Superhydrophobic hierarchically structured surfaces in biology: evolution, structural principles and biomimetic applications.

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Research Cite this article: 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: 20160191. http://dx.doi.org/10.1098/rsta.2016.0191 Accepted: 3 May 2016 One contribution of 12 to a theme issue ‘Bioinspired hierarchically structured surfaces for green science’. Subject Areas: biochemistry, materials science, structural engineering, nanotechnology Keywords: bionics, lotus, Salvinia effect, Notonecta, air-retaining grids, evolution Author for correspondence: W. Barthlott e-mail: [email protected]

Superhydrophobic hierarchically structured surfaces in biology: evolution, structural principles and biomimetic applications W. Barthlott1 , M. Mail1,2 and C. Neinhuis3,4 1 Nees Institute for Biodiversity of Plants, University of Bonn,

Venusbergweg 22, Bonn 53115, Germany 2 Institute of Crop Science and Resource Conservation (INRES)-Horticultural Science, University of Bonn, Auf dem Hügel 6, Bonn 53121, Germany 3 Institute of Botany, Technische Universität Dresden, Zellescher Weg 20b, Dresden 01217, Germany 4 B CUBE Innovation Center for Molecular Bioengineering, Technische Universität Dresden, Arnoldstrasse 18, Dresden 01217, Germany WB, 0000-0002-1990-1912 A comprehensive survey of the construction principles and occurrences of superhydrophobic surfaces in plants, animals and other organisms is provided and is based on our own scanning electron microscopic examinations of almost 20 000 different species and the existing literature. Properties such as self-cleaning (lotus effect), fluid drag reduction (Salvinia effect) and the introduction of new functions (air layers as sensory systems) are described and biomimetic applications are discussed: self-cleaning is established, drag reduction becomes increasingly important, and novel air-retaining grid technology is introduced. Surprisingly, no evidence for lasting superhydrophobicity in non-biological surfaces exists (except technical materials). Phylogenetic trees indicate that superhydrophobicity evolved as a consequence of the conquest of land about 450 million years ago and may be a key innovation in the evolution of terrestrial life. The approximate 10 million extant species exhibit a stunning diversity of materials and structures, many of which are formed by self-assembly, and are solely based on a limited number of molecules. A short historical survey shows that bionics (today often called biomimetics) dates back more than 100 years. Statistical data 2016 The Author(s) Published by the Royal Society. All rights reserved.

Surfaces define the boundaries for the well-structured world of solids, and it is surfaces that define their interactions. They play crucial roles in our interaction with the environment: from the retinal membranes in our eye, which enable us to see the touch screen surface of our smart phone and the road surface we drive on with our metallic coated car. Surfaces also influence our perception of the world. We know a great deal about solids, but less about their surfaces; surfaces may have very different properties from the bulk of the solid material. It was the eminent quantum physicist Wolfgang Pauli who used to say: ‘God made solids, but surfaces were the work of devil’. Today, surface technologies are a central topic for material scientists and engineers (survey in [1]). It is estimated that the global nanocoating market will reach a value of US$ 14.2 billion by 2019 [2]. Extremely water-repellent superhydrophobic surfaces play an important role in surface technology (survey in [3]). Surfaces of living organisms can be very elaborated and complex on many hierarchical levels (figure 1); superhydrophobic plants cover millions of square kilometres of our planet (figure 2). They are the living prototypes of bionics or biomimetics. In this paper, we will demonstrate that superhydrophobicity was a key evolutionary innovation of biological species for conquering land around 450 million years ago (Ma). The probability is convincingly high that the giant dragonfly Meganeura, which lived during the carboniferous period and had ultrathin delicate wings, was superhydrophobic (figure 3). Additionally, a phylogenetic tree with the distribution of superhydrophobic plant surfaces indicates that the Ginkgo trees had hierarchically structured surfaces composed of the secondary alcohol nonacosan-10-ol as early as the Jurassic period (figures 4–6). The overwhelming diversity of plants and animals in shape, colour and function has always fascinated students and scientists. Each of the approximately 10 million existing species has optimized ‘technical’ solutions to respond to particular environmental conditions. The results of millions of years of biological evolution of millions of species are freely available to scientists that begin to look to biologically inspired solutions for technical products [6]. On the basis of our personal experience analysing around 16 000 plant species (plus several thousands of animal and technical surfaces) documented in approximately 220 000 scanning electron micrographs in our archives, we provide a survey of construction principles, occurrence and the evolution of superhydrophobic surfaces in biology. The biomimetic applicability, including a new functionality, is highlighted.

2. Mimicry of nature? Biomimetics, bionics, lotus effect and bioinspired design—history and terminological confusions A new science was born between 1800 and 1926: biotechnik [7], today abbreviated to bionik, bionics or biomimetics (survey and literature in [6]). The early works concentrated on electricity and flying machines, fundamental are the construction of the first electric battery based on the prototype of the electric ray (Torpedo torpedo) by Alessandro Volta in 1800 and the construction of aeroplanes by Otto Lilienthal in the 1890s. However, the idea of biological inspiration is considered much older: Icarus in Greek mythology or the drawings of Leonardo da Vinci. We keep forgetting: a modern Boeing or Airbus plane is based on bionic ideas. Surfaces were largely neglected by biologists and engineers and came late into play: the first bionic invention

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1. Introduction

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rsta.royalsocietypublishing.org Phil. Trans. R. Soc. A 374: 20160191

illustrate that the interest in biomimetic surfaces is much younger still. Superhydrophobicity caught the attention of scientists only after the extreme superhydrophobicity of lotus leaves was published in 1997. Regrettably, parabionic products play an increasing role in marketing. This article is part of the themed issue ‘Bioinspired hierarchically structured surfaces for green science’.

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in this field was the loop and hoop fasteners (Velcro ) by George de Mestral in Switzerland in 1958. Structural–spatial surface analysis was—as is often the case in science—a result of a new technique: the introduction of scanning electron microscopes (SEMs) in the late 1960s. Superhydrophobic hierarchically structured surfaces were first described in [8–10]. Materials scientists and engineers entered the research field only after 1997 when we [11] described the technical potential under the name the Lotus Effect . This led to a paradigm shift from flat to

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Figure 2. Plants, the green blanket of our planet, are the basis of our existence (food, timber, pharmaceuticals and oxygen production). They also provide millions of square kilometres of superhydrophobic surfaces like in the picture (Oder National Park, Germany). The reed (Phragmites australis) in the background has self-cleaning superhydrophobic surfaces, an inspiration for the biomimetic Lotus Effect products. The superhydrophobic floating fern (Salvinia natans) has led to fluid drag reducing Salvinia Effect surfaces and could be applied to the boat hull. Like in many crops (e.g. wheat, rice), superhydrophobicity is a crucial factor in our biotic environment. Source: Christoph Nowicki. (Online version in colour.)


Figure 1. Complex hierarchical surface structuring of more than five levels in the succulent Crassula columnaris. The single leaves show waxes, papillate epidermal cells and elaborated leaf margins, plus a spoon-like curvature of each leaf. The particular arrangement of the leaf along the shoot axis prevents an insolation of the whole lamina: the plant grows in its own shade in South African deserts. Crassula exhibits high complexity of multifunctional hierarchical surface sculpturing in the extreme. Some succulents are marvels of surface ‘technologies’: within closely related genera, superhydrophilic and superhydrophobic species occur; sometimes, in the same species with chemical heterogeneities to absorb dew and to repel fungal spores by self-cleaning. (Online version in colour.)

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Figure 4. (a) The gymnosperm Gingko tree (pictured a leaf of Ginkgo biloba with water droplets) exists unchanged since the Jurassic, almost like the ancestral angiosperm (b) Lotus (Nelumbo nucifera). In both plants, the superhydrophobicity is a result of a dense layer (c) of nona-10-cosanol, each tubule with a diameter of 110 nm. The phylogenetic tree (figure 6) shows that this secondary alcohol is shared by all groups of vascular plants and is responsible for superhydrophobicity. (Online version in colour.)

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Figure 5. Biomimetic technical surfaces. (a) Waxes of different composition assembled on the tips of a silicon wafer structured by lithography. This biomimetic surface is generated in a biomimetic process (self-assembly): both architecture and the fabrication process are bioinspired. (b) Dust-contaminated surface of a superhydrophobic Lotus textile is cleaned by rolling tomato ketchup drops. Source: (a) from [5]. (Online version in colour.)

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Figure 3. Dragonflies have existed for more than 450 myr. Their very thin stable and superhydrophobic wings are self-cleaning and transparent as seen in (a): In 1995, this was the first proof by a ‘living prototype’ that the Lotus Effect can be applied to transparent media even before technical prototypes existed. (b) The largest insect that ever existed is Meganeura monyi with its light-weight wings spanning around 70 cm. This ancient giant lived about 360 Ma during the wet and moist Upper Carboniferous and would not have flown without superhydrophobic wings like the modern dragonfly species. (b) Source: adapted from Brongniart [4]. (Online version in colour.)


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Amborellales, Nymphaeales, Austrobaileyales, Chloranthales, Magnoliidae. Monocots Ceratophyllales, Ranunculales, Sabiaceae, Proteales, Trochodendrales, Buxales, Gunnerales, Superasteridae, Dilleniaceae, Superrosidae

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Figure 6. The occurrence of the fatty secondary alcohol nonacosan-10-ol, responsible, e.g. for the superhydrophobicity of Lotus or Gingko, is restricted to land plants (Embryophyta), marked blue in the phylogenetic tree. Probably, this most successful chemical compound in plants evolved for hydrophobicity in the same biosynthetic pathway in the Silurian some 450 Ma. (Online version in colour.) 35 1200

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Figure 7. Number of mentions of the terms ‘lotus effect’ (black bars) and ‘superhydrophobic’ (white bars, including ‘superhydrophobicity’) in the publications listed by the ISI. The lotus effect was first coined in 1992 in our German publication [10] not listed by ISI, but was noted with the publication of Barthlott & Neinhuis [11]. Superhydrophobic was possibly first mentioned in 1986 [12], but starts to appear in significant numbers only after 2002, as a consequence of the 1997 lotus effect paper [11]. hierarchically structured technical surfaces—today’s vast number of publications (figure 7) attests to this (surveys in [13] and [3]). With our discovery of the Salvinia effect for persistent airretaining surfaces under water [14,15], additional interest in drag reduction and other functions arose. Bionics and Biomimetics are considered here to be synonyms. The field may be defined as the ‘Study and application of construction principles and systems in living organisms for the design of sustainable technical solutions’. For a detailed discussion of these terms, we refer to Barthlott et al. [6], who provide an analysis of the vast literature on the confusing definitions and historic background of bionics, biomimetics and bioinspiration between science, arts and marketing.

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Biologically inspired design (BID) or bioinspiration means ‘inspired by biology’ and is as old as mankind: from the biomorphic palaeolithic paintings in the caves of Lascaux, Daedalus and Icarus, and the Trojan Horse, to the sculpture Queens vagina in the gardens of Versailles of 2015. The impressive Cadillac tail fins of the 1960s represent a classic example of bioinspired design. We may call this category biodecoration; it does not claim to be functional. The ambiguous term bioinspiration has become part of colloquial speech and is a term commonly accepted in the fashion industry, marketing and science. Functional BID is usually called ‘bionics’ or ‘biomimetics’. The geologist Henry Shaler Williams coined ‘bionic’ as a scientific term as early as 1901—although in a different sense than it is used today. Bionik, as an abbreviation derived from ‘biologie und technik’ [7], was established as a science between 1880 and 1926. The term was re-invented by W. V. Foerster W. McCulloch and J. Steele at the military symposium ‘Bionics—living prototypes, the key to new technology’ [16] and was possibly derived from the terms biology and cybernetics. Warren McCulloch and Otto Schmitt also first published the more or less synonymous terms biomimesis and biomimetics in the same year, 1961. The superfluous and misleading term biomimicry was introduced in a thesis in 1982. Mimicry is well defined and discussed in biology since its introduction into science in 1862 and means the imitation of a biological role model (‘living prototype’ of bionics) by another species, but with a different function. An intriguing example is illustrated in figure 8: the leafhopper (Paulinia acuminata) imitates the protective coloration and surface appearance of its host plant Salvinia: a phenomenon called camouflage, a form of mimicry, to deceive predators [17]. Mimicry (in this case, camouflage) is just the opposite of what bionics is meant to be—mimicry is per definition the story of cheats and deceits. Fundamental misunderstandings exist: biomimetics is regarded as ‘mimicry of nature’ [18]. However, bionics is exclusively inspired by living nature: atomic reactors are inspired by nature too, e.g. by natural nuclear fission or the nuclear fusion in our sun, but they are neither biomimetic nor bionic or even ‘mimicry’. There is no clear separation between the terms bionics, biotechnology (coined 1919), and bioengineering (coined 1939), the latter of which often defining bionics as a subdiscipline [19]. Bionics tends to be used in reference to constructions, whereas biomimetics, possibly the more commonly used term today, tends to be used for materials. For example, a building may be referred to as bionic but its surface as biomimetic (figure 9). Bionics and biomimetics are buzzwords in marketing, like all the prefixes bio-, eco- or ‘green’. They are increasingly used for products and processes that are non-bionic. This might


Figure 8. Mimicry and parabionics. (a) The leafhopper Paulinia acuminata feeds exclusively on Salvinia and is hard to detect because of its protective coloration and surface appearance imitating its host plant: camouflage, a form of mimicry. But in convergent evolution, Paulinia also developed superhydrophobicity by analogous, but chemically different, wax crystals for its life in a semi-aquatic habitat. (b) Package of a fluorized polymer-coated (e.g. ‘Teflon ’) baking pan. The product suggests that it is bionic and refers to the Lotus Effect in detail and is named ‘Lotex-everclean’. However, it does not differ from the billions of other pans in use since the 1960s. We expect the majority of ‘bionic products’ currently on the market are in fact parabionic: Bionics is purely a marketing tool. Sources: (a) from [17] and (b) photo taken from the package bought in a department store. (Online version in colour.)

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Figure 9. A biomimetic superhydrophobic Lotus Effect coated building (Technoseum, a technical museum in Mannheim, Germany). The self-cleaning paint (STO Lotusan ) is sustainable and lasts several decades—facades must be repainted after this time normally anyway. The building itself may last in the optimal case more than a century. Time-limited adequate sustainability is a principle of living prototypes and thus an essential component of the definition of bionic/biomimetic products. Source: Photo, Technoseum, zooey braun’. (Online version in colour.)

be motivated by ‘marketing considerations’ that have intruded into these domains. This watering down of established terminology has led to mixed feelings in the scientific communities working in these fields. For obvious reasons, no reliable statistics are available. But by investigating Internet sources (the term bionic had about 22 million hits on Google in early 2016) and from personal experience gathered over two decades with the Lotus Effect , the term bionic seems to be predominantly used as a marketing tool for non-bionic products. In the specific case of lotus surfaces, it is estimated to apply to more than 80% of products on the market. Therefore, we use the term parabionic for products or processes pretending to be bionic but having neither a bionic function nor a bionic origin. Parabionics plays many important roles: from product marketing (figure 8) to fundraising in research programmes. For further reading and references concerning this chapter, we refer to [6]. Superhydrophobicity and the lotus effect are terms in general use today. The chemically based physical interaction between flat surfaces and liquids, i.e. wettability, dates back to 1805 with the introduction of Thomas Young’s equation, which limits the contact angle to about 120◦ or less on flat surfaces. Superhydrophobicity is usually defined as exhibiting a contact angle between water and solid of greater than 150◦ . For these contact angles in non-ideal rough solid surfaces the models by Wenzel [20] and Cassie & Baxter [21] used non-ideal rough solid surfaces as a basis. ‘Sculptural element’ (spatial hierarchy) is responsible; but chemical heterogeneities may also lead to superhydrophobicity [22,23]. Hierarchical surface sculpturing (not necessarily structuring: discussion in [8]) is usually the prerequisite for the phenomenon known as superhydrophobicity. The term ‘superhydrophobic’ has been used informally since 1976 [24] and first used as ‘superhydrophobic’ in a publication

This paper is based on our own—and only partially published—research and the knowledge in the vast amount of existing literature. The first author (W.B.) started to analyse biological surfaces with a focus on plants using an SEM in 1971. We analysed around 16 000 different species of plants plus about 4000 animal and technical surfaces over more than four decades and almost 220 000 SEM micrographs have been accumulated in our archives for scientific studies and are used as a source for this paper. The methods we applied for our own research were not only refined light microscopy, but also mainly SEM supported by transmission EM and atomic force microscopy (AFM). Additional techniques such as the focused ion beam technique, white light profilometry, pulse amplitude modulated fluorometry and laser confocal microscopy were also used. Barthlott & Ehler [8] summarized the early literature on plant surfaces. Waxes—the main reason for superhydrophobicity in plants—are discussed in [9,11,29]. A very large database on the surfaces of virtually all groups of vascular plants is published in six comprehensive monographs published in the transactions of the Academy of Science and Literature in Mainz [30–35]. All volumes are available as pdf files under www.lotus-salvinia.de or ResearchGate. Additional surveys of the development, functionality and biomimetic applications of superhydrophobic plant surfaces and waxes were published in [3,5,28,36–50]. Functions like self-cleaning (lotus effect) are analysed in [8,9,51,52], and in detail in [11] as well as in [3], whereas the biomimetic applicability is reviewed in [13]. Persistent air layers under water (Salvinia effect) are discussed in [14,15,53–62]. In animals, much of the existing research concentrates on insect surfaces. Specific examples can be found in [3,63–70]. The physics and biomimetic application of superhydrophobicity is summarized by [13] and in general in [3]. For the physics and wetting of surfaces, we refer to [71–73].

4. Hydrophobicity in non-biological natural surfaces In non-biological natural surfaces, we have found no evidence for stable hydrophobic or even superhydrophobic surfaces. Excluded are the synthetic man-made materials such as fluoropolymers such as polytetrafluoroethylene (PTFE) and others, which may have contact

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3. Database, literature, methods and material

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1986 by [12]. In recent years, the synonymous and superfluous term ultrahydrophobic has been used. The principle of biological hierarchically structured superhydrophobic and antiadhesive surfaces was first described in 1977 for a system of usually two to three ‘superimposed sculptural levels’ to reach mechanically stable extreme non-wettability, and low adhesion for selfcleaning abilities [8] and for drag reduction [15,25,26]. The self-cleaning, later called the ‘lotus effect’ [10,11], was discovered in the leaves of Indian cress (Tropaeolum), cabbage (Brassica), reed (Phragmites) and others. Lotus leaves (Nelumbo) were only analysed after 1985; they are still considered to be the ultimate biological role model [27,28]. The publication on The purity of sacred lotus [11] was rejected for publication by five renowned journals; the reviewers were not ready for a change in paradigms in surface technologies. In 2016, the lotus effect (Barthlott and Neinhuis [11]) had gained almost 4000 citations according to Google Scholar (compare figure 7). Indian and Chinese co-workers and students drew our attention to the fact that the remarkable properties of the lotus were mentioned in the ancient texts of the Bhagavad-Gita and in Chinese writings. The properties of the lotus were traditional knowledge in Hinduism and Buddhism; in contrast, there was a complete omission the general western knowledge at the time. The usage of the term ‘lotus effect’, closely followed by ‘superhydrophobic’, shows the remarkable increase (figure 7) starting in 1990, based on the data supplied by the Institute of Scientific Information (ISI). A general search machine such as ‘Google’ provides (May 2016) around 600 000 hits for ‘lotus effect’ and about 520 000 hits for ‘superhydrophobic’.

We restrict the definition of superhydrophobicity to stable non-wettable entire surfaces. Temporary short-lived superhydrophobicity occurs in hierarchically structured organic materials like peat: when rinsed with water, droplets roll off with high contact angles mainly caused by humic acids that cover the fibrous organic matter. After a few minutes, the surface becomes hydrophilic [76,77]: the absorption of water causes a switch from a superhydrophobic to a superhydrophilic state, an experience every gardener has undergone while preparing substrate for potting plants. We are also aware that hierarchically structured soot layers deposited by a burning wax candle are superhydrophobic, but these are derivatives of fossil organisms containing a broad spectrum of organic substances and the layers are again very unstable. A burning candle is a simple reactor to generate nanoparticles, which again leads to the point discussed in §4. One can easily observe that agglomerations of very small particles may cause superhydrophobicity such as brochosomes in grasshoppers [78]. In another context, hydrophobic particles may cause severe ecological and economic problems connected with soil water repellence in many regions of the world [79]. The structure alone may cause temporary hydrophobicity even in hydrophilic materials: water droplets may roll of a tilted plate when covered with flour (starch, an organic hydrophilic polysaccharide) like on a lotus surface. This is also a part of the secret of the well-known Lycopodium powders: the clubmossspores (diameter ca 30 μm) are weakly hydrophobic, but as powder, they exhibit remarkable functionalities. Many spores—even of aquatic organisms such as the spores of Isoetes or fungi, or myxomycetes [80] are hydrophobic for dispersal purpose. While even the prokaryotic bacteria are able to synthesize waxes and related substances [81], it is no surprise that bacterial spores like in Bacillus and Clostridium are hydrophobic [82,83]. Powdery agglomerations of hydrophobic particles may exhibit instable superhydrophobic properties like flour. However, true stable hydrophobicity in surfaces has only evolved in living organisms.

(a) Chemistry and hydrophobicity Surfaces of plants and animals—with the exception of primary aquatic members such as molluscs or anthozoa—are composed of mechanically and chemically very stable polymers. In higher plants, the polymer cutin (omegahydroxyl-fatty acids and their derivatives) is the most important, whereas cutan (a hydrocarbon polymer) is less prominent and possibly absent in some groups [84–86]. The vast majority of animals are arthropods such as insects,

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5. Superhydrophobicity in biological surfaces: construction principles

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angles with water up to 120◦ on flat surfaces. Literature on the wettability of natural occurring non-biological surfaces is surprisingly scarce. Flat non-biological materials that are hydrophobic can be found; they have contact angles of around 100◦ , e.g. in layered graphite crystals, in pyrophyllite, in sulfur or its derivatives like pyrite, molybdenum disulfide, and oxides of rare earths [74]. If these surfaces become rough, they reach higher contact angles and may reach superhydrophobicity under artificial conditions: for example, diamond films [75] or phosphates of rare earths like lanthanum [74], in which nanorods are the morphological basis. Hierarchically structured inorganic surfaces of these or similar materials may occur in nature in statu nascendi and are often associated with volcanic activities (e.g. sublimate sulfur) or on fresh fractured surfaces of a weakly hydrophobic bulk material and may have higher contact angles owing to hierarchical structuring, but this is an unstable condition. When water is applied to various ‘powders’, agglomerations of very small particles often show short-term superhydrophobic behaviour and even without being hydrophobic, the droplets roll off. However, this is an unstable condition (see §5). To conclude, there is no evidence for persistent superhydrophobic materials in nature, with the exception of biological surfaces. It is a physical phenomenon based on the properties of chemically and structurally complex surfaces; restricted to and evolved in living organisms during the last 450 million years (Myr) of life in terrestrial habitats.

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Figure 11. Fungal hyphae are absorbing hydrophilic structures growing in wet substrates with chitinose cell walls, but aerial hyphae can become superhydrophobic like in the conidiophores (a) of Aspergillus and (b) the grey mould (Botrytis).

spiders and crustaceans. Their exoskeleton is composed of chitin, a long-chain polymer of an N-acetylglucosamine, a derivate of glucose. Chitin is also the main cell wall constituent of fungi and occurs in several other groups of organisms (e.g. molluscs) and even in algae [87]. The second relevant groups are terrestrial vertebrates such as mammals, reptiles and birds. Their skins, hairs, nails and feathers are basically formed by the fibrous structural protein keratin. All these materials are not very hydrophobic. The contact angle of chitin measured by [66] reached 100◦ , but a pretreatment to remove molecular wax films was not done. One crucial factor is sometimes overlooked: surfaces of land-living organisms are probably all covered with fatty or waxy layers. They may often occur only as molecular films, but can also be found in crusts up to 1 cm thick in plants. The most important chemical group in plants is ‘waxes’ of very differing composition, mostly occurring in mixtures of different compounds. They are able to form crystals and thus contribute to the hierarchical sculpturing of the surface (figures 10–12). ‘Waxes’ can be removed by treating the surface with organic solvents (cutin is not soluble); this is also a good test to prove their presence. A still unidentified chemistry is responsible for the large nonsoluble rodlets covering the seeds of Scleletium (figure 13) [88]. Another unresolved phenomenon is the arrangement of wax platelets around stomata in certain monocotyledons, which brings to mind magnetic field lines (figure 12). A survey of the chemistry and morphology of waxes among plants is provided in [29,89–91], and waxy compounds are even identified from fossilized species of Azolla [92]. The important compound nonacosan-10-ol was synthesized by Dommisse et al. [93]; wax chemistry and crystallinity is discussed in more detail under Evolution (§8). Crystalline waxes occur in some insects such as mealybugs, beetles, grasshoppers, dragonflies and butterflies [65]. Fatty or oily compounds are produced on the keratinous skin of most

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Figure 10. Superhydrophobicity in plants is usually the result of wax crystals formed by self-assembly. (a) On the lower side of a leaf of Strelitzia reginae, (b) on a fruit of Benicasa hispida, which gives an impression that the polymer cuticle is also covered by an ultrathin wax film, possibly present in almost all plant and insect surfaces. Source: (a) and (b) from [29].

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Figure 13. (a) A seed coat surface of Sceletium tortuosum, a South African succulent plant. Sculptures on three hierarchical levels are visible: very small grain-like structures, large rodlets, the shape of the cells form the last level. The chemical nature of the rodlets is not known. (b) Leaf surface of a tropical tree (Virola surinamensis) exhibiting complex hierarchical structuring and chemical heterogeneities on four levels: superhydrophobic wax crystals, convex curvature of the epidermal cells and a superimposed large star-shaped trichome with a flat surface, which may exhibit a chemical heterogeneity for water absorption functions. Sources: (a) from [88] and (b) from [29].

vertebrates or they are produced by specific glands (e.g. uropygial gland in birds) and spread over the whole surface to induce superhydrophobicity.

(b) Hierarchical structuring: the key to superhydrophobicity in biological surfaces In reference to the foundational papers and principles previously introduced in §3, the basis for superhydrophobicity is surface structuring. In the Cassie state, water is only in contact with the tips of the structural elements, thus causing a chemical heterogeneity of the ‘surface’. Living organisms have optimized this principle over 450 Myr of evolution, resulting in an astonishing diversity of complex hierarchically structured surfaces. Hierarchical structures cause an extreme reduction of surface contact area (figure 14) and prove to be mechanically more stable [11] under dynamic conditions than simple structured surfaces. This is the principle of superimposed hierarchical sculptures [8,51,52]. Contact angles approaching almost 180◦ are realized in lotus leaves [28,94].

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Figure 12. A challenge for physicists: the highly peculiar arrangement of wax platelets around stomata in certain monocotyledons like the lily of the valley (Convallaria majalis) brings to mind magnetic field lines, but the physical cause is still unknown. Source: Frölich & Barthlott [32].

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Figure 14. A schematic of the simple relation between a hydrophobic material, simple and double hierarchical structuring, water and contaminating particle. The small rodlets represent a diameter of 0.15 μm and a spacing of 0.45 μm. The contact angles between ca. 100◦ and 175◦ are indicated by the water droplets (left), the result of hierarchical structures is extreme superhydrophobicity. The contact area of the contaminating particle is reduced dramatically (right): in the ideal case between the flat surface and particle, it should be 100%, with one hierarchical level 6% and with two hierarchical levels about 0.7%. The lower schematic represents the lotus effect, but in a real lotus leaf the rodlets and cells are irregular and the contact area can become less than 0.09%. Source: Redrawn from Barthlott & Neinhuis in various publications. (Online version in colour.) (a)

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Figure 15. Cuticular fold on plant surfaces. The polymer cuticle can form regular patterns by an overproduction of cutin. (a) On a flower surface of Anthemis, (b) exhibits the cuticular folding principle above the flat cellulosic cell wall in Aztekium in a section. The cuticular fold pattern is partially removed. Wax crystals and cuticular folds exclude each other on the same surface: there will only be one group of structures within one hierarchical level. Thus, folds are typical for many flower surfaces, because insect pollinators do not like to walk on slippery waxy surfaces. Source: (a,b) from [52]. Levels of hierarchical sculpturing of biological surfaces: First structural level. Flat surfaces defined by their hydrophilic or hydrophobic chemistry on the scale of the resolution of an SEM. Flat is a relative category that depends on the scale. Here, we define such surfaces as flat that feature structures of less than 10 nm height. Flat surfaces are rarely found in plants and animals, e.g. the leaves of rubber figs (Ficus elastica). Second structural level. Cell surfaces covered with structures up to 20 μm. Structures at this level on plants are usually formed by epicuticular wax crystals (figures 12 and 13) which may exhibit a large spectrum of shapes such as rodlets, platelets or tubules. But they may exceed 200 μm in height (e.g. Strelitzia, Copernicia, Benincasa: figure 10). Another common type of the second-level structures are cuticular fold (figure 15). Functionally, a superimposition of fold and wax crystals are not necessary: structuring on a specific level is performed by one group of elements, which seems to be a basic law. The data of

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Figure 17. Almost all insects that cannot actively clean their wings have superhydrophobic surfaces with self-cleaning properties. Particularly intriguing are the multifunctional scales (b) of butterflies like in Lysandra which fulfil several functions. Their nanostructures generate the bright structural colour (a) of the blue iridescent Morpho menelaus. Source: (a) from Wikipedia and (b) from [66]. (Online version in colour.)

thousands of plant surfaces constitute the rule, that e.g. wax crystals and cuticular fold exclude each other. In insects, these structures are often formed by the chitin layer, e.g. as bristles (figure 16), or scales on butterfly wings (figure 17) or by microvilli (figure 16), in vertebrates by keratinous material (Gecko foot, rami of the first order in birds). Third structural level. Unicellular (multicellular in certain hair types in plants) structures usually caused by particular shapes of the outer cell wall which may vary from convex to papillose cells and ultimately to hairs (figure 13b), which may be unicellular or multicellular (for a terminology, see [8,14]; dimensions range from about 2 μm to several centimetres, i.e. in trichomes (hairs). Structures of the second level may be superimposed to structures of the third level (figure 13b). Fourth structural level. Multicellular structures caused by specific arrangement patterns of groups of epidermal cells (figure 18a). There is a wide variety of possibilities for this group of structuring. Fifth structural level. Macroscopically visible curvatures of the whole organ surface, often to separate functional compartments on the surface of an organism (figures 1 and 18b,c). Hierarchical structuring is defined as having a combination of at least two levels, in the simplest case level one and two, which is sufficient to create a superhydrophobic surface. For a persistent superhydrophobicity, a combination of levels one to three is required, like in the example of the lotus (figures 14 and 19). On the complex surface of e.g. Crassula columnaris (figure 1), one can discern more than five levels.

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Figure 16. Bristles and microvilli are present in these semi-aquatic insects. (a) An eye of Clunio marinus. (b) The microvillicovered forewing surface of the backswimmer Notonecta with two large bristles (setae). The upper bristle reveals at its base a part of the bulb-like mechanoreceptor responsible for the sensing (figure 28) of the dynamic air–water interface.

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Figure 19. Biological model and biomimetic copy: lotus (Nelumbo) surface (a) and in the same magnification a electrochemically structured copper foil (Bolta) (b), the structures are a product of self-assembly processes. In cases like this, technical prototypes can quickly and easily be fabricated. Source: (a,b) from publications by Fürstner, Neinhuis & Barthlott.

Air-retention under water requires particular conditions—perhaps the most complex biological surfaces are evolved to retain persistent air layers under water. Air layers per se are present in all superhydrophobic surfaces submersed in water, but in the case of the lotus they are thin (around 15 μm) and not very stable. In organisms that depend on the air layer for different ecological reasons (respiration, drag reduction, sensing), these layers have to be thick and stable. Air layers with a thickness up to 3.5 mm and more (figure 20) can be found in nature. Salvinia evolved the most efficient complex and sophisticated surfaces we have observed (figures 21 and 22). Thus, we named the air-retention syndrome of four essential criteria Salvinia effect [14]. A fifth nonessential criterion (chemical heterogeneities of anchor cells) occurs in Salvinia molesta and closely related species [15]. The physical dependence has been analysed by [55,96]. The four essential criteria for the Salvinia effect are listed below, the additional non-essential criterion is added: 1. Hydrophobic chemistry. The material must be hydrophobic. Smaller hierarchical sculptures (wax crystals or microvilli) support the maintenance of the superhydrophobicity caused by the filaments (2) under dynamic conditions. 2. Filaments, hairs or bristles determine the distance between the solid and the liquid and thus provide space for the amount of air to be enclosed. Their lengths range from micrometre to the centimetre dimension, preferably between 1 and 5 mm. 3. Undercuts of the filaments, hairs or bristles. Undercuts or often simple inclinations are necessary to better retain the air and they are the precondition for the elasticity [57].

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Figure 18. Compartmentation of surfaces generating small functional units for air-retention: (a) in microscopic dimension in the seed of Eschscholzia californica for temporary floating. A particularly refined compartmentation system exhibits Salvina cucullata: in microscopic dimension, the superhydrophobic leaf is covered by trichomes distantly resembling figure 21, but each leaf with a diameter of ca. 1.5 cm forms a hood-like compartment (b) and submersed under water (c) it holds a very stable large air bubble. Source: (a) from [52]. (Online version in colour.)

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Figure 21. (a) A leaf of Salvinia molesta with a water droplet, the egg-beater hairs can be seen even at this low magnification, as well as the elaborate margin for the edge effect to prevent the escape of the air layer under water. Each leaf thus forms a compartment (compare figure 18). (c,d) The schematic explains the function of the elastic undercuts of the superhydrophobic hairs, the anchor cells on their tips pin the air–water interface. The chemical heterogeneities of the hydrophilic anchor cells on the tip of each elastic egg-beater-shaped superhydrophobic hair in S. molesta are marked in red. The hairs deform under dynamic changing pressure conditions ((c) versus (d)) and the pins stabilize the air–water interface. Sources: (a) from [95] and (b) J. Bertling, Fraunhofer Institute Umsicht. (Online version in colour.)

4. Elasticity of the hairs or filaments supporting the air–water interface plays a crucial role for the stability of the air layers. In the case of increasing pressure, the air layer becomes compressed, and thus the interface is pressed towards the surface and water would penetrate between the structures. Elasticity allows a flexible movement [57]. Air layers in Salvinia show a higher stability than expected just from the hair layer elasticity [59], most likely because a significant part of the energy is absorbed like in a spring in the compression of the air layer. The refined adhesion technique used by [97] may confirm this.

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Figure 20. Spiders are land-living—but the South American Fishing Spider (Ancylometes bogotensis) hunts fish. It is superhydrophobic and coated by a silvery air layer (a) under water; the layer is maintained by complex hierarchical indumentum of hairs (b), which may also function as mechanoreceptors like in Notonecta (figure 28). (Online version in colour.)

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Figure 23. Schematic of the physical base for fluid drag reduction by air-retaining surfaces: (a) velocity profile of water on a solid surface and (b) velocity profile of water on an air-retaining surface. Owing to the 55 times lower viscosity of air compared with that of water, the air layer serves as a slip agent. (Online version in colour.)

5. Chemical heterogeneities (Salvinia paradox) is an additional refined mechanism to stabilize the air–water interface under dynamic conditions [15]. In contrast to the otherwise superhydrophobic surface (nanoscopic wax crystals), the tips (the four anchor cells) of the elastic egg-beater-shaped multicellular hairs of S. molesta [53] are hydrophilic. This causes a stable spatially restricted connection (pinning) of the interface between the solid and liquid (figures 21, 22 and 23). The pinning prevents the loss of air under negative pressures by reducing the formation of large air bubbles. The adhesion forces in trichomes with chemical heterogeneities are doubled [15]. We observed an additional sophisticated mechanism that enhances the pinning effect: the hydrophilic anchor cells show a slight hygroscopic movement in contact with water; this optimizes contact area and angles, allowing for the chemical heterogeneities to maximize air layer stabilization. Air-retaining grids. Grid-like-structures, introduced as a technical biomimetic solution in §9, are extremely scarce in biological surfaces owing to developmental reasons. The only biological role model seems to be the mite Hydrozetes [98], where the grid fulfils the function of a plastron. Structures similar to grid-like structures occur in Aeginetia indica (figure 24) and in many other miniature seeds, like in orchids [99] and Orobanchaeae [52]. True biological grids are embedded in plasmatic covers, e.g. in the mineralized skeletons of diatoms or radiolaria. Spectacular grids occur in certain Phallus-related fungi, like the Veiled Lady (Dictyophora indusiata) or in the aquatic Lace Plant (Aponogeton madagascariensis), but their functions are unrelated to air retention.

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Figure 22. Salvinia molesta leaf under water (a) with a trapped air layer and (b) SEM of the elaborate leaf edge. (Online version in colour.)

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6. Biological functions Biological surfaces are always multifunctional (overviews in [26,50,51,100]). The functions are always sustainably persistent and are maintained as long as the function of the surface is essential. Aspects of mechanical stabilization (cuticles in plants and animals) are connected with the interactions of gas (air exchange), loss or uptake of water, coloration (e.g. butterflies, figure 17), adhesion (e.g. geckos), non-adhesion (e.g. lotus) or water-repellency per se, often with the physical constraint to maintain an air layer submersed in water (e.g. Notonecta). Superhydrophobicity plays many functional roles, which may coincide with intriguing interactions. 1. Water repellency per se to avoid wetting mainly for mechanical (weight) reasons. Thin laminar organs become too heavy when wetted, e.g. the leaves of lotus or the Mexican Tree Fern (figure 25) with their thin stalks would be mechanically unstable when becoming wet. Water repellency is important for insects with thin membranous wings (figure 26 and 17; compare [66]), even in Carboniferous giant dragonflies Meganeura (figure 3) or Clunio (figure 16) living in the oceanic surf regions. Aquatic submersed flowering plants are always hydrophilic, but when shoots rise above the water level, they may become superhydrophobic (e.g. Myriophyllum aquaticum, rice, reed). This can be observed within a single leaf: the submerged leaf bases of Tillandsia

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Compartmentation. Independent of the criteria listed above is compartmentation—defined as a fragmentation of the air-retaining surfaces into smaller units (figures 18 and 24). Compartmentation of the air layer plays a crucial role: small compartments are more stable under dynamic conditions. Vertically surfaces inserted in water (as is the case in ship hulls) would not be able to maintain the air layer within the increasing hydrostatic pressure without compartments. Thus, we find many examples of biological surface compartmentation; the dimensions vary from the microscopic in Eschscholtzia or Aeginetia seeds (figures 18a and 24) to the much larger units the entire leaf of Salvinia cucullata (figure 18b,c). The margins of the compartments show an elaborated architecture [53], a particular ‘edge effect’ preventing the escape of air [60]. These biological construction details provide important information for biomimetic technical surfaces (§9). The biological diversity of hierarchical structured surfaces is almost endless and does not fit in an ultimate classification system: figure 1 exhibits such an overly complex system of leaves, which when investigated at the SEM dimension-scale, are all equipped with structures up to more than five levels and particular elaborate margins for their multifunctionality.


Figure 24. The miniature seeds of Aeginetia indica are wind-dispersed and superhydrophobic: upon landing on ground, they float with the first rain. (a) Their complex thin seed coat is stabilized by net-like cellulose thickenings in the wall, covered by a molecular wax film and fragmented into miniature compartments. Immersed in water (b) these compartments hold air bubbles. Fragmentation and compartmentation of surfaces play a crucial role in stabilizing air layers under water. Source: (a) from [51].

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Figure 26. (a) Contaminating dust particle on an insect wing (Cicada orni) indicating the reduced contact area of the particle, which reminds one of a fakir on his bed of nails. (b) A rolling droplet removes dirt particles from a lotus surface. Source: (a,b) from [11].

rauhii, a ‘tank bromeliad’, are hydrophilic, whereas the aerial parts are superhydrophobic. The submersed leaves of the floating fern Salvinia are hydrophilic, the leaf surfaces exposed to the air superhydrophobic. Alternatively, floating leaves of Marsilea are hydrophilic, whereas those raised above the water surface are hydrophobic [101]. Terrestrial mammals and birds, which temporarily live on water or dive, are—in contrast to amphibians and reptiles—usually superhydrophobic: ducks and geese, shrews and others. These organisms remain dry, like the fishing spider (figure 20) and some other arthropods. In almost all birds, hydrophobicity is an essential prerequisite to maintaining flight in rain or mist (see §7). 2. Reduction of adhesion to trap insects: wax surfaces in carnivorous plants are used to capture prey (e.g. Sarracenia and Nepenthes) or in flowers to temporarily trap pollinators (e.g. Ceropegia, Aristolochia) or to avoid unwanted nectar thieves (e.g. Fritillaria imperialis and Lapageria rosea). Superhydrophobicity is not the primary function in anti-adhesive surfaces, but only a result of a coating of nanoscopic wax crystals. 3. Reduction of adhesion to avoid contamination: the well-known example of the lotus-effect [11] enables plants to be cleaned from any kind of contaminating particle by raindrops (figures 14 and 26). Biologically, such surfaces in plants and animals should be primarily seen as a defence mechanism against fungal spores (figure 27) and colonization with other microorganisms. 4. Maintenance of air layers under water. Basically, air layers may fulfil five different functions, which are often combined and multifunctional: Air layers for buoyancy. Non-persistent air layers for temporary buoyancy in water play an often underestimated role in very small seeds, insect eggs and spores which may fall or are dispersed

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Figure 25. (a) The Mexican tree fern Cibotium schiedei has delicate pinnate leaves up to 2 m long. In heavy tropical rain, they are mechanically protected from heavy water loads by their (b) superhydrophobic wax cover, but the surface has millions of stomata, openings for intense gas exchange. Source: (a,b) from [29].

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into water, but after a short period (often only minutes) they change into a hydrophilic state to absorb water for their function. Examples are very common in the so-called dust seeds, which are dispersed by wind (figure 24). The hierarchically structured surface results in high Reynold numbers, enabling the seed to fly/float in the air over a longer period of time—they are usually superhydrophobic, but when they land on the ground they gradually lose their hydrophobic surfaces (Drosera) to take up water for germination. A full range of these structures is described and illustrated by orchids in [99]. Buoyancy certainly also plays a critical role in certain insects such as Clunio or some Collembola that live on water surfaces (e.g. Podura aquatica). Air layers for thermal isolation. In semi-aquatic homoeothermic vertebrates (birds and mammals), a persistent air layer may play a role as an isolation device for the survival of warm-blooded animals in cold water like in the water shrew Neomys fodiens [103]. Air layers for gas exchange (respiration) in primarily non-aquatic organisms living temporarily or permanently under water. This so-called plastron function for respiration—and sometimes buoyancy—is well known from terrestrial insects that secondarily live under water (e.g. Aphelocheirus aestivalis [54] and spiders (Argyroneta)) and need air for respiration. The remarkable undercut, grid-like structure in the mite Hydrozetes [98] serves as plastron. Springtails (Collembola) even withstand considerable external pressure without losing the ability to restore the plastron [104]. This is probably also the biological function of the Salvinia leaf and other plant surfaces: this extremely fast-growing pest plant (they can double their biomass within 4 days) maintain their function when temporarily pushed under water. Air layers for fluid drag reduction, there are several well-known examples. The mechanism is fairly simple: the air layer serves as a slip agent. On solid surfaces, the velocity of the water directly at the surface is zero owing to the friction between the water molecules and the surface (figure 23a). If an air layer is mounted between the water and the solid surface, then the water streams over the air layer. The viscosity of air compared with water is 55 times lower, because of this the air layer serves as a slip agent, and the drag is reduced [105]. As the air layer must be supported by solid structures, the value of drag reduction highly depends on the contact area of these structures with the water and their properties. Air layers as slip agents have evolved in many insects. We have focused on the forewings (elytra) of backswimmers (Notonecta) as a biological role model for biomimetic fluid drag reducing air-retaining surfaces (figure 23). Notonecta uses its air layer for fluid drag deduction, as well as other functions (below). A double structure of hairs and microvilli (figure 16b; [69]) is responsible for the air retention [54,106]. In other arthropods (e.g. the fishing spider Ancylometes), the air layer most likely serves as a slip agent. In addition to insects, several other aquatic and semi-aquatic


Figure 27. The biological–ecological role of the lotus effect in plants is mostly the defence against pathogens trying to colonize their surfaces: (a) the germinating spore of the corn mildew Blumeria graminis has obvious difficulties to establish itself on the superhydrophobic grass leaf. To overcome the superhydrophobic barrier in agriculture worldwide, the application of pesticides is possible only by adding surfactants. (b) Shows the leaf area after evaporation of the surfactant droplet in which the wax cover has turned from a hydrophobic to a hydrophilic behaviour resulting in an accumulation of contaminating particles and fungal spores. This is an overlooked or ignored effect in agricultural industries. Source: (b) from [102].

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Figure 28. An air layer retained under water results in the silvery reflecting forewings of the backswimmer Notonecta. (a) The air layer has the benefit of fluid drag reduction. The superhydrophobic structural base (b) is a hierarchic dense cover of small microvilli and two types of long elastic inclined bristles. (c) The bristles have mechanoreceptors at their base (figure 16b) which localize prey by the displacement of the highly sensitive air–water interface: a novel sensory system for biomimetic underwater applications. Source: (b) from [55]. (Online version in colour.)

species are able to keep air layers under water, and some of them (ducks, kingfishers, etc.) might also profit from the drag reduction capability of the air layer. It should be added that other surface modifications not involving an air layer have evolved for drag reduction, primarily in aquatic organisms: the riblets of sharks as well as the compliant skin of dolphins [107]. The elegant controlled release of air trapped inside the plumage of penguins immediately before jumping out of the water is a completely different mechanism [108]. Air layers for sensory functions. In the backswimmer Notonecta, the forewings (elytra) exposed to the water (figure 28a) are covered by an air layer to reduce drag [106]. The air layer is stabilized by up to 250 curved bristles per square millimetre (figure 28b) which have an additional sensory function. Notonecta uses the compressibility of the air layer and the flexible air–water interface touching the elastic bristles as a ‘membrane’ to detect pressure changes: the bristles displacement is recognized by mechanosensitive cells. The backswimmer uses this sophisticated sensory system for pray detection as it hunts small fish. Notonecta sensors will probably have many biomimetic technical applications. Air layers for camouflage. In Notonecta, the air layer may have an additional and unrelated communication function: there is evidence that it camouflages the ‘silvery’ reflecting insect (figure 28a) as seen from the perspective of a fish against the ‘silvery’ reflecting water surface. The elastic air layer may even camouflage Notonecta from sensory detection by its prey: it could prevent location detection by sonar, which may have an important future technical application (see §9).

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Superhydrophobicity evolved with the conquest of land some 450 Ma. Aquatic organisms are hydrophilic, but may produce superhydrophobic surfaces when organs or structures (mainly dispersal units: seeds, eggs or spores; flowers) emerge from water. The particular case of ‘superhydrophobic’ spores in prokaryotic bacteria is discussed in §5. For the non-biologist, it should be added that hydrophobicity is usually restricted to particular organs or even portions of them: in leaves, there can be a fundamental difference between the upper and lower side of the leaf and the stem of the same plant may also be functionally different. The water-absorbing roots are always hydrophilic. To illustrate this phenomenon: when systematically analysing wax covers for phylogenetic reasons, we never found superhydrophobic surfaces in the epiphytic and thus hydrophilic leaves of hundreds of Orchid species [32]. It took us decades to discover superhydrophobicity in some fruits and even in some seeds [99].

(a) Plants Aquatic submersed plants are all hydrophilic and therefore wettable; they have flat surfaces and are colonized by biofilms. All terrestrial groups of plants have evolved superhydrophobic surfaces (figures 6 and 29). Primarily aquatic organisms like algae are hydrophilic, but may exhibit complex hierarchically structured surfaces (e.g. Coccolithophorida). Plant groups that ecologically depend on the cuticular absorption of water (‘ectohydric’ plants) predominantly have hydrophilic surfaces, but may be partially non-wettable for functional reasons (figure 30). A comprehensive overview of wax crystals with respect to systematic affinities covering all vascular plants is given in [110]. Mosses. Virtually, all species are ectohydric, but in Bryophyta (e.g. Polytrichales, Andreaea, Saelania) and Marchantiophyta (e.g. Plagiochasma rupestre), there are a few species that are superhydrophobic. In bryophytes, the reproductive structures of the diploid sporophyte, specifically the peristome, may exhibit epicuticular wax crystals (figure 30). No superhydrophobicity has been detected in hornworts (Anthocerotophyta). Ferns and allies. Primarily, the ectohydric Sellaginales and virtually all species of Lycopodiales have non-structured wettable surfaces. One of the few exceptions is Huperzia saururus. In addition, the spores of aquatic representatives like Isoetes sometimes exhibit wax-like sculptures on the surfaces. True ferns (monilophytes) are fully equipped with the full range of superhydrophobic wax coatings (figure 25) in a surprisingly high chemical diversity including crystalline flavonoids and triterpenoids (surveys in [9,111]).

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7. Distribution of superhydrophobicity in organisms

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Multifunctionality, like in the backswimmer Notonecta, probably occurs in other species, e.g. the underwater fishing spider Ancylometes bogotensis (figure 20). The spider has an indumentum of thousands of hairs, which in spiders generally fulfil mechanosensory functions [109]. It is possible that they show all the functions mentioned for Notonecta. There is an additional broad range of biological surface sculpturing functions which are not linked to superhydrophobicity: such as structural coloration, friction, adhesion or abrasion. Air bubbles under water fulfil a very peculiar function in the flowers of the aquatic or wetland plants of the family Menyanthaceae (Nymphoides, Liparophyllum, Villarisia, Menyanthes), like in the pantropical white ‘water snowflake’ Nymphoides indica or the Australian yellow N. crenata and N. geminata. The star-shaped flowers (1–3 cm diameter) are covered by hairs like a spider or have elaborate fringes, they open above the water surface. When pulled under the water, the flower entraps a large air bubble and rapidly closes like a bud. When it again appears above the water, it opens instantly; both movements are very fast and jumpy. This is an elegant mechanism to maintain the function of the flower by the criteria of the Salvinia Effect with an additional peculiarity: the petals behave like flexible solids, the movement is caused by the dynamic forces of the solid–air–water interfaces on elastic thin plates.

Amborellales, Nymphaeales, Austrobaileyales, Chloranthales, Magnoliidae. Monocots Ceratophyllales, Ranunculales, Sabiaceae, Proteales, Trochodendrales, Buxales, Gunnerales, Superasteridae, Dilleniaceae, Superrosidae

Acrogymnospermae

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Anthocerotophyta.

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Bryophyta,

Barthlott, Mail & Neinhuis; 2016

Figure 29. A phylogenetic tree of green plants from algae (left) to highly evolved flowering plants (right). On the basis of our own examination of around 16 000 species, all groups exhibiting superhydrophobic representatives are marked light blue. The analysis confirms that superhydrophobicity has evolved in earliest branching clades dating back into the Late Ordovician or Silurian some 430–500 Ma. This indicates that superhydrophobicity may be a key adaptation for the conquest of land. (Online version in colour.)

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Figure 30. Lower plants such as mosses have no water-conducting elements and depend on the surface absorption of water. However, the structures exposed to the wind to disperse the spores are often superhydrophobic, like in the mechanically complex diaphragm shutter-like peristome (a) of Funaria hygrometrica, a single tooth (b) reveals a nanoscopic wax coating.

Gymnosperms. Superhydrophobicity caused by crystalline wax coatings, usually based on the fatty alcohol nonacosan-10-ol (figures 4, 6 and 31), is very common in all orders and families of the gymnosperms. The relatively thick cuticles may be a functional constraint, which could explain that a complex hierarchical structuring (level 3–4) is absent in most species. Among the few exceptions is Taxus with papillose structures formed by the cuticle. Angiosperms. The evolutionary youngest and most speciose (ca 340 000 species) lineage of land plants exhibits the full range of superhydrophobic hierarchically structured surfaces in all major

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groups with at least one representative that has super-hydrophobic surfaces based on epicuticular wax crystals

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Chlorophyta, Chlorokybophyceae, Mesostigmatophyceae, Charophyceae, Coleochaetophyceae, Zygnematophyceae,

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(b) Animals As in plants, superhydrophobic surfaces have evolved in all land-living major clades in the animal kingdom. The diversity of structures and functions covers all interactions (§6), not only water repellency for respiration, but also for increasing complex sensory systems. Arthropods. The most speciose group of animals with predicted 4 million different species living on our planet. Their massive exoskeleton consists of chitin, which is hydrophilic in the primarily aquatic groups like the crustaceans. Spiders are usually covered by an indumentum of hydrophobic hairs (figure 20) which fulfil sensory functions (survey in [109]). In particular, spiders living temporarily in water have developed extreme superhydrophobicity like Argyroneta argo or the water-hunting spider Ancylometes. Insects—the largest group—are required to be water-repellent because of their respiration mechanism. The chitin may be covered by a molecular wax film, and contact angles of about 100◦ have been measured [66]. Massive crystalline wax protrusions can occur. Insect surfaces are often hierarchically sculptured by bristles and microvilli [69] and are thus superhydrophobic. The literature on insect surfaces is vast (surveys in [63–70]). The delicate thin wings of insects are usually superhydrophobic (survey in [66]). Specifically, the multifunctionality of the complex structuring of the microscopic scales in butterflies (figure 17) is well researched, the functions reaching from self-cleaning to the properties in iridescence. In the Namib Black beetles, the chemically heterogeneous waxy surface of the elytra with hydrophilic spots fulfils a rather complex fog harvesting function [112,113].

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groups. However, presence or absence may differ even among closely related taxa, even two species of one genus. Surface wettability differs dramatically in the particular organ surfaces, depending on the functional constraints: completely wettable plants may have superhydrophobic seeds and vice versa. Aquatic submersed angiosperms have non-hierarchical wettable surfaces (e.g. Zosteraceae) usually colonized by biofilms, but may become superhydrophobic within hours in flower producing shoots emerging above the water surface (e.g. Myriophyllum). Epiphytic plants—e.g. the large families of Orchidaceae and Bromeliaceae—depend on foliar uptake of water and are hydrophilic as a basic rule.


Figure 31. The giant leaves of the conifer Welwitschia mirabilis exhibit square metres of superhydrophobic surfaces covered by nonacosan-10-ol crystals. Each plant has two leaves which continuously grow from their base over more than 100 years: an ideal organism to study the limited long-term stability of superhydrophobicity. (Online version in colour.)

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Collembola have recently been investigated in detail. As springtails respire through their body surface, it is essential to keep this surface dry and clean, as otherwise they risk suffocation. The remarkable surfaces (figure 32) consist of a primary structure of rhombical or hexagonally arranged granules, as well as bristles. Additional secondary granules may exist in several species. The variation of these patterns seems to be an adaptation to the habitat [114]. The chemical composition, however, is similar to other arthropods [104]. In addition to a perfect superhydrophobicity, the collembola surfaces also repel a broad range of organic solvents and may resist pressures up to six bar [115]. The most surprising fact still is that the superhydrophobicity is purely structurally determined and independent of the chemical basis [115,116]. For this reason, the highly complex surface topography exhibiting overhanging surface structures with undercuts evolved. First attempts have been made to transfer these properties to technical materials [117,118]. Some aquatic insects have wettable surfaces such as diving beetles (Dytiscus) or giant water bugs (Belastomidae); however, the tracheal endings are superhydrophobic to ensure the uptake of air at the water surface. Many aquatic insects hold an air layer that functions as a plastron for gas exchange [98,119–121]: for example Aphelocheirus aestivalis [54], which spends all its life in an air pocket on river bottoms. Insects living on the water surface are almost all superhydrophilic and may exhibit a most peculiar mechanism for moving at high speed on the interface between water and air [122,123]. The best analysed example is the very complex mechanism of the water striders (Gerridae) [122,124]. Some superhydrophobic species such as Halobates even live in the open ocean far away from continents [125]. As a final example of a sophisticated multifunctional superhydrophobic surface in insects, we present some unpublished results on the backswimmer Notonecta (figures 16b and 28). The insect saccadically moves at high speed under the water surface. The forewings (elytra) exposed to the water are covered in a hierarchical system by a fine indumentum of microvilli overlapped by two types of large, curved and elastic bristles (setae) [54]. Approximately 250 setae per square millimetre retain a persistent air layer and reduce the fluid drag. The recent work on the related backswimmer Anisops [121] indicates that the superhydrophobic surface may have an additional plastron function. Additionally, the Notonecta air layer serves as a sensory device and may camouflage the insect. Reptiles. Geckos with their adhesive pads show superhydrophobicity resulting from hierarchical structures of microsetae split into hundreds of nanoscale spatula [126,127] of up to 160◦ [128]. The adhesion forces to water droplets are very high, owing to the large contact area with the water droplet. Some Geckos also exhibit superhydrophobic skins [129]. Spinner et al. [130] discovered superhydrophobic abilities in snake skin (e.g. in the Gaboon viper).


Figure 32. Springtails (Collembola) respire through their body surface. (a) The (possibly sensory) bristles at low magnification, (b) details of the body surface reveal fine structures with small undercut chitinos granules resulting in extreme superhydrophobicity.

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(c) Fungi and other organisms Fungi most probably moved simultaneously with plants onto land. The earliest true land plants had a close association with mycorrhizal fungi, replacing non-existing roots [141]. There is evidence that lichens [142] and ascomycetes [143] came into existence around the same time. Within the large number of extant species, the moulds such as Botrytis, Aspergillus or Penicillium show superhydrophobic surfaces resulting from minute rodlets on the vegetative hyphae, specifically conidiophores (figure 11). The surfaces are most probably formed from a specific class of proteins called hydrophobins [144,145], but wax-like hydrocarbons might also be involved (figure 11). Fungi are not only specialized to live on plant surfaces, but they also are simultaneously capable of dissolving epicuticular wax layers and also locally modifying the

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Birds. The body is almost completely covered by a plumage of complicated hierarchical structures; the feathers are an epidermal outgrowth of keratin. This separates birds from all other vertebrates, with the exception of certain extinct theropod dinosaurs. Structurally, they are the most complex integumentary appendages in vertebrates. Keratin is also the basis of mammalian hairs and wettable with a contact angle of about 78◦ [131]. All birds must maintain a hydrophobicity: the plumage would absorb water in rain or even in mist and is thus too heavy to maintain its mechanical function for flight; an example of adroit hydrophobicity is the refined spatially differentiated plumage of the blue swallow [132]. On the other hand, the plumage forms the thermal isolation layer: a warm-blooded homoeothermic penguin with plumage soaked with freezing water could hardly survive in Antarctic conditions. Thus, plumage keratin is coated by fatty oily substances (‘preening oil’) and becomes waterrepellent [133]. In particular, this is essential for birds living on water or diving under water. In water birds, many additional and particularly specialized functions may occur. Examples are the buoyancy function in ducks, a differentiation between an isolating hydrophobic inner plumage and a water-repellent outer layer in the diving cormorant [133,134]. The most intriguing case may again be the penguin: in addition to thermal isolation, its superhydrophobicity functions as drag reduction and fulfils a particular function when the bird jumps from water onto an ice sheet. Iridescent feathers may show different wetting properties from the rest of the plumage [135]. Mammals. Superhydrophobic surfaces are absent or very rare in mammals. Examples reported for the semi-aquatic water shrews N. fodiens [136,137]; however, there are contradicting observations [138–140] suggest that static electricity charge could play a role, which is still unconfirmed as superhydrophobicity in our own unpublished studies. Superhydrophobicity may occur in the inner layers of the fur of diving animals that keep an air layer for isolation.


Figure 33. Slime moulds (Mycetozoa) are not related to fungi, but rather a sort of social amoeba. This picture reveals for the first time the superhydrophobicity of the (a) fruiting bodies of Stemonitis caused by (b) the nanoscopic granular coating of unknown chemical composition of the sterile capillitium fibres.

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Today’s biodiversity is reflective of about 4 billion years of evolutionary history. Despite several major extinction events, the number of species has been constantly increasing resulting in an estimated number of 5–30 million species in existence today, 1.8 million of which are known to science. Today, we are facing a dramatic loss of biodiversity, mainly caused by human activities now known as ‘the sixth mass extinction’ [148]. For the majority of time, life existed only in marine environments; a major change took place about 450–500 Ma when the first organisms moved on land. It was necessary to address the new challenges of gravitation, exposure to different wavelengths of radiation (especially UV), and most of all, the risk of desiccation. These challenges needed a number of different new structures, materials and processes; this eventually led to a rapid emergence and radiation of new species. One of the most impressive results of this process was the progymnosperm tree Archeopteris; early on, it developed a bifacial cambium and formed the earliest forests in the Devonian [149]. One of these key innovations was the cuticle, the major prerequisites for the development of superhydrophobic surfaces in plants (figures 6 and 29). This will be addressed in the following section. For a general overview of biomimetics and biodiversity, including the risks and benefits of current developments, we refer to [6].

(a) Superhydrophobicity and plant evolution Water-repellent or superhydrophobic surfaces depend on three interfaces between liquid, solid and air; these surfaces are not expected to be found in aquatic plants. A representative survey of submerged plants or parts of plants did not reveal any surface structures apart from a few cuticular folds such as in Fontinalis, an aquatic moss. Additionally, no structures that might serve as a basis for water repellency are reported, from the various green algae that are related to embryophytes, including those adapted to terrestrial life such as Trentepohlia, Trebouxia or Coleochaete. Consequently, these groups are treated as one functional group of primarily aquatic, non-embryophyte green plants (figure 29). The first group that has at least a few members with waxy water-repellent surfaces, implying having a cuticle, is Marchantiophyta, the sister to all other embryophytes according to recent phylogenies [150,151]. This raises the question: at which point in plant evolution does this trait appear for the first time? Although Marchantiophyta may be the most probable candidate, a few other groups of extinct plants could be considered to be the putative ancestor of embryophytes. Although the systematic nature of these organisms that may have formed a cuticle or a similar extracellular covering is controversial, they may have played an important role in the transition from water to land. One of these groups is Nematophytes, puzzling organisms with a tubular organization of uncertain affinities [152–155].

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8. Evolution of superhydrophobicity: 450 myr of trial and error

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wetting properties, therefore creating its own microhabitat. They probably do this by excreting a certain type of surfactant, which is also known from epiphyllous bacteria. Similar structures have been described in lichens. In view of the results that some lichens also have superhydrophobic external and internal surfaces, they may represent a second lineage that developed such adaptations [146,147]. In fact, only the fungal partner exhibits hydrophobic surface characteristics, which points to fungi as a huge group of terrestrial organisms that most probably colonized land in a close association with plants. Today, there are quite a number of species known that exhibit superhydrophobic surfaces (see above). Slime moulds (Mycetozoa) are a group of unrelated Protista, sometimes called social amoeba. The spores of certain species are hydrophobic [80]. However, we have observed in Stemonitis parts of the sporangia are superhydrophobic, in particular a nanoscopic layer of unknown composition covers the sterile fibres (capillitium; figure 33). This new finding again proves: (super)hydrophobicity evolved even if only a part of an organism is exposed to air or for the dispersal of spores and fructification unit.

There has long been an uncertainty about the actual nature of epicuticular waxes, but recent investigations show that most of them, if not all, are of crystalline nature [37,40,41], implying a self-assembly processes as the driving force for their formation. Self-assembly has been proved by recrystallization of waxes from organic solvents, resulting in morphologically similar structures when compared with the plant surface [40,41,43,45,47,48,167,169,170]. Re-crystallization of extracted waxes, however, reveals a vast variety of different structures and is heavily influenced by temperature, the chemical nature of the solvent and the underlying substrate [40,43].

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(b) Crystallinity

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However, recent investigations have led to the hypothesis that at least some fossil remnants assigned to Nematophytes are in fact Marchantiophyta [153]. This would fit to the results of the above-mentioned phylogenies, although other groups of organisms should also be considered in this context. There are no superhydrophobic plant surfaces yet known that do not have an underlying cuticle, thus the cuticle must have evolved prior to the emergence and radiation of land plants in the Early Silurian. Some fossils assigned to Nematophytes suggest that cuticles may have existed as early as the Ordovician. The cuticle is one of the key innovations of plants facing the challenges of living on land, specifically, the risk of desiccation [156]. The cuticle is a multicomponent thin extracellular membrane [157] covering the primary aerial parts of vascular plants and many, if not all, bryophytes. It consists of a polymer fraction with embedded soluble components serving as the interface between plants and their atmospheric environment [84,158,159]. The cuticle may be regarded as a natural composite comprising two major hydrophobic components: an insoluble polymer fraction composed of cutin, and in some species cutan, as well as soluble lipids of diverse chemistry, collectively called waxes. Additionally, a certain amount of polysaccharides are present (overview in [50,84,159,160]). The outer very thin region (usually less than 100 nm), called cuticle proper, contributes to 99% of the barrier efficiency [156]. The region determining the thickness, up to 20 μm, is called the cuticle layer [160,161]. Although extensive research has been conducted on cuticle structure development and function, many aspects remain unresolved, including the detailed three-dimensional structure of cutin—within the different organs and during development [162]. Cuticular waxes are found within the cuticle, as well as deposited upon the surface—known as epicuticular waxes. Depending on the chemical composition, epicuticular waxes are able to form complex three-dimensional crystalline structures, which may be valuable characteristics in plant systematics (overview in [107]). Cuticular waxes are mixtures composed of aliphatic and aromatic components [29,91,163]. Depending on the functional groups (-hydroxyl, -carboxyl, -ketoyl), a broad spectrum of fatty acids, primary alcohols, aldehydes, β-diketones and secondary alcohols are produced [89,90]. Cuticular wax composition is widely variable among plant species and even in different organs, as well as during ontogeny [164,165]. The chemical diversity is mirrored by micromorphological diversity [29]. A specific component or substance class often dominates epicuticular wax crystal composition, resulting in a characteristic morphology. Such dependencies between chemistry and morphology have been intensively studied for some wax platelets and wax tubules. Wax platelets are found quite often in plants; they differ in shape, chemical composition and distribution [107]. Besides aliphatic components such as primary alcohols (e.g. Poaceae, Fabaceae and the genus Eucalyptus [166]), wax tubules can be composed of secondary alcohols, predominantly nonacosan-10-ol and its homologues [48,93,167,168], whereas the second type is dominated by β-diketones such as riacontan-14,16-dione [48]. Tubules based on nonacosan-10-ol are of particular interest with respect to plant phylogeny. Mapping the occurrence of this particular component on a phylogeny of embryophytes shows that nonacosanol appears scattered throughout all major groups including mosses, indicating an ancient common biosynthetic pathway (figure 6).

Biologically inspired products have gained an astonishing and rapidly increasing market share in the last decades. Assessments, like those by the ‘Da Vinci index’ [175], provide estimations of US $425 billion for the 2039 U.S. GDP for all bioinspired technologies, including biotechnological products. On the basis of works of D.W. Bechert, friction reduction by riblet foils (not a superhydrophobic technology) has grabbed the public’s attention: the America’s Cup races of 1987 and 2010 included ships with bioinspired hulls. Bionic swimsuits have been in use since 1996; biomimetic Fastskin technologies influenced the gold medal results in the 2008 Beijing Olympics. Superhydrophobic air-retaining Salvinia effect [15] surfaces may provide another solution for drag reduction. Gould [2] estimated that the global nanocoating market will reach a value of 14.2 billion US Dollars by 2019. New institutions, research programmes, and networks such as the International Society of Bionic Engineering ISBE and the BIOKON and many other institutions (e.g. Biomimicry 3.8) have been established to work on bionic technologies. The statistical analysis (figure 7) shows the rapidly increasing presence of research and technologies in the global awareness. The first use of the term ‘superhydrophobic’ seems to have been in 1976 in an US Patent [24] and 12 years later in a publication [12]. The principle of superhydrophobic hierarchically structured and self-cleaning surfaces we first published in [8], the term for this phenomenon, the lotus effect, was first coined in a small publication for a general audience by Barthlott in 1992 [10]. After the first thorough explanation of the physico-chemical basis in The purity of sacred lotus by Barthlott & Neinhuis [11] Lotus Effect gained public interest only 5 years later: the diagram (figure 7) shows the dramatic increase of publications based on the statistical data provided by the Institute of Scientific Research ISI. In 2015, around 1200 articles were published on the subject, mainly dealing with aspects for biomimetic applications. The number of citations of the term ‘superhydrophobic’ is closely followed by that for ‘lotus effect’. The Lotus-technology was patented (1996) and registered in the same year as the trademark Lotus Effect (today STO company). Search machines like ‘Google’ provided (May 2016) some 600 000 hits for ‘lotus effect’ and some 520 000 hits for ‘superhydrophobic’. The 1997 physical explanation of the sacred

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9. Biomimetic technical applications

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One of the major problems associated with epicuticular waxes was the way these molecules move onto the surface, i.e. passing through the cell wall and the cuticle. Several explanations were formulated starting with ectodesmata and finally proposing lipid transfer proteins [171–173]. However, all these hypotheses lack experimental evidence. No channel-like structures have been unequivocally proved to serve as pathways for wax molecules in the plant cuticle using SEM, TEM or AFM investigations [45,174]. A more recent hypothesis formulated [49] is based on the assumption that wax components are co-transported with water, because the latter is constantly lost in small amounts via cuticular transpiration. This mechanism does not require pathways, carrier molecules or sensors and is also self-regulating. While cuticular waxes are the main barriers for water permeability, the transport decreases when more wax is deposited on the surface; this easily explains the ability of many plants to regenerate disrupted partial or missing wax layer. Removing epicuticular waxes also partly removes the barrier, resulting in more wax deposited in that particular area, re-establishing a new wax layer without affecting adjacent areas has been demonstrated in situ by AFM [42,45]. Given that this hypothesis is correct, the formation and regeneration of waxes is associated with terrestrial life, because there is not a water gradient that might act as driving force in an aqueous environment. Support for this assumption was provided by experiments on wax formation with variable air humidity [44]. In summary, superhydrophobicity is a biological phenomenon which evolved in the late Ordovician or Silurian, some 430–500 million years ago with the conquest of land habitats. For plants and possibly insects this should be considered a key innovation for life outside of water: to avoid water films, ensuring free gas exchange, and at the same time to reduce the colonization with pathogens (e.g. fungal spores).

(a)

(b)

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lotus of Hinduism and Buddhism was the accelerator for the interest of engineers and physicists in biomimetic surfaces of today. It caused a shift in paradigms and is the basis for modern biomimetic superhydrophobic surface technologies. There is a broad spectrum of technologies used to fabricate hierarchically structured superhydrophobic surfaces (surveys in [13]). For prototypic copies, replica techniques were developed in the 1990s [39,176,177], reproducing the biological model surfaces with an astonishing and unrecalled precision down to the nanoscale. Plasma etching and related techniques enable the fabrication of simple ‘rough’ surfaces in hydrophobic materials (overview in [178]). In contrast, three-dimensional lithographic methods allow highly complex architectures with complex undercuts like in the replica of the Salvinia trichomes (figure 34b) by Tricinci et al. [62]. The self-assembly techniques are unsurpassed. They are biomimetic in a twofold sense: not only the biological structure, but also the technical process is also biomimetic. A hydrophobic coating is added to a hydrophilic base to generate a superhydrophobic surface: e.g. in electrochemically structured copper foils (figure 19) [39]. The most successful product economically on the market, the facade paint Lotusan , is based on various inorganic particles, including TiO2 as pigment in a hydrophobic silicone resin resulting in a perfect hierarchically structured surface. On a much smaller scale, carbon nanotubules provide an example of superhydrophobic surfaces [179–182]. Meanwhile, light transparent superhydrophobic surfaces like those of the dragonfly wings (figure 3a) are of great interest for transparent glass and polymers [183,184]. Another technology, liquid infused superhydrophobic slippery surfaces, has gained particular interest. Here, chemical heterogeneities are achieved not by ‘air pockets’ (figure 24), but by hydrophobic liquids like fluorated oils [22,185,186]. The broad spectrum of applications of biomimetic superhydrophobic surfaces involves the functions inspired by the biological role models (§6) and can be divided into three categories, as is often the case in biology, they may often fall into multiple categories. Water repellency and anti-icing. Technological functionalities are added to avoid wetting with water or to obtain anti-icing properties. A whole range of products and techniques are on the market, mostly coatings or sprays, the product names often indicate their function (e.g. ‘NeverWet’). Dry surfaces may allow new dimensions in textile-based architecture owing to weight reduction during rainfall. Anti-ice and anti-frost performance are increasing in importance [187,188]. Adhesion reduction. There is a vast amount of literature about lotus effect (figures 14 and 26) technologies (survey in [13]). Permutations of the lotus effect technology have been described, for example ‘rose petal effect’ ‘rice effect’ or ‘butterfly effect’ (survey in [3]). However, the physical frame conditions for self-cleaning by the rolling-off of water droplets and self-cleaning are not

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Figure 34. (a) A replica of a Salvina oblongifolia leaf. The water droplet forms a nearly perfect sphere as in its biological prototype. The replica can hold an air layer under water for 4 days. (b) A biomimetic copy of the Salvinia molesta egg-beater trichomes (figure 21) fabricated with a sophisticated lithographic process. Sources: (a) from [7], (b) from [62].


10 mm

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always completely understood by the general public. An example are the leaves of the lady’s mantle (Alchemilla), which are hierarchically structured and superhydrophobic [189], but they have only limited self-cleaning abilities, because the structures are too large, exhibit chemical heterogeneities and even trap small contaminating particles. The same applies for most airretaining surfaces such as in Salvinia or Pistia: only within a certain scope of structural dimensions previously outlined in [11] self-cleaning is physically possible. We observed that when large rain droplets with a high kinetic energy hit the surface, they are deformed and penetrate between the large hairs and remove particles. Air-retaining surfaces for underwater applications. The Salvinia effect technology to maintain stable air layers up to several months or even permanently was recently described [15,54,57,106] and usually requires a complex microarchitecture (see [62]). Air-retaining surfaces are described by the same physical frame conditions for biomimetic applications, the same four/five principles given in §5 apply—chemical hydrophobicity, hair-like structures, undercuts/overhangs and elasticity. Additionally, chemical heterogeneities for air layer stabilization (Salvinia paradox) could be added. The technical applicable functions are also similar to those found in the biological role models (§6). Air-retaining surfaces are possibly the most complex biological (e.g. Salvinia) surfaces and the biomimetic application may include Air layers for isolation: thermal isolation might be a possible application for air layers under water, or for conductive isolation or for protecting a corrosive material. An air layer as a barrier between a corrosive or current-carrying material prevents the material from being in contact with the liquid phase (e.g. also corrosive acids). Air layers for fluid drag reduction: This seems to be the most interesting application for ship building [190] and other applications for the Salvinia effect. A fluid drag reduction of up to 10% was measured in 2007 on a prototype boat, 7 m long [58] and up to 30% for smaller advanced surfaces in a hydrodynamic water channel [191]. Because the majority of goods are transported globally by large container ships, our calculations and assessments indicate a possible global reduction of fuel (oil) consumption of 125 million tonnes and of 395 million tonnes of CO2 emission per year. For literature and the physical background, we refer to the discussion and dates in the previous §§1 and 5a. Air retaining grids are a novel technology introduced here; biological role models were introduced in §5. Grids are a simpler and relatively cost-effective technique for maintaining a persistent air layer under water (compare [62]). The superhydrophobic grid- or netlike structures act as spacers above the superhydrophobic coated surface (figure 35)—a rather simple technological solution that can be applied to many different surface materials. Additionally, elastic grids can be superimposed onto compartmented surfaces (‘honeybee comb structures’) to stabilize the air layer under dynamic conditions (see §5a). Chemical heterogeneities (pinning points for the air–water interface: Salvinia paradox) could also easily be added. Air layers to avoid biofouling (antifouling): air layers cause an additional important drag reducing effect in fluids. The colonization of ship hulls with organisms (biofouling) such as crustacean barnacles (e.g. Pollicipes) and other organisms is an economic problem for the global shipping industry, and comprehensive literature is available. A permanent air layer is predicted to prevent a biotic colonization [26,192]. Furthermore, as we previously discussed on isolation, ship hulls could be equipped with toxic coatings and still minimize environmental pollution if there is an air layer present. Air layers for sensory functions: as indicated under ‘biological functions’ (§6), the backswimmer Notonecta uses the compressibility of the air layer in combination with around 13.000 mechanoreceptors on each forewing to measure pressure waves for prey detection (figure 28). Notonecta sensors provide a novel principle for under water detection, hydrophones and other applications. Air layers for camouflage: as described in the biological functions (§6), elastic air layers under water could possibly be used to avoid sonar, and to a certain extent, optical detection methods. They may imply very different fields between fishing sport and military applications.

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10. Stability and sustainability: the gilded age of surface technologies Surfaces are the thin interfaces between the solid bulk material and its environment. They are the boundary layers that determine all environmental interactions: this is the reason that surfaces play such a crucial role in the evolution of organisms and in technical applications: ‘small things—big effects’. ‘Surfaces’ in engineering are considered to be the thin boundary layers exposed to the physical and chemical influences of the environment. In plants, it is not the stable polymer cutin which ultimately determines the interaction, but the epicuticular wax crystals or even only the monomolecular films of wax. Thus, surfaces—in particular hierarchically structured surfaces— are very sensitive to mechanical, physical (e.g. ultraviolet radiation) and chemical (e.g. oxidation, water, solvents, surfactants) influences. The stability and durability of these layers is a major technological challenge. Biological surfaces may be very stable and last a long time—like the shells of turtles or the leathery wettable leaves of certain plants. However, refined hierarchically structured superhydrophobic surfaces maintain their functionality only for a limited period of time. Superhydrophobic lotus leaves only last a year or less. The persistence of superhydrophobicity can be studied in the permanent growing shoots of certain ‘blue’ columnar cacti (e.g. Pilosocereus pachycladus). However, the ideal example is the leaves of Welwitschia mirabilis (figure 31) that are covered by nonacosan-10-ol crystals (figure 4c) and grow continuously from their base; they may reach an age of more than 100 years. We have observed under greenhouse conditions the wax layer is eroded after about 1 year and the surfaces became wettable. Conversely, we have previously shown that surfactants added to commercially applied pesticides destroy the structural integrity of epicuticular wax crystals, removing the hydrophobicity and thus the selfcleaning abilities (figure 27); as a consequence, the natural defence barriers of many crop plants against fungal spores are removed [102,193,194]. This should have drastic consequences in the application of pesticides in agriculture. Technical products are not necessarily based on waxes, but are from refined other technologies, and are thus significantly more stable. Facade paints based on particles embedded into a hydrophobic silicone resin (such as Lotusan ) maintain the (super-)hydrophobic properties by chalking, i.e. the outermost layers are lost owing to weathering. Such Lotus Effect surfaces (figure 9) are known to maintain their functionality for at least two decades.

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Air layers for gas exchange: as an application found in insects or plants, and also in technical applications where gas exchange is important, air layers could serve as gas reservoir (‘plastron’) or could be used to enhance specific processes. The technology could be applied to bionic medicine.


Figure 35. The air-retaining grid is a novel technique to maintain stable air retention under water. Grids are a simple (compare figure 34) solution that is easy to fabricate, they can even be elastic and chemical heterogeneities may be added. Grids are mounted over small compartments creating fragmented surfaces; the compartment boarders may exhibit a refined architecture to allow the air layer stabilization under hydrodynamic conditions or changing pressures. Grids are extremely rare in organisms, due to developmental reason (examples see §5b). This technique is somewhat contrasting to the Salvinia principles (figure 21). (Online version in colour.)

On the basis of our own research of almost 20 000 species and many abiotic and technical surfaces, we have demonstrated that hierarchically structured superhydrophobic surfaces evolved in living organisms about 450 Ma. A systematic survey of biological superhydrophobicity is provided: higher plants and insects provide, by far, the largest number and most sophisticated structures for biomimetic applications. A comprehensive survey of the biological construction principles is provided: chemistry and hierarchical sculpturing up to three or more superimposed levels. Bionics as a science was established between 1880 and 1926. However, the interest in biomimetic surfaces arrived surprisingly late with the introduction of the Velcro principle in 1958. Superhydrophobicity plays a notable role only after 1997. The biomimetic technical potential of biological surfaces was largely ignored over the last century, but it provided inspiration for many exciting technical innovations in the last three decades. Ironically, the terms ‘bionic’ and ‘biomimetic’, as they are defined by the scientific community, are increasingly applied for purely marketing reason to non-bionic (parabionic) products. Biological evolution is a slow process spanning millions of years. It works by undirected processes such as mutation and selection and thus tries all constructional possibilities—the vast majority of mutations are detrimental and will disappear. But out of discussion are million years of research and development for technical engineering: the material scientist has a goal to fabricate a particular product in a limited time, using experimental trial-and-error approaches, calculation and modelling. The crucial point is the fact that an engineer must have a particular target of what he wants to reach. The unexpected, the unthinkable, cannot be in his thoughts: this is the second crucial difference to biological evolution. It may have taken a couple of decades to identify microscopic elastic egg-beaters with nanoscopic wax crystals and hydrophilic pins for persistent air retention under water, but the floating fern Salvinia had over 30 myr to perfect them by mutation and selection in its evolution. We still have insufficient knowledge of the incredible spectrum of biological surface structures. We do not even understand the structural base or function of the magnetic field like wax crystal orientation on a leaf of the lily of the valley (figure 12) in our garden.

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11. Conclusion

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Surface nanocoating technologies play an increasing economic role (compare [2]). To use Mark Twain’s title of his novel published in 1873: we live in ‘the gilded age’ of surface technologies. However, it is a trivial experience of every good restaurant owner: there is a basic difference between a massive solid silver spoon and a silvered utensil. Often the surface limits the lifespan of a product: from the high-tech-coated repellent lavatory in the bathroom to the most convenient anti-reflex coatings of spectacle glasses: after a few years, the whole product may be ruined, its optical appearance spoiled and it will need to be replaced. The colloquial language knows the difference between ‘solid’ and ‘superficial’. It is increasingly the surface that determines the lifespan of products: the biggest challenge in surface technologies may be the ultimate stability and durability of the products. In biology, the functionalities of surfaces are adapted to the lifespan of the organ or organism: a superhydrophobic hierarchically structured delicate lotus leaf only needs to function for less than a year. In contrast, lotus seeds with a hard seed coat have a lifespan and viability of more than 1400 years. Nature’s prototypes are sustainable for the time spans and environments they have been designed for through the process of evolution. Are expensive bathroom lavatories or spectacle glasses designed for a lifespan of only a few years, to ultimately end up in the trash? Living in the anthropocene with its ever-increasing world population, as opposed to its decreasing resources, we increasingly and urgently have to address the question of sustainability of products. Natural resources are decreasing along with the number of living species: the loss of biodiversity inherently means the loss of ‘living prototypes’, the biological role models of bionics and biomimetics [95]. It may be another neglected but crucial lesson from the surprising biological diversity: biomimetics must include the concept of sustainability for its products—otherwise, it remains only mimicry.

the German Research Council DFG, the Federal Ministry for Science and Education BMBF, and the Academy of Science and Literature in Mainz. Acknowledgements. This paper is based on over four decades of research on surfaces by a large working group with ever-changing members: first and foremost, we acknowledge all the students who had successful theses in this field. Their names can be found in the papers quoted in the references. Birte Böhnlein and Peter Häger are yet to finish their works. We acknowledge the discussions with co-workers and friends in the ARES working group in Rostock (Alfred Leder, Martin Brede) and Karlsruhe (Thomas Schimmel, Stefan Walheim, Torsten Scherer), in particular, we thank Bharat Bhushan (Ohio), Horst Bleckmann (Bonn), Walter Erdelen (former UNESCO Paris), Daud Rafiqpoor (Bonn), Gerhard Gottsberger (Ulm), Kerstin Koch (Kleve), Stanislav Gorb (Kiel) and Georg Noga (Bonn). Technical assistance was provided over the years by Hans-Jürgen Ensikat, the late Wolfgang Roden, Alexandra Runge, Bernd Haeseling, Markus Moosmann and Danica Christensen, who also edited the English in the manuscript. We obtained the plant material from the Botanical Gardens of the University of Bonn; we thank the Curator Wolfram Lobin and the experienced gardeners such as Stefan Giefer and Michael Neumann as well as many others.

References 1. Bhushan B. 2010 Springer handbook of nanotechnology, 3rd edn. Heidelberg, Germany: Springer. 2. Gould J. 2015 Learning from naturés best. Nature 519 S2–S3. (doi:10.1038/519S2a) 3. Bhushan B. 2016 Biomimetics – bioinspired hierarchical-structured surfaces for green science and technology, 2nd edn. Heidelberg, Germany: Springer International Publishing. 4. Brongniart C. 1893 Recherches pour servir a l’histoire des Insectes fossiles des temps primaires precedees d’une Etude sur la nervations des ailes des Insectes. Thesis, Fac. Sciences Paris, Saint-Etienne, Imprimerie Théolier. 5. Koch K, Bhushan B, Barthlott W. 2010 Multifunctional plant surfaces and smart materials. In Springer handbook of nanotechnology (ed. B Bhushan), pp. 1399–1436. Berlin, Germany: Springer. 6. Barthlott W, Rafiqpoor D, Erdelen W. 2016 Bionics and biodiversity – bio-inspired technical innovations for a sustainable future. In Biologically-inspired systems and integrative structures (eds J Knippers, K Nickel, T Speck), pp. 24–56. Berlin, Germany: Springer Publishers. 7. Francé RH. 1920 Die Pflanze als Erfinder. Stuttgart, Germany: Franckh’sche Verlagshandlung (Engl. edition: Plants as inventors. London: Simpkin and Marshall). 8. Barthlott W, Ehler N. 1977 Raster-Elektronenmikroskopie der Epidermis–Oberflächen von Spermatophyten. Trop. Subtrop. Pflanzenwelt 19, 1–105. 9. Barthlott W, Wollenweber E. 1981 Zur Feinstruktur, Chemie und taxonomischen Signifikanz epicuticularer Wachse und ähnlicher Sekrete. Trop. Subtrop. Pflanzenwelt 32, 1–67. 10. Barthlott W. 1992 Die Selbstreinigungsfähigkeit pflanzlicher Oberflächen durch Epicuticularwachse. In Klima- und Umweltforschung an der Universität Bonn, pp. 117–120. Bonn, Germany: Rheinische Friedrich-Wilhelms-Universität Bonn. 11. Barthlott W, Neinhuis C. 1997 Purity of the sacred lotus, or escape from contamination in biological surfaces. Planta 202, 1–8. (doi:10.1007/s004250050096) 12. Gobas FAPC, Clark KE, Shiu WY, Mackay D. 1989 Bioconcentration of polybrominated benzenes and biphenyls and related superhydrophobic chemicals in fish: role of bioavailability and elimination into the feces. Environ. Toxicol. Chem. 8, 231–245. (doi:10.1002/ etc.5620080306) 13. Yan YY, Gao N, Barthlott W. 2011 Mimicking natural superhydrophobic surfaces and grasping the wetting process: a review on recent progress in preparing superhydrophobic surfaces. Adv. Colloid Interface Sci. 169, 80–105. (doi:10.1016/j.cis.2011. 08.005)

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Competing interests. We declare we have no competing interests. Funding. Our work in Bionics and Biodiversity was supported by the Deutsche Bundesstiftung Umwelt DBU,

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The current dramatic loss of biodiversity also means the loss of biological role models—the ‘living prototypes’ of bionics for technical applications [6]. They should be treasured as inspiration for future—another intrinsic value of biodiversity.

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14. Koch K, Bohn HF, Barthlott W. 2009 Hierarchical sculpturing of plant surfaces and superhydrophobicity. Part of the ‘Langmuir 25th year: wetting and superhydrophobicity’ special issue’. Langmuir 25, 14 116–14 120. (doi:10.1021/la9017322) 15. Barthlott W et al. 2010 The Salvinia paradox: superhydrophobic surfaces with hydrophilic pins for air retention under water. Adv. Mater. 22, 2325–2328. (doi:10.1002/adma.200904411) 16. Robinette JC (ed.). 1961 Living prototypes – the key to new technology. In Proc. Bionic Symp. 13–15. September 1960. Wright Air Development Division. 17. Barthlott W, Riede K, Wolter M. 1994 Mimicry and ultrastructural analogy between the semi-aquatic grasshopper Paulinia acuminata (Orthoptera: Pauliniidae) and its foodplant, the water-fern Salvinia auriculata (Filicateae: Salviniaceae). Amazoniana 13, 47–58. 18. Darmanin T, Guittard F. 2015 Superhydrophobic and superoleophobic properties in nature. Mater. Today 18, 273–285. (doi:10.1016/j.mattod.2015.01.001) 19. Goujon P. 2001 From biotechnology to genomes. Singapore: World Scientific Publishing Co Pte Ltd. 20. Wenzel RN. 1936 Resistance of solid surfaces to wetting by water. Ind. Eng. Chem. 28, 988–994. (doi:10.1021/ie50320a024) 21. Cassie ABD, Baxter S. 1944 Wettability of porous surfaces. Trans. Faraday Soc. 40, 546–551. (doi:10.1039/tf9444000546) 22. Nosonovsky M. 2011 Materials science: slippery when wetted. Nature 477, 412–413. (doi:10.1038/477412a21) 23. Wong TS, Kang SH, Tang SK, Smythe EJ, Hatton BD, Grinthal A, Aizenberg J. 2011 Bioinspired self-repairing slippery surfaces with pressure-stable omniphobicity. Nature 477, 443–447. (doi:10.1038/nature10447) 24. Reick FG. 1976 U.S. Patent No. 3,931,428. Washington, DC: U.S. Patent and Trademark Office. 25. Solga A, Cerman Z, Striffler BF, Spaeth M, Barthlott W. 2007 The dream of staying clean: lotus and biomimetic surfaces. Bioinspir. Biomim. 2, 126–134. (doi:10.1088/1748-3182/2/4/S02) 26. Koch K, Barthlott W. 2009 Superhydrophobic and superhydrophilic plant surfaces: an inspiration for biomimetic materials. Phil. Trans. R. Soc. A 367, 1487–1509. (doi:10.1098/ rsta.2009.002) 27. Wagner P, Fürstner R, Barthlott W, Neinhuis C. 2003 Quantitative assessment to the structural basis of water repellency in natural and technical surfaces. J. Exp. Bot. 54, 1295–1303. (doi:10.1093/jxb/erg127) 28. Ensikat HJ, Ditsche-Kuru P, Neinhuis C, Barthlott W. 2011 Superhydrophobicity in perfection: the outstanding properties of the lotus leaf. Beilstein J. Nanotechnol. 2, 152–161. (doi:10.3762/bjnano.2.19) 29. Barthlott W, Neinhuis C, Cutler D, Ditsch F, Meusel I, Theisen I, Wilhelmi H. 1998 Classification and terminology of plant epicuticular waxes. Bot. J. Linn. Soc. 126, 237–260. (doi:10.1111/j.1095-8339.1998.tb02529.x) 30. Ditsch F, Barthlott W. 1994 Mikromorphologie der Epicuticularwachse und die Systematik der Dilleniales, Lecythidales, Malvales und Theales. Trop. Subtrop. Pflanzenwelt 88, 1–74. 31. Ditsch F, Barthlott W. 1997 Mikromorphologie der Epicuticularwachse und das System der Dilleniidae und Rosidae. Trop. Subtrop. Pflanzenwelt 97, 1–248. 32. Frölich D, Barthlott W. 1988 Die Mikromorphologie der epicuticularen Wachse und das System der Monocotylen. Trop. Subtrop. Pflanzenwelt 63, 1–135. 33. Hennig S, Barthlott W, Meusel I, Theisen I. 1994 Mikromorphologie der Epicuticularwachse und die Systematik der Hamamelididae, Magnoliidae und Ranunculidae. Trop. Subtrop. Pflanzenwelt 90, 1–60. 34. Theisen I, Barthlott W. 1994 Mikromorphologie der Epicuticularwachse und die Systematik der Calycerales, Dipsacales, Gentianales und Rubiales. Trop. Subtrop. Pflanzenwelt 89, 1–62. 35. Wilhelmi H, Barthlott W. 1997 Mikromorphologie der Epicuticularwachse und die Systematik der Gymnospermen. Trop. Subtrop. Pflanzenwelt 96, 1–49. 36. Koch K, Bhushan B, Barthlott W. 2008 Diversity of structure, morphology and wetting of plant surfaces. Soft Matter 4, 1943–1963. (doi:10.1039/b804854a) 37. Ensikat HJ, Boese B, Mader W, Barthlott W, Koch K. 2006 Crystallinity of plant epicuticular waxes: electron and X-ray diffraction studies. Chem. Phys. Lipids 144, 45–59. (doi:10.1016/j. chemphyslip.2006.06.016)

35 .........................................................


38. Ensikat HJ, Schulte AJ, Koch K, Barthlott W. 2009 Droplets on superhydrophobic surfaces: visualization of the contact area by cryo-scanning electron microscopy. Langmuir 25, 13 077–13 083. (doi:10.1021/la9017536) 39. Fürstner R, Barthlott W, Neinhuis C, Walzel P. 2005 Wetting and self-cleaning properties of artificial superhydrophobic surfaces. Langmuir 21, 956–961. (doi:10.1021/la0401011) 40. Koch K, Barthlott W, Koch S, Hommes A, Wandelt K, Mamdouh W, De-Feyter S, Broekmann P. 2005 Structural analysis of wheat wax (Triticum aestivum, c.v. ‘Naturastar’ L.): from the molecular level to three dimensional crystals. Planta 223, 258–270. (doi:10.1007/ s00425-005-0081-3) 41. Koch K, Domisse A, Barthlott W. 2006 Chemistry and crystal growth of plant wax tubules of lotus (Nelumbo nucifera) and Nasturtium (Tropaeolum majus) leaves on technical substrates. Cryst. Growth Des. 6, 2571–2578. (doi:10.1021/cg060035w) 42. Koch K, Dommisse A, Neinhuis C, Barthlott W. 2003 Self-assembly of epicuticular waxes on living plant surfaces by atomic force microscopy. In Scanning tunneling microscopy/spectroscopy and related techniques (eds PM Koenraad, M Kemerink), pp. 457–460. Melville, NY: American Institute of Physics. 43. Koch K, Dommisse A, Niemietz A, Barthlott W, Wandelt K. 2009 Nanostructure of epicuticular plant waxes: self-assembly of wax tubules. Surf. Sci. 603, 1961–1968. (doi:10.1016/j.susc.2009.03.019) 44. Koch K, Hartmann KD, Schreiber L, Barthlott W, Neinhuis C. 2006 Influences of air humidity during the cultivation of plants on wax chemical composition, morphology and leaf surface wettability. Environ. Exp. Bot. 56, 1–9. (doi:10.1016/j.envexpbot.2004.09.013) 45. Koch K, Neinhuis C, Ensikat HJ, Barthlott W. 2004 Self assembly of epicuticular waxes on living plant surfaces imaged by atomic force microscopy (AFM). J. Exp. Bot. 55, 711–718. (doi:10.1093/jxb/erh077) 46. Koch K, Bhushan B, Barthlott W. 2009 Multifunctional surface structures of plants: an inspiration for biomimetics. Prog. Mater. Sci. 54, 137–178. (doi:10.1016/j.pmatsci2008.07.003) 47. Meusel I, Neinhuis C, Markstadter C, Barthlott W. 1999 Ultrastructure, chemical composition, and recrystallization of epicuticular waxes: transversely ridged rodlets. Can. J. Bot. 77, 706–720. (doi:10.1139/cjb-77-5-706) 48. Meusel I, Neinhuis C, Markstadter C, Barthlott W. 2000 Chemical composition and recrystallization of epicuticular waxes: coiled rodlets and tubules. Plant Biol. 2, 462–470. (doi:10.1055/s-2000-5961) 49. Neinhuis C, Koch K, Barthlott W. 2001 Movement and regeneration of epicuticular waxes through plant cuticles. Planta 213, 427–434. (doi:10.1007/s004250100530) 50. Bargel H, Koch K, Cerman Z, Neinhuis C. 2006 Structure–function relationships of the plant cuticle and cuticular waxes – a smart material? Funct. Plant Biol. 33, 893–910. (doi:10.1071/ FP06139) 51. Barthlott W. 1990 Scanning electron microscopy of the epidermal surface in plants. In Application of the scanning EM in taxonomy and functional morphology. Systematics associations’ special volume (ed. D Claugher), pp. 69–94. Oxford, UK: Clarendon Press. 52. Barthlott W. 1981 Epidermal and seed surface characters of plants: systematic applicability and some evolutionary aspects. Nordic J. Bot. 1, 345–355. (doi:10.1111/j.1756-1051.1981. tb00704.x) 53. Barthlott W, Wiersch S, Colic Z, Koch K. 2009 Classification of trichome types within species of the water fern Salvinia, and ontogeny of the egg-beater trichomes. Botany-Botanique 87, 830–836. (doi:10.1139/B09-048) 54. Balmert A, Bohn HF, Ditsche-Kuru P, Barthlott W. 2011 Dry under water: comparative morphology and functional aspects of air-retaining insect surfaces. J. Morphol. 272, 442–451. (doi:10.1002/jmor.10921) 55. Amabili M, Giacomello A, Meloni S, Casciola CM. 2015 Unraveling the Salvinia paradox: design principles for submerged superhydrophobicity. Adv. Mater. Interfaces 2, 1500248. (doi:10.1002/admi.201500248) 56. Cerman Z, Striffler BF, Barthlott W. 2009 Dry in the water: the superhydro-phobic water fern Salvinia – a model for biomimetic surfaces. In Functional surfaces in biology (ed. SN Gorb), ppp. 740. Berlin, Germany: Springer. 57. Ditsche P, Gorb E, Mayser M, Gorb S, Schimmel T, Barthlott W. 2015 Elasticity of the hair cover in air-retaining Salvinia surfaces. Appl. Phys. A 121, 505–511. (doi:10.1007/s00339015-9439-y)

36 .........................................................


58. Mail M, Böhnlein B, Mayser M, Barthlott W. 2015 Bionische Reibungsreduktion: Eine Lufthülle hilft Schiffen Treibstoff zu sparen. In Bionik: Patente aus der Natur – 7. Bremer Bionik-Kongress (eds AB Kesel, D Zehren). Bremen, Germany: Bionik-Innovations-Centrum (B-I-C) Hochschule Bremen. 59. Mayser MJ, Barthlott W. 2014 Layers of air in the water beneath the floating fern Salvinia are exposed to fluctuations in pressure. Integr. Comp. Biol. 54, 1001–1007. (doi:10.1093/ icb/icu072) 60. Mayser MJ, Bohn HF, Reker M, Barthlott W. 2014 Measuring air layer volumes retained by submerged floating-ferns Salvinia and biomimetic superhydrophobic surfaces. Beilstein J. Nanotechnol. 5, 812–821. (doi:10.3762/bjnano.5.93) 61. Melskotte J-E, Brede M, Ott A, Mayser M, Barthlott W, Leder A. 2012 Künstliche Luft haltende Oberflächen zur Reibungsreduktion am Schiff/artificial air retaining surfaces for drag reduction on shiphulls. In Lasermethoden in der Strömungsmesstechnik, vol. 39 (ed. M Brede, B Ruck, D Dopheide), pp. 1–6. Karlsruhe, Germany: Deutsche Gesellschaft für Laser-Anemometrie GALA e.V. 62. Tricinci O, Terencio T, Mazzolai B, Pugno NM, Greco F, Mattoli V. 2015 3D micropatterned surfaces inspired by Salvinia molesta via direct laser lithography. ACS Appl. Mater. Interfaces 7, 25 560–25 567. (doi:10.1021/acsami.5b07722) 63. Gorb SN (ed.). 2009 Functional surfaces in biology: adhesion related phenomena, vol. 1. Berlin, Germany: Springer Science & Business Media. 64. Gorb S (ed.). 2001 Attachment devices of insect cuticle. Berlin, Germany: Springer Science & Business Media. 65. Nelson DRGJB. 1995 Insect waxes. In Waxes: chemistry, molecular Biology and functions (ed. RJ Hamilton). Dundee, Scotland: the oily press. 66. Wagner T, Neinhuis C, Barthlott W. 1996 Wettability and contaminability of insect wings as a function of their surface sculptures. Acta Zool. 77, 213–225. (doi:10.1111/j.14636395.1996.tb01265.x) 67. Sun J, Bhushan B. 2012 Structure and mechanical properties of beetle wings: a review. RSC Adv. 2, 12 606–12 623. (doi:10.1039/c2ra21276e) 68. Zheng Y, Gao X, Jiang L. 2007 Directional adhesion of superhydrophobic butterfly wings. Soft Matter 3, 178–182. (doi:10.1039/B612667G) 69. Neumann D, Woermann D. 2009 Physical conditions for trapping air by a microtrichiacovered insect cuticle during temporary submersion. Naturwissenschaften 96, 933–941. (doi:10.1007/s00114-009-0551-8) 70. Heckman CW. 1983 Comparative morphology of arthropod exterior surfaces with the capability of binding a film of air underwater. Int. Rev. Gesamten Hydrobiol. Hydrogr. 68, 715–736. (doi:10.1002/iroh.3510680515) 71. de Gennes PG, Brochard-Wyart F, Quéré D. 2004 Capillarity and wetting phenomena – drops, bubbles, pearls, waves. New York, NY: Springer. 72. Mittal KL (ed). 2006 Contact angle, wettability and adhesion, vol. 4. Boston, MA: CRC Press. 73. Crawford RJ, Ivanova EP (eds). 2015 Superhydrophobic surfaces, 165. Oxford, UK: Elsevier. 74. Sankar S, Nair BN, Suzuki T, Anilkumar GM, Padmanabhan M, Hareesh UNS, Warrier KG. 2016 Hydrophobic and metallophobic surfaces: highly stable non-wetting inorganic surfaces based on lanthanum phosphate nanorods. Sci. Rep. 6, 22732. (doi:10.1038/srep22732) 75. Tian S, Sun W, Hu Z, Quan B, Xia X, Li Y, Han D, Li J, Gu C. 2014 Morphology modulating the wettability of a diamond film. Langmuir 30, 12 647–12 653. (doi:10.1021/la5022643) 76. Sheldrake Jr R, Matkin OA. 1969 Wetting agents for peat moss. Symp. Peat Horticult. 18, 37–42. 77. Michel JC, Bellon-Fontaine MN, Rivière LM. 1997 Characterisation of the wettability of organic substrates (peat and composted bark) by adsorption measurements. Int. Symp. Growing Media Hydropon. 481, 129–136. 78. Rakitov R, Gorb SN. 2013 Brochosomal coats turn leafhopper (Insecta, Hemiptera, Cicadellidae) integument to superhydrophobic state. Proc. R. Soc. B 280, 20122391. (doi:10.1098/rspb.2012.2391) 79. Doerr SH, Shakesby RA, Walsh RPD. 2000 Soil water repellency: its causes, characteristics and hydro-geomorphological significance. Earth-Sci. Rev. 51, 33–65. (doi:10.1016/S00128252(00)00011-8) 80. Hoppe T, Schwippert WW. 2014 Hydrophobicity of myxomycete spores: an undescribed aspect of spore ornamentation. Mycosphere 5, 601–606.

37 .........................................................


81. Ishige T, Tani A, Sakai Y, Kato N. 2003 Wax ester production by bacteria. Curr. Opin. Microbiol. 6, 244–250. (doi:10.1016/S1369-5274(03)00053-5) 82. Wiencek KM, Klapes NA, Foegeding PM. 1990 Hydrophobicity of Bacillus and Clostridium spores. Appl. Environ. Microbiol. 56, 2600–2605. 83. McNamara CJ, Lemke MJ, Leff LG. 1997 Brief note: characterization of hydrophobic stream bacteria based on adhesion to n-octane. Ohio J. Sci. 97, 59–61. 84. Kolattukudy PE. 2001 Polyesters in higher plants. In Advances in biochemical engineering/biotechnology (eds T Scheper et al.), pp. 4–49. Berlin, Germany: Springer. 85. Naafs DFW, van Bergen PFM, Boogert SJ, de Leeuw JW. 2004 Solvent-extractable lipids in an andic forest soil. Soil Biol. Biochem. 36, 297–308. (doi:10.1016/j.soilbio.2003.10.005) 86. Fernandez JM, Lembrino-Canales JJ, Villena R. 1994 Copper (II) compexes oft Schiffe bases derived oft 2-hydroxy-3-naphthaldehyde. The crystal and molecular structures. Chem. Mon. 125, 275–284. (doi:10.1007/BF00811313) 87. Herth W, Barthlott W. 1979 The site of b-chitin fibril formation in centric diatoms. J. Ultrastruct. Res. 68, 6–15. (doi:10.1016/S0022-5320(79)90137-0) 88. Ehler N, Barthlott W. 1978 Die epicuticulare Skulptur der Testa-Zellwände einiger Mesembryanthemaceae. Bot. Jahrb. Syst. 99, 329–340. 89. Bianchi G. 1995 Plant waxes. In Waxes: chemistry, molecular biology and functions (ed. RJ Hamilton), pp. 175–222. Glasgow, UK: The Oily Press. 90. Walton TJ. 1990 Waxes, cutin and suberin. In Lipids, membranes and aspects of photobiology (eds JL Harwood, JR Bowyer), pp. 105–158. London, UK: Academic Press. 91. Jetter R, Kunst L, Samuels AL. 2006 Composition of plant cuticular waxes. In Annual Plant Reviews, Biology of the plant cuticle (eds M Riederer, C Müller), pp. 145–181. Oxford, UK: Blackwell. 92. Speelman EN, Reichart GJ, de Leeuw JW, Rijpstra WIC, Damsté JSS. 2009 Biomarker lipids of the freshwater fern Azolla and its fossil counterpart from the Eocene Arctic Ocean. Org. Geochem. 40, 628–637. (doi:10.1016/j.orggeochem.2009.02.001) 93. Dommisse A, Wirtz J, Koch K, Wandelt K, Barthlott W, Kolter T. 2007 Synthesis of Snonacosan-10-ol, the main component of plant surface tubular wax crystals. Eur J. Org. Chem. 2007, 3508–3511. (doi:10.1002/ejoc.200700262) 94. Extrand CW, Moon SI. 2014 Repellency of the lotus leaf: contact angles, drop retention, and sliding angles. Langmuir 30, 8791–8797. (doi:10.1021/la5019482) 95. Barthlott W, Erdelen W, Rafiqpoor MD. 2014 Biodiversity and technical innovations: bionics. In Concept and value in biodiversity. Routledge studies in biodiversity politics and management (eds D Lanzerath, M Friele), pp. 300–315. 96. Konrad W, Apeltauer C, Frauendiener J, Barthlott W, Roth-Nebelsick A. 2009 Applying methods from differential geometry to devise stable and persistent air layers attached to objects immersed in water. J. Bion. Eng. 6, 350–356. (doi:10.1016/S1672-6529(08)60133-X) 97. Gandyra D, Walheim S, Gorb S, Barthlott W, Schimmel T. 2015 The capillary adhesion technique: a versatile method for determining the liquid adhesion force and sample stiffness. Beilstein J. Nanotchnol. 6, 11–18. (doi:10.3762/bjnano.6.2) 98. Crowe JH, Magnus KA. 1974 Studies on acarine cuticles. II. Plastron respiration and levitation in a water mite. Comp. Biochem. Physiol. A, Physiol. 49, 301IN5303–302IN8309. (doi:10.1016/0300-9629(74)90121-2) 99. Barthlott W, Große-Veldmann B, Korotkova N. 2014 Orchid seed diversity: a scanning electron microscopy survey. Englera 32, 1–244. 100. Bargel H, Barthlott W, Koch K, Schreiber L, Neinhuis C. 2003 Plant cuticles: multifunctional interfaces between plant and environment. In The evolution of plant physiology (eds AR Hemsley, I Poole), pp. 171–194. London, UK: Academic Press. 101. Neinhuis C, Barthlott W. 1997 Characterization and distribution of water-repellent, selfcleaning plant surfaces. Ann. Bot. 79, 667–677. (doi:10.1006/anbo.1997.0400) 102. Neinhuis C, Wolter M, Barthlott W. 1992 Epicuticular wax of Brassica oleracea: changes in microstructure and ability to be contaminated of leaf surfaces after application of Triton X-100. Z. f. Pflanzenkrankheiten u. Pflanzenschutz 99, 542–549. 103. Vogel P. 1990 Body temperature and fur quality in swimming Water-Shrews, Neomys fodiens (Mammalia, Insectivora). Z. Säugetierkunde 55, 73–80. 104. Helbig R, Nickerl J, Neinhuis C, Werner C. 2011 Smart skin patterns protect springtails. PLoS ONE 6, e25105. (doi:10.1371/journal.pone.0025105)

38 .........................................................


105. McHale G, Newton MI, Shirtcliffe NJ. 2010 Immersed superhydrophobic surfaces: gas exchange, slip and drag reduction properties. Soft Matter 6, 714–719. (doi:10.1039/ b917861a) 106. Ditsche-Kuru P, Schneider ES, Melskotte J-E, Brede M, Leder A, Barthlott W. 2011 Superhydrophobic surfaces of the water bug Notonecta glauca: a model for friction reduction and air retention. Beilstein J. Nanotechnol. 2, 137–144. (doi:10.3762/bjnano.2.17) 107. Nagamine H, Yamahata K, Hagiwara Y, Matsubara R. 2004 Turbulence modification by compliant skin and strata-corneas desquamation of a swimming dolphin. J. Turbul. 5, N18. (doi:10.1088/1468-5248/5/1/018) 108. Davenport J, Hughes RN, Shorten M, Larsen PS. 2011 Drag reduction by air release promotes fast ascent in jumping emperor penguins – a novel hypothesis. Mar. Ecol. Progr. Ser. 430, 171–182. (doi:10.3354/meps08868) 109. Barth FG. 2013 Sinne und Verhalten: aus dem Leben einer Spinne. Berlin, Germany: Springer. 110. Barthlott W, Theisen I, Borsch T, Neinhuis C. 2003 Epicuticular waxes and vascular plant systematics: integrating micromorphological and chemical data. In Deep morphology toward a renaissance of morphology in plant systematics (eds TF Stuessy, V Meyer, E Hörnandl), pp. 189–206. Ruggell, Germany: Gantner. 111. Wollenweber E. 1989 Exkret-Flavonoide bei Blütenpflanzen und Farnen. Naturwiss 76, 458–463. (doi:10.1007/BF00366222) 112. Parker AR, Lawrence CR. 2001 Water capture by a desert beetle. Nature 414, 33–34. (doi:10.1038/35102108) 113. Zhai L, Berg MC, Cebeci FC, Kim Y, Milwid JM, Rubner MF, Cohen RE. 2006 Patterned superhydrophobic surfaces: toward a synthetic mimic of the Namib Desert beetle. Nano Letters 6, 1213–1217. (doi:10.1021/nl060644q) 114. Nickerl J, Helbig R, Schulz Jr H, Werner C, Neinhuis C. 2012 Diversity and potential correlations to the function of Collembola cuticle structures. Zoomorphology 132, 1–13. 115. Hensel R, Helbig R, Aland S, Braun H-G, Voigt A, Neinhuis C, Werner C. 2013 Wetting resistance at its topographical limit – the benefit of mushroom and serif T structures. Langmuir 29, 1100–1112. (doi:10.1021/la304179b) 116. Hensel R, Helbig R, Aland S, Voigt A, Neinhuis C, Werner C. 2013 Tunable nano-replication to explore the omniphobic characteristics of springtail skin. NPG Asia Mater. 5, e37. (doi:10.1038/am.2012.66) 117. Hensel R, Neinhuis C, Werner C. 2015 The springtail cuticle as a blueprint for omniphobic surfaces. Chem. Soc. Rev. 45, 323–341. (doi:10.1039/c5cs00438a) 118. 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, 2029–2033. (doi:10.1002/adma.201305408) 119. Thorpe WH, Crisp DJ. 1947 Studies on plastron respiration; the orientation responses of Aphelocheirus [Hemiptera, Aphelocheiridae (Naucoridae)] in relation to plastron respiration; together with an account of specialized pressure receptors in aquatic insects. J. Exp. Biol. 24, 310. 120. Hinton HE. 1976 Plastron respiration in bugs and beetles. J. Insect Physiol. 22, 1529–1550. (doi:10.1016/0022-1910(76)90221-3) 121. Jones KK, Snelling EP, Watson AP, Seymour RS. 2015 Gas exchange and dive characteristics of the free-swimming backswimmer Anisops deanei. J. Exp. Biol. 218, 3478–3486. (doi:10.1242/jeb.125047) 122. Hu DL, Bush JWM. 2005 Meniscus-climbing insects. Nature 437, 733–736. (doi:10.1038/ nature03995) 123. Hu DL, Chan B, Bush JW. 2003 The hydrodynamics of water strider locomotion. Nature 424, 663–666. (doi:10.1038/nature01793) 124. Feng X-Q, Gao X, Wu Z, Jiang L, Zheng Q-S. 2007 Superior water repellency of water strider legs with hierarchical structures: experiments and analysis. Langmuir 23, 4892–4896. (doi:10.1021/la063039b) 125. Andersen NM, Cheng L. 2004 The marine insect Halobates (Heteroptera: Gerridae): biology, adaptations, distribution, and phylogeny. Oceanogr. Mar. Biol. 42, 119–180. 126. Gao H, Wang X, Yao H, Gorb S, Arzt E. 2005 Mechanics of hierarchical adhesion structures of geckos. Mech. Mater. 37, 275–285. (doi:10.1016/j.mechmat.2004.03.008)

39 .........................................................


127. Liu K, Du J, Wu J, Jiang L. 2012 Superhydrophobic gecko feet with high adhesive forces towards water and their bio-inspired materials. Nanoscale 4, 768–772. (doi:10.1039/ C1NR11369K) 128. Autumn K et al. 2002 Evidence for van der Waals adhesion in gecko setae. Proc. Natl Acad. Sci. USA 99, 12 252–12 256. (doi:10.1073/pnas.192252799) 129. Hiller UN. 2009 Water repellence in gecko skin: how do geckos keep clean? In Functional surfaces in biology (ed. SN Gorb), pp. 47–53. Amsterdam, The Netherlands: Springer. 130. Spinner M, Gorb SN, Balmert A, Bleckmann H, Westhoff G. 2014 Non-contaminating camouflage: multifunctional skin microornamentation in the West African Gaboon viper (Bitis rhinoceros). PLoS ONE 9, e91087. (doi:10.1371/journal.pone.0091087) 131. Martinez-Hernandez AL, Celasco-Santos C, de Icaza M, Castano VM. 2005 Microstructural characteization oft keratin fibres from chicken feathers. Int. J. Environ. Pollut. 23, 162–178. (doi:10.1504/IJEP.2005.006858) 132. Rijke AM, Jesser WA, Evans SW, Bouwman H. 2000 Water repellency and feather structure of the blue swallow Hirundo atrocaerulea. Ostrich 71, 143–145. (doi:10.1080/00306525.2000. 9639893) 133. Srinivasan S, Chhatre SS, Guardado JO, Park K-C, Parker AR, Rubner MF, McKinley GH, Cohen RE. 2014 Quantification of feather structure, wettability and resistance to liquid penetration. J. R. Soc. Interface 11, 20140287. (doi:10.1098/rsif.2014.0287) 134. Grémillet D, Chauvin C, Wilson RP, Le Maho Y, Wanless S. 2005 Unusual feather structure allows partial plumage wettability in diving great cormorants Phalacrocorax carbo. J. Avian Biol. 36, 57–63. (doi:10.1111/j.0908-8857.2005.03331.x) 135. Eliason CM, Shawkey MD. 2011 Decreased hydrophobicity of iridescent feathers: a potential cost of shiny plumage. J. Exp. Biol. 214, 2157–2163. (doi:10.1242/jeb.055822) 136. Appelt H. 1973 Fellstrukturuntersuchungen an Wasserspitzmäusen. Abh. U. Ber. Naturkundl. Mus. Mauritianum ‘Altenburg 8, 81–87. 137. Hutterer R, Hürter T. 1981 AdaptiveHaarstrukturen bei Wasserspitzmäusen (Insectivora, Soricinae). Z. Säugetierkunde 46, 1–11. 138. Köhler D. 1984 Zum Verhaltensinventar der Wasserspitzmaus (Neomys fodiens). Säugetierkd. Inform, Jena 2, 175–199. 139. Ruthardt M, Schröpfer R. 1985 Zum Verhalten der Wasserspitzmaus Neomys fodiens (Pennant, 1771) unter Wasser. Z. Angew. Zool. 72, 49–57. 140. Köhler D. 1991 Notes on the diving behaviour of the water shrew, Neomys fodiens (Mammalia, Soricidae). Zool Anz. 227, 218–228. 141. Remy W, Taylor TN, Hass H, Kerp H. 1994 Four hundred-million-year-old vesicular arbuscular mycorrhizae. Proc. Natl Acad. Sci. USA 91, 11 841–11 843. (doi:10.1073/pnas. 91.25.11841) 142. Honegger R, Edwards D, Axe L. 2013 The earliest records of internally stratified cyanobacterial and algal lichens from the Lower Devonian of the Welsh Borderland. New Phytol. 197, 264–275. (doi:10.1111/nph.12009) 143. Taylor TN, Hass H, Kerp H, Krings M, Hanlin RT. 2005 Perithecial ascomycetes from the 400 million year old Rhynie chert: an example of ancestral polymorphism. Mycologia 97, 269–285. (doi:10.3852/mycologia.97.1.269) 144. Wessels JGH. 1996 Fungal hydrophobins: proteins that function at an interface. Tr. Pl. Sci. 1, 9–15. (doi:10.1016/S1360-1385(96)80017-3) 145. Wösten HAB. 2001 Hydrophobins: multipurpose proteins. Annu. Rev. Microbiol. 55, 625–646. (doi:10.1146/annurev.micro.55.1.625) 146. Shirtcliffe NJ, Brian Pyatt F, Newton MI, McHale G. 2006 A lichen protected by a superhydrophobic and breathable structure. J. Plant Physiol. 163, 1193–1197. (doi:10.1016/j. jplph.2005.11.007) 147. Lakatos M, Rascher U, Büdel B. 2006 Functional characteristics of corticolous lichens in the understory of a tropical lowland rain forest. New Phytol. 172, 679–695. (doi:10.1111/j. 1469-8137.2006.01871.x) 148. Ceballos G, Ehrlich PR, Barnosky AD, García A, Pringle RM, Palmer TM. 2015 Accelerated modern human-induced species losses: entering the sixth mass extinction. Sci. Adv. 1, e1400253. (doi:10.1126/sciadv.1400253) 149. Meyer-Berthaud B, Scheckler SE, Wendt J. 1999 Archaeopteris is the earliest known modern tree. Nature 398, 700–701. (doi:10.1038/19516)

40 .........................................................


150. Qiu Y-L et al. 2006 The deepest divergences in land plants inferred from phylogenomic evidence. Proc. Natl Acad. Sci. USA 103, 15 511–15 516. (doi:10.1073/pnas.0603335103) 151. Ruhfel BR, Gitzendanner MA, Soltis PS, Soltis DE, Burleigh JG. 2014 From algae to angiosperms–inferring the phylogeny of green plants (Viridiplantae) from 360 plastid genomes. BMC Evol. Biol. 14, 1–27. (doi:10.1186/1471-2148-14-23) 152. Filipiak P, Szaniawski H. 2016 Nematophytes from the Lower Devonian of Podolia, Ukraine. Rev. Palaeobot. Palynol. 224, 109–120. (doi:10.1016/j.revpalbo.2015.09.005) 153. Graham LE, Wilcox LW, Cook ME, Gensel PG. 2004 Resistant tissues of modern marchantioid liverworts resemble enigmatic Early Paleozoic microfossils. Proc. Natl Acad . Sci. USA 101, 11 025–11 029. (doi:10.1073/pnas.0400484101) 154. Smith MR, Butterfield NJ. 2013 A new view on Nematothallus: coralline red algae from the Silurian of Gotland. Palaeontology 56, 345–357. (doi:10.1111/j.1475-4983.2012. 01203.x) 155. Taylor TN, Taylor EL, Krings M. 2009 Paleobotany. Amsterdam, The Netherlands: Academic Press. 156. Riederer M, Schreiber L. 1995 Waxes – the transport barriers of plant cuticles. In Waxes: chemistry, molecular biology and functions (ed. RJ Hamilton), pp. 131–156. Dundee, Scotland: The Oily Press. 157. Schreiber L, Schonherr J. 2009 Water and solute permeability of plant cuticles. Heidelberg, Germany: Springer. 158. Kolattukudy PE. 2001 Plant cuticle and suberin. eLS. (doi:10.1038/npg.els.0001920) 159. Heredia A. 2003 Biophysical and biochemical characteristics of cutin, a plant barrier biopolymer. Biochim. Biophys. Acta, Gen. Subjects 1620, 1–7. (doi:10.1016/s0304-4165(02) 00510-x) 160. Jeffree CE. 2006 The fine structure of the plant cuticle. In Biology of the plant cuticle (eds M Riederer, C Müller), pp. 11–125. Oxford, UK: Blackwell. 161. Holloway PJ. 1994 Plant cuticles: physicochemical characteristics and biosynthesis. In Air pollution and the leaf cuticle (eds KE Percy, JN Cape, R Jagels, CJ Simpson), pp. 1–13. Berlin, Germany: Springer. 162. Stark RE, Tian S. 2006 The cutin biopolymer matrix. In Biology of the plant cuticle (eds M Riederer, C Müller). London, UK: Blackwell. 163. Jeffree CE. 1986 The cuticle, epicuticular waxes and trichomes of plants, with reference to their structure, functions and evolution. In Insects and the plant surface (eds BE Juniper, R Southwood), pp. 23–63. London, UK: Edward Arnold. 164. Riederer M, Markstädter C. 1996 Cuticular waxes: a critical assessment of current knowledge. In Plant cuticles an integrated functional approach (ed. G Kerstiens), pp. 189–200. Oxford, UK: University Scientific. 165. Riederer M, Schreiber L. 2001 Protecting against water loss: analysis of the barrier properties of plant cuticles. J. Exp. Bot. 52, 2023–2032. (doi:10.1093/jexbot/52.363.2023) 166. Hallam ND, Chambers TC. 1970 The leaf waxes of the genus Eucalyptus L’Heritier. Aust. J. Bot. 18, 335–386. (doi:10.1071/BT9700335) 167. Jetter R, Riederer M. 1994 Epicuticular crystals of nonacosan-10-ol: in vitro reconstitution and factors influencing crystal habits. Planta 195, 257–270. (doi:10.1007/BF00199686) 168. Matas AJ, Sanz MJ, Heredia A. 2003 Studies on the structure of the plant wax nonacosan10-ol, the main component of epicuticular wax conifers. Int. J. Biol. Macromol. 33, 31–35. (doi:10.1016/S0141-8130(03)00061-8) 169. Jeffree CE, Baker EA, Holloway PJ. 1975 Ultrastructure and recrystallization of plant epicuticular waxes. New Phytol. 75, 539–549. (doi:10.1111/j.1469-8137.1975.tb01417.x) 170. Jetter R, Riederer M. 1995 In vitro reconstitution of epicuticular wax crystals: formation of tubular aggregates by long chain secondary alkanediols. Bot. Acta 108, 111–120. (doi:10.1111/ j.1438-8677.1995.tb00840.x) 171. Franke W. 1970 Ectodesmata and the cuticular penetration of leaves. Pest. Sci. 1, 164–167. (doi:10.1002/ps.2780010412) 172. Samuels L, Jetter R, Kunst L. 2005 First steps in understanding the export of lipids to the plant cuticle. Plant Biosyst. 139, 65–68. (doi:10.1080/11263500500059868) 173. Schreiber L. 2005 Polar paths of diffusion across plant cuticles: new evidence for an old hypothesis. Ann. Bot. 95, 1069–1073. (doi:10.1093/aob/mci122)

41 .........................................................


174. Canet D, Rohr R, Chamel A, Guillain F. 1996 Atomic force microscopy study of isolated ivy leaf cuticles observed directly and after embedding in Epon(R). New Phytol. 134, 571–577. (doi:10.1111/j.1469-8137.1996.tb04922.x) 175. San Diego Zoo Global and Fermanian Business and Economic Institute Point Loma (eds). 2013 Bioninspiration: an economic progress report, pp. 1–45. San Diego. 176. Koch K, Schulte AJ, Fischer A, Gorb SN, Barthlott W. 2008 A fast, precise and low-cost replication technique for nano- and high-aspect-ratio structures of biological and artificial surfaces. Bioinsp. Biomim. 3, 046002. (doi:10.1088/1748-3182/3/4/046002) 177. Schulte AJ, Koch K, Spaeth M, Barthlott W. 2009 Biomimetic replicas: transfer of complex architectures with different optical properties from plant surfaces onto technical materials. Acta Biomater. 5, 1848–1854. (doi:10.1016/j.actbio.2009.01.028) 178. Feng L et al. 2002 Super-hydrophobic surfaces: from natural to artificial. Adv. Mater. 14, 1857–1860. (doi:10.1002/adma.200290020) 179. Lau KK, Bico J, Teo KB, Chhowalla M, Amaratunga GA, Milne WI, McKinley GH, Gleason KK. 2003 Superhydrophobic carbon nanotube forests. Nano Letters 3, 1701–1705. (doi:10.1021/nl034704t) 180. Huang L, Lau SP, Yang HY, Leong ESP, Yu SF, Prawer S. 2005 Stable superhydrophobic surface via carbon nanotubes coated with a ZnO thin film. J. Phys. Chem. B 109, 7746–7748. (doi:10.1021/jp046549s) 181. Han ZJ, Tay BK, Shakerzadeh M, Ostrikovet K. 2009 Superhydrophobic amorphous carbon/carbon nanotube nanocomposites. Appl. Phys. Lett. 94, 223106. (doi:10.1063/1. 3148667) 182. Babu DJ, Varanakkottu SN, Eifert A, de Koning D, Cherkashinin G, Hardt S, Schneider JJ. 2014 Inscribing wettability gradients onto superhydrophobic carbon nanotube surfaces. Adv. Mater. Interfaces 1, 1300049. (doi:10.1002/admi.201300049) 183. Her EK et al. 2013 Superhydrophobic transparent surface of nanostructured poly (methyl methacrylate) enhanced by a hydrolysis reaction. Plasma Process Polym. 10, 481–488. (doi:10.1002/ppap.201200131) 184. Rahmawan Y, Xu L, Yang S. 2013 Self-assembly of nanostructures towards transparent, superhydrophobic surfaces. J. Mater. Chem. A 1, 2955–2969. (doi:10.1039/C2TA00288D) 185. Bico J, Tordeux C, Quere D. 2001 Rough wetting. Europhys. Lett. 55, 214–220. (doi:10.1209/ epl/i2001-00402-x) 186. Grinthal A, Aizenberg J. 2013 Mobile interfaces: liquids as a perfect structural material for multifunctional, antifouling surfaces. Chem. Mater. 26, 698–708. (doi:10.1021/cm402364d) 187. Farhadi S, Farzaneh M, Kulinich SA. 2011 Anti-icing performance of superhydrophobic surfaces. Appl. Surf. Sci. 257, 6264–6269. (doi:10.1016/j.apsusc.2011.02.057) 188. Cao L, Jones AK, Sikka VK, Wu J, Gao D. 2009 Anti-icing superhydrophobic coatings. Langmuir 25, 12 444–12 448. (doi:10.1021/la902882b) 189. Otten A, Herminghaus S. 2004 How plants keep dry: a physicist’s point of view. Langmuir 20, 2405–2408. (doi:10.1021/la034961d) 190. Klein S. 2012 Effizienzsteigerung in der Frachtschifffahrt unter ökonomischen und ökologischen Aspekten am Beispiel der Reederei Hapag Lloyd. Projektarbeit Gepr. Betriebswirt (IHK), Akademie für Welthandel. 191. Melskotte J-E, Brede M, Wolter A, Barthlott W, Leder A. 2013 Schleppversuche an künstlichen, Luft haltenden Oberflächen zur Reibungsreduktion am Schiff in Lasermethoden in der Strömungsmesstechnik, 21. Fachtagung, 3–5. September 2013, München (eds CJ Kähler et al.) 53, 1–7. 192. Genzer J, Efimenko K. 2006 Recent developments in superhydrophobic surfaces and their relevance to marine fouling: a review. Biofouling 22, 339–360. (doi:10.1080/089270 10600980223) 193. Noga G, Wolter M, Barthlott W, Petry W. 1991 Quantitative evaluation of epicuticular wax alterations as induced by surfactant treatment. Angew. Bot. 65, 239–252. 194. Schwab M, Noga G, Barthlott W. 1995 Bedeutung der Epicuticularwachse für die Pathogenabwehr am Beispiel von Botrytis cinerea – Infektionen bei Kohlrabi und Erbse. Gartenbauwissenschaft 60, 102–109.

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