Diversity of plant surface structures

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Diversity of structure, morphology and wetting of plant surfaces

Kerstin Koch,*ab Bharat Bhushanb and Wilhelm Barthlotta
Received 26th March 2008, Accepted 13th May 2008
First published as an Advance Article on the web 28th July 2008
DOI: 10.1039/b804854a
This review paper presents the diversity of plant surface structures from a single cell to multi-cellular
surface sculptures. There is still no comprehensive book which provides an overview of the diversity of
plant surface structures. This article presents a guide for the description of cellular and sub-cellular
plant surface structures, which include hairs, wax crystals and surface folding. Biological surfaces are
multifunctional boundary layers to their environment. Functionally optimized surfaces are one of the
Published on 28 July 2008 on http://pubs.rsc.org | doi:10.1039/B804854A
key innovations in the more than 400 million years of evolution of land plants. In the plant surface,
micro- and nanostructures play a special role, and a large diversity of surface structures exists at
different size levels. Well known functional aspects of plant surface structures are the reduction of
particle adhesion, the sliding structures of carnivorous plants for insect catching, and the self-cleaning
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properties of the superhydrophobic Lotus (Nelumbo nucifera) leaves. Their structures and functions
might be useful models for the development of functional materials. The surface properties of plants are
based on physico-chemical principles and can be transferred to technical ‘‘biomimetic’’ materials, as
successfully done for the self-cleaning properties of the Lotus leaves. This article is designed as an
introduction for biologists and non biologists and should stimulate the reader to initiate or intensify the
study of biological surfaces.
1. Introduction leaves, fruits and seeds of all lower (e.g., ferns) and higher land
plants (e.g., flowering plants). Only the roots of plants, some
1.1 Plant surfaces and their multifunctional properties mosses and secondary plant tissues, such as wood and bark, can
Approximately 460 million years ago, the first plants moved from forgo this protective layer. The development of the cuticle as
their aqueous environment to the drier atmosphere on land, and hydrophobic outer coverage was one of the key innovations that
they needed a protective outer coverage. The key innovation was enabled plants to leave their primarily aquatic habitat and to
the plant cuticle, a continuous extracellular membrane, which overcome the physical and physiological problems connected to
covers the primary above-ground organs of flowers, stems, an ambient environment, such as desiccation. Plants settled into
nearly all conceivable habitats. In their specific environments, the
cuticle serves as the crucial multifunctional layer representing
a
Nees Institute for Biodiversity of Plants, Rheinische Friedrich-Wilhelms one of the largest interfaces between biosphere and atmosphere,
University of Bonn, Meckenheimer Allee 170, 53115 Bonn, Germany. covering more than 1.2 109 km2 in total.1 Cuticles stabilize the
E-mail: koch@uni-bonn.de
b
Nanoprobe Laboratory for Bio & Nanotechnology and Biomimetics, The
plant tissue and have several protective properties. One of the
Ohio State University, 201 W. 19 th Avenue, Columbus, OH 43210-1142, most important properties is the transpiration barrier. Cuticles
USA. E-mail: Bhushan.2@osu.edu reduce the loss of water to the same, or even higher degree, as
2001 PhD at the University of Since 1985 Chair of Systematic

Bonn. 2001–2007 Assistant Botany and head of the Depart-
Professor at the University of ment, and director of the
Bonn; Habilitation in 2006. Botanical Garden of the
Since 2008 Research Scholar at University of Bonn. Research:
the Nanoprobe Laboratory for global mapping of biodiversity;
Bio- & Nanotechnology and systematics and ecology of
Biomimetics, Ohio State flowering plants; biological
University. Research: function interfaces: functional aspects of
of micro- and nanostructures micro- and nanostructured
of plant surfaces; molecular surfaces; biomimetics: surface
self-assembly, architecture and technologies and Lotus effect.
crystallinity of plant waxes,
PD Dr Kerstin Koch biomimetic surfaces and replica Prof: Dr Wilhelm Barthlott
techniques.
This journal is ª The Royal Society of Chemistry 2008 Soft Matter, 2008, 4, 1943–1963 | 1943
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plant12 and plant surface waxes and insect behavior13 can be

found.
1.2 Importance of studies—wettability of surfaces and

biomimetics
Based on the large variations of surface chemistry and structures,

plant surfaces provide a huge variety of functions. Some surfaces,
Fig. 1 Schematic survey of the most prominent functions of the plant like the leaves of the Lotus plant (Nelumbo nucifera), are
boundary layer on a hydrophobic micro-structured surface. A) Transport
extremely water repellent (superhydrophobic).5,14 However,
barrier: limitation of uncontrolled water loss/leaching from interior and
others, such as the air-roots of epiphytic orchids, some lichens
foliar uptake; B) surface wettability; C) anti-adhesive, self-cleaning
properties: reduction of contamination, pathogen attack and reduction of and mosses, show opposite behavior; these are constructed for
attachment/locomotion of insects; D) signaling: cues for host–pathogen/ the most efficient water absorption (superhydrophilic) through
insect recognition and epidermal cell development; E) optical properties: their surfaces. Such wetting phenomena are based on physico-
protection against harmful radiation; F) mechanical properties: resis- chemical factors, and these are not restricted to the living
tance against mechanical stress and maintenance of physiological integ- organism, but transferable into technical surfaces, with a biomi-
rity; G) reduction of surface temperature by increasing turbulent air flow metic approach. Bionics or ‘‘biomimicry describes a process in
over the boundary air layer (modified after ref. 8). which the ideas and concepts developed by nature are taken and
implemented into technology’’.15 A large area of biomimetic
research deals with functional micro- and nanostructures and the

a synthetic polymer of comparable thickness would.2 This transmission of biological principles and functional structures,
property is based on their hydrophobic material, made basically and is of great interest for the design of modern functional
of a polymer called cutin and integrated and superimposed lipids ‘‘biomimetic’’ materials. Prominent examples are the develop-
called ‘‘waxes’’.3,4 ment of superhydrophobic surfaces after the model plant
The cuticle and their waxes play an important role in cellular Lotus16–20 and the feet of several arthropods and some verte-
structuring and surface wettability, e.g., by folding of the cuticle, brates and their remarkable ability to reversibly attach to varying
or by formation of three dimensional wax crystals on the plant surfaces.21–23 Several new methods for surface functionalization
surface. Cell forms, sizes and their fine structures have a great have been developed,24 and special interest has been given to
influence on several functional approaches of the plant boundary techniques for the development of superhydrophobic surfaces.25
layer. The multifunctional properties of the plant cuticle,
summarized in Fig. 1, are the reduction of water loss and 2. Function and diversity of plant surface structures
leaching of ions from the inside of the cells to the environment,
2.1 The plant epidermis and its functional approaches
the reduction or increase of surface wetting and reduction of
particle adhesion, as for example, pathogen adhesion. The plant The epidermis of plants is the outermost layer of primary tissues.
cuticle also plays an important role for insect and microorganism Several morphological modifications of the epidermis cells are
interaction, as in attachment or sliding of insects. It protects the known; thus, the model presented in Fig. 2a shows only the basic,
plants against harmful radiation, e.g., it can increase the reflec- layered stratification. Starting with the outside of the epidermis
tion of visible light for temperature control and can induce cell, we find as the outermost layer a thin extracellular
turbulent air flow to increase mass and heat transfer from the membrane, called cuticle. The plant cuticle is a composite-
plant surface to the environment. Additionally, it is a stabiliza- material mainly built up of a cutin network and hydrophobic
tion element for the cells. The diversity of plant surface structures waxes. Waxes are the main transport barrier, preventing water
arises from the variability of cells shapes and their surface loss and leaching of molecules from inside of the living cells.2,26,27
structures, and by the formation of multi-cellular surface struc- This barrier function reduces also the uptake of molecules from
tures. Some of these structures, such as special morphological the environment, which might become a crucial factor when the
types of cells like hairs or epicuticular waxes (introduced later), uptake of, e.g., nutrients or fungicides in agricultural systems is
are characteristic for a special group of plants, thus they are desired. The cuticle is present on all primary tissues of the above-
useful features for grouping of plants in systematic orders ground organs of lower (e.g., ferns) and higher land plants.
(taxons).5–7 SEM micrographs presented in the article were taken Tissues and species without a cuticle have no transpiration
from a data base of some 250 000 micrographs at the University barrier; thus, only few exceptional species or tissues can exist
of Bonn, which has been built up as a result of over thirty years of without this protective layer (some examples were given in
SEM research on biological surfaces, by the senior author and paragraph 1.1). In terms of functional aspects, which were
his collaborators. summarized in Fig. 1, the most important part of the epidermis
The book by Riederer and Müller 9 provides a comprehensive cell is the cuticle. Hence the cutin and its integrated (intra-
overview about the fine structure of the plant cuticle and its cuticular) and overlying (epicuticular) waxes will be introduced
waxes, cutin biosynthesis and transport processes through the in more detail in the following paragraphs. The next layer, shown
cuticle. Functional approaches of the plant cuticle are summa- in Fig. 2a, is the pectin layer. It connects the cuticle to the much
rized by Kerstiens.10 In non-biotic environmental interactions, thicker underlying cellulose wall and the finer cellulose fibrils
reviews of the behavior of electromagnetic radiation11 and biotic which are shown in the more detailed scheme of Holloway28 in
interactions such as fungal attachment and penetration into the Fig. 2b. Because pectin is not always formed as a layer, visible in
1944 | Soft Matter, 2008, 4, 1943–1963 This journal is ª The Royal Society of Chemistry 2008
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Fig. 2 (a) Shows a simplified model of the stratification of the outermost layers of the plant epidermis cells. The cuticle and its connection to the cell wall
is presented in more detail in (b). In this hypothetical scheme of the structural features of the plant cuticle (modified after ref. 28) cellulose fibers and
polysaccharides exist in the cuticle layer. Pectin is not visualized as a layer, because evidence for a layered arrangement of pectins exists only for some
species.
transmission electron microscopy, Holloway did not include it biosynthesis of the cuticle have been reviewed by several
into his scheme, but he adds polysaccharides, which are also authors.3,4,28 The schematic drawing of Holloway28 is still an
integrated into the cellulose wall. The last shown layer, below the appropriate scheme for the general stratification of the plant
cell wall, is the plasma membrane. This membrane separates cuticle and is shown in Fig. 2b. However, at the molecular level,
the living part of the water containing cell from the outer the structure of the cuticle is still unknown. Even though the
nonliving part of the epidermis. cuticle is a relatively thin layer, with thicknesses between a few
On the cuticle surface of most plants, the epicuticular waxes nanometres to some micrometres, it is an important structural
form thin two-dimensional films and/or three-dimensional stabilization component for the primary epidermis tissue.41,42
structures. If three-dimensional waxes exist, these are combined The mechanical properties of isolated cuticles, e.g., their
with a thin 2-dimensional wax film, which covers the cuticle elasticity modules, are in the same range as that of technical
surface. The dimensions of wax structures range from a few polypropylene membranes with comparable thickness.43,44
nanometres to several micrometres. Waxes exist in different
morphologies,29 but most common are tubules and platelets (see
2.2 Plant surface structures: from single cells to multi-cellular
section 3). The three-dimensional waxes and the wax films are
sculpturing
crystals, which originate by self-assembly.30,31 Three dimensional
epicuticular waxes are responsible for the maintenance of Even in a cursory look, different plant surfaces appear very
wettability and self-cleaning properties,32,33 sliding of insects,34 different, for example, in their optical appearance. Some
reflection of visible light, adsorption of UV-radiation,11,35,36 and surfaces, like the flower leaves of a dark red rose appear velvety
reduction of particle adhesion.14,37 The chemistry of waxes is and soft, whereas others, as the leaves of a rubber tree, appear
a mixture of long chain hydrocarbons and, in some waxes, cyclic glossy. Some fruits, like grapes and plums, for example, are
hydrocarbons. Several research studies have been carried out for covered with a white or bluish appearing outermost layer. These
wax analysis, and recent overviews are given by Kunst and optical effects arise from the surface structures in the micro- and
Samuels,38 Jeffree3 and Jetter et al.39 However, most existing data nanoscale dimension.
refer to complete wax extractions, not differentiating between the With the application of scanning electron microscopy (SEM)
epicuticular and intracuticular waxes, which might be different. in biology in the 1960s, the large diversity of plant microstruc-
Appropriate methods for selective wax isolation are introduced tures became known, ranging from the nanometre scale up to
and discussed by Koch and Ensikat.30 The chemical composition several micrometres. This great diversity in surface structures
of plant waxes is highly variable amongst plant species as well as originates from the diversity of species, combined with the
the organs of one species (e.g., different leaves) and varies during different structures found on a single species. Today, plant
organ ontogeny.40 biodiversity contains approximately 270 000 different species,
Based on structural characteristics, the cuticle can be divided but recent calculations suggest that most species on earth have
into the cuticle proper and the thicker underlying cuticle layer not yet been described and will not be, because of high rates of
(Fig. 2b). In both layers the cuticle network is formed by cutin, species extinction (50/day). Each species extinction is a loss of
a polyester like biopolymer, composed of hydroxyl and information and thus might be the loss of a potential solution for
hydroxyepoxy fatty acids, and sometimes also by cutan, which is a technical or medical problem.
built up of polymethylene chains. Non-lipoidic compounds of The description of micro-morphologies of plant surface
the cuticle are cellulose, pectin, phenolics and proteins. Large structures requires some uniform rules of terminology. Here, we
differences in chemical composition and microstructure of use the compendium of plant surface structures, imaged by SEM,
the waxes and the cutin network have been found by given by Barthlott and Ehler.5 Most known three-dimensional
comparing different species and different developmental stages shapes of a single cell, such as the outline of the boundary and the
of organ ontogeny. Chemical composition, microstructure and curvatures of the cells, and the fine structure of the cell surfaces,
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are defined and examples are given. For the description of wax rough for AFM examination, but the isolation and transfer of
morphologies we use the terminology defined by Barthlott single hairs or wax crystals onto smooth technical surfaces allows
et al.,29 but the formerly used term crystalloids has been changed the investigation of these isolated structures by AFM.30,50 Sample
into crystals, because all waxes are crystalline.45 sizes typically range from a few nanometres up to several
The investigation of specimens by SEM occurs in a vacuum micrometres. In this technique, the cantilever tip shape, specifi-
chamber, and this leads in most cases to shrinkage or collapse of cally the radius of the tip, determines the lateral resolution.51,52
the cells of plant tissues. Appropriate specimen preparation is The diversity of plant surface structures is divided into three
necessary to avoid morphological artifacts caused by loss of parts. The first part gives an overview of plant surface structures
water before or during specimen investigation by SEM. Different which are formed by a single cell. This includes the shape and
SEM preparation methods (fixation) for water-containing spec- sculpture of the cell and the structures of the cell surface. The
imens have been developed to reduce shrinking of the material. second part includes hierarchical structures built up by a combi-
The best known one is the critical point drying method.46 Here, nation of convex cell sculptures and a structured cell surface. The
the water inside the specimen is exchanged with an alcohol third part describes larger scale structures, built up by more than
solution (methanol or ethanol) before the drying process starts. a single cell. For a wider understanding, we try to avoid the use of
However, during the whole fixation and drying process, the many specialist terms here and use more common names, and
surfaces of the specimens are in direct contact with the exchange scientific designations are placed in brackets. Here, examples of
solutions, and this can lead to structural changes. For example, surface sculpturing are shown at different scale sizes, but exam-
the waxes on the surface can completely or partially dissolve. ples are restricted to the primary epidermis of fruits, leaves and
Ensikat and Barthlott47 described a widely used preparation other herbaceous plant material. Structures of pollen from flowers
method for SEM investigations of leaves and other water con- and the woody stems of trees and shrubs are excluded here.
taining specimens. In this method, the liquid exchange occurs
without contact between the specimen surface and the exchange 2.2.1 Primary shape of single cells and their surface structures.
solution (glycerol), so the native surface structures, and if desired The outline of a single epidermis cell is usually visible at low
also their native contaminations, can be visualized by SEM. magnifications by SEM or light microscopy. The boundaries of
Without appropriate preparation significant shrinking of cells two perpendicular cell walls are called anticlines or anticlinal
occurs by water loss, as demonstrated here by two SEM figures walls, whereas the outer area of the cell surface is called the
of a Dahlia flower leaf (petal), with and without any special periclinal wall. The primary sculpture encompasses the outline of
drying process (Fig. 3). epidermal cells, including the shape and relief of the anticlines
In addition to SEM, atomic force microscopy (AFM) has and curvature of the outer periclinal wall. Anticlines of cell
proven to be a useful tool for investigations of biological boundaries are important for the description of the cell outlines,
surfaces. The range of AFM applications includes imaging of but they are only visible in SEM when they are exposed or
single molecules, cells and tissues, up to complex plant surface sunken. If anticlines are in the same level as the cell surface, they
structures.20,31,48,49 Compared to SEM, the main advantage of can only be identified by SEM in side views of a cut through the
AFM is the ability to operate with living biomaterial in liquid or specimen or by the use of light microscopy. The two basic forms
gaseous environments. A lateral resolution of better than one of cells are tetragonal and polygonal and are shown schemati-
nanometre can be achieved, but the maximum height variation of cally in Fig. 4a. These two basic forms might vary; if all sides of
surface structures between adjacent pixels is about 6 mm; thus the cell have a uniform length, the form is called isodiametric,
the roughness of some biological surfaces is too high for AFM and when two cell sides are longer than the others, the form is
investigations. Therefore many hairy plant surfaces are too called elongated. For example, the cells of the upper side
(adaxial) of a grass blade of the annual bluegrass (Poa annua) are
polygonal (Fig. 4b), whereas the cells of the lower (abaxial) side
are tetragonal-elongated (Fig. 4c). For the characterization of
plant micromorphology, it is important to note that the outline
of the epidermal cells might be different in different tissues of
a species. Additionally, the course of the anticlines can be
straight or uneven. Uneven anticlines could be further divided
into V, U, U, or S, undulations (Fig. 5a). An example of straight
anticlines is given by the cells of the lower side of the grass leaf
(Fig. 4c). Anticline undulation can be regular or non-regular, and
amplitudes of undulations may vary. Undulations of anticlines
Fig. 3 SEM micrographs of the upper (adaxial) side of a flower leaf of lead to a dense gearing of the epidermis cells, and it is assumed
a Dahlia petal leaf. In figure (a) a convex cell form with irregular cuticular that these undulations increase the mechanical stability of the
folding in the central fields and parallel folding in the anticlinal field of
epidermis tissue.5 However, experimental evidence for this
the cells is shown. The specimen shown in figure (b) has been taken from
hypothesis is not available. Anticlines might also be tabular,
the same leaf, but was investigated without any fixation or special drying
procedure. Thus the loss of the water from the cells led them to collapse.
which means in the same level as the cell surface, as shown in (I)
These figures demonstrate, that the loss of water from the specimen might of the scheme in Fig. 5b. In such a case, the cell boundaries are
have a great influence on the cell morphology, and shows also that only visible in SEM by cross-section through the epidermis.
specimen preparation like critical point drying, prevents shrinking of cells Exposed or sunken anticlines shown in Fig. 5b (II and III) point
by water evaporation in the vacuum chamber of the SEM. out the boundaries of the cells and are the more common ones.
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Fig. 6 Schematic of the structural division of a single cell surface.

Anticlines (A) and the directly connected cell area, called anticline field
(AF). The central wall (CW), delimits the central field (CF) in the middle
of the cell surface (modified after ref. 5).
Fig. 4 (a) Schematic of the basic outlines of epidermal cells. In (I)

tetragonal cells with equal length of the cell anticlines are shown. If two
opposite anticlines of a tetragonal cell are longer than the other ones, the
cell form is called tetragonal-elongated (II). In (III) polygonal cells with
more than four edges are shown. Elongated polygonal cells are shown in
(IV). The SEM micrographs of the common annual bluegrass (Poa
annua) show polygonal cells on the upper (adaxial) (b) and tetragonal-
elongated cells on lower (abaxial) leaf side (c).
Fig. 7 Schematic drawings of cross sections through epidermis cells. In

(a) the three possible basic sculptures of cell surfaces are shown: (I) flat
cells, also referred to as tabular cells, (II) convex outlines of cells, and (III)
a concave outline with a sunken profile. Figure (b) shows variations of
tabular cells with (I) completely flat cells, (II) with convex hunches and
(III) with concave hunches. In (c), different convex cell shapes are shown:
Fig. 5 (a) Schematics of different outlines of cell boundaries (anticlines)
(I) convex, (II) hemispherical, (III) cupola, (IV) conical, (V) papilla, (VI)
in top view: (I) straight, (II) V-undulated, (III) U-undulated, (IV) omega-
hair-papilla, (VII) hair. The aspect ratios, which determine the cell types,
undulated (V) and S-undulated. In (b), cross sections through the cells
are given in the text (modified after ref. 5).
and possible sculpturing of the cell boundaries are shown: (I) flat anti-
clines (not visible in SEM), (II) sunken anticlines and (III) exposed
anticlines.
the most common cell type in epidermal surfaces. They are found
on flower-leaves, stems and leaves.53 Convex cell morphologies
Cell surfaces are not always homogeneous in their structure. In always form a three dimensional microstructure on the surface.
many cases a single cell can be divided by structural pattern on These cell morphologies originate by expansion of the outer side
the surface. The different regions within a cell surface divide the (periclinal wall) of the epidermis cells. Most epidermal cell sizes
cell area into an inner part, called the central field, and an outer range between a few to more than hundred micrometres. Convex
part, called the anticline field (Fig. 6). In this scheme the fields are sculptures can be divided into several subtypes, depending on the
formed by the different patterns of surface structures. In other outline of the epidermis cells and their aspect ratio (width to
cases the fields within the cell area can be differentiated by height) (Fig. 7c). Additionally, the aspect ratio of the cells
particular enhanced or decreased parts of the cell. determines whether it is called a papilla or a hair. Aspect ratio
The cell sculptures or curvature of the outer epidermis wall (b ¼ width/height) of the convex cell types and their terminology
(periclinal wall) has an important influence on the surface is as follows: convex (b $ 3/1), hemispherical (b z 2/1), cupola
roughness in the micrometre scale. The three basic forms of cell (b < 3/2), conical (b > 3/2), papilla (b < 3/2 and > 1/2), hair-
curvatures, tabular (flat), convex (arced to the outside) and papilla (b < 1/3 and > 1/6), hair (b < 1/7).
concave (arced to the inside), are shown in Fig. 7a. Tabular cells Hairs are also named trichome (Gr.: trichoma). These are
might be completely smooth or may have raised or sunken areas, outgrowths from an epidermal cell (unicellular), or they are built
Fig. 7b. The central area of a cell can form a convex outgrowth, up of several cells (multicellular). Further, trichomes can be
which forms papilla or hair like structures. The convex cell type is divided into glandular and non-glandular (non-secreting), and
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into dead and living ones. Here unicellular or simple-trichomes

are described, and multi-cellular glands and trichomes are
described later. Simple trichomes can be found on the aerial
surfaces of most flower-plants (angiosperms), some conifers
(gymnosperms) and on some mosses (bryophytes).54 The func-
tions of hairs are correlated to several factors, which include their
density and orientation, their sizes, shapes and their surface
structures. Simple, non-glandular or sticky hairs might reduce
the movement of insects on the plant surface. Many plants of dry
habitats show a dense cover of dead, air filled hairs, which reduce
mechanical abrasion by sand particles, and reflect the visible
light, which makes the surfaces appear white. Two representa-
tives with un-branched hairs are the leaf surfaces of Leucaden-
dron argenteum and Kalanchoe tomentosa (Fig. 8a, b). Dense
layers of hairs might also decrease or increase the loss of water

and influence the wettability of the surfaces.55 In seeds, hairs
might also function as an anchor for seed dispersal by animals or
by wind. An overview and several references for the functions
of plant hairs are given by Wagner et al.,54 and more recently

by Martin and Glover.53 However, regarding the terminology of
convex cell structures, Martin and Glover found that even some
hairs can be difficult to distinguish from conical-papilla cells and
emphasize that often, the only distinguishing feature is the
patterning of the different cell types. In this, papillae cells are
almost always found in groups, whereas trichomes are more
usually separated by one or more tabular or slightly convex cells.
The structures of hairs are often more complex; thus, the
definition based on the aspect ratio fits well only for simple,
undivided hairs. Other morphologies are hairs with lateral
barbed hooks in Caiophora coronaria (Fig. 8c), or hairs of Hip-
pophae rhamnoides, which form lobbed shields (Fig. 8d) and
Fig. 8 SEM micrographs of hairs and glands on plant surfaces. (a)
simple or double branched hairs as shown in Fig. 8e, f for Cistus Leucadendron argenteum with a dense layer of straight, un-branched hairs
symphytifolius and Lavendula angustifolia. These complex hair almost orientated parallel to the leaf surface. (b) The un-branched hairs
structures require a more differentiated description than the of Kalanchoe tomentosa are orientated upright. (c) Single hairs with
aspect ratio used for simple hairs.56,57 terminal and lateral barbed hooks on a leaf of Caiophora coronaria. (d)
Further examples of trichomes are unicellular secretion glands. The peltate hairs of Hippophae rhamnoides form lobed shields, which lie
They are characteristic for all members of the Lamiaceae, e.g., flat on the leaf surface. (e) Simple branched, star like hairs and two
Lavendula (Fig. 8f), which secrete volatile oils, and the leaves of morphological different glands (arrows) on the leaf of Cistus symphyti-
Pelargonium zonale (Fig. 8g) and Cannabis sativa (Fig. 8h). folius. (f) Multiple ramified hairs and short stalked glands (arrow) on
Glandular and simple trichomes are not directly connected to the a leaf of Lavendual angustifolia. In (g) a single-cell gland on Perlagonium
zonale with secretion head is shown. In figure (h) an exposed leaf vessel
vascular system of the organ tissues. The sizes and morphologies
with hair-papilla and un-stalked gland (arrow) of Cannabis sativa is
of trichomes are often species specific and that makes some kinds
shown. Figures a–g obtained from upper (adaxial) leaf sides and figure
of trichomes useful morphological features in plant systematics.57 (h) from the lower (abaxial) leaf side.
Another surface structure is formed by concave cells. Concave
cells are seldom found on fresh epidermal cells, but occur often
on dry seed surfaces (testa cells).58 They are characterized by kind of cuticle structuring results from the folding of the cuticle
a complete or particular deflection of the outer epidermis wall. itself (Fig. 9c). Additionally, on many plants a wax layer on top
Cell shrinking induced by water loss of the cells might lead to of the cuticle leads to surface structuring as shown in Fig. 9d. The
concave cell morphology. structuring of the epidermal surface is responsible for several
Most surface structures within a single epidermis cell range in surface properties. Most prominent properties are the increase or
the dimension of less than one micrometre, but can also reach decrease of surface wettability, light reflection and particle or
several micrometres. Here we describe the four frequently found insect adhesion. All four types of surface structuring are intro-
modifications of the outermost layers of the epidermis which are duced in the following parts.
responsible for the creation of a structured cell surface. All four
types are schematically shown in Fig. 9. The first kinds of
Cuticular folds
structures are coves and folding of the cuticle, which originate
from coves of the underlying cell wall (Fig. 9a). The second kind Cuticular folds have been described for nearly all above-ground
of structure of the cuticle might originate by sub-cuticular inserts surfaces of plants, but are very frequently found in the leaves of
of mineral crystals, such as silicon oxides (Fig. 9b). The third flowers (petals), as shown here for the flower leaf (petal) of
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Fig. 9 Schematic of cross sections through plant epidermis cells show

different sources leading to microstructuring of plant surfaces. In (a), the Fig. 10 SEM micrograph of the cell surface structures of the common
surface profile is induced by coves of the underlying cell wall, in (b) by Horsetail (Equisetum arvensis). In the middle of the figure a stomata is
insertion of sub-cuticular minerals, in (c) by folding of the cuticle and in shown. The stomatal cells and the surrounding cells are convex, and have
(d) by waxes, which are located on top of the cuticle (epicuticular wax). a micro-pattern of some small enhanced spots on the cells. The latter are
Wax ¼ epicuticular waxes, CM ¼ cuticular membrane, P ¼ pectin, formed by sub-cuticular inserts of silicon-oxide crystals.
PM ¼ plasma membrane (modified after ref. 5).
Dahlia in Fig. 3. Cuticular folds might originate due to the cuticle can be solid crystals of silica (Si-ox), as described for the
itself, or by the expression of the bulk of the cell wall below, or by leaves of rice (Oryza sativa) and, as shown in Fig. 10, for the
sub-cuticular deposits. The resulting structures are folding or members of the genus of Equisetum (tin plant or horse tail).
tubercular (verrucate) patterns of the surface. For identification Calcium oxalate crystals are also frequently found in plants,
of the actual cause, it is necessary to analyze cross-sections of the and verification of silicon or calcium presence can simply be
epidermal cells by SEM, or by staining the cuticle with a lipoid made by energy dispersive X-rays (EDX) analysis, equipped in
colorant, followed by an investigation of the cross section by an SEM.
high resolution light microscopy. Several examples of cuticular Silicon (Si) is a bioactive element associated with beneficial
folds have been described by Barthlott and Ehler.5 They cate- effects on mechanical and physiological properties of plants. It is
gorize the cuticle pattern according to the thickness (width) of a common element found in plants and occurs as monosilic acid
the folding, distances between the folding, and orientation of or in the polymerized form as phytoliths (SiO2–nH2O).61 In
the folding, and generated several subcategories to describe the plants, Si tends to polymerize in cell walls, cell lumen, and occurs
distances between, and width of the folding. Additionally, at intercellular spaces and in the sub-cuticular layer.62 Fauteux
the pattern of folding in the central and anticline field of a cell et al.63 reviewed the existing literature and presented evidence
might be different, as shown schematically in Fig. 6 and with an that silicon increases the resistance of plants to pathogenic fungi.
example in Fig. 11b (to be discussed later). They conclude that the protective function of silicon against
The functional aspects of cuticle folding are rarely investi- pathogen infection could be only rarely interpreted as an increase
gated, but their frequent occurrence on flower leaves led to the of mechanical stability, but it enhances the expression of genet-
assumption that cuticular folding forms a favourable structure ically controlled defense mechanisms in plants.
for insect pollinators to capture and walk on such leaves. Calcium oxalates have been reported for more than 250 plant
Maheshwari59 described that cuticular folding is a signal for the families of the gymnosperms and angiosperms.64 Calcium
germination of fungi and guides the growing fungi to the stomata oxalate crystals occur in five different morphological variations,
entrance into a leaf. Evidence for this thesis is based on in-vitro like raphides (needles), druses (spherical aggregates) or prisms.
investigations with structured technical surfaces. Hoch et al.60 With some exceptions like in the Nympha and Cassuarina, they
microfabricated ridges and grooves of defined height, width and are rarely found on the outer epidermal cell walls. Because of
spacing on inert templates by electron beam lithography. In the their location within the plant body (in roots, stems, leaves,
bean rust fungus (Uromyces appendiculatus), 0.2 mm width ridges seeds), they are believed to be of limited taxonomic value. Their
in the surface guided the germ tube to grow perpendicularly, but protective function against herbivorous animals has been dis-
did not induce an anchor (appressorium) formation, which is cussed for a long time, but this function is still almost a question
necessary for a successful colonization. of the relation of sizes of both the herbivorous animal and crystal
Barthlott and Ehler 5 observed that the cuticular folding and sizes.65
its characteristic patterns already exist in very young organs, and
that only the amount of folding per area might increase during Cell wall induced sculpturing
parthenogenesis of the organs. But formation and function of
these complex structures are yet not completely understood. Another principle of cuticle folding is induced by an undulated
morphology of the underlying cellulose cell wall. This kind of
structuring has been described for the epidermis surfaces
Sub-cuticular inserts
of some seeds.66 For example, the sculpturing within a single cell
Microstructures on epidermis cells might also arise from sub- of the seed coat of some Epilobium species is built by cell wall
cuticular inserts of mineral crystals. These sub-cuticular inserts thickening.67
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Epicuticular waxes
Epicuticular waxes are the most common type of cellular struc-

turing. Several investigations by SEM showed that most of the
epicuticular waxes form three-dimensional structures with large
variations in their morphologies. These waxes are sometimes
visible as a white or bluish coloration on some fruits like grapes
and plums. A smooth, 2-dimensional wax film exists also on
glossy plant surfaces. Because waxes are a component of the
plant cuticle, one may conclude that all the primary epidermal
cells are covered with waxes, at least with a thin layer of wax
molecules, not visible by SEM. The known exceptions are those
surfaces which are not covered by a cuticle, such as wood
(secondary cells) roots, and some mosses.
Three dimensional epicuticular wax structures usually occur in
sizes from 0.5 to 100 micrometres, whereas 2-dimensional wax

films range from a few molecular layers up to 0.5 micrometres.
Recent overviews about terminology and micro-morphology are
given by Barthlott et al.29 and Jeffree.3 Jeffree distinguishes six
main morphological wax types, including a background epicu-

ticular wax film, which covers the cuticle surface below and
between the 3-D waxes. This wax film is rarely visible in SEM
when leaves are investigated, but can be well visualized after
mechanical separation of the waxes from the plant surface and by
AFM investigation.30 The classification of Barthlott et al.29
includes 23 different wax types, based on chemical and
morphological features, and also considers orientation and
pattern of the waxes. With respect to both classifications, the
most common wax morphologies are thin films and several three-
dimensional structures such as massive crusts, threads, flat lying Fig. 11 SEM micrographs of epicuticular waxes: (a) fissured wax crust
plates, upright standing platelets, filaments, rods, and tubules on a leaf of Crassula ovata. A cross section through the periclinal wall of
which have a hollow centre. In Fig. 11, wax layers, tubules, Aloe striata (b) shows the cuticle (indicated by C) and a wax layer
platelets and rodlets are shown. However, some wax types, such (indicated by an arrow) with wax platelets on top. In (c) b-diketone wax
tubules of Eucalyptus gunnii are shown, and in (d) nonacosan-ol tubules
as the tubules, have been further divided in sub-types depending
on Thalictrum flavum glaucum leaves. (e) Shows randomly orientated wax
on their dominating chemical compounds3 or in morphological
plates of Aloe porphyrostachys and (f) wax platelets on Robinia pseu-
sub-types as, for example, entire and non-entire wax platelets.29 doacaia leaves arranged in rosettes. Wax rodleds on a cabbage leaf
A further sub-classification is based on the arrangement of the (Brasiica oleracea) (g), and transversely ridged rodlets on a leaf of
crystals, e.g., whether they are randomly distributed, in clusters, Sassafras albidum (h).
in parallel orientation or in specific arrangements around
stomata as in the ‘‘Convallaria’’ type.29 In particular, the parallel
However, during the formation process the wax chemistry has
orientation of platelets on the leaves of several plant species leads
a formative, but not exclusive, influence on the final form. For
to the question as to how the orientation is controlled by the
example, isolated nonacosan-10-ol may recrystallize in-vitro into
plant.3 It is assumed that the cutin network functions as
tubules, but under varying crystallization conditions, may also
a template for the growth of the three-dimensional wax crystals,
recrystallize into different morphological shapes.72 Additionally,
but there is still a lack of information about the molecular
the substrates on which the crystals grow might also influence the
structure of the cuticle, so this question could not be answered
crystal morphology and their orientation on the substrate;74 thus
yet.
in-vitro recrystallization of waxes could be used to create
Certain surface wax types and their orientation patterns are
different kinds of nano- and micropattern on technical
characteristic for certain groups of plants, thus patterns and the
surfaces.74–76
morphology of plant waxes have been used in plant system-
atics.68–70 Barthlott et al.7 provide an overview of the existence of
2.2.2 Hierarchical structures of single cells (double structured
most important wax types in plants, based on SEM analysis of at
surfaces). Hierarchical structures are built by a combination of
least 13 000 species, representing all major groups of vascular
micro- and nanostructures. In plants, there are two frequently
plants.
occurring combinations: a convex cell with a cuticular folding or
There is much evidence that the different wax morphologies
verrucose cuticle structure, and a convex cell with three-dimen-
arise by self-assembly of the wax molecules.31,71–75 This has been
sional wax crystals. The terminology of Barthlott and Ehler5
shown by the recrystallization of waxes, which were isolated
describes surface structures like the epicuticular waxes as the
from plant surfaces. In this, most waxes recrystallized in their
tertiary structure of a cell, and cuticular folding of the cell is
original morphology, as before found on the plant surfaces.
added to the secondary structures. However, the pretension here
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is strictly hierarchical, and in this sense, we determine the (Fig. 12e) are nonacosan-ol tubules. The wax crystals on the cell
combination of a microstructured surface, built up of convex papilla of Oryza sativa are platelets (Fig. 12g), but here a single
cells, with a fine structure on it as a double-structure or hierar- cell has more than one papilla. The right column of Fig. 12 shows
chical structure. convex cells with cuticular folding. The seed surface (testa) of
Both the three-dimensional epicuticular waxes and cuticular Parodia alacriportana subspecies buenekeri is characterized by
folding are able to create the double-structure. Examples for single convex cells (Fig. 12b). These are divided by the arrange-
both kinds of double-structures are shown in the left column of ment of the cuticular folds in a central and an anticlinal field.
Fig. 12. These surface examples are characterized by papilla and This type of structuring represents the basic structure of all
convex cells with three-dimensional waxes on top. In Colocasia existing patterns of cuticular folding.5 A similar pattern is shown
esculenta (Fig. 12a) and Euphorbia myrsinites (Fig. 12c) the wax on the conical cells of a flower leaf of Rosa montana (adaxial
crystals are wax platelets, whereas the waxes of Nelumbo nucifera side). Here, a rippled folded cuticle forms the central field of the
cells and parallel folds occur at the anticline field (Fig. 12d).
Another example is the hair-papilla cells of the inner side of
a tube like leaf of the carnivorous plant Sarracenia leucophylla
(Fig. 12f). The cells are downward trending hair-papilla, with

a parallel cuticle folding and with larger distances at the basis and
denser arrangement at the cell tip. A combination of convex cells
with both a cuticular folding and three-dimensional waxes is very
rare for plant surfaces, but not excluded. The sliding zone of the
inner tube surface of the carnivorous plant Sarracenia leuco-
phylla is built up of downward trending cells of hair papilla (same
micro-morphology as described above), but here wax platelets
form a further level of structure (Fig. 12h). A combination of
convex cells with granular cuticular structure of each epidermal
cell and superimposed wax crystals has been found for Hygro-
ryza aristata. The epidermis cells of these leaves each form up to
50 hemispherical papillae and thereby create a superhydrophobic
structure.33
2.2.3 Multi-cellular surface structures: glands and hairs.

Structuring of plant surfaces might also originate from more
than one cell. The most common multicellular structures are
secreting glands, and non-secreting multicellular trichomes. The
next section introduces hairy and glandular multicellular surface
structures and their functions.
Glands or glandular trichomes can be found on approximately
30% of all vascular plants.77 Multicellular glands include salt
glands, nectarines, or the adhesive secreting glands of some
carnivorous plants.54 These glands have multicellular heads,
while others, like those of geraniums (Perlagonium) (introduced
before in Fig. 8), are formed by a single cell. The exudates of
glands are, for example, terpenoids, nicotine, alkaloids or
flavonoids. Flavonoids occur as aglycones in trichome exudates
in many plants. The exudates of some ferns and angiosperms, in
Fig. 12 SEM micrographs of hierarchical structures on plant surfaces. particular several members of the Primulaceae, are composed of
Left column shows double structured plant surfaces with convex cell flavonoids.78,79 These exudates are morphologically similar to
shapes and superimposed three-dimensional epicuticular waxes on the waxes, but due to their chemical divergence to plant waxes, which
upper (adaxial) leaf sides of (a) Colocasia esculenta, (c) Euphorbia are composed of cyclic and aliphatic long chain hydrocarbons,
mysinites, (e) Nelumbo nucifera and (g) Oryza sativa. Convex cells with they are widely referred to as ‘‘farina’’ or ‘‘farinose’’. Secretion
cuticular folding are shown in the right column. In (b) the seed surface of and accumulation of toxic compounds at the plant surface allows
Parodia alacriportana subspecies buenekeri is shown. In (d) the flower leaf direct contact with insects, pathogens and herbivores, and might
of Rosa montana (adaxial side) with a rippled folded cuticle in the central therefore be an effective defense strategy.54 However, other
field of the cells and parallel folding, which trend to the anticline walls of
glandular trichomes are also known to attract insects. Glands of
the cells is shown. The cells of the inner side of a tube like leaf of the
the carnivorous plants of the genus Drosera (sundew) and Pin-
carnivorous plant Sarracenia leucophylla are shown in (f). These cells are
downward trending hair-papilla with a parallel cuticle folding, with larger
guicula (butterworts) secrete adhesives and enzymes to trap and
distances at the basis and denser arrangement at the cell tip. The same digest small insects like mosquitoes and fruit flies. On the surface
species as before is shown in (h), but the micrograph is taken in a different of the leaves exists stalked glands, which are the sticky ones
area within the pitcher. In this a structure combination of hair papilla which trap the insects by secreting an adhesive solution
cells with both a cuticular folding and three dimensional waxes is shown. (Fig. 13a–c). The shorter ones are those which secrete digestive
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In contrast, leaves with waxy trichomes were extremely water-

repellent, although the trichomes were up to 2 mm high and only
loosely distributed over the leaf surface, as for example on leaves
of Salvinia auriculata and Pistia stratiotes.
3. Surfaces and wetting

3.1 Introduction
Wetting is the fundamental process of liquid interaction at solid–

gaseous interfaces. It describes how a liquid comes into contact
with a solid surface. Wetting is important in many everyday
situations, for example, liquid paintings on walls, printing of
texts and for the transport of fluids (water, oil, blood and many
others) through pipe systems, and it is the basis of several
cleaning procedures. However, there are many situations where it

is desirable to minimize wetting, because adhering water droplets
on window glass and car windshields reduce the view and leave
residuals after evaporation. Rainwear should stay dry even
during heavy showers, and also movement in water costs extra

energy because of friction force at the interfaces. At the two
Fig. 13 Multicellular trichomes on plant surfaces. In figure (a) glandular surfaces in relative motion, condensation water vapor from the
hairs of the carnivorous plant Pinguicula gypsicola on the upper (adaxial) environment forms meniscus forces responsible for the adhering,
side of the leaf are shown. (b) Shows a detail of the stalked and (c) of non- friction and wear.24,51,84 Wetting is also important for many
stalked glands. The stalked glands secrete an adhesive secretion to trap biological processes like the germination of seeds or microor-
small insects, un-stalked glands provide the enzymes for digestion of the ganisms like fungi, reproduction of bacteria, and is essential for
insects. (d) The water fern Salvinia biloba and (e) Salvinia oblongifolia. water uptake in soils.85 Under suitable conditions, microor-
The water drop on the hairy leaf in figure (e) shows the hydrophobic ganism proliferation results in the formation of larger pop-
character of the surface. The SEM micrographs of the leaf surface of ulations called bio-films. Bio-films induce apparent defects in
Salvinia minima (f) show the multi-cellular hairs with two and three-
technical materials, and also their acidic excretions are damaging
armed structures. In higher magnification (g) the epidermis cells and the
to buildings and technical materials.86 Thus, it is not surprising
wax rodlets (h) on the epidermis cells are shown.
that the basics of surface wetting processes have been of scientific
interest for several decades. In particular since the early 1990s
enzymes, including protease and phosphatase, and later resorb a large amount of scientific work has been carried out to under-
the digested material.80 stand and produce surfaces which are extremely water repellent.
Multicellular hairs are common in many flowering plant The basics of surface wetting are summarized here. For a deeper
groups. Particularly interesting forms occur in the floating water study, specific literature such as the books of Adamson,87
ferns of the genus Salvinia. Within this genus, morphologically Israelachvili,88 Bhushan,51 de Gennes et al.89 and Bhushan 52 are
different kinds of water repellent (superhydrophobic) hairs exist. recommended.
The multicellular hairs on the upper (adaxial) side of the leaves of
the species of genus Salvinia form complex hierarchical surface
3.2 General remarks about surface wetting
structures which are able to retain an air layer at the surface, even
when leaves were fixed under water for several days.81,82 The hairs 3.2.1 Surface wetting and contact angle (CA). A droplet on
are multicellular and have the shape of tiny crowns. Dependent a solid surface wets the surface to a certain degree. To what
on the species, the hair sizes range in the dimensions of several extent a surface gets wet can be described by the contact angle
hundreds of micrometres, and are visible with the naked eye (CA). A high contact angle describes surfaces on which a water
(Fig. 13d, e). In SEM, the fine structure of the hair surfaces shows droplet forms a spherical shape; thus the real contact between the
small wax rodlets on the epidermis cells (Fig. 13f–h).83 adhering droplet and the surface is very small compared to
Trichomes in general might have a strong influence on leaf wettable surfaces, on which an applied drop of water tends to
wettability (water repellency). Brewer et al.55 investigated 38 spread, and contact angle is low. The CA of a liquid on a surface
plant species from 21 families and found that leaves with depends on the surface tension (molecular forces) of the involved
trichomes were more water repellent, especially where trichome liquid, solid surface and the surrounding vapor. Thus, wetting
density was greater than 25 mm2, but in some species droplet depends on the ratio between the energy necessary for the
repellency and retention were both high, and in some species enlargement of the surface and the gain of energy due to
trichomes entrapped droplets. However, the contact angles for adsorption.87,88 In the following explanation wetting with water
the single species surfaces were not presented. Neinhuis and and air as the surrounding vapor is assumed. The behavior of
Barthlott33 found that the wettability of hairy leaves strongly liquids is different when applied to smooth or structured
depended on the presence or absence of wax crystals on the surfaces. The contact angle given by Young’s equation or the
trichomes. Leaves with non-waxy trichomes were only water- Young contact angle (YCA) is a static (equilibrium) angle. The
repellent for a short time after a water droplet had been applied. interfacial tensions between liquid–air, liquid–solid and solid–air
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On rough surfaces where an applied water droplet cannot

completely move into the structure grooves air pockets exist
between the water and the surface. In this case, the air pockets
inside the grooves underneath the liquid reduce the contact area
between liquid and surface. For such surfaces, a heterogeneous
wetting regime has been described by the Cassie & Baxter
equation. The transition between the homogeneous and hetero-
geneous wetting regimes plays a major role in super-
hydrophobicity because the latter reduces the solid–liquid
contact area.92–94
However, Wenzel’s equation applies to a CA where droplets
are in equilibrium, but not to advancing and receding angles of
a droplet on a rough solid surface that give rise to contact-angle
hysteresis (CAH). Hysteresis is responsible for the sticking of
liquids on a surface, and is defined as the difference of the

advancing and receding angles of a moving or evaporating water
droplet (CAH ¼ CAadv – CArec). If additional liquid is added to
a sessile drop, the contact line advances; if liquid is removed from
the drop, the CA decreases to a receding value before the contact

retreats. If a droplet moves over a solid surface, the CA at the
front of the droplet (advancing CA) is greater than that at the
Fig. 14 Wetting of a solid surface with water, with air as the back of the droplet (receding CA). However, the droplet rolls
surrounding medium. gLA, gLS and gSA are the interfacial tensions at the with little resistance if the contact angle hysteresis is small.92,93,95
boundaries between liquid (L), solid (S), and air (A), which determine
the CA of an applied water droplet and are described by Young’s 3.2.2 Tilting angle (TA). On water repellent surfaces an
equation. The hysteresis of a water droplet on a tilted surface represents applied droplet starts to roll off the surface when the surface gets
the adhesion of the liquid on the surface and can be determined by
tilted to a specific degree. This tilt angle (TA) (Fig. 14) is defined
measuring the tilting angle or the advanced and receding angle of a water
as the tilting degree of a surface upon which an applied drop
droplet.
of water starts to move. Low TAs (<10 ) are characteristic for
superhydrophobic and self-cleaning surfaces, whereas the
determine the contact angle of a liquid droplet on a given surface
combination of high CA and high TA is not. The TA is not equal
and are described by Young‘s equation, shown in Fig. 14.
to the hysteresis angle, which reflects the difference between the
The YCA is also referred to as ideal CA, which means it is the
advancing and receding CAs.
CA of an ideal smooth, rigid, chemically homogeneous, insol-
uble, and inert surface. Biological surfaces and other surfaces of
3.2.3 Bouncing droplet. Another important phenomenon
technological interest are far away from these theoretical
related to wetting behavior is the bouncing of droplets. When
approaches, because they are always rough, seldom rigid,
a droplet hits a surface, it can bounce, spread or stick. In prac-
chemically heterogeneous, particularly soluble, and reactive
tical applications of superhydrophobic surfaces, surfaces should
surfaces. The basis for studying equilibrium wetting on rough
maintain their ability to repel penetrating droplets under
surfaces was established many years ago by Wenzel90 and Cassie
dynamic conditions. Many researchers have considered the
and Baxter.91 The influence of roughness on the wetting behavior
dynamic effects of droplets on superhydrophobic surfaces.
can be expressed by the Wenzel equation. The assumption that
Richard et al.,96 Bartolo et al.,97 Reyssat et al.98 and Jung and
the surface chemistry is homogeneous, and the roughness of the
Bhushan99 showed that on a patterned surface the transition
surface is much smaller than the applied water droplet, leads to
from wetting to non wetting can occur with a critical geometric
the Wenzel equation:
parameter. A criterion was presented by Jung and Bhushan99 to
cos qW ¼ rfcos qY (1) predict the transition based on the impact velocity and the
geometric parameter of the patterned surface.
where qW is the Wenzel angle, rf is the roughness ratio defined as
the ratio between the actual and projected solid surface area (rf ¼ 3.2.4 Classification and definition of surface wetting. The
1 for a smooth surface, and >1 for a rough one) and qY is the contact angle (CA) measurement is the main method for the
Young’s CA. It is important to recognize that the Wenzel characterization of the hydrophobicity of surfaces, and the CA is
equation is based on the assumption that the liquid completely a unit for the wettability of surfaces. However, there are only two
penetrates the grooves of a rough surface (homogeneous well-defined categories of hydrophobicity; the hydrophilic one
wetting). Thus, the key parameter controlling the contact angle having a CA of less than 90 , and the hydrophobic one with CA
on this surface is the solid roughness, where the Wenzel equation higher than 90 . The limit of this classification is that super-
expresses a general amplification of the wettability induced by hydrophilic surfaces are not defined and different definitions and
roughness. That means a hydrophilic smooth surface gets more classifications for superhydrophobic surfaces exist. Recently
hydrophilic, and a hydrophobic surface gets more hydrophobic several authors have attempted to establish a uniform definition
by an increase of the surface roughness. for superhydrophobic surfaces, but there are more wetting stages
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modifications induce variations in surface wetting, ranging from

superhydrophilic to superhydrophobic. The sculptures of the
cells, the presence of hairs and the fine structure of the surfaces,
e.g., folding of the cuticle or existing epicuticular waxes, have
a strong influence on surface wettability. Next, representative
plants and their structures and wettability are given for the four
defined classes of surface wettability (hydrophobic, hydrophilic,
superhydrophobic and superhydrophilic). The different struc-
tural characteristics of plant surfaces and their wetting behavior
are summarized in Fig. 16, and examples are given in Table 1 and
in the following section. The required low hysteresis for the class
of superhydrophobic self-cleaning surfaces has not been inves-
Fig. 15 Four classes of surface wettability, the characteristic static
tigated for most of the plants.
contact angles, and with a schematic demonstration of possible surface
Several data on plant surface wettability exist in the literature,
sculpturing of plant surfaces.
but only a few publications present a general overview of a larger

number of species.33,107–109 In these, the static CAs of single water
than the superhydrophobic one. Here, we like to classify the droplets and, if present, descriptions of epicuticular waxes are
wetting behavior of solid surfaces in four classes, defined by their given. General remarks about the coherence of plant surface
CA, and for superhydrophobic ones also by their hysteresis. structures and their wetting behavior are given in the early work
On wettable surfaces with low contact angles, fluid will spread of Holloway.110–112
and cover a larger area of the surface. Such surfaces should be
termed superhydrophilic when the CA is <10 . Surfaces with 3.3.1 Hydrophilic and hydrophobic plant surfaces. The
CAs of $10 and #89 are termed hydrophilic surfaces. Un- chemical nature of most plant surfaces is hydrophobic, meaning
wettable surfaces have high contact angles, meaning the liquid on that a water droplet applied to the surface has a static contact
the surface forms a semispherical or spherical droplet (Fig. 15). angle between $90 and <150 . This phenomenon is based on
Surfaces on which the CA is $90 and #150 are hydrophobic the hydrophobic waxy nature of the plant cuticle, whose primary
surfaces. A superhydrophobic surface is defined as the one that function is a barrier against water loss.
has a static CA of $150 , and if those superhydrophobic surfaces The micro-morphological characteristics of hydrophobic plant
have a low hysteresis or a low tilting angle of less than <10 they surfaces are tabular cells or only slightly convex epidermal cells,
are superhydrophobic and self-cleaning surfaces. This definition covered with a thin wax film (2-D waxes) or by a relatively low
of superhydrophobic surfaces has been used in most recent amount of 3-D waxes. Additionally, tabular cells might be
reviews20,25,100–103 and is the preferred one, which might be used to structured by cuticular folding, in which case a 2-D wax layer is
overcome the existing variety of definitions. present on the surface. However, for most plants, these wax
layers have not been referred to in the literature, because they are
not or are only rarely visible in SEM. It might also be that hairy
3.3 Plant surfaces and their wetting behavior
leaf surfaces form hydrophobic structures, but evidence with
The plant cuticle with its integrated and exposed waxes is in given contact angles has not been found; thus, we forego adding
general a hydrophobic material, but structural and chemical these structures into the more frequent surface morphologies.
Fig. 16 Four groups of plant surface wettability and the possible surface structures and structure combinations. The wetting symbols used for the four
groups are correlated to specific contact angles, which were defined in the text and are shown in Fig. 15. Both the hydrophobic and superhydrophobic
surfaces can be built from convex cells with three dimensional waxes on them, but only a high density of wax crystals per area leads to superhydrophobic
surfaces. *After Neinhuis and Barthlott;33 defined as temporary superhydrophobic surface structures, because erosion of 3-D waxes by environmental
impacts can reduce the contact angle.
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Table 1 Four groups of plant surface wettability and some representative species. The characteristic microstructures (cell form) and fine structure of the
cell surfaces (waxes, cuticular folds) are shown, and contact angles are given. The abbreviation spp. means several non named species of the genus
Wetting of plant surfaces: species, structures and contact angles (CA)
Hydrophobic (90 # CA < 150 ) Hydrophilic (10 # CA # 90 )
Species CA/ Surface structure Species CA/ Surface structure
Fagus sylvatica 103a Tabular cells + 3-D wax Prunus laurocerasus — Tabular cells + 2-D wax
Zea mays 138b Nymphea spp. c
Carya tomentosa 41e Convex cells + 2-D wax Viola tricolor (petal) e
Papilla cells + 2-D wax
Quercus robur 40e Rosa montana (petal) e
+cuticula folds
Fouquieria columnaris 117c Tabular cells + cuticular Artemisia tridentata c
Hairs
Schismatoglottis 77e folds + 2-D wax Senecio cinerea c
neoguineensis
Superhydrophobic (CA $ 150 ) Superhydrophilic (CA < 10 )

Species CA/ Surface structure Species CA/ Surface structure
Nelumbo nucifera 162c Papilla cells + 3-D wax Spahgnum 0e Porous cells
Euphorbia myrsinites 162c Rhamnocarpus purpur. 0e
Pistia stratoides >150c Hairs + 3-D wax Calathea zebrina <10e Papila cells + 2-D wax
Salvinia oblongifolia 162d Marantha leuconeura <10e
Tropaeolum majus 160e Convex cells + 3-D wax Annanas comosus 0e Hairs
Eucalyptus macrocarpa 162c Tillandsia usneoides 0e
Crambe maritima >160e Tabular cells + 3-D wax
Brassica oleracea 161c
a
Data are taken from Paoletti et al.104b Beatie and Marcell.105c Neinhuis and Barthlott33d Cerman et al.82e Barthlott (unpublished data).106
On hydrophilic surfaces, a drop of water has a contact angle surface, e.g., secretion of hydrophilic compounds by epidermal
between $10 and <90 . Hydrophilic surfaces are known from glands. Optimized organs for the uptake of water are the roots of
many flower leaves which have a papilla cell morphology and the plants. Most roots are characterized by papillae and hairy
cuticula folding, but also from leaves which have tabular cells. cells, but also porous surface structures have been described for
Those surfaces have only smooth 2-D wax films on their surface the air roots of epiphytic plants. Superhydrophilicity is also
and no 3-D wax crystals. Examples with these characteristic a great advantage for lower plants (mosses), which have no roots
structures are given in Table 1. Some other hydrophilic surfaces for water uptake and lack vessels for water transport. In those
have trichomes (hairs and glands) on their surface. In this case, species, superhydrophilicity of the surface is the basis for the
the hairs are not covered with 3-D waxes. However it is not to be uptake of water and nutrients from the environment. The two
assumed that these hairs are wax free, because this would lead to most common structures are water absorbing trichomes and
an enormous increase in water transpiration. porous structures of mosses.
Why are the leaves of most flowers hydrophilic? There is Lower plants is a collective term for three groups of plants; the
a simple explanation for this phenomenon. Flowers are devel- mosses, liverworts and lichens. Lower plants have no roots for
oped to attract pollinators, in most cases small insects, and these water-uptake and no vascular system for water transport. Some
should be able to walk on the surfaces, but coverage with three species have not even developed a waxy cuticle as a transpiration
dimensional waxes forms a slippery surface for most insects,34 and stabilization element. Water uptake and the uptake of
and would lead to less pollination. Additionally, it is important nutrients in many lower plants occurs over the complete surface.
to notice that hydrophobic leaves might become hydrophilic by Peat mosses (Sphagnum) belong to the lower plants. Their
the accumulation of environmental, hydrophilic contaminations natural habitats are wet swamps and mires, where they might
like spores, bacteria, dirt particles and chemical aerosols on their represent the dominant biomass. The complete plant surface is
surfaces. Atmospheric particles are mostly a conglomerate of free of stomata, which function in higher plants for water tran-
different salts and organic materials.113 These salts dissolve spiration control. Due to their limited ability to control water
by rain, fog and dew, or may become dissolved by stomatal loss via stomata, Sphagnum plants are highly dependent on
transpiration of the leaf114 and have a hydrophilic influence on regular water availability. Water uptake and gas exchange occur
the wettability of the plant surfaces.115 via pores, which are spread over the plant body. Sphagnum plants
are able to uptake 20 times their own dry weight.116 However,
3.3.2 Superhydrophilic plant surfaces. Superhydrophilic water loss occurs relatively fast by evaporation and must be
surfaces are characterized by the spreading of water on the replaced by capillary transport of free water. In some dry
surface. Contact angles of such surfaces are, if measurable, 10 or periods, Sphagnum species show high tolerance to desiccation
less. Superhydrophilicity is based on different morphological and the ability to recover from desiccation.117 Pores are relatively
structures, as shown in Fig. 16, and summarized in Table 1. large openings of 10–20 mm in diameter, whereas the openings of
However, wetting is also influenced by the chemistry of the a porous surface texture are much smaller. An example of
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microorganisms, including bacteria and fungi, is limited by water

shortage. Additionally, the lensing effects of water droplets on
leaf surfaces can increase incident sunlight by over 20-fold
directly beneath individual droplets,55 which may have important
implications for processes such as photosynthesis and transpi-
ration for a large variety of plant species.
Some leaves of tropical plants, such as those of Marantha
leuconeura and Calathea zebrina, are also superhydrophilic. But,
for these plants neither the physico-chemical basis of this kind of
wettability is known, nor has the biological advantage of these
properties been studied.
3.3.3 Superhydrophobic plant surfaces and the Lotus leaf.

Many terrestrial plants and animals are water repellent due to
their hydrophobic surface components in connection with

microscopic roughness. As defined above, a superhydrophobic
Fig. 17 SEM micrographs of superhydrophilic plant surfaces. In (a) the surface is given when the static contact angle (CA) is equal to or
epiphytic growing Spanish moss (Tillandsia usneoides) is shown. (b) above 150 , and low hysteresis lets a water droplet roll off at
Shows a higher magnification of the water absorbing hair structure of T. surface inclinations below 10 .
usneoides. In (c), the water adsorbing porous surface of the moss Rha- The static contact angles of 200 water-repellent plant species
cocarpus purpurescens and in (d) the water uptaking pores of a Sphagnum have been presented by Neinhuis and Barthlott.33 Most of these
moss are shown. The specimen shown in (d) was hydrated and than
leaves showed CAs of 150 , and can therefore be termed super-
critical-point-dried before SEM investigation, thus the figure here
hydrophobic. The morphological characteristics of those leaves
represents a hydrated leaf surface.
were a hierarchical surface structure of convex to papillose
epidermal cells and a very dense arrangement of three-dimen-
a water absorbing porous surface structure is given by the leaf sional epicuticular waxes. In these surfaces only some or all
surface of the moss Rhacocarpus purpurescens. The super- epidermal cells formed a papilla. The shape of individual wax
hydrophilic surface of the R. purpurescens is shown in SEM crystals was found to be irrelevant with regard to wettability as
micrographs presented in Fig. 17. The sizes of the porous were their dimensions (to be presented later). All known crystal
apertures are 2 mm and smaller. The architectural, composi- forms were found on superhydrophobic leaves and their size
tional and functional characteristics of the cell walls of the ranged from 0.5 mm to about 20 mm in length.14 Four examples of
leaves of the moss R. purpurescens have been analyzed by such hierarchical superhydrophobic surface structures are shown
Barthlott and Schultze-Motel 118 and by Edelmann et al.119 They in the left column of Fig. 12.
conclude that the surface exhibits no particular properties for Based on these investigations, we can conclude that the
external water conduction but is adapted to rapid absorption of superhydrophobicity of most plant surfaces is achieved by hier-
fog, dew, or rain. archical structures of convex or papilla epidermal cells with
Water absorption via the leaf surface is not limited to lower three-dimensional wax structures on top. It has also been found
plants. In higher plants, all specimens of the Bromelia family, e.g. that tabular cells with a dense arrangement of wax crystals are
pineapple (Ananas comosus) or Spanish moss (Tillandsia superhydrophobic (e.g., Brassica oleracea and Crambe mar-
usneoides) (Fig. 17) have water absorbing, multicellular absorp- itima), but those leaves are water-repellent for only a limited
tive trichomes on the epidermis cells. The way for the absorbed period of time. This, in most cases, is the case when leaves are in
water goes over the absorbing hairs through to their centre. development, and wax biosynthesis is active, but on mature
There, hydraulic epidermis cells allow the uptake of water by leaves damage or erosion of the waxes can influence the wax
opening the epidermis. In dry periods, these cuticle covered cells structure and result in a less hydrophobic surface.
prevent the loss of water from inside the cells. Some genera in this The hierarchical (double structured) surface is characteristic
group form funnels by arranging their leaves in form of a rosette. for the Lotus leaf (Nelumbo nucifera), as stated earlier, but it also
In these funnels, water can be stored after a rain shower and exists on many other superhydrophobic leaves. On Lotus leaves
organic litter can accumulate and decay, so hairs at the funnel (Fig. 18a) the composite or hierarchical surface structure is built
surface also absorb nutrients dissolved in the water. The hairs of up of convex cells and a much smaller superimposed layer of
different species of the Bromeliaceae might vary morphologi- hydrophobic three-dimensional wax tubules. Wetting of such
cally, but function after the same mechanism. surfaces is minimized, because air is trapped in the cavities of the
For lower plants and the species of the Bromeliaceae, super- convex cell sculptures and the hierarchical roughness enlarges the
hydrophilic surfaces are the basis for water and nutrient uptake. water–air interface while the solid–water interface is reduced.
However, on wet leaves, where a liquid water film exists, the Water on such a surface gains very little energy through
uptake of CO2 for photosynthesis is reduced, because CO2 adsorption and forms a spherical droplet (Fig. 18d, e), and both
diffuses 10 000 times more slowly through water than air.55 Thus, the contact area and the adhesion to the surface are dramatically
there may be strong selective pressure for increased water reduced.14 Wagner et al.120 investigated the influence of different
repellency in terrestrial plant leaves. Another reason why plants structural parameters of hierarchical surfaces in plants on water
profit from dry surfaces is that the growth of most pathogen and methanol repellence. In this study the repellency of 33 water
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by shrinking of the cells (see Fig. 3). Additionally, waxes are able
to self assemble into their original morphology;75 thus, it is
required that such measurements are performed immediately
after heating and cooling of the specimen and wax morphology
should be controlled by SEM.
The superhydrophobicity of combined plant surface structures
has been theoretically postulated earlier by Otten and Her-
minghaus123 and was also confirmed by Extrand,124 who inves-
tigated the interaction of capillary forces and gravity for a single
asperity to suspend a liquid drop. In this investigation a micro-
structured surface was modified with a secondary structure by
adding notches with sharp edges on it. It was stated that if an
asperity has a hierarchical structure, the secondary features can
greatly enhance the surface repellence. Marmur125 carried out
a theoretical analysis of the underlying mechanisms of super-

hydrophobicity and indicated that nature uses metastable
wetting states as the key to superhydrophobicity. He concluded
that the specific shape of the Lotus leaf protrusions (cell papilla)
lower the sensitivity of the superhydrophobic state to the

protrusion distances. In these calculations simple parabolic
shapes were used to simulate the morphology of the Lotus cell
papilla, but the influence of the secondary level structure on the
wetting behavior of the surfaces was not addressed.
Fig. 18 Superhydrophobic and self-cleaning surfaces. A flowering plant The degree of hysteresis is correlated with the wetting state of
of Lotus (Nelumbo nucifera) is shown in (a). A Lotus leaf contaminated a liquid on a surface. Wetting states of superhydrophobic
with clay (b) and removal of the adhering particles by water (c). In (d), surfaces are described by the Wenzel- and Cassie-states. In these
a spherical water droplet on a superhydrophobic leaf is shown. In figure
states, on rough surfaces, an applied water droplet in the Wenzel-
(e) the SEM micrograph of a droplet illustrates the low wettability of
state creates a wet-contact mode with a high hysteresis. In the
superhydrophobic microstructured surfaces. The SEM micrographs
show the Lotus leaf surface in different magnifications: (f) shows
Cassie-state, the droplet sits on top of the structure asperities,
randomly distributed cell papilla, (g) shows a detail of the cell papilla and and a low hysteresis (CAH) lets the liquid roll of at low incli-
in (h) the epicuticular wax tubules on the cells are shown. nation angles. The intermediate wetting state occurs, when the
droplet sinks particularly into the surface structures, but cavities
of the surfaces are still air filled. Further wetting states have
repellent plants with wax crystals in the sizes of 0.5 to 5 mm, were recently been described by Wang and Jiang126 and were called
compared. Whereas the wax crystal sizes had no significant gecko-wetting or petal-effect.127 In both wetting states the
influence on the hydrophobicity of the surfaces, increased water described surfaces have a high static contact angle but also a high
and methanol repellency was found when the aspect ratio of the adhesive force (high hysteresis). However, these phenomena
waxy cells increased. Wagner et al.120 also characterized the seem to need still more explanations before they will be accepted
number, height and average lateral distance of papillae per unit as new classifications of wetting states of superhydrophobic
area of six species with superhydrophobic surfaces. Even when surfaces. Li and Amirfazli128 combined theoretical calculations
papillae density varied between 737 and 3431 per mm2 and cell with experimental data, by analyzing the thermodynamics of
aspect ratios ranged from 0.8 to 0.5, no significant variations in surface wetting of different surface textures (pillar height, width
superhydrophobicity was found. However, higher amounts of and spacing). Different variable parameters such as the intrinsic
smaller papillae seem to be more effective in terms of water CA, drop size and vibrational energy have been included and
repellence than surfaces with larger but lower numbers of CAH for different wetting states have been calculated. These
papillae. Additionally Wagner et al.120 used AFM and confocal calculations showed that small pillar spacing is needed for
light microscopy to calculate the solid–liquid contact area during composite wetting states (Cassie-state), whereas large pillar
wetting. They found, that roughening in two hierarchical levels spacing is needed for large stable CA. Thus for achievement of
results in a reduction of the contact area of more than 95% large CA and small CAH simultaneously, a compromise between
compared with the projected area of a water droplet. Cheng pillar spacing and other geometrical parameters such as pillar
et al.,121 Burton and Bhushan,49 and Bhushan and Jung122 height and width spacing is necessary. Li and Amirfazli129
investigated the influence of the micro- and nanostructures on calculated the CAH by analyzing the thermodynamic status
the wettability of Lotus leaves. Cheng et al.121 removed the wax of a system consisting of a solid surface and a liquid drop.
structures from the leaves by melting the waxes at 150 C. After They revealed that a harmonious combination of hydrophobic
that, the static CA was reduced from 146 (untreated dry Lotus materials and adequately rough geometry of surfaces can
leaf) to 126 (dry Lotus leaf with molten wax), and hysteresis lead to stable composite wetting states. Nosonovsky and
allowed water drops to adhere, even at tilting angles of 90 . The Bhushan93,130–132 demonstrated that the effect of roughness on
melting of the wax, might prevent the chemical composition of wetting and also the mechanisms that lead to destabilization of
the surface, but led to a dramatic reduction of the cell aspect ratio a composite interface are scale dependent. They concluded that
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a multiscale roughness, or hierarchical roughness, based on of the wax crystals results in only temporary super-
tightly packed convex papillae (asperities) with ‘‘nanobumps’’ as hydrophobicity and self-cleaning behavior.
well as a hydrophobic nature of the material is optimum for In nature, the self-cleaning is not restricted to plant surfaces.
superhydrophobicity. Optimal parameters for the development Insects, especially those with large wings which cannot be
of stable, superhydrophobic rough surfaces have been calculated, cleaned by their legs, have water repellent wing surfaces and
and their requirements for optimal superhydrophobic surfaces fit exhibit self-cleaning ability.140 Here not only the removal of
well to the already realized biological water-repellent leaf particles is of interest, but also the maintenance of flight capa-
surfaces with hierarchical structures. bility, which may be lost due to a load of weight on the wings.
Self-cleaning properties of the Lotus leaf. The ability to self- Superhydrophobic hairy surfaces. Besides the super-
clean of microstructured, superhydrophobic plant surfaces has hydrophobic leaf structures described above, a second method of
first been described by Barthlott and Ehler,5 and the large shield water repellence has been developed in plants. Hairy leaf
shaped leaves of the sacred Lotus plant (Nelumbo nucifera) surfaces, such as those on the leaves of the lady’s mantle
showed this phenomenon to perfection.14,133 However, without (Alchemilla vulgaris L.),123 and the hydrophobic hairs of the
knowing the physico-chemical basics of this phenomenon, Lotus water ferns Salvinia (Fig. 13), can very efficiently repel water. On
has been a symbol of purity in Asian religions for over 2000 such surfaces, a deposited drop bends the fibers (hairs), but the
years.134 Even emerging from muddy waters it unfolds its leaves stiffness of the hairs prevents contact with the substrate, and
unblemished and untouched by pollution. The leaves of Lotus promotes a fakir state of the water droplet.123 Superhydrophobic
(Nelumbo nucifera) (Fig. 18a) are not only water-repellent but hairy surface structures are also known from animals, as for
anti-adhesive with respect to particulate contamination; thus example water beetles and the water spider. These hairy systems
contaminant particles are carried away by water droplets, may also be extremely useful for underwater systems because
resulting in a cleaned surface, as shown in Fig. 18b, c. A particle they minimize the wetted area of immersed surfaces and there-
on a structured surface is like a fakir on his bed of nails. On such fore may greatly reduce drag, as well as the rate of biofouling.
surfaces, the contact area between a particle and the underlying Therefore, underwater superhydrophobicity is of great interest in
leaf surface is considerably reduced, and as a consequence, the biomimetics.
physical adhesion forces between the particle and the surface are
reduced. If water roles over such a structured hydrophobic Air trapping surfaces. Within the water ferns of the genus
surface, contaminating particles are picked up by the water Salvinia, multicellular hairs form different structures on the
droplets, or they adhere to the surface of the droplets and are adaxial side of the floating leaves (Fig. 13). In some species (e.g.,
then removed with the droplets as they roll off the leaves S. cucullata and S. hastata) only single trichomes are found,
(Fig. 18d, e). The reason for this, is that only weak van der Waals whereas in others two hairs are apically connected to an inverted
forces bond the particle to the surface,135,136 whereas much horseshoe structure (S. oblongifolia). Even four hairs can be
stronger capillary forces between the particle and an adhering found on a more or less developed emergence. These four hairs
water droplet occur.137,138 Thus, self-cleaning occurs on super- can either be unconnected (apical open) (e.g., S. natans and S.
hydrophobic leaves on which water moves over the surface to minima), or connected, forming eggbeater or crownlike struc-
remove particles. tures (e.g., S. auriculata and S. molesta). Trichome sizes of
The leaves of the Lotus plant (Nelumbo nucifera) afford an different species range from 200 mm (S. oblongifolia) to 800 mm
impressive demonstration of self-cleaning14. This self-cleaning (S. minima), and earlier SEM examinations of Salvinia revealed
effect was found to be a result of the intrinsic hierarchical surface these plants to have very small rodlet-shaped waxes on the leaf as
structure built by randomly oriented small hydrophobic wax well as on the trichome surfaces (Fig. 14).83 The combination of
tubules on the top of convex cell papillae (Fig. 18f–h).This trichomes and waxes makes the surfaces of Salvinia super-
self-cleaning process is independent of the chemistry of the hydrophobic and has a positive effect on their buoyancy through
adhering particles, i.e., whether hydrophilic or hydrophobic, maintaining an air film underwater. All these hairy surfaces of
and results in smart protection against particle accumulation Salvinia species retain air films under water very efficiently and
and is also a protection against plant pathogens like fungi and made Salvinia a successful model for biomimetic applications for
bacteria.14,33,139 In 2000 the trademark Lotus-Effect was regis- drag reducing surfaces in technology.82 A patent protecting the
tered to label self-cleaning products based on the model of Lotus. technical conversion has been applied, and the potential tech-
The effectiveness of the self-cleaning ability decreases in the nical use of these surface structures is discussed in section 4.2.
case of fog and dew, in contrast to rain. In the case of the
superhydrophobic papillose leaves of Nelumbo nucifera and also
4. Technical applications of biomimetic surfaces
Colocasia esculenta, a certain amount of very small particles is
retained after fog treatment, whereas rain droplets have a high Bionics contains a wide spectrum of research fields such as, for
kinetic energy, and elastic deformation allows them to penetrate example, lightweight constructions, fluid dynamics, robotics,
between epidermal papillae to remove small particles from the micro- and nano-electromechanical systems (MEMS, NEMS),
grooves. In contrast to this, adhering particles can be completely and sensors. The dimensions of interest reach from the molecular
removed by fog and dew from the superhydrophobic, but non- level up to the function of complex organisms. Biological
papillose leaves of Brassica oleracea. These leaves are charac- surfaces are evolutionarily optimized interfaces and provide
terized by smooth (tabular) cells and a dense layer of large wax a large diversity of structures and functions. The first prominent
rodlets on the surface. However, on such surfaces natural erosion example of a successful transfer of biological surface structures is
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the drag reducing surface structure of shark skin and the artificial a superhydrophobic film on artificial surfaces and can, if no
surfaces (rippled foils) developed after this model. The second longer required, simply be removed by wiping. Additionally
one was the description of superhydrophobic and self-cleaning self-cleaning glasses have been installed in sensors of traffic
plant surfaces by Barthlott and Neinhuis,14 which can be inter- control units on German autobahns, and in the near future, the
preted as a stimulating moment for many scientists to focus introduction of building textiles including awnings, tents and
research on functional biological surfaces.141,142 Today, well flags is to be expected. Additionally, the list of applications
described examples are the feet of the gecko, which are perfectly for external surfaces includes lacquers for vehicles,150,151 water-
adapted for reversible attachment on surfaces, and the self- proofing of clothes152 and other textiles,153,154 glasses such as
adhesive surface structure of beetle feet.143 Another bio-inspired windshields and window glasses,155 plastics,156 roof tiles,157
attachment system is the hook and loop fastener, which plants temporary coatings158 and plastics for microfluidics. These are
use for the dispersal of their seeds by attaching the fruits to some existing and potential applications for superhydrophobic
animals. Recently the structure of shark skin has been used as surfaces. However, some existing products are only easy to clean.
a model for the development of swimming dresses with reduced Those surfaces have very low surface energies and are smooth in
surface drag when diving into water.144 Self-repairing processes the micro dimension. These surfaces are superhydrophobic, but
in plants sealing fissures serve as concept generators for the not able to remove adhering particles by the movement of water.
development of biomimetic coatings for membranes of pneu- There are only two mechanisms which led to a self-cleaning of
matic structures.145 These are only a few biomimetic examples; surfaces. First is the described superhydrophobic double struc-
comprehensive overviews are given by Benyus,146 Forbes 142 and tured surface as described for the Lotus leaf. The second is
Bar-Cohen.147 a photo-catalytic hydrophilic surface. In this, titanium dioxide is

However, even when nature has successful solutions these are present in the outermost surface layer, which disintegrated any
not necessarily optimal for technical performance. Thus it is adhering organic materials. Applications of these functional
more the understanding of the principles of nature’s solutions surfaces are, for example, roof tiles or glasses.
and transferring them into artificial systems rather than copying The use of self-cleaning surfaces is limited by the following
nature. In the following, plant surfaces and their wetting aspects. First, the micro- and nanoscale of superhydrophobic
behavior as models for biomimetic materials are discussed. surface structures require low wear for the maintenance of the
material functionality, thus materials must be very wear resistant
or have low friction.159 The second demand for self-cleaning is
4.1 Existing and potential applications of the wetting behavior
the removal of particles by moving water; thus, outside appli-
of plant surfaces
cations where surfaces are exposed to rain or can be artificially
Plant surfaces and their properties stimulated the development of sprayed with water are preferred. Self-cleaning surfaces
new functional biomimetic surfaces and materials, and many have limited success in glass materials, because surface micro-
investigations have been made to create superhydrophobic structures affect the diffraction of light and thus change the
surfaces. Superhydrophobicity is based on micro- and nano- optical properties of lenses. Thus, for integration of super-
scaled surface roughness in combination with hydrophobic hydrophobicity and transparency within the same surface, the
surface chemistry. dimensions of roughness should be lower than the wavelength of
For manufacturing surfaces with these properties, several visible light (ca. 380–760 nm).103
different technologies exist. The techniques range from lithog-
raphy24,148 which can be used to develop geometric structures in 4.1.2 Superhydrophobicity lets surfaces stay dry under water.
scale sizes from a few nanometres to several micrometres, to The advantage of staying dry under water is obviously the
replication techniques, which are simple and fast methods of reduction of drag during movement, but might also be a solution
surface structuring.32,76 Other techniques include phase separa- for the reduction of accumulation of algae, bacteria and other
tion of multi-component mixtures, self-assembly processes and sessile marine organisms on underwater surfaces. When a small
structuring by colloidal particles, and are recently reviewed by layer of air adheres to a superhydrophobic surface a reduction of
Roach et al.25 friction drag of 80% at a speed of 4 m s1 and 55% at 8 m s1 was
reached.160,161 The surfaces of a number of floating plants and
4.1.1 Technical application of superhydrophobic and self- semi-aquatic animals provide technical solutions for the design
cleaning surfaces. Inspired by the self-cleaning behavior of Lotus of underwater air-trapping surfaces, and some have recently
leaves, various synthetic superhydrophobic self-cleaning surfaces successfully transferred into technical prototypes by Solga et al.81
with a water contact angle greater than 150 have been prepared and Cerman et al.82 Solga et al.81 list five surface characteristics as
by creating appropriate surface morphology and roughness. A crucial for a stable long-lasting underwater air film: (1) hydro-
patent on technical micro- and nanostructured self-cleaning phobicity, (2) hairs with lengths of a few micrometres to several
surfaces was assigned to Barthlott.149 After the patent and the millimetres, (3) additional fine structures such as ridges, hairs
introduction of the trademark Lotus-Effect several collabora- or waxes, (4) micro- and nanocavities, and (5) elasticity of the
tions with industrial manufactures led to the first products. structures. Based on these, a textile prototype which stays dry
Existing superhydrophobic surfaces with self-cleaning properties for about four days when submerged in water has been devel-
are products with the trademark Lotus-Effect. The first oped. Cerman et al.82 performed experiments with biological
product available on the market was a facade paint named templates, different Salvinia species, and showed that the leaves
Lotusan, which is now successfully on the market since retain air films underwater for up to 17 days. A patent for air
1999. Sprays for temporary covering of surfaces create retraining surfaces has been submitted outlining different fields
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of application, like textiles, varnishes and coatings by Cerman surfaces and their multifunctional approaches has been intro-
et al.162 However, Cerman et al. 82 discuss that it is obvious that duced here to stimulate scientists of different research areas
even hairy superhydrophobic surfaces alone cannot stay to analyze structures and architectures of biomaterials and to
permanently dry under water and suggest that the solution will scrutinize their specific functions. The article provides an intro-
lie in a combination of microbubble technology (a technique, in duction to the origin and description of plant surface structures
which the air layer is permanently refilled) and optimized air and it may help to break barriers between the different fields of
retaining superhydrophobic surfaces. research in, e.g., biology and materials science. More interdisci-
Whether underwater superhydrophobic surfaces are a solution plinary research and communication might stimulate the work,
against marine fouling has recently been discussed in a review by increase our knowledge and might also lead to new solutions for
Genzler and Efimenko.163 In this, superhydrophobicity and its various technical applications.
implications for marine fouling are presented, and potential
designs of effective coatings are considered. Various chemical
approaches and surface topographies have been shown to play Acknowledgements
a role in defense against adhesion and growth of marine organ-
The authors are grateful for financial support of their work by
isms.163 Several studies showed that topographically corrugated

the Deutsche Bundesstiftung Umwelt (DBU), the Bundesminis-
surfaces reduced biofouling, i.e., settlement and attachment of,
terium für Bildung, Forschung und Technologie (BMBF), the
e.g., bacteria and algae. Genzler and Efimenko163 conclude that
German Science Foundation (Deutsche Forschungsgemein-
the coatings comprising roughness on multiple length scales
schaft) (Project ‘‘Biomimetic surfaces’’), the Akademie der
may represent a new and promising platform for fabricating

Wissenschaften Mainz. The first author thanks the Maria von
efficient foul-release marine coatings, but confirm also that still
Linden Scholarship Program of the University of Bonn for
some work needs to be done to fully understand the phenomenon
financial support of a sabbatical year at the Nanoprobe Labo-
of the different mechanisms of adhesion by different marine
ratory for Bio- & Nanotechnology and Biomimetics (NLB2) of
organisms.
the Ohio State University.
4.1.3 Superhydrophobicity for energy conversion and energy
conservation. Superhydrophobic surfaces can also be used for References
energy conservation.164 Recent advances in superhydrophobic
surfaces make such applications possible. Several concepts can 1 M. Riederer and L. Schreiber, Waxes – the transport barriers of
plant cuticles, in Waxes: chemistry, molecular biology and
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of the barrier properties of plant cuticles, J. Exp. Bot., 2001, 52,
of solid surfaces. Selection of a proper superhydrophobic surface
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discovered effect of reversible superhydrophobicity provides plant cuticle, ed. M. Riederer and C. Müller, Blackwell, Oxford,
a potential for new ways of energy conversion such as the 2006, pp. 11–125.
4 P. E. Kolattukudy, Polyesters in higher plants, in Advances in
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technical surfaces with a biomimetic approach, in which the waxes and vascular plant systematics: Integrating
ideas and concepts from nature are implemented in a field of micromorphological and chemical data, in Deep morphology:
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REVIEW www.rsc.org/softmatter | Soft Matter

Diversity of structure, morphology and wetting of plant surfaces

2001 PhD at the University of Since 1985 Chair of Systematic

plant12 and plant surface waxes and insect behavior13 can be

1.2 Importance of studies—wettability of surfaces and

Based on the large variations of surface chemistry and structures,

research deals with functional micro- and nanostructures and the

Fig. 6 Schematic of the structural division of a single cell surface.

Fig. 4 (a) Schematic of the basic outlines of epidermal cells. In (I)

Fig. 7 Schematic drawings of cross sections through epidermis cells. In

into dead and living ones. Here unicellular or simple-trichomes

layers of hairs might also decrease or increase the loss of water

of plant hairs are given by Wagner et al.,54 and more recently

Fig. 9 Schematic of cross sections through plant epidermis cells show

Epicuticular waxes are the most common type of cellular struc-

sizes from 0.5 to 100 micrometres, whereas 2-dimensional wax

main morphological wax types, including a background epicu-

(Fig. 12f). The cells are downward trending hair-papilla, with

2.2.3 Multi-cellular surface structures: glands and hairs.

In contrast, leaves with waxy trichomes were extremely water-

3. Surfaces and wetting

Wetting is the fundamental process of liquid interaction at solid–

cleaning procedures. However, there are many situations where it

during heavy showers, and also movement in water costs extra

On rough surfaces where an applied water droplet cannot

liquids on a surface, and is defined as the difference of the

the drop, the CA decreases to a receding value before the contact

modifications induce variations in surface wetting, ranging from

but only a few publications present a general overview of a larger

Wetting of plant surfaces: species, structures and contact angles (CA)

Hydrophobic (90 # CA < 150 ) Hydrophilic (10 # CA # 90 )

Species CA/ Surface structure Species CA/ Surface structure

Superhydrophobic (CA $ 150 ) Superhydrophilic (CA < 10 )

Species CA/ Surface structure Species CA/ Surface structure

microorganisms, including bacteria and fungi, is limited by water

3.3.3 Superhydrophobic plant surfaces and the Lotus leaf.

their hydrophobic surface components in connection with

a theoretical analysis of the underlying mechanisms of super-

lower the sensitivity of the superhydrophobic state to the

Bar-Cohen.147 a photo-catalytic hydrophilic surface. In this, titanium dioxide is

isms.163 Several studies showed that topographically corrugated

may represent a new and promising platform for fabricating

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