Plant Surfaces: Structures and Functions for Biomimetic Innovations
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An overview of plant surface structures and their evolution is presented. It combines surface chemistry and architecture with their functions and refers to possible biomimetic applications. Within some 3.5 billion years biological species evolved highly complex multifunctional surfaces for interacting with their environments: some 10 million living prototypes (i.e., estimated number of existing plants and animals) for engineers. The complexity of the hierarchical structures and their functionality in biological organisms surpasses all abiotic natural surfaces: even superhydrophobicity is restricted in nature to living organisms and was probably a key evolutionary step with the invasion of terrestrial habitats some 350–450 million years ago in plants and insects. Special attention should be paid to the fact that global environmental change implies a dramatic loss of species and with it the biological role models. Plants, the dominating group of organisms on our planet, are sessile organisms with large multifunctional surfaces and thus exhibit particular intriguing features. Superhydrophilicity and superhydrophobicity are focal points in this work. We estimate that superhydrophobic plant leaves (e.g., grasses) comprise in total an area of around 250 million km2, which is about 50% of the total surface of our planet. A survey of structures and functions based on own examinations of almost 20,000 species is provided, for further references we refer to Barthlott et al. (Philos. Trans. R. Soc. A 374: 20160191, 1). A basic difference exists between aquatic non-vascular and land-living vascular plants; the latter exhibit a particular intriguing surface chemistry and architecture. The diversity of features is described in detail according to their hierarchical structural order. The first underlying and essential feature is the polymer cuticle superimposed by epicuticular wax and the curvature of single cells up to complex multicellular structures. A descriptive terminology for this diversity is provided. Simplified, the functions of plant surface characteristics may be grouped into six categories: (1) mechanical properties, (2) influence on reflection and absorption of spectral radiation, (3) reduction of water loss or increase of water uptake, moisture harvesting, (4) adhesion and non-adhesion (lotus effect, insect trapping), (5) drag and turbulence increase, or (6) air retention under water for drag reduction or gas exchange (Salvinia effect). This list is far from complete. A short overview of the history of bionics and the impressive spectrum of existing and anticipated biomimetic applications are provided. The major challenge for engineers and materials scientists, the durability of the fragile nanocoatings, is also discussed.
KeywordsBionics Superhydrophobicity Hierarchical structuring Lotus effect Salvinia effect Evolution
The cuticle is basically a biopolymer made of polyester called cutin, impregnated with integrated (intracuticular) waxes. Additionally, waxes on the cuticle surface (epicuticular waxes) play an important role in surface structuring at the sub-cellular scale. They occur in different morphologies, show a large variability in their chemistry, and are able to self-assemble into three-dimensional crystals. Intracuticular waxes function as the main transport barrier to reduce the loss of water and small molecules such as ions from inside of the cell, and also for reducing the uptake of liquids and molecules from the outside. Epicuticular waxes form the boundary layer for many interactions with the plant´s environment, like wettability or spectral reflection (see Sect. 6). The next layer (Fig. 6) is the pectin layer. It connects the cuticle to the much thicker underlying cellulose wall, which is built by single cellulose fibrils. Pectin is not always formed as a layer, but in some species, especially during the early ontogeny of the cuticle, a layered structure has been shown by transmission electron microscopy (TEM). Additionally polysaccharides, not shown in this schematic, are integrated into the cellulose wall. The last layer shown is the plasma membrane, which separates the living, water-containing compartment cell from the outer non-living part of the epidermis.
We focus on superhydrophobic and superhydrophilic surfaces, which are of particular importance for biomimetic applications (e.g., self-cleaning: lotus effect). Superhydrophilicity means, a droplet imposed on a surface “spreads” instantly and a contact angle cannot even be measured, e.g., in the leaves of Ruellia . In contrast, on a superhydrophobic surface water remains as an almost globular droplet with a contact angle of more than 150°. The SEM micrographs presented were largely taken from our archive of almost 220,000 SEM micrographs at the University of Bonn which has been built up as a result of over four decades of research on biological surfaces (compare Ref. ) by the first author and his collaborators.
Biomimetics and bionics (which we consider here as synonymous) are surmised to be modern scientific fields; despite the evidence that inspiration from living organisms is as old as mankind. The magnificent 17,000-year-old paleolithic paintings in the caves of Lascaux are bioinspired—like the Cadillac tail fins in the 1960s. Bio-inspiration in the sense of non-functional “biodecoration” is an inspiration for art and design into modern times [11, 12]. Early attempts to copy mechanical functions were not particularly successful—Ovid’s story of Daedalus and Icarus and Leonardo da Vinci´s design of flying machines and other devices did not translate into technical success stories.
Historically, the dream of flying and the use of the strange phenomena “electricity” were the two fundamental forces for the foundation of what we call today bionics or biomimetics. The construction of an electric battery based on observations of the Torpedo fish (today we call it Electric Ray) by Alessandro Volta in 1800 was the first milestone  of bionics. And Icarus´ dream was realized with the first well-documented, repeated, and successful flights by Otto Lilienthal from 1894 onwards; his design was based on his analysis of the flight of birds. The term “Biotechnik” (usually abbreviated in German as “Bionik”) for the new field was coined by Raul Francé in 1920  and finally rediscovered under the influence of cybernetics under the name “Bionics”  and “Biomimetics” between 1960 and 1964; the misleading term “Biomimicry” arose in 1982 (for a historical survey see Ref. ). Surfaces came surprisingly late into the focus of bionics: The Swiss engineer George de Mestral observed in 1941 the way that the burrs (Arctium) clung to his trousers and his dog—in 1958, he developed the bionic hook-and-loop fastener under the trade mark Velcro®. Starting with the discovery of hierarchically structured superhydrophobic lotus-surfaces [2, 15, 16] and the drag-reducing shark skin [17, 18], biomimetic surface technologies (e.g., lotus-, shark-, gecko-, moth eye-, and salvinia-effect) became a most important field [1, 19, 20]. The publication of the “Lotus Effect®” in 1997  led to a change of paradigms in surface technologies . Biological role models provide an extraordinary diversity for innovative surface technologies, which are described for plants in the following chapters primarily under the view of biologists.
This paper is completely based on our Sect. 3.6 “Plant Surfaces: Structures and Functions for Biomimetic Applications” in the 4th edition of B. Bhushan, Handbook of Nanotechnology (Springer 2017) .
2 Chemistry of Plant Surfaces
2.1 Chemical Composition of Wax
The most common chemical compounds in plant waxes and their spectrum of chain length
1 Aliphatic compounds
1.1 In waxes frequently existing, but mostly as minor compounds
1.2 In waxes rarely existing, but if, than as major wax compounds
Ketones e.g., palmitones
Sec. alcohols e.g., nonacosan-10-ol
2 Cyclic Compounds
e.g., Quercetin Open image in new window
Common wax types in plant species and their major chemical compounds
Dominating chemical compound(s)
Prim. alcohols, aldehydes
Fatty acids C24–C30, prim. alcohols C24–C28
Alkanes C29, C31
Aldehydes C30, C32, alkane C31
Beta-diketone C31, hydroxy-beta-diketone C31
Sec. alcohol C29
Sec. alkanediols C29
Thalictrum flavum glaucum
Sec. alcohol C29
Sec. alcohol C29
Sec. alcohol C29
Prim. alcohol C26, C28, aldehydes
Prim. alcohol C26, aldehydes
Prim. alcohol C26
Prim. alcohol C26
Prim. alcohol C28
Transversely ridged rodlets
Transversely ridged rodlets
Transversely ridged rodlets
Longitudinal ridged rodlets
Many or even most plant “waxes” do not match the chemical definition of true waxes and they are usually complex mixtures of differing compounds. For example, triterpenoids are cyclic hydrocarbons, which occur in high concentrations in the epicuticular coatings of grapes (Vitis vinifera) . Other plant waxes contain polymeric components such as polymerized aldehydes which are only slightly soluble in chloroform [33, 34]. It should be noted that nearly all the existing data of the chemical composition of plant waxes are based on solvent-extracted waxes. These are mixtures of epicuticular and intracuticular waxes, which may be chemically different, as shown for the waxes of Prunus laurocerasus by Jetter and Schäffer  and by Wen et al. , for Taxus baccata. The development of more selective methods of wax sampling allows selective removal of the epicuticular waxes and their analysis separately from the intracuticular wax fractions [27, 36].
Epicuticular wax structures usually occur in the size ranging from 0.2 to 100 µm (Fig. 7); thus, the appropriate microscopic techniques for investigation of their morphology are SEM and low pressure- or environmental SEM. Several SEM investigations showed that most of the epicuticular waxes form three-dimensional structures, with great variations of their morphologies. Comprehensive overviews of the terminology and micromorphology of epicuticular waxes are given by Barthlott et al. , Jeffree , and in Ref. . The comprehensive classification of Barthlott et al. , which we follow here, includes 23 different wax types. It is based on chemical and morphological features and also considers orientation of single crystals on the surface and the orientation of the waxes to each other (pattern formation). In this classification, the wax morphologies include thin films and several three-dimensional structures such as crusts, platelets, filaments, rods, and tubules which have a hollow center. Morphological sub-types are, for example, entire and non-entire wax platelets. A further sub-classification is based on the arrangement of the crystals, e.g., whether they are randomly distributed, in clusters, in parallel orientation, or in specific arrangements around stomata, as the “Convallaria” type (Fig. 7h). The most common wax morphologies are introduced in the following section and are shown in Table 2.
Three-dimensional waxes occur in different morphologies. Most common are tubules, platelets, rodlets, and longitudinally aggregated rodlets shown in Fig. 7d–i.
Wax tubules are hollow structures, which can be distinguished chemically and morphologically. The first type, called nonacosanol tubules, contains large amounts of asymmetrical secondary alcohols, predominantly nonacosan-10-ol and its homologues and to a certain degree also asymmetrical diols [23, 44, 45]. Nonacosan-10-ol is the most common “waxy” coating of all major vascular plant groups and was evolved with the conquest of land some 450 million years ago, a phylogenetic tree is provided by Ref. . The nonacosanol tubules are usually 0.3–1.1 µm long and 0.1–0.2 µm wide. The second type of tubules contains high amounts of ß-diketones, such as hentriacontane-14,16-dione . This particular kind of wax tubule is characteristic for many grasses (Poaceae) and also occurs in various other groups . Figure 7e shows that the ß-diketone tubules are two to five times longer than the nonacosanol tubules shown in Fig. 7d. Their length reaches from 2 to 5 µm, and diameters vary between 0.2 and 0.3 µm.
Platelets, as shown in Fig. 7f, are the very common wax structures found in all major groups of plants. Following the terminology of Barthlott et al. , waxes are termed platelets when flat crystals are connected with their narrow side to the surface. Platelets can be further differentiated by their outline into, e.g., entire or undulated ones. Platelets vary considerably in shape, chemical composition, and spatial pattern. For platelets, only limited information about the connection between morphology and chemical composition is available. In some species, wax platelets are dominated by high amounts of a single chemical compound, which can be primary alcohols, alkanes, aldehydes, esters, secondary alcohols, or flavonoids . In contrast to platelets, plates are polygonal crystalloids with distinct edges and are attached to the surface at varying angles.
The morphology of three-dimensional wax structures is not necessarily determined by the dominating chemical compound or compound class. One example of wax crystals determined by a minor component of a complex mixture is the transversely ridged rodlets, shown in Fig. 7g, which contain high amounts of hentriacontane-16-one (palmitone) . Wax rodlets are massive sculptures which are irregular, polygonal, triangular, or circular in their cross sections. They have a distinct longitudinal axis, with a length/width ratio usually not exceeding 50:1. In addition, rodlets may have a variable diameter along the length of their axis. More complex structures are the longitudinally ridged rodlets, as those found on banana leaves (Musa species), shown in Fig. 7h. These waxes consist exclusively of aliphatic compounds, with high amounts of wax esters and less of hydrocarbons, aldehydes, primary alcohols, and fatty acids. The origin of these wax aggregates is still not clear, and so far all attempts to recrystallize these wax types have failed. As a consequence of that, it is assumed that their origin is connected to structural properties of the underlying plant cuticle.
Brassica oleracea is known to have very complex wax crystal morphology, several cultivars form several different wax types, and where several different wax morphologies can occur on the same cell surface . Why the different three-dimensional wax morphologies co-exist on the surface of a single cell is unknown, as is whether these different morphologies are built up by phase separation of different compounds or if they are formed by the same compound.
The last example in Fig. 7i represents plant surfaces on which waxes are arranged in a specific pattern. Examples are parallel rows of longitudinally aligned platelets, with the orientation extending over several cells (e.g., in Convallaria majalis, shown in Fig. 7i), or rosettes, in which the arrangements of platelets are more or less in radially assembled clusters. In particular, the parallel orientation of platelets on the leaves of several plant species leads to the question of how the orientation is controlled by the plant. It is assumed that the cutin network functions as a template for the growth of the three-dimensional wax crystals, but there is still a lack of information about the molecular structure of the cuticle, so this question is still unanswered.
Certain surface wax morphologies and their orientation patterns are characteristic for certain groups of plants; thus, patterns and the morphology of plant waxes have been used in plant systematics. Barthlott et al.  provide an overview of the existence of the most important wax types in plants, based on SEM analysis of at least 13,000 species, representing all major groups of vascular plants.
2.2 Chemical Heterogeneities
Surfaces of a particular plant species may exhibit chemical heterogeneities in the classical sense, the best example are the superhydrophilic pinning anchor cells on top of each superhydrophobic trichome of Salvinia molesta (Fig. 28): In a broader sense, all organism have chemically heterogeneous surfaces: root surfaces differ dramatically from leaf surfaces. And within one leaf, the upper side differs from the underside. In leaves of Quercus robur, contact angles range from 30° to 130° depending on the part of the leaves where wettability was determined .
The aquatic watermilfoil Myriophyllum brasiliense is—like all submersed water plants—superhydrophilic, a contact angle of the leaves cannot be determined. However, as soon a flowering shoot approaches the water level, wax crystals are generated and the new leaves outside of the water exhibit a contact angle of 162° like in a lotus leaf .
All aliphatic plant surface waxes have a crystalline order. The classical definition for crystals implies a periodic structure in three dimensions, but with the increasing importance of liquid crystals and the detection of quasicrystals, it has become necessary to extend the definition, so that certain less periodic and helical structures, as found for some waxes, were included .
Self-assembly of waxes is an inherent result of the crystalline nature. That different wax morphologies on plant surfaces originate by self-assembly of the wax molecules has been shown by the recrystallization of waxes, which were isolated from plant surfaces [28, 40, 45, 50, 51, 52]. In these studies, most waxes recrystallized in their original morphology, as found on the plant surfaces.
Self-assembly processes resulting in nano- and micro-structures are found in nature, as well as in engineering. They are the basis for highly efficient ways of structuring surfaces down to the molecular level. Self-assembly is a general process of structuring in which atoms, molecules, particles, or other building units interact and self-organize to form well-defined structures. The processes of self-assembly in molecular systems are determined by five characteristics: the components, interactions, reversibility, environment, and mass transport with agitation . The most important driving forces are weak and non-covalent intermolecular interactions, such as Van der Waals and Coulomb interactions, hydrophobic interactions, and hydrogen bonds. During self-assembly, their interactions start from a less-ordered state, e.g., dissolved waxes in a solution, to a final more-ordered state, a crystal [54, 55]. Environmental factors such as temperature, solvent, and substrate might influence the self-assembly process, and in the case of waxes, their morphology.
An example of wax crystals composed of more than one compound is the transversely ridged rodlets. These waxes can be recrystallized from the total wax mixture, but not from individual compounds such as alkanes or palmitones. For these waxes, it is assumed that their morphologies are also formed by a self-assembly-based crystallization process, but the presence of minor amounts of other compounds is required as an additive for crystal growth .
Chemical analysis of the leaf waxes of Lotus and Nasturtium (Tropaeolum majus) shows that waxes of both species are composed of a mixture of aliphatic compounds, with nonacosan-10-ol (a secondary alcohol) and nonacosandiols (an C29 alkane with two alcohol groups) as their main components . These compounds have been separated from the rest of the wax compounds and used for recrystallization experiments. It could be shown with mixtures of nonacosan-10-ol and nonacosandiols components that a minimum amount of two percent of nonacosandiols support tubules formation .
Analysis of wax chemistry, crystalline order, and their self-assembly has led to a better understanding of the molecular architecture of three-dimensional waxes . Based on these data, a model of nonacosan-10-ol tubule structure has been developed, as shown in Fig. 13a. Here it is assumed that the lateral oxygen atoms at the side of the straight molecules hinder the formation of the normal, densely packed, orthorhombic structure and require additional space, causing a local disorder between the molecules and cause a spiral growth, leading to the tubule form.
Glands or glandular trichomes may produce very particular substances, they can be found on approximately 30% of all vascular plants . Multicellular glands include salt glands, nectaries, or the adhesive-secreting glands of some carnivorous plants . Secretion and accumulation of toxic compounds at the plant surface allows direct contact with insects, pathogens, and herbivores, and might therefore be an effective defense strategy . The exudates of glands are, for example, terpenoids, nicotine, alkaloids, or flavonoids. The exudates of some ferns and angiosperms, in particular several members of the Primulaceae, are composed of flavonoids [65, 66]. These flavonoid exudates or “farina” are morphologically similar to waxes, but are chemically distinct from plant waxes. Other glandular trichomes, such as the glands of the carnivorous plants of the genera Drosera (sundew) and Pinguicula (butterworts) secrete adhesives and enzymes to trap and digest small insects like mosquitoes and fruit flies.
Chemical heterogeneities are implied by the presence of other glands. The definition of this phenomenon depends on the scale: all biological surfaces show chemical heterogeneities, the most common case are leaves with a hydrophilic upper side and a superhydrophobic lower side. On a much smaller scale, the trichomes of certain Salvinia species are most remarkable for hydrophilic islands within a superhydrophobic surface, the Salvinia paradox (Fig. 28) [1, 67].
3 Structuring of Plant Surfaces: Hierarchical Architecture between Nano- and Macrostructures
3.1 The Cuticle
Primarily water plants (from unicellular algae to giant seaweeds) lack a cuticle; this particular polymer layer is restricted to higher plants (see Sect. 8).
The cuticle covers leaves, flowers, stems, fruits, and seeds and serves as a protective continuous layer covering the primary organs of all vascular plants and mosses. But in roots and secondary structures (e.g., bark) a cuticle is not present. The cuticle is a hydrophobic composite material, composed of a polymer called cutin and integrated and superimposed lipids called “waxes” (see Sect. 2). The cuticle network is formed by cutin, a polyester-like biopolymer composed of hydroxyl and hydroxyepoxy fatty acids, and sometimes also by cutan, which is built by polymethylene chains. Non-lipid compounds of the cuticle are cellulose, pectin, phenols, and proteins. Large differences in the chemical composition and microstructure of the cuticle have been found by comparing different species and different developmental stages. Chemical composition, microstructure, and biosynthesis of the cuticle have been reviewed by several authors [26, 68, 69, 70, 71, 72, 73, 74, 75].
3.2 Hierarchical Sculpturing
3.3 First Sculptural Level
Flat surfaces defined by their hydrophilic or hydrophobic chemistry on the scale of the resolution of a scanning electron microscope (SEM). Flat is a relative category that depends on the scale. Here, we limit the definition of flat to surfaces that feature structures of usually less than 10 nm in height. Flat surfaces are rarely found in plants and animals, e.g., the leaves of Rubber Figs (Ficus elastic).
3.4 Second Sculptural Level
Cell surfaces are covered with structures between 50 nm and 20 µm. Structures at this level on plants are usually formed by epicuticular wax crystals (e.g., Fig. 7) which may exhibit a large spectrum of shapes like rodlets, platelets, or tubules. They may exceed 200 µm in height (e.g., Strelitzia, Copernicia, Benincasa).
Cuticular foldings have been described for nearly all epidermal surfaces of plants, but are frequently found in the leaves of flowers (petals), and on seed surfaces. They occur as folding or tubercular (verrucate) patterns, which originate due to the cuticle itself by an overproduction of cutin . The pattern of cuticular folds can be categorized according to the thickness (width) of the folds, distances between the folds, and by their orientation . Additionally, the pattern of folding within a single cell can be different in the central (inner area) and anticlinal field (outer area) of a cell. Figure 15 shows different patterns of cuticle folding. On the leaves of Schismatoglottis neoguinensis (Fig. 15a, b) the folding is orderless and covers the central and anticlinal field of the cells. On the lower leaf side (adaxial) of Alocasia macrorrhiza, shown in Fig. 15c, the cuticle forms node-like folding in the central part of each cell. The flower petals of Rosa montana, shown in Fig. 15d, have convex cells with a small central field with a rippled-folded cuticle and parallel folds in the anticlinal field. The papilla cells of the flower petals of Viola tricolor, shown in Fig. 15e, have a parallel folding from the center to the anticlines of the cells. The cells inside the trap of the carnivorous plant Sarracenia leucophylla, shown in Fig. 15f, are hair-papillae, with a conical shape curved in a downward direction. On these, a parallel cuticle folding exists with larger distance at the base and a denser arrangement at the cell tip. The seed surface of Austrocactus patagonicus, shown in Fig. 15g, has cupular formed cells with unstructured central fields and broad parallel folds in the anticlinal fields. A high-magnification SEM micrograph of the seed surface of Aztekium ritteri, shown in Fig. 15h, i, shows a partially removed cuticle and demonstrates that the origin of surface folding is caused by the cuticle itself.
Some micro-structures on epidermis cells arise from sub-cuticular inserts of mineral crystals, as indicated in Fig. 17b. These sub-cuticular inserts can be solid crystals of silicon dioxide, as shown in Fig. 16a, b for tin plant or horse tail (Equisetum) plants. Calcium oxalate crystals are also frequently found in plants, and verification of silicon or calcium presence can be made simply by energy dispersive X-rays (EDX) analysis, included in SEM. Silicon (Si) is a bioactive element associated with beneficial effects on mechanical and physiological properties of plants. It is a common element found in plants and occurs as monosilic acid or in the polymerized form as phytoliths (SiO2–nH2O) . In plants, Silica tends to crystallize in the form of silica in cell walls, cell lumina, at intercellular spaces and in the sub-cuticular layer . Recently Ensikat et al.  investigated calcium apatite, a material which plays a crucial role in animals, in the complex trichomes of the family Loasaceae (Fig. 16c–e). Calcium oxalate crystals have been reported for more than 250 plant families ; they are deposed within the living tissue.
3.5 Third Sculptural 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, which may be unicellular or multicellular (for a terminology see Ref. ); dimensions range from about 2 µm to several centimeters, i.e., in trichomes, (hairs). Structures of the second level may be superimposed to structures of the third level (e.g., Fig. 22). To understand this level, often a thorough microscopic analysis is essential, as the description and terminology for this diversity are complex.
The outlines of cells. The description of plant micro- and nanostructures requires the use of some basic uniform terms, for example, to describe the outline of a single epidermis cell. Several variations are known and introduced in detail by Barthlott and Ehler , Barthlott , and Koch et al. [82, 83]. In the following, a brief introduction is given.
The leaf surfaces of Leucadendron argenteum and Kalanchoe tomentosa, shown in the SEM micrographs in Figs. 14a, b, are two representative surfaces with hairs. Hairs can decrease, but also increase the loss of water and influence the wettability of the surfaces . The wide spectrum of functions of plant hairs has been reviewed by Wagner et al. , and more recently by Martin and Glover . With respect to their functions, it is important to notice that hairs can be glandular or non-glandular (non-secreting), dead or living, and hairs can also be built up by several cells (multicellular), which are introduced later. Unicellular trichomes can be found on the aerial surfaces of most flower-plants (angiosperms), some conifers (gymnosperms) and on some mosses (bryophytes) . Many plants of dry habitats show a dense cover of dead, air-filled hairs to reflect the visible light, which makes the surfaces appear white. The structures of hairs are often more complex; thus, the definition based on the aspect ratio fits well only for simple, undivided hairs. On the shoots of common beans (Phaseolus vulgaris), hairs form hooks to get better adhesion for climbing (Fig. 14c) and in Caiophora coronaria (Fig. 14d) and Cynoglossum officinale (Fig. 14e) the hairs have lateral barbed hooks. The stellate hairs of Virola surinamensis differ by having completely smooth surfaces from the other epidermal cells covered by a dense layer of wax crystals (Fig. 14f). Further trichomes are the simple or double-branched hairs and secretion glands on the leaves of Cistus symphytifolius and Lavandula angustifolia as shown in Fig. 14g, h. These complex hair structures require a more differentiated description than the aspect ratio used for simple hairs [86, 87]. The sizes and morphologies of trichomes are often species specific, making some trichomes useful as morphological features in plant systematics . Deformation induced by water loss of dead-desiccated cells can leads to concave cell morphologies and other complex modifications (Fig. 3). This is characteristic for seed coats and can result in most complex hierarchical sculpturing formed in cacti  or orchids .
3.6 Fourth Sculptural Level
Multicellular structures caused by specific arrangement patterns of several of epidermal cells. There is a wide variety of possibilities for this group of structuring. Multicellular hairs are common in all groups of vascular plants, apart from conifers.
Particularly interesting forms occur in the floating ferns of the genus Salvinia. Within this genus, morphologically different kinds of water-repellent (superhydrophobic) hairs exist , which in some species (S. auriculata, S. molesta) show functionally important chemical heterogeneities (see Sect. 2) by utilizing hydrophilic anchor cells at the tip of the trichomes to stabilize the air–water interfaces [1, 67]. Four different hair types have been described for the genus Salvinia . Based on these morphological types, the genus Salvinia is divided into four groups, each with several species. The Cucullata-type is characterized by solitary and slightly bent trichomes and occurs in S. cucullata and S. hastate. The Oblongifolia-type forms groups of two trichomes, which bend in the same direction and sit on an emergence. This type occurs on S. oblongifolia. The Natans-type, shown in Fig. 14i, has four trichome branches, each elevated on a large multicellular base and in total has a height of up to 1300 µm. The heights of the trichome-groups decrease towards the leaf margins. This type occurs in S. natans and S. minima. In the Molesta-type (Fig. 23c), four trichome branches are grouped together, connected with each other by their terminal cells and sitting on a large emergence. The heights of these trichomes reach up to 2200 µm in S. molesta, but also decrease towards the leaf margins. This trichome-type is characteristic for, e.g., S. molesta and S. biloba. In all these species, the epidermis is covered with small three-dimensional waxes in the form of transversely ridged rodlets. The development of these complex structures has been studied in S. biloba, by Barthlott et al. . In an early stage of leaf development, the hair formation starts with a grouping of four cells. During the ontogeny of the leaf, four branches develop from these initial cells and form a crown-like structure, in which the single branches are connected with each other. Later, the base grows by cell division and cell expansion to develop a large base below the crown structure.
4 Physical Basis of Surface Wetting
Wetting is the fundamental process of liquid interaction at solid–gaseous interfaces. It describes how a liquid comes in contact with a solid surface. The basics of surface wetting are summarized here; extensive literature on the topic exists: Israelachvili , Bhushan , De Gennes et al.  and Bhushan , Nosonovsky and Bhushan , Bormashenko , Butt et al. , Schellenberger et al. , and Bhushan .
On water-repellent surfaces, a droplet applied starts to roll-off the surface when it is tilted to a specific angle. This tilt angle (TA) is simply defined as the tilting angle of a surface on which an applied drop of water starts to move. Low TA (<10°) is characteristic for superhydrophobic and self-cleaning surfaces. If the droplet is in Cassie–Baxter stage , with air trapped between the surface and the applied water droplet, the real contact between the droplet and the surface is very small compared to wettable surfaces, on which an applied drop of water tends to spread, and contact angle is low. In intermediate wetting stages , high contact angles correspond with an increased contact between the surface and the water droplet applied. This phenomenon has also been described as petal-effect [107, 112] because of its occurrence in the flower leaves (petals) of some roses.
Dynamic interactions are bouncing, splashing, and spreading of droplets. The impact behavior of falling drops has been subject to studies for several liquids, such as water, ethanol, emulsions, and various types of structured and unstructured, solid and liquid surfaces [113, 114]. In addition to the physicochemical surface properties and structures, other factors determine the impact behavior of falling drops: their velocity, size, surface tension, and viscosity [115, 116, 117]. Falling drops can impact without any breakup or impact with a splash or splashing, in which the impacting drop releases smaller droplets flying away from the point of impact. Roughly two different types of splashing on incompliant surfaces are described, the “prompt splash” and the “corona splash”. The “corona splash” consists of relatively large droplets and is the outcome of breaking up fingers developing at a flattening drop’s rim. In “prompt splash” very small and fast droplets are generated when the advancing lamella of a spreading drop is disturbed by rough surface structures higher than a specific fraction of the lamella, causing the lamella to rupture locally and release small splash droplets .
Dynamic interactions between water droplets and the surfaces are well researched in the different types of splash-phenomena described, e.g., in Rioboo et al. , Yarin , Xu et al. , Motzkus et al. , Gilet and Bourouiba , and Koch and Grichnik . More recently in focus came the contact times between droplets and surfaces: the time span a drop impacting and bouncing on a hydrophobic surface is in contact with the surface. The contact time as well as the shape of the rebound droplet strongly depends on the structure and the chemistry of the surface. A reduction of this contact time is of advantage in several applications, e.g., anti-icing, self-cleaning, or spray cooling . But also in biological surfaces, the contact time might be important.
Dynamic wetting processes and their control may play an underestimated role in the interaction between plant surfaces and rain, the maintenance of air layers under water, or pesticide applications.
5 Superhydrophilic and Superhydrophobic Plant Surfaces
Hydrophilic and superhydrophilic surfaces (contact angle—if measurable—between 0° and <90°) are known from all aquatic plants and many surfaces of land plants which usually have a papillate cell morphology and cuticular folds, but also from leaves with flat, tabular cells. Surfaces covered by wax may become hydrophilic with the erosion of theses layers (e.g., Carnegiea, Fig. 1a), a very common process in many plants (see below). Modified wax layers may even become superhydrophilic like in the Atacama desert cactus Copiapoa cinerea adapted to fog harvesting. Hydrophilic behavior in flower petals of the daisy family (Asteraceae) and their polymer replica was analyzed in detail by Koch et al.  and provides information for biomimetic applications (see Sect. 7).
Superhydrophobicity is usually not very persistent in plant surfaces. Leaves, with a limited life span, do usually not last longer than one year. Persistent leathery leaves (like in many Mediterranean and tropical climates) are usually hydrophilic—but they may start to be hydrophobic in their earliest developmental stages. This dynamics can be measured in the persistent leaves of Welwitschia mirabilis, a single leaf growing over two centuries from its base. They start being superhydrophobic exhibiting tubular nonacosan-crystals which eroded after the first year and the leaf becomes wettable . Plums are covered by a mechanically delicate whitish wax cover—touching it with a finger is enough to destroy the structure and thus the “glaucous” color. An extreme provides the chemically complex brilliant white waxy coating of the succulent desert plants of the genus Dudleya (e.g., D. brittonii): it only takes a rain drop to destroy the instable coating . Dudleya is not self-healing, in contrast to other plants, where a wax cover destroyed may regenerate within hours.
Only few surfaces like lotus leaves have a very stable superhydrophobicity. As indicated in the introduction, superhydrophobicity usually disappears in aging biological surfaces and they become wettable (compare, Fig. 1a).
6 Functional Diversity of Plant Surfaces
6.1 Mechanical Properties
The cuticle itself is a highly sophisticated chemically stable layer which serves as an elastic mechanical protective structure [74, 128]. The shape of a ripe tomato is maintained to a high degree by its thin cuticle. Hierarchical surface structures fulfill various mechanical tasks; they can reduce the ability of insects to walk (e.g., fish-hooked hairs on bean leaves against aphids, trapping surfaces in insectivorous plants or flowers of Arum) or increase the ability of insects to walk, as is the case in flowers and even orient the visitors with cuticular folds . Mechanochemical defense trichomes are common like in nettles (Urtica) or in Loasaceae (Fig. 14d).
Attachment mechanisms are most common in zoochorous fruits like burrs; complicated hooked spines, and hairs are evolved in many groups (Asteraceae, Krameriaceae, Pedaliaceae) . A particularly refined attachment mechanism with extractable cellulose threads occurs in the seeds of the orchid Chiloschista . Attachment plays a role in the interaction between pollen and its disperser and the stigma, where it becomes deposed. Climbing plants like Ivy (Hedera) or some highly specialized water plants that are growing on rocks in currents (e.g., Podostemaceae) exhibit attachment devices by glue-like adhesives, which are not really surface phenomena.
6.3 Reflection, Absorption, and Transmission of Spectral Radiation
Reflection, absorption, and transmission of spectral radiation are of crucial importance for light harvesting and temperature control under insolation; colors as well as light reflection play an important role in the interaction between flowers and their pollinators.
6.3.1 Light Management
Absorption of light for photosynthesis is the precondition for plant life. Leaves need to collect electromagnetic radiation through photosynthesis while flowers need to harvest radiation in order to intensify their coloration to be more attractive for pollinators. In these processes, the architecture of the plant surfaces plays an important role. While self-cleaning surfaces often combine convex- or concave-shaped epidermal cells with water-repellent 3D waxes, light-harvesting leaf surfaces often possess only convexly shaped epidermal cells. Specifically plants under low-light conditions reduce the loss of light due to specular surface reflection by increasing the transmittance of energy via multiple reflections between the surface structures . An extreme example is the “luminescent moss” Schistostega living in caves with batteries of spherical cells collecting the faintest light-like lenses . However, convexly shaped cells combined with a cuticular folding on top are well known for petal surfaces, especially in angiosperms . These cuticular folds were thought to reduce the surface reflection , act as a specific optical signal for pollinators  and cause iridescence generated through diffraction gratings .
6.3.2 Coloration Signals
6.3.3 Temperature Control Under Insolation
The plant surface can only tolerate temperatures of up to 45 °C for living tissue. As for example, a car top heats up to more the 60 °C on a hot summer day, avoiding such temperatures is a crucial challenge for living tissue under solar radiation. Transpiration cooling is an obvious adaption, but inevitably connected with loss of water. Obviously, the highly reflective wax coatings or an indumentum of hairs decreases the heating [143, 144, 145, 146]. An important aspect of temperature control—apart from reflections—may be the increase of turbulences by mechanical turbulence aids (e.g., the diversity of leaf margins) under dynamic (wind) conditions, which enhance the temperature exchange between the cooler air and the heated isolated leaf surfaces [147, 148, 149, 150]. It is not by chance that succulents of the arid hot regions exhibit a high complexity of hierarchical surfaces sculpturing.
6.4 Reduction of Water Loss
Many of the land plant surface structures must be observed in context of reduction of water loss—a well-researched field. The cuticle, wax layers, and an indumentum of dense hairs play the crucial role in preventing loss of water, in some desert plants like Sarcocaulon the waxy layer might be more than one centimeter in thickness. This function is rather irrelevant for biomimetic applications: non-organic materials like metals and synthetic polymers provide better solutions. Uptake of water is connected with superhydrophilicity (see Sect. 6.5).
Some superhydrophilic water plants have optimized surfaces and morphologies to resist water flows. By exhibiting grid-like leaves the Madagascar Laceleaf (Fig. 5c) reduces its flow resistance. The superhydrophilic wave-swept giant seaweeds (Phaeophyta) are adapted by their morphology to reduce drag . Their leathery thallus is covered by a mucilage; recent work indicates that the superhydrophilicity of the mucilaginous surface acts as a drag-reducing agent like the mucilage of fish.
Unwettability per se to avoid wetting for mechanical reasons: thin laminar leaves become too heavy when wetted. This is probably an important determination leading to the adaptation of superhydrophobicity in larger leaves in rain forests (e.g., Cibotium )—an extreme provides the Titan Arum Amorphophallus (Fig. 1b).
Reduction of adhesion for insects—usually connected with superhydrophobicity—is caused by epicuticular wax crystals in insect-catching plants (e.g., Sarracenia, Nepenthes) or flowers which trap their pollinators (Ceropegia, Aristolochia) or to avoid unwanted nectar thieves (Fritillaria, Lapageria). Superhydrophobicity itself is not the primary function in these surfaces.
Reduction of adhesion to avoid contamination (lotus effect, shown in Fig. 21) enables the plants to be cleaned from any kind of contaminating particle by raindrops, it is probably the most important function of superhydrophobicity in plants [1, 15, 157, 158]. Biologically, such surfaces in plants and animals should be primarily seen as a defense mechanism against fungal spores and the colonization with other micro-organisms.
Air layers for buoyancy. Non-persistent air layers for temporary buoyancy in water play an often underestimated role in very small seeds (see Fig. 27a) and spores which may fall or are dispersed into water.
- (vi)Air layers for fluid drag reduction. We could show (survey in Ref. ) that persistent air layers reduce the friction. The mechanism of this drag reduction 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 due to the friction between the water and the surface molecules. 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 to water is 55 times lower, because of this the air layer serves as a slip agent and the drag is reduced. Air layers as slip agents have evolved in many insects and play probably no role in plants. However, Salvinia provides the best example for the maintenance of permanent air layers under water (salvinia effect), showing the four essential criteria for air retention: hydrophobic chemistry, hair-like structures, undercuts and elasticity of the structures. Also the fifth, non-essential criteria, hydrophilic chemical heterogeneities of anchor cells within its superhydrophobic surface (Salvinia paradox, Fig. 28) could be found in some Salvinia species [67, 161, 162, 163, 164, 165, 166, 167, 168].
6.7 Anti-adhesive “Slippery” Surfaces and Aquaplaning
Many plants have evolved special structured surfaces which hinder the attachment of animals, especially insects, to protect themselves against herbivores . Most insects possess two different types of attachment structures, claws and adhesive pads [170, 171]. Whereas the former are used to cling to rough surfaces, the latter enable them to stick to perfectly smooth substrates. One strategy to reduce the attachment of insects is the secretion of epicuticular waxes which assemble into three-dimensional micro-structures. The other strategy is the development of a slippery surface by inducing aquaplaning.
7 Biomimetic Application
Bionics or biomimetics describes the processes in which structures and concepts evolved by living organisms are taken and implemented into technologies (surveys in [1, 11, 19]). Bionics or biomimetics is an old field (historical survey in Ref. ), but functional surfaces came surprisingly very late to bionic applications. The first example was the hook-and-loop fastener by the Swiss engineer Georges de Mestral in the 1950s, popularly known as Velcro®. It is based on plant surfaces (burrs). The drag-reducing riblets of the shark skin were analyzed in the 1980s  and together with the self-cleaning lotus-surfaces [2, 15] ushered in a new era of biomimetic applications—including the swimming competition in Olympic games (see Sect. 7.6).
“Surfaces” in engineering are thin boundary layers, and they are exposed to the harsh physicochemical and mechanical influences of the environment. Thin layers, and in particular, the biomimetic interesting hierarchical structures, have a restricted stability and durability. Nanocoatings play a most important and increasing economic role (compare Ref. ). We live—in the literal sense of Mark Twain’s novel—in “the gilded age” of surface applications. The bulk of a technical solid is usually stable, but every homemaker knows the difference between the durability of a silver spoon in contrast to a silvered utensil. A medieval iron pan could still be used in the kitchen over the next centuries—but a polymer-coated anti-adhesive pan lasts a few years. The extremely long lifespan of spectacle glasses is today limited by the sophisticated and convenient anti-reflex coatings. In colloquial language, there is an obvious difference between “solid” and “superficial.” We need coating technologies—but durability and persistence are major technical challenges for engineers and material scientists in a world of decreasing natural resources which must be used sustainably.
7.1 Mechanical Properties
Mechanical Properties play a very important role in biomimetic composite materials—but are nearly negligible for surfaces. Technical materials available today (polymers, metals, etc.) have often superior mechanical properties.
Attachment mechanisms of plants were the first biomimetic surface application and have been around since 1958 (see above) with the Velcro® hook-and-loop fasteners. Plants, in contrast to animals (e.g., geckos) are only a limited source of inspirations for attachment mechanisms.
7.3 Reflection, Transmission, and Absorption of Spectral Radiation
Reflection, transmission, and absorption of spectral radiation are of great importance for biomimetics. The applications concentrate on light harvesting by bioinspired surfaces of solar panels. An appropriate model for such surfaces is the petals of Viola tricolor and it is related species (see Sect. 6.3). They show a highly reduced reflection of light, an optimized scattering within the petals; additionally, they are superhydrophobic, showing a contact angle of 169° . Temperature control under insolation (e.g., car tops, roofs) is another field of interest. Coloration technologies have always been bioinspired (like indigo and purple as ancient dyes used for millennia). Flowers exhibit sophisticated structures to intensify colors by hierarchical structuring. However, most inspirations are provided by animal coloration, like the iridescence of peacock feathers or butterfly (Morpho) wings. Butterflies also provide ultrablack colorations  like the Gaboon viper . It is not by chance that the darkest technical black (Vantablack) is produced by carbon nanotubes.
7.4 Reduction of Water Loss
Reduction of water loss is essential for terrestrial plants—but like the many mechanical properties (see Sect. 7.1) of minor importance for biomimetic applications. Technical materials like an aluminum foil prevent loss better than a cuticle.
Superhydrophilicity has recently become relevant for technical applications, which are most diverse. Biomimetic fog-collecting meshes and other devices will probably play an increasing role in certain arid regions (e.g., Chile, Namibia), and it was shown that a biomimetic superhydrophilic hierarchical structuring increases the collection efficiency [154, 155, 178]. Koch et al.  have shown that the hydrophilic Gazania petal structures provide a model for the design of microfluidic devices for small volume liquid transport by capillary forces; beneficial in both fog harvesting and microfluidic devices.
Evidently, superhydrophilic surfaces are wettable, but the water film evaporates very fast and leads to the fast drying “no-drop” glasses (e.g., Alltop®) and a sophisticated façade paint (StoColor Dryonic®). Drag reduction by mucilaginous surfaces seen in fish also plays a technical role; we have seen evidence in seaweed surfaces that plants have also evolved a similar technology.
Pure water repellency (umbrellas to textile building) is usually applied by sprays providing a sculpturing by nanoparticles on, e.g., textiles (which are intrinsically hierarchically structured). It is obvious, that dry conditions further reduce corrosion, and anti-corrosion coatings are the focus of technical applications . This also applies for anti-icing properties. A whole range of products and techniques are available, 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 is increasing in importance [182, 183].
Self-cleaning Lotus Effect® surfaces are farout most important  and a vast literature exists since 1997 (see Ref. [19, 52, 184, 185, 186]). It is also one of the most important applications in façade paints, with the added advantage that they remain functional for several decades.
Superhydrophobic plants surfaces, like those of Salvinia, have a striking capacity to collect and adsorb spilled oil from water , a basis for biomimetic materials. Hydrophobic sand coating can be used to control deep drainage in tailings .
Air-retaining Salvinia ® Effect surfaces are a recent development, only prototypes exist [1, 195, 196]. Fluid drag reduction of up to 30% in a hydrodynamic water channel has been measured . The main application is seen in ship hulls: container ships transport about 80% of the global goods, and a reduction of the fuel (oil) consumption of 125 million tons and of 395 million tons of CO2 is estimated. A novel technology using air-retaining grids has recently been introduced and can be combined with the existing-refined micro-bubble technologies: micro-bubbles adhere to the grid-surface and the air layer under the grid can be regenerated. It is obvious that a permanent intact air layer prevents biofouling. Oil pollution is an unfortunate and unavoidable problem in our oceans. One possible solution is to create a hydrophobic barrier at the waterline of the ship to separate the ship hull from the water interface to avoid oil from creeping into the structures and suppressing the air.
7.7 Other Applications
As indicated in the preceding chapter, there are additional functions. Like the “aquaplaning” effect of the surfaces of the carnivorous Nepenthes plants which produce water films and become slippery to trap insects [172, 199]. In particular slippery liquid-infused surfaces (SLIPS) are of focal interest (e.g., Ref. [200, 201]).
8 Living Prototypes: Evolution of Plant Surfaces and Biodiversity
The often used phrase “inspired by nature” for biomimetics is misleading: a nuclear reactor is inspired by natural nuclear fission or the nuclear fusion in our sun. Thus a nuclear reactor is inspired by nature—but not bionic. Biomimetics is exclusively based on living organisms and the evolution of some 10 million living prototypes (survey in Ref. ). Superhydrophobic surfaces occur exclusively in living organisms, which evolved hierarchical structured superhydrophobic surfaces based on a very limited selection of molecules. There is no evidence for the occurrence of superhydrophobic surfaces in anorganic nature (man-made technical products are excluded). Surfaces are the crucial interface between an organism and its environment—3.5 billion years of mutation and selection have created a stunning diversity in an estimated 10 million different species of plants and animals (survey in Ref. ). The two basic phases with contrasting physical constraints are life in water and life outside of water.
8.1 Water Plants
Non-vascular primary water plants evolved in water (originally the oceans) a couple of trillion years ago and have no true conductive tissue. The groups are phylogenetically very different non-related clades; they comprise microscopic unicellular algae up to seaweeds which might reach a height of more than 45 m in Macrocystis. The common feature is their wettability (superhydrophilicity) and usually the absence of hierarchical structuring: flat and mucilaginous surfaces are characteristic. In certain groups of unicellular algae (e.g., Coccolithophores and Diatoms) complex surface structures occur, but usually embedded in mucilaginous or plasmatic covers: they are probably not the environmental interface.
8.2 Land Plants
True land plants are the vascular or higher plants, a well-defined phylogenetic unit. They comprise the Ferns, Clubmosses and Horsetails, Gymnosperms (incl. Conifers), and the flowering plants (Angiosperms). Higher plants evolved with the conquest of land in the late Ordovician or Silurian, 430–500 million years ago and evolved mechanically stabilizing lignose vascular tissues and a protective polymer layer, the cuticle (see Sect. 3) on their stem, and leaf surfaces; as a consequence of this rather impermeability, surface pores (stomata) evolved to enable and control the gas exchange. It was shown by a phylogenetic analysis  that superhydrophobicity caused by epicuticular wax crystals evolved simultaneously with the conquest of land—a possibly overlooked evolutionary key invention for plant life outside of water and probably also for insects. One of the most common waxy substances is the fatty secondary alcohol nonacosan-10-ol, which is responsible for the superhydrophobicity of many ferns, conifers, or even lotus leaves as long ago as 250 million years .
Some 450,000 different species of plants are part of the astonishing biodiversity of our planet: including animals, some 10 million species—but we know of less the 20% of them. Plants have evolved most intriguing functional surfaces over millions of years, like in the Lotus (Nelumbo) or the floating ferns (Salvinia). Evolution is a slow process which has been spanning billions of years. Mutation and selection (“trial and error”) exploited all constructional possibilities within this time and with the limited materials. But million years of research and development for technical engineering today is not a possibility: the materials science has a goal of fabricating a particular product within a limited time, using experimental trial-and-error approaches, calculation, and modeling. We lose a high amount of biodiversity in our changing world and it has been brought to our attention [11, 203] that this also means the loss of biological role models, the “living prototypes” for engineers.
The diversity of plant surface structures is a result of several billions of years of evolutionary processes. Plants evolved a stunningly high diversity of surfaces and functionality for their interaction with the environment—the self-cleaning properties of Lotus is only one example. Millions of years of mutation and selection, trial and error: free information for engineers and materials scientists.
Bionics is an old field of research and development starting around 1800—but surfaces played a surprisingly late role for biomimetic applications, the only exception is the hook-and-loop fasteners (“Velcro®”) in the 1950s based on burrs. The publication of the lotus effect in 1997  created awareness by engineers and materials scientists, terms like “superhydrophobicity” came into use in the last two decades and opened a new era in surface technologies (survey in Ref. ). Surfaces play an increasing roll, the global market for nanocoatings is estimated to reach 14.2 billion US dollars by 2019 .
Biological surfaces have provided a remarkable number of innovations in the last three decades. Surface technologies have been largely influenced by research on biological interfaces and came rather late into focus of technical innovations. All data indicate we are only in the beginning of a new era of biologically inspired surface technologies.
Understanding biological surfaces is crucial—we have shown that we are still in the beginning of this process. But we are also in the beginning of a dramatic loss of biodiversity in the Anthropocene. Some 10 million different species (possible biological role models) exist—We lose a high amount of biodiversity in our changing world and it has been brought to our attention [11, 202] that this also means the loss of biological role models, the “living prototypes” for engineers. Bionics is another intrinsic value to the diversity of life which should be treasured.
This survey is based on over three 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. We acknowledge the discussions with colleagues and friends; in particular, we would like to thank Horst Bleckmann (Bonn), Alfred Leder, Martin Brede (both Rostock), Thomas Schimmel, Stefan Walheim, Markus Moosmann, Torsten Scherer (all KIT Karlsruhe), Walter Erdelen (former UNESCO Paris), Anna-Julia Schulte (Euskirchen), Daud Rafiqpoor, Birte Böhnlein, Peter Häger (all Bonn), Gerhard Gottsberger (Ulm), Stanislav Gorb (Kiel), Georg Noga (Bonn), and Maximilian Weigend (Bonn). Technical assistance was provided over the years by Hans-Jürgen Ensikat, the late Wolfgang Roden, Alexandra Runge, Bernd Haeseling, and Danica Christensen. Our work in Bionics and Biodiversity was supported by the Deutsche Bundesstiftung Umwelt DBU, the German Research Council DFG, the Federal Ministry for Science and Education BMBF, and the Academy of Science and Literature in Mainz.
- 2.W. Barthlott, N. Ehler, Raster-Elektronenmikroskopie der Epidermis-Oberflächen von Spermatophyten. Trop. Subtrop. Pflanzenwelt 19, 1–105 (1977)Google Scholar
- 3.S. Blackmore, K. Ferguson (eds.), in Pollen and Sres: Form and Function, vol. 12. Linnean Society Symposium Series (Academic Press, London, 1986)Google Scholar
- 8.S. Porembski, B. Martens-Aly, W. Barthlott, Surface/volume-rations of plants with special consideration of succulents. Beitr. Biol. Pflanzen 66, 189–209 (1992)Google Scholar
- 9.J.M. Suttie, S.G. Reynolds, C. Batello, Grasslands of the World (Food and Agricultural Organisations of the UN, Rome, 2005)Google Scholar
- 11.W. Barthlott, D. Rafiqpoor, W. Erdelen, Bionics and Biodiversity- Bio-Inspired Technical Innovation for a Sustainable Future, in Biomimetic Research for Architecture and Building Construction-Biological Design and Integrative Structures, ed. by J. Knippers, K. Nickel, T. Speck (Springer, Berlin, 2016)Google Scholar
- 13.R.H. Francé, Die Pflanze als Erfinder. Stuttgart, Germany: Franckh’sche Verlagshandlung (Engl. edition: Plants as inventors. London: Simpkin and Marshall, 1920)Google Scholar
- 14.J.C. Robinette (ed.), Living Prototypes–the Key to New Technology, in Proceeding of the Symposium. (Wright Air Development Division, 13–15 September 1960)Google Scholar
- 19.B. Bhushan, Biomimetics-Bioinspired Hierarchical-Structured Surfaces for Green Science and Technology, 2nd edn. (Springer, Heidelberg, 2016)Google Scholar
- 20.P. Forbes, The Gecko’s Foot (Fourth Estate, London, 2005)Google Scholar
- 21.W. Barthlott, M. Mail, B. Bhushan, K. Koch, Plant Surfaces: Structures and Functions for Biomimetic Applications, in Springer Handbook of Nanotechnology, 4th edn., ed. by B. Bhushan (Springer, Heidelberg, 2017)Google Scholar
- 24.M. Riederer, C. Markstädter, Cuticular Waxes: A Critical Assessment of Current Knowledge, in Plant Cuticles an Integrated Functional Approach, ed. by G. Kerstiens (University Scientific, Oxford, 1996), pp. 189–200Google Scholar
- 28.K. Koch, W. Barthlott, S. Koch, A. Hommes, K. Wandelt, W. Mamdouh, S. De-Feyter, P. Broekmann, Structural analysis of wheat wax (Triticum aestivum, c.v. ‘Naturastar’ L.): from the molecular level to three dimensional crystals. Planta 223, 258–270 (2005). doi: 10.1007/s00425-005-0081-3 CrossRefGoogle Scholar
- 29.R. Jetter, L. Kunst, A.L. Samuels, Composition of Plant Cuticular Waxes, in Biology of the Plant Cuticle, in Annual Plant Reviews, ed. by M. Riederer, C. Müller (Blackwell, Oxford, 2006), pp. 145–175Google Scholar
- 30.E.A. Baker, Chemistry and Morphology of Plant Epicuticular Waxes, in The Plant Cuticle, ed. by D.F. Cutler, K.L. Alvin, C.E. Price (Academic Press, London, 1982), pp. 139–165Google Scholar
- 37.D. Frölich, W. Barthlott, Die mikromorphologie der epicuticularen wachse und das system der monocotylen. Trop. Subtrop. Pflanzenwelt 63, 1–135 (1988)Google Scholar
- 38.N.D. Hallam, B.E. Juniper, The Anatomy of the Leaf surface, in The Ecology of Leaf Surface Micro-organisms, ed. by T.F. Preece, C.H. Dickinson (Academic Press, London, 1971), pp. 3–37Google Scholar
- 39.C.E. Jeffree, The Cuticle, Epicuticular Waxes and Trichomes of Plants, with Reference to Their Structure, Functions and Evolution, in Insects and the Plant Surface, ed. by B.E. Juniper, R. Southwood (Edward Arnold, London, 1986), pp. 23–63Google Scholar
- 43.K. Koch, A. Dommisse, C. Neinhuis, W. Barthlott, Self-assembly of Epicuticular Waxes on Living Plant Surfaces by Atomic Force Microscopy, in Scanning Tunneling Microscopy/Spectroscopy and Related Techniques, ed. by P.M. Koenraad, M. Kemerink (American Institute of Physics, Melville, 2003), pp. 457–460Google Scholar
- 47.W. Barthlott, I. Theisen, T. Borsch, C. Neinhuis, Epicuticular Waxes and Vascular Plant Systematics: Integrating Micromorphological and Chemical Data, in Deep Morphology: Toward a Renaissance of Morphology in Plant Systematics, ed. by T.F. Stuessy, V. Mayer, E. Hörandl (Reg. Veg. Gantner Verlag, Ruggell, 2003), pp. 457–460Google Scholar
- 49.International Union of Crystallography, Report of the Executive Committee for 1991. Acta Crystalogr. A 48, 922–946 (1992). doi: 10.1107/S0108767392008328
- 54.J. Zhang, W. Zhong-Lin, J. Liu, C. Shaowei, G. Liu, Self-assembled Nanostructures (Kluwer Academic Publishers, New York, 2003)Google Scholar
- 55.N. Boden, P.J.B. Edwards, K.W. Jolley, C. Neinhuis, Self-assembly and Self-organization in Micellar Liquid Crystals, in Structure and Dynamics of Strongly Interacting Colloids and Supermolecular Aggregates in Solutions, ed. by S.H. Chen, J.S. Huang, P. Tartaglia (Kluwer Academic Publishers, Dordrecht, 1992)Google Scholar
- 66.W. Barthlott, E. Wollenweber, Zur Feinstruktur, Chemie und taxonomischen Signifikanz epicuticularer Wachse und ähnlicher Sekrete. Tropische und subtropische Pflanzenwelt 32, 7–67 (1981)Google Scholar
- 70.J.T. Martin, B.E. Juniper, The Cuticles of Plants (Edward Arnold, London, 1970)Google Scholar
- 71.D.F. Cutler, K.L. Alvin, C.E. Price, The Plant Cuticle (Academic Press, London, 1982)Google Scholar
- 72.G. Kerstiens, Plant Cuticles: An Integrated Functional Approach (Bios Scient Pub, Oxford, 1996)Google Scholar
- 76.W. Barthlott, 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. by D. Claugher (Clarendon Press, Oxford, 1990), pp. 69–94Google Scholar
- 77.W. Barthlott, Morphogenese und mikromorphologie komplexer cuticular-faltungsmuster an blüten-trichomen von antirrhinum L. (Scrophulariaceae). Ber. Dt. Bot. Ges. 93, 379–390 (1980)Google Scholar
- 81.R.K. Saeedur, Calcium Oxalate in Biological Systems (CRC Press, Boca Raton, 1995)Google Scholar
- 87.H.D. Behnke, Plant Trichomes-structure and Ultrastructure: General Terminology, Taxonomic Applications, and Aspects of Trichome Bacterial Interaction in Leaf Tips of Dioscorea, in Biology and Chemistry of Plant Trichomes, ed. by E. Rodriguez, P.L. Healey, I. Mehta (Plenum Press, New York, 1984), pp. 1–21CrossRefGoogle Scholar
- 88.W. Barthlott, D. Hunt, Seed-Diversity in Cactaceae Subfam. Cactoideae, in Succulent Plant Research, vol. 5, ed. by D. Hundt (Milborne Port, Sherborne, 2000)Google Scholar
- 89.W. Barthlott, B. Große-Veldmann, N. Korotkova, Orchid seed diversity: a scanning electron microscopy survey. Englera 32, 1–244 (2014)Google Scholar
- 91.J.N. Israelachvili, Intermolecular and Surface Forces, 2nd edn. (Academic Press, London, 1992)Google Scholar
- 95.M. Nosonovsky, B. Bhushan, Green Tribology, Biomimetics, Energy Conservation and Sustainability (Springer, Berlin, 2012)Google Scholar
- 96.E.Y. Bormashenko, Wetting of Real Surfaces, in De Gruyter Studies in Mathematical Physics, vol. 19 (Verlag Walter de Gruyter, 2013), pp. 187Google Scholar
- 97.H.J. Butt, K. Graf, M. Kappl, Physics and Chemistry of interfaces, 3rd edn. (Wiley-VCH, Weinheim, 2013)Google Scholar
- 106.A.V. Adamson, Physical Chemistry of Surfaces (Wiley, New York, 1990)Google Scholar
- 107.M. Nosonovsky, B. Bhushan, Lotus Versus Rose: Biomimetic Surface Effects, in Green Tribology, Biomimetics, Energy Conservation and Sustainability, ed. by M. Nosonovsky, B. Bhushan (Springer, Berlin, 2012), pp. 25–40Google Scholar
- 127.W. Barthlott, K. Riede, M. Wolter, 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 (1994)Google Scholar
- 128.H. Bargel, W. Barthlott, K. Koch, L. Schreiber, C. Neinhuis, Plant Cuticles: Multifunctional Interfaces Between Plant and Environment, in The Evolution of Plant Physiology, ed. by A.R. Hemsley, I. Poole (Academic Press, London, 2003), pp. 171–194Google Scholar
- 129.L. Schreiber, J. Schonherr, Water and Solute Permeability of Plant Cuticles (Springer, Heidelberg, 2009)Google Scholar
- 134.F. Exner, S. Exner, Die physikalischen Grundlagen der Blütenfärbungen. Sitzungsber. Kais. Akad. Wiss. Wien, Math.-nat. Kl 119, 191–245 (1910)Google Scholar
- 135.Y. Toda, Physiological studies on Schistostega osmundacea (Dicks.) Mohr. J. Coll. Sci. Imp. Univ. Tokyo 40(5), 1–30 (1918)Google Scholar
- 138.D.G. Lloyd, S.C.H. Barret, Floral Biology-Studies on Floral Evolution in Animal-pollinated Plants (Springer, Berlin, 1995)Google Scholar
- 139.B. Burr, D. Rosen, W. Barthlott, Untersuchungen zur Ultraviolettreflexion von Angiospermenblüten. III. Dilleniidae und Asteridae S. I. Trop. Subtrop. Pflanzenwelt 93 (Akad. Wiss. Lit. Mainz, F. Steiner Verlag, Stuttgart, 1995), 186 ppGoogle Scholar
- 140.B. Burr, W. Barthlott, Untersuchungen zur Ultraviolettreflexion von Angiospermenblüten. II. Magnoliidae, Ranunculidae, Hamamelididae, Caryophyllidae, Rosidae. Trop. subtrop. Pflanzenwelt 87 (Akad. Wiss. Lit. Mainz, F. Steiner Verlag, Stuttgart, 1993), 193 ppGoogle Scholar
- 141.N. Biedinger, W. Barthlott, Untersuchungen zur Ultraviolettreflexion von Angiospermenblüten. I. Monocotyledoneae. Trop. Subtrop. Pflanzenwelt 86 (Akad. Wiss. Lit. Mainz, F. Steiner Verlag, Stuttgart, 1993), 122 ppGoogle Scholar
- 150.H.G. Jones, E. Rotenberg, Radiation and Temperature Regulation in Plants, in Encyclopedia of Life Science, ed. by A.M. Hetherington (Wiley, New York, 2001), pp. 1–8Google Scholar
- 151.W. Barthlott, W. Schultze-Motel, Zur feinstruktur der blattoberflächen und systematischen stellung der laubmoosgattung rhacocarpus und anderer hedwigiaceae. Willdenowia 11, 3–11 (1981)Google Scholar
- 157.W. Barthlott, Die Selbstreinigungsfähigkeit Pflanzlicher Oberflächen Durch Epicuticularwachse, in Klima- und Umweltforschung an der Universität Bonn, ed. by H. Koch (Rheinische Friedrich-Wilhelms-Universität Bonn, Bonn, 1992), pp. 117–120Google Scholar
- 169.S.D. Eigenbrode, Plant Surface Waxes and insect Behaviour, in Plant Cuticles: An Integrated Functional Approach, ed. by G. Kerstiens (BIOS Scientific Publishers, Oxford, 1996), pp. 201–222Google Scholar
- 171.S. Gorb, Attachment Devices of Insect Cuticle (Springer Science & Business Media, Berlin, 2001)Google Scholar
- 178.M.A.K. Azad, Fog Collection on Plant Surfaces and Biomimetic Applications, (Dissertation, University of Bonn, 2016)Google Scholar
- 180.G. Zouridakis, J.E. Moore, J. Maitland, Biomedical Technology and Devices, 2nd edn. (CRC Press, Boca Raton, 2013)Google Scholar
- 181.C.J. Weng, C.H. Chang, C.W. Peng, S.W. Chen, J.M. Yeh, C.L. Hsu, Y. Wei, Advanced anticorrosive coatings prepared from the mimicked Xanthosoma sagittifolium-leaf-like electroactive epoxy with synergistic effects of superhydrophobicity and redox catalytic capability. Chem. Mater. 23(8), 2075–2083 (2011). doi: 10.1021/cm1030377 CrossRefGoogle Scholar
- 187.M. Schwab, G. Noga, W. Barthlott, Bedeutung der epicuticularwachse für die pathogenabwehr am beispiel von botrytis cinerea-infektionen bei kohlrabi und erbse. Gartenbauwissenschaft 60, 102–109 (1995)Google Scholar
- 188.G.J. Noga, M. Knoche, M. Wolter, W. Barthlott, Changes in leaf micro-morphology induced by surfactant application. Angew. Bot. 61, 521–528 (1987)Google Scholar
- 189.M. Wolter, W. Barthlott, M. Knoche, G.J. Noga, Concentration effects and regeneration of epicuticular waxes after treatment with Triton-X-100 surfactant. Angew. Bot. 62(1–2), 53–62 (1988)Google Scholar
- 190.G. Noga, M. Wolter, W. Barthlott, W. Petry, Quantitative evaluation of epicuticular wax alterations as induced by surfactant treatment. Angew. Botanik 65, 239–252 (1991)Google Scholar
- 191.G. Noga, M. Knoche, M. Wolter, The impact of Triton X-100 surfactant on leaf micromorphology. HortScience 23(3), 808 (1988)Google Scholar
- 192.C. Neinhuis, M. Wolter, W. Barthlott, Epicuticular wax of Brassica oleracea: changes in microstructure and ability to be contaminated of leaf surfaces after application of Triton X-100. J. Plant Dis. Prot. 99, 542–549 (1992)Google Scholar
- 195.J.-E. Melskotte, M. Brede, A. Ott, M. Mayser, W. Barthlott, A. Leder, 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. by M. Brede, B. Ruck, D. Dopheide (Deutsche Gesellschaft für Laser-Anemometrie GALA e.V, Karlsruhe, 2012), pp. 1–6Google Scholar
- 197.J.-E. Melskotte, M. Brede, A. Wolter, W. Barthlott, A. Leder, Schleppversuche an Künstlichen, Luft Haltenden Oberflächen zur Reibungsreduktion am Schiff, in Lasermethoden in der Strömungsmesstechnik, 21. Fachtagung, 3–5. September 2013, ed. by C.J. Kähler et al. (München, Germany, 2013) 53, 1–7Google Scholar
- 203.W. Barthlott, W. Erdelen, M.D. Rafiqpoor, Biodiversity and Technical Innovations: Bionics, in Concept and Value in Biodiversity. Routledge Studies in Biodiversity Politics and Management, ed. by D. Lanzerath, M. Friele, D. Dopheide (Routledge, New York, 2014), pp. 300–315Google Scholar
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