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

Abstract

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 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'.

Keywords: Notonecta; Salvinia effect; air-retaining grids; bionics; evolution; lotus.

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.)

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 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.)

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.)

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.)

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.)

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].

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.)

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.)

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].

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).

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].

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].

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.)

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 .

Figure 16.

Bristles and microvilli are present in these semi-aquatic insects. (a) An eye of Clunio marinus. (b) The microvilli-covered 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.

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.)

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 . (Online version in colour.)

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.

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.)

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.)

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.)

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.)

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].

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].

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].

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].

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.)

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.)

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.

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.)

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.

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.

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].

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.)