gorb E, Mayser M, Gorb S, Schimmel T, Barthlott W. Elasticity of the hair cover in air-retaining Salvinia surfaces. Appl. Phys. A. 2015;121:505-511.

     Not in our library10.1007/s00339-015-9439-y

164. 164.

     Gandyra D, Walheim S, Gorb S, Barthlott W, Schimmel T. The capillary adhesion technique: a versatile method for determining the liquid adhesion force and sample stiffness. Beilstein J. Nanotchnol. 2015;6:11-18.

     Not in our library10.3762/bjnano.6.2

165. 165.

     Konrad W, Apeltauer C, Frauendiener J, Barthlott W, Roth-Nebelsick A. Applying methods from differential geometry to devise stable and persistent air layers attached to objects immersed in water. J. Bion. Eng. 2009;6:350-356.

     Not in our library10.1016/s1672-6529(08)60133-x

166. 166.

     Mayser MJ, Barthlott W. Layers of air in the water beneath the floating fern Salvinia are exposed to fluctuations in pressure. Integr. Comp. Biol. 2014;54:1001-1007.

     Not in our library10.1093/icb/icu072

167. 167.

     Mayser MJ, Bohn HF, Reker M, Barthlott W. Measuring air layer volumes retained by submerged floating-ferns Salvinia and biomimetic superhydrophobic surfaces. Beilstein J. Nanotechnol. 2014;5:812-821.

     Not in our library10.3762/bjnano.5.93

168. 168.

     Solga A, Cerman Z, Striffler BF, Spaeth M, Barthlott W. The dream of staying clean: lotus and biomimetic surfaces. Bioinspir. Biomim. 2007;2:126-134.

     Not in our library10.1088/1748-3182/2/4/s02

169. 169.

     Eigenbrode SD, Kerstiens G. Plant Surface Waxes and insect Behaviour. Plant Cuticles: An Integrated Functional Approach. 1996;201-222.

     Not in our library

170. 170.

     Beutel RG, Gorb SN. Ultrastructure of attachment specializations of hexapods (Arthropoda): evolutionary patterns inferred from a revised ordinal phylogeny. J. Zool Syst. 2001;39(4):177-207.

     Not in our library10.1046/j.1439-0469.2001.00155.x

171. 171.

     Gorb S. Attachment Devices of Insect Cuticle. 2001.

     Not in our library

172. 172.

     Bohn HF, Federle W. Insect aquaplaning: nepenthes pitcher plants capture prey with the peristome, a fully wettable water-lubricated anisotropic surface. Proc. Nat. Acad. Sci. USA. 2004;101(39):14138-14143.

     Not in our library10.1073/pnas.0405885101

173. 173.

     Bauer U, Bohn HF, Federle W. Harmless nectar source or deadly trap: nepenthes pitchers are activated by rain, condensation and nectar. Proc. R. Soc. B. 2008;275:259-265.

     Not in our library10.1098/rspb.2007.1402

174. 174.

     Gould J. Learning from naturés best. Nature. 2015;519:S2-S3.

     Not in our library10.1038/519s2a

175. 175.

     Schulte AJ, Droste DM, Koch K, Barthlott W. Hierarchically structured superhydrophobic flowers with low hysteresis of the wild pansy (Viola tricolor)-new design principles for biomimetic materials. Beilstein J. Nanotechnol. 2011;2:228-236.

     Not in our library10.3762/bjnano.2.27

176. 176.

     Hopkin M. Butterflies boast ultrablack wings: insects use optical trick to get the blackest black out of dark pigments. Nat. News. 2004.

     Not in our library

177. 177.

     Spinner M, Gorb SN, Balmert A, Bleckmann H, Westhoff G. Non-contaminating camouflage: multifunctional skin microornamentation in the West African Gaboon viper (Bitis rhinoceros). PLoS ONE. 2014;9:e91087.

     Not in our library10.1371/journal.pone.0091087

178. 178.

     M.A.K. Azad, Fog Collection on Plant Surfaces and Biomimetic Applications, (Dissertation, University of Bonn, 2016)

     Not in our library

179. 179.

     Nosonovsky M, Bhushan B. Energy transitions in superhydrophobicity: low adhesion, easy flow and bouncing. J. Phys.: Condens. Matter. 2008;20:395005.

     Not in our library

180. 180.

     Zouridakis G, Moore JE, Maitland J. Biomedical Technology and Devices. 2013.

     Not in our library

181. 181.

     Weng CJ, Chang CH, Peng CW, Chen SW, Yeh JM, Hsu CL, Wei Y. Advanced anticorrosive coatings prepared from the mimicked Xanthosoma sagittifolium-leaf-like electroactive epoxy with synergistic effects of superhydrophobicity and redox catalytic capability. Chem. Mater. 2011;23(8):2075-2083.

     Not in our library10.1021/cm1030377

182. 182.

     Farhadi S, Farzaneh M, Kulinich SA. Anti-icing performance of superhydrophobic surfaces. Appl. Surf. Sci. 2011;257:6264-6269.

     Not in our library10.1016/j.apsusc.2011.02.057

183. 183.

     Cao L, Jones AK, Sikka VK, Wu J, Gao D. Anti-icing superhydrophobic coatings. Langmuir. 2009;25:12444-12448.

     Not in our library10.1021/la902882b

184. 184.

     Yan YY, Gao N, Barthlott W. Mimicking natural superhydrophobic surfaces and grasping the wetting process: a review on recent progress in preparing superhydrophobic surfaces. Adv. Colloid Interface Sci. 2011;169:80-105.

     Not in our library10.1016/j.cis.2011.08.005

185. 185.

     Fürstner R, Barthlott W, Neinhuis C, Walzel P. Wetting and self-cleaning properties of artificial superhydrophobic surfaces. Langmuir. 2005;21:956-961.

     Not in our library10.1021/la0401011

186. 186.

     Koch K, Bhushan B, Jung YC, Barthlott W. Fabrication of artificial Lotus leaves and significance of hierarchical structure for superhydrophobicity and low adhesion. Soft Matter. 2009;5(7):1386-1393.

     Not in our library10.1039/b818940d

187. 187.

     Schwab M, Noga G, Barthlott W. Bedeutung der epicuticularwachse für die pathogenabwehr am beispiel von botrytis cinerea-infektionen bei kohlrabi und erbse. Gartenbauwissenschaft. 1995;60:102-109.

     Not in our library

188. 188.

     Noga GJ, Knoche M, Wolter M, Barthlott W. Changes in leaf micro-morphology induced by surfactant application. Angew. Bot. 1987;61:521-528.

     Not in our library

189. 189.

     Wolter M, Barthlott W, Knoche M, Noga GJ. Concentration effects and regeneration of epicuticular waxes after treatment with Triton-X-100 surfactant. Angew. Bot. 1988;62(1–2):53-62.

     Not in our library

190. 190.

     Noga G, Wolter M, Barthlott W, Petry W. Quantitative evaluation of epicuticular wax alterations as induced by surfactant treatment. Angew. Botanik. 1991;65:239-252.

     Not in our library

191. 191.

     Noga G, Knoche M, Wolter M. The impact of Triton X-100 surfactant on leaf micromorphology. HortScience. 1988;23(3):808.

     Not in our library

192. 192.

     Neinhuis C, Wolter M, Barthlott W. Epicuticular wax of Brassica oleracea: changes in microstructure and ability to be contaminated of leaf surfaces after application of Triton X-100. J. Plant Dis. Prot. 1992;99:542-549.

     Not in our library

193. 193.

     Zeiger C, da Silva ICR, Mail M, Kavalenka MN, Barthlott W, Hölscher H. Microstructures of superhydrophobic plant leaves-inspiration for efficient oil spill cleanup materials. Bioinspir. Biomim. 2016;11(5):056003.

     Not in our library10.1088/1748-3190/11/5/056003

194. 194.

     Salem MA, Al-Zayadneh W, Schulze HF, Cheruth AJ. Effect of nanohydrophobic sand layer on Bermudagrass (Cynodon spp.) in urban landscaping. Urban Water J. 2013;11:167-173.

     Not in our library10.1080/1573062x.2013.768684

195. 195.

     Melskotte J-E, Brede M, Ott A, Mayser M, Barthlott W, Leder A, Brede M, Ruck B, Dopheide D. Künstliche Luft Haltende Oberflächen zur Reibungsreduktion am Schiff/artificial Air Retaining Surfaces for Drag reduction on Shiphulls. Lasermethoden in der Strömungsmesstechnik. 2012;1-6.

     Not in our library

196. 196.

     Tricinci O, Terencio T, Mazzolai B, Pugno NM, Greco F, Mattoli V. 3D micropatterned surfaces inspired by Salvinia molesta via direct laser lithography. ACS Appl. Mater. Interfaces. 2015;7(46):25560-25567.

     Not in our library10.1021/acsami.5b07722

197. 197.

     J.-E. Melskotte, M. Brede, A. Wolter, W. Barthlott, A. Leder, Schleppversuche an Künstlichen, Luft Haltenden Oberflächen zur Reibungsreduktion am Schiff, in Lasermethoden in der Strömungsmesstechnik, 21. Fachtagung, 3–5. September 2013, ed. by C.J. Kähler et al. (München, Germany, 2013) 53, 1–7

     Not in our library

198. 198.
     Superhydrophobic surfaces of the water bug Notonecta glauca: a model for friction reduction and air retention · 2011

     Not checked
199. 199.

     Federle W, Maschwitz U, Fiala B, Riederer M, Hölldobler B. Slippery ant-plants and skilful climbers: selection and protection of specific ant partners by epicuticular wax blooms in Macaranga (Euphorbiaceae). Oeco. 1997;112:217-224.

     Not in our library10.1007/s004420050303

200. 200.

     Kim P, Kreder MJ, Alvarenga J, Aizenberg J. Hierarchical or not? effect of the length scale and hierarchy of the surface roughness on omniphobicity of lubricant-infused substrates. Nano Lett. 2013;13(4):1793-1799.

     Not in our library10.1021/nl4003969

201. 201.

     Wong TS, Kang SH, Tang SK, Smythe EJ, Hatton BD, Grinthal A, Aizenberg J. Bioinspired self-repairing slippery surfaces with pressure-stable omniphobicity. Nature. 2011;477:443-447.

     Not in our library10.1038/nature10447

202. 202.

     Hamlett CAE, Shirtcliffe NJ, Pyatt FB, Newton MI, McHale G, Koch K. Passive water control at the surface of a superhydrophobic lichen. Planta. 2011;234(6):1267-1274.

     Not in our library10.1007/s00425-011-1475-z

203. 203.

     Barthlott W, Erdelen W, Rafiqpoor MD, Lanzerath D, Friele M, Dopheide D. Biodiversity and Technical Innovations: Bionics. Concept and Value in Biodiversity. Routledge Studies in Biodiversity Politics and Management. 2014;300-315.

     Not in our library

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