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Brochosomal coats turn leafhopper
(Insecta, Hemiptera, Cicadellidae)
integument to superhydrophobic state
rspb.royalsocietypublishing.org
Roman Rakitov1 and Stanislav N. Gorb2
1
Borissiak Paleontological Institute, Russian Academy of Sciences, Profsoyuznaya Street 123,
Moscow 117647, Russia
2
Functional Morphology and Biomechanics, Zoological Institute, University of Kiel, Kiel 24118, Germany
Research
Cite this article: Rakitov R, Gorb SN. 2013
Brochosomal coats turn leafhopper (Insecta,
Hemiptera, Cicadellidae) integument to
superhydrophobic state. Proc R Soc B 280:
20122391.
http://dx.doi.org/10.1098/rspb.2012.2391
Received: 9 October 2012
Accepted: 21 November 2012
Leafhoppers (Insecta, Hemiptera, Cicadellidae) actively coat their integuments
with brochosomes, hollow proteinaceous spheres of usually 200–700 nm in
diameter, with honeycombed walls. The coats have been previously suggested
to act as a water-repellent and anti-adhesive protective barrier against the
insect’s own exudates. We estimated their wettability through contact angle
(CA) measurements of water, diiodomethane, ethylene glycol and ethanol
on detached wings of the leafhoppers Alnetoidia alneti, Athysanus argentarius
and Cicadella viridis. Intact brochosome-coated integuments were repellent to
all test liquids, except ethanol, and exhibited superhydrophobicity, with the
average water CAs of 165–1728, and the apparent surface free energy (SFE)
estimates not exceeding 0.74 mN m21. By contrast, the integuments from
which brochosomes were removed with a peeling technique using fluid
polyvinylsiloxane displayed water CAs of only 103–1298 and SFEs above
20 mN m21. Observations of water-sprayed wings in a cryo-scanning electron
microscope confirmed that brochosomal coats prevented water from contacting the integument. Their superhydrophobic properties appear to result
from fractal roughness, which dramatically reduces the area of contact with
high-surface-tension liquids, including, presumably, leafhopper exudates.
Subject Areas:
biomaterials
Keywords:
brochosome, surface, insect,
superhydrophobicity, wettability,
contact mechanics
Author for correspondence:
Roman Rakitov
e-mail: [email protected]
Electronic supplementary material is available
at http://dx.doi.org/10.1098/rspb.2012.2391 or
via http://rspb.royalsocietypublishing.org.
1. Introduction
Surface textures, formed by integuments or their lipid secretions, waxes, have been
previously reported to be responsible for reduction of wettability in insects and
plants [1–6]. Here, we report a similar function for micro-sized proteinaceous
powder actively applied onto the body by representatives of the insect family
Cicadellidae.
Members of the highly diverse family Cicadellidae, or leafhoppers, are unique in
having their integuments coated with intricately structured particles known as
brochosomes ([7–10], for review see Rakitov [11]). In most leafhopper species,
brochosomes are spherical honeycombs, 200–700 nm in diameter, with pentaand hexagonal wall compartments open into the hollow core (figure 1a–e).
Brochosomes are composed of proteins, possibly with additional components,
and are produced in vast numbers inside specialized cells of the Malpighian tubules
(insect primary excretory organs, associated with the digestive tract, in some insects
additionally performing synthetic functions), where they undergo gradual
maturation within Golgi-derived vesicles [12–15]. Soon after moult, leafhopper
adults and, in some lineages, also immatures release colloidal suspension of brochosomes through the hindgut and apply it with their legs onto the new integument.
Once the liquid has dried out, brochosomes are further spread during bouts of
grooming behaviour, in which leafhoppers rapidly brush their integuments with
the legs bearing comb-like rows of specialized setae; as a result, the entire
integument becomes coated with a thin pruinose layer of brochosomes [11,16–21].
Several authors noticed that the integuments of leafhoppers are waterrepellent and argued that brochosomal coats can protect these predominantly
small and delicate sap-sucking insects from getting trapped into water and
their own liquid exudates [11,16 –18,21]. However, the wettability of leafhopper
& 2012 The Author(s) Published by the Royal Society. All rights reserved.
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(a)
(b)
(c)
2
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(f)
Proc R Soc B 280: 20122391
(d )
(e)
(g)
Figure 1. Structure of brochosomes. (a,b) Model of a typical brochosome, based on present results and published ultrastructural data [12,13], a three-dimensional
reconstruction by O. Karengina, showing a general view (a) and cross-section (b). (c) Brochosome on the surface of eye of Athysanus argentarius, note that the wall
compartment in the centre allows seeing through the entire hollow particle. (d ) Brochosomes of Alnetoidia alneti accidentally trapped between two layers of
polyvinylsiloxane and torn in halves when one layer was peeled off; note the holes connecting the central core with the outside. (e) Brochosomes of A. argentarius;
the touching particles are in fact connected. ( f ) Brochosomal coat on the intact hindwing of A. alneti. (g) Same, brochosomes interconnected in branching chains.
Scale bars: 50 nm (a,b), 100 nm (c–e) and 1 mm ( f,g).
integuments has not yet been subject to a quantitative
study, and the alleged role of brochosomes has not yet been
experimentally demonstrated. The goal of this study was,
therefore, to experimentally characterize the wettability
properties of leafhopper integuments coated and not coated
with brochosomes.
mesic grasslands; forewing length 5.5–6.7 mm; (iii) Cicadella
viridis (L.) (the subfamily Cicadellinae, feed on xylem sap) occurs
on wetlands and mesic grasslands; forewing length 5.2–6.6 mm.
Prior to experiments, leafhoppers were kept in the laboratory
in 30 30 30 cm meshed cages (LiveMonarch, USA) on
cuttings of host plants standing in water.
2. Material and methods
(b) Wing preparations
(a) Insects
Adults of three leafhopper species representing different
subfamilies, diets and habitats were collected in Kiel and
Kronshagen, the state of Schleswig-Holstein, Northern Germany:
(i) Alnetoidia alneti (Dahlbom; the subfamily Typhlocybinae, feed
on mesophyll cell contents); occurs on tree leaves; forewing
length 3.1– 3.5 mm. Specimens were collected from Acer
campestris L.; (ii) Athysanus argentarius Metcalf (the subfamily
Deltocephalinae, feed on phloem sap); occurs in dry and
Because measuring static contact angles (CAs) of liquid droplets
requires that the studied surface is flat, we focused our experiments on wings. Wings of leafhoppers anaesthetized with
carbon dioxide were carefully detached at the bases and glued
flat onto ca 6 10 mm rectangular chunks of glass microscope
slides with a thin layer of commercial Rimmel 60-s nail polish
(Coty Inc., UK). For convenience, such individual wing
preparations were arranged into linear series on microscope
slides coated with double-sided sticky tape (see electronic
supplementary material, figure S1).
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To remove brochosomes from the integument, we developed a
peeling-off technique using polyvinylsiloxane (PVS) elastomer.
This silicone-based material has been used for preparing
impressions of micro-sculptured surfaces [22,23]. We used a
Coltène President light body kit, art. no. 4667, from Coltène/
Whaledent Inc. (USA), which includes two components, the base
and the catalyst, combined in equal volumes to create a mixture
polymerizing within 4–5 min. The wings glued onto the glass
were covered with this mixture, which readily wetted the brochosomal coats. Once polymerized, the overlay of PVS was carefully
peeled off together with trapped brochosomes to expose the
bare wing surface. Scanning electron microscopy (SEM) study confirmed that this method removed brochosomes nearly completely,
while at the same time preserving microsculpture and other fine
structures of the integument (see §3).
(d) Freshly moulted (naturally bare) specimens
Adult leafhoppers apply brochosomes onto their bodies before they
start feeding, typically within the first 3 h after the moult [19]. In the
interim, the new integument is naturally free of brochosomes.
Therefore, to prove that our technique for removal of brochosomes
using PVS did not affect other properties of the integument, we
examined wings of four freshly moulted A. alneti adults. On these
specimens, only CAs of water were measured.
(e) Measuring contact angles and estimation of
apparent surface free energy
Surface wettability is commonly characterized by measuring CAs
with standard well-characterized liquids and calculating from
these measurements the surface free energy (SFE), an integral
characteristic that takes into account both chemistry and geometry of the surface [24]. To emphasize that the CAs of liquid
droplets are observed on the rough instead of ideally flat surface,
these are referred to as the apparent CAs and the corresponding
energies as the apparent SFEs [25].
To examine wettability of brochosomal coats and bare integuments, we measured apparent static CAs of water, ethylene
glycol, diiodomethane and ethanol. On artificially bared and
naturally bare wings of A. alneti, measuring CAs of ethylene
glycol and diiodomethane were not practical because, in this
small species, keeping the droplets from spreading beyond the
wing area proved not possible. Ethanol droplets spread outside
the wing area on all tested surfaces; thus estimating their CAs
proved also impossible.
We used an OCAH 200 high-speed CA-measuring system
(DataPhysics Instruments GmbH, Filderstadt, Germany) fitted
with silanized glass capillaries (diameter of the tip ¼ 0.15 mm).
Static CAs were measured using the ‘needle in’ (in the case of
unwettable surfaces; see electronic supplementary material,
figure S2) or ‘sessile drop’ (wettable surfaces) methods with
circle- or ellipse-fitting. The drop volume was 1 ml. The contact
between the liquid and insect surface was documented by
(f ) Scanning electron microscopy
For ultrastructural observations, we used a Hitachi S-4800
cryo-scanning electron microscope (cryo-SEM; Hitachi HighTechnologies Corp., Tokyo, Japan) equipped with a Gatan
ALTO 2500 cryo-preparation system (Gatan Inc., Abingdon, UK).
To examine the structure of brochosomes, brochosomal coats
and bared wings, glass chunks with wings prepared for CA
measurements were glued onto SEM metal stubs with a
double-sided carbon tape, sputter-coated with gold – palladium
(3– 6 nm), and examined in the microscope’s standard mode at
accelerating voltages of 3 – 5 kV.
Previous cryo-SEM studies demonstrated that interactions of
hydrophilic and hydrophobic surfaces with water droplets can
be visualized at high resolution upon freezing of the sample
[27]. To obtain close-up views of brochosomal coats interacting
with water droplets, intact leafhopper wings were glued onto a
metal holder using Tissue-Tek OCT Compound (Sakura Finetek
Europe B. V., Zoeterwoude, the Netherlands), the holder was
attached to the SEM’s insertion rod, finely sprayed with distilled
water from a 30 cm distance from a mist bottle, immediately
dipped into liquid nitrogen (21968C), and inserted into the
SEM’s slush chamber. Then, the sample was transferred into
the cryo-preparation chamber, sputter-coated with 6 nm of
gold – palladium, and examined in the SEM in the frozen state
at 5 kV and 21208C. Alternatively, the holder with insect specimens was cooled down on dry ice, then taken off the ice (which
prompted condensation of atmospheric water vapour on the surface), immediately dipped into liquid nitrogen, and then
processed as above.
3. Results
(a) Morphology of brochosomes and brochosomal coats
The brochosomes of all three species were highly similar
in both structure and size. The diameter of the particles
was 0.43 + 0.044 mm for A. alneti, 0.50 + 0.084 mm
for A. argentarius and 0.49 + 0.061 mm for C. viridis
(mean + s.d. of mean); the brochosomes of A. alneti were
significantly smaller than those of either of the other two
species ( p , 0.00001), while the difference between the
latter was not significant ( p ¼ 0.30). Most particles appeared
hollow, with the air-filled core visible through perforated
bottoms of the wall compartments (figure 1c,e). The internal
structure was visible on several particles inadvertently torn
open during removal of PVS layer (figure 1d).
The brochosomal coats were similarly uniform and dense
in all the wings studied (figures 1f and 2a–c). Brochosomes
3
Proc R Soc B 280: 20122391
(c) Removal of brochosomes
taking still images or video. A clean glass plate was used as a
reference surface. The air temperature during the experiments
was 24.8 + 2.08C, and the relative humidity was 50.4 + 7.1%
(mean + s.d.).
For each individual leafhopper, CAs were measured on one
dorsal forewing, one ventral forewing and one hindwing. On each
wing, only one droplet was tested before and one droplet, of the
same liquid, after removal of brochosomes. The number of examined
wings for each combination of wing type, liquid and treatment
(intact or bared) varied from 5 to 15 (mean, 9.4); for exact numbers,
see electronic supplementary material, tables S1–S3.
The apparent SFE and its components were calculated
from the CAs of water, ethylene glycol and diiodomethane
using the universal Owens – Wendt – Kaelble method [26] as
implemented in SCA20 software (DataPhysics Instruments). For
additional theory and comparison of alternative methods, see
Zenkiewicz [24].
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Resting leafhoppers keep their wings folded over the
abdomen. The dorsal forewing side is exposed and, therefore,
is most likely to have protective properties but at the same
time is most prone to surface damage, whereas the ventral forewing side and the hindwings are concealed, except during flight.
To account for potential variation in wettability between different body parts, in each of the studied species, we examined
three surfaces: the dorsal and ventral sides of the forewing,
referred to below as the dorsal and ventral forewing, respectively, and the dorsal side of the hindwing, referred to as
the hindwing.
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(c)
(d )
(e)
(f)
(g)
(h)
(i)
( j)
(k)
(l)
Figure 2. Integuments of leafhopper species: Alnetoidia alneti (a – f ), Athysanus argentarius (g – i) and Cicadella viridis ( j – l). (a – c) Intact integuments; (d –l)
bared integuments; (a,d,g,j) dorsal forewings; (b,e,h,k) ventral forewings; (c,f,i,l) dorsal hindwings. Scale bars: 2 mm.
formed no visible bonds to the surface, but were often interconnected in chains of variable length, sometimes branching
or forming loops (figure 1g).
(b) Morphology of bare integuments
Surface peeling with PVS resulted in a complete or nearly
complete removal of brochosomes, with no more than a
few isolated particles remaining, while at the same time preserving fine details of the integument proper, including setae
and microsculpture (figure 2d–l).
The dorsal forewings of all three species displayed shallow shagreen texture at the submicron scale (figure 2d,g,j).
In A. alneti, the only additional surface features were wellspaced conical microtrichia (both height and basal diameter
between 0.5 and 0.8 mm, figure 2d; electronic supplementary
material, figure S3a) and occasional rosette-like coeloconic
sensilla. By contrast, in both C. viridis and A. argentarius,
the dorsal forewings lacked microtrichia but bore larger
structures. In C. viridis, they were covered with sparse
scattered setae, 10–30 mm in length, and numerous (ca
530 per mm2) pit-shaped coeloconic sensilla of ca 3 mm
in diameter (see electronic supplementary material, figure
S3b). On the dorsal forewings of A. argentarius, similar setae
were present along the veins.
The ventral forewings and the hindwings of all three
species lacked any submicron textures, bearing only
conical microtrichia and smoothed wrinkles (figure
2e,f,h,i,k,l). In C. viridis, the basal one-third of the hindwing
was additionally sculptured with needle- and plate-like
wax crystals (not illustrated); this area was excluded
from the wettability assay.
(c) Wettability of brochosomal coats and
bared integuments
The static CAs of water, diiodomethane and ethylene
glycol on the assayed integuments are summarized in
figure 3 and electronic supplementary material, tables S1 –S3.
For each integument type and each liquid, the values on the
intact surfaces were significantly larger ( p , 0.00001) than on
the bared surfaces. Compared with these differences, the
differences between body parts and between species, for a
given surface type, were small, although some of these
were statistically significant ( p , 0.05; electronic supplementary material, table S4). On the intact wings, the
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(b)
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(a)
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(a) 180
contact angle (°)
160
140
120
100
80
60
dm
eg
C. viridis
w
dm
eg
A. argentarius
w
dm
eg
A. alneti
contact angle (°)
(b) 140
120
100
80
60
w
dm eg
C. viridis
w
dm eg
A. argentarius
w
A. alneti
Figure 3. Contact angles of water, diiodomethane and ethylene glycol, measured on intact (a) and bared (b) leafhopper integuments. Error bars indicate standard
deviation. w, water; dm, diiodomethane; eg ethylene glycol. Note the scale difference between (a,b).
average CAs of water droplets varied between 164.9–167.88 for
A. alneti, 170.0–172.38 for A. argentarius (see electronic supplementary material, figure S2), and 166.6–169.58 for C. viridis.
The analogous measurements on the bared wings were
112.8–116.28 for A. alneti, 107.6–128.98 for A. argentarius and
103.1–114.98 for C. viridis (see electronic supplementary
material, table S1).
The CAs of ethylene glycol and diiodomethane on
brochosomal coats were 152.7–164.18 and 148.2–156.08,
respectively (figure 3a; see also electronic supplementary
material, tables S2 and S3). On the bared wings, the CAs
were much lower, and the difference between the two liquids
was more distinct (81.4– 90.38 for ethylene glycol, 64.2–73.98
for diiodomethane; figure 3b).
In contrast to the other three liquids, on both intact and
bared wings, ethanol droplets quickly spread across and
beyond the wing area, which was interpreted as full wetting.
Estimates of the apparent SFE for the examined surfaces
ranged between 0.09 and 0.74 mN m21 for the intact brochosomal coats (figure 4a) and between 20.0 and 34.1 mN m21
for the bared wings (figure 4b). In both cases, the dispersion
surface energy was the dominant component.
During measuring of CAs, we noticed small amounts of
brochosomes apparently getting stuck to the surface of
water droplets. The specimen stage allowed us to bring the
droplet in contact with the same integument area multiple
times by moving the specimen up and down. Such repeated
contacts resulted in the surface becoming increasingly wettable, apparently due to a progressive wear of the brochosomal
coat (see electronic supplementary material, movie S1).
(d) Wettability of naturally bare integuments
The static CAs of water droplets on the naturally bare hindwings (n ¼ 4) and dorsal forewings (n ¼ 3) of freshly
moulted A. alneti, 119.9 + 7.568 and 124.9 + 7.978, respectively, were larger than those on the artificially bared wings of
that species: 113.53 + 7.978 and 112.8 + 8.608, respectively
(mean + s.d.; electronic supplementary material, table S1).
The differences proved to be significant in a two-way
ANOVA with ‘condition’ (intact, bared or naturally bare) and
‘wing type’ (dorsal forewing, hindwing) as the parameters
( p , 0.00001).
(e) Interactions between microscopic water
droplets and brochosomal coats, visualized
in cryo-SEM
We observed multiple frozen droplets of water, between
20 and 200 mm in size, attached to the integuments
(figure 5a –c). Most sites of attachment were cracks, sutures,
veins and other features that created discontinuity of the brochosomal coat. The observed CAs of droplets varied from
superhydrophobic (figure 5a) to hydrophobic (figure 5c).
Almost invariably, the surface of the frozen droplet carried
pieces of the brochosomal coat removed from the adjacent
integument (figure 5b – d).
4. Discussion
We have demonstrated that brochosomes form superhydrophobic coats of leafhopper integuments with water CAs
above 1648 and apparent SFEs not exceeding 0.74 mN m21.
The structure and properties of the coats were similar in
adults of three species representing different subfamilies of
Cicadellidae and different types of diet. Thus, our results
can be considered to be representative of integumental
brochosomal coats in general.
Proc R Soc B 280: 20122391
w
5
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dorsal forewing
ventral forewing
hindwing
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6
0.8
0.4
0.2
0
FWD FWV HW
C. viridis
(b)
FWD FWV HW
A. argentarius
FWD FWV HW
A. alneti
35
Proc R Soc B 280: 20122391
30
surface free
energy (mN m–1)
25
20
15
10
5
0
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surface free
energy (mN m–1)
(a)
FWD FWV HW
FWD FWV HW
C. viridis
A. argentarius
Figure 4. Estimates of apparent surface free energy for intact (a) and bared (b) leafhopper integuments, partitioned into polar (white) and dispersion (black)
components. FWD, forewings, dorsal surface; FWV, forewings, ventral surface; HW, hindwings, dorsal surface. Note the scale difference between (a,b).
(a)
(b)
(c)
(d)
Figure 5. Leafhopper integuments sprayed with water, frozen in liquid nitrogen, sputter-coated with Au – Pa, and visualized in a cryo-scanning electron microscope.
(a) Frozen droplet reveals the superhydrophobic state of the hindwing of Athysanus argentarius; the metal coat of the droplet has multiple cracks; the light powder
on the lower half of the droplet is brochosomes; the droplet is anchored to a wing vein. (b) Frozen droplet situated on top of the claval suture on the forewing of
Alnetoidia alneti; note the darker area of the integument, from which brochosomes were collected onto the surface of the droplet. (c) Frozen droplet anchored to the
claval suture next to a broken wing area; the metal coat of the droplet has multiple cracks; the light powder on the lower front side of the droplet is brochosomes
collected from the integument. (d ) Same, close-up; note chains of brochosomes. Scale bars: (a – c) 50 mm, (d ) 2 mm.
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Many thanks go to Dagmar Voigt, Elena Gorb, and Esther Appel for
advice and assistance during the study and to Olga Karengina for
creating the reconstruction shown in figure 1a,b. We also thank two
anonymous reviewers for valuable criticism. The work of the first
author in Germany was made possible by a grant from the
German Academic Exchange Service (DAAD) to R.R. and the SPP
1420 priority programme of the German Science Foundation (DFG)
‘Biomimetic Materials Research: Functionality by Hierarchical
Structuring of Materials’ ( project no. GO 995/9-1) to S.N.G.
7
Proc R Soc B 280: 20122391
insect integuments [1–3]. Nevertheless, leafhoppers attain
water CAs well above the superhydrophobic threshold of
1508 by coating their integuments with brochosomes.
Such water CAs are among the largest observed among
animals [3,32,33,53] and plants [5,31]. What sets the superhydrophobic coat of brochosomes apart from such previously
studied biological surfaces is that it is applied onto the
body actively, on demand, during specialized behaviour
[11,17,19,20] and is composed predominantly or exclusively
of protein [11,14,15].
It appears that such strong water-repellence in leafhoppers—a group of exclusively terrestrial insects—primarily
serves as protection from contamination by or getting
trapped into liquid exudates produced by leafhoppers as a
consequence of their feeding on plant sap [11,16–18,21].
The physico-chemical properties of leafhopper exudates
remain unstudied. However, those of xylem-feeding leafhoppers (such as C. viridis) are close in composition to pure
water [54,55], and those of phloem-feeding species (such as
A. argentarius) contain excess sugars and are expected to be
similar to honeydew of other phloem-sucking hemipterans,
such as aphids. Using the capillary method, Pike et al. [56]
estimated the surface tension of honeydew produced by the
aphid Pemphigus spirothecae as 50 mN m21. In this study,
two liquids with the surface tension of 48 and 50 mN m21,
non-polar diiodomethane and polar ethylene glycol, respectively, exhibited superhydrophobic CAs (greater than 1508) on
brochosomal coats, suggesting that the latter are repellent to
honeydew as well.
Previous cryo-SEM studies demonstrated that frozen
water droplets retain a nearly spherical shape on strongly
hydrophobic surfaces [27]. Therefore, our cryo-SEM observations (figure 5a–d) confirmed the superhydrophobicity of
brochosomal coats. We assume that most droplets that did
not get anchored to local discontinuities of brochosomal
coats, such as wing cracks (figure 5c), had rolled off the
wings prior to examination. Additionally, these observations
demonstrated the loose nature of brochosomal coats, indicated by the fact that the droplets collected brochosomes off
the integument onto their surface (figure 5c,d). Such erosion
of the coat explains the decrease of the observed CA when
the water droplet was repeatedly brought in contact with
the same area of the wing (see electronic supplementary
material, movie S1). Because brochosomal coats are easily
erodible, they can additionally reduce the risk of the leafhopper being captured by arthropod predators relying in their
capture mechanisms on adhesion (adhesive pads of spiders
and some predatory insects, sticky orb webs of spiders).
Upon contact with adhesive surfaces, brochosomal coats
will be easily detached from the leafhopper integument and
will contaminate and disable the adhesive surface. Similar
easily erodible structures are known from some carnivorous
plants of the genus Nepenthes, where they are responsible
for slippery properties of the insect traps [57].
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The observed similarity between CAs of water on
naturally bare (freshly moulted) and PVS-bared wings
of A. alneti generally validates our use of PVS for
demonstrating that the superhydrophobicity of leafhopper
integuments is created by brochosomes. The slightly lower
water-repellence of artificially bared integuments probably
reflects chemical differences between freshly moulted and
older cuticles.
The estimated extremely low SFE suggests that brochosomal coats are repellent to high-surface-tension liquids, such
as water and aqueous solutions. Similarly, low SFEs below
1.0 mN m21 have been previously estimated for some
artificial superhydrophobic surfaces [25]. The dominant
dispersive component suggests that the surface of brochosomes contains a low proportion of polar molecules and that,
given the same surface tension, brochosomal coats are
more repellent to polar liquids. In our experiments, they were
most strongly repellent to water (surface tension ¼
72.1 mN m21, dispersion component ¼ 19.9 mN m21, polar
component ¼ 52.2 mN m21; [28]), less so to ethylene glycol
(surf. tension ¼ 48.0 mN m21, disp. comp. ¼ 29.0 mN m21,
pol. comp. ¼ 19.0 mN m21; [29]), and less yet to diiodomethane
(surf. tension ¼ 50.0 mN m21, disp. comp. ¼ 47.4 mN m21, pol.
comp. ¼ 2.6 mN m21; [28]) (figure 3a).
The structure of brochosomal coats suggests the same
mechanism of water-repellence as was previously found in
many biological surfaces [3–5,30 –34]: rough surface texture
allows the solid and the liquid to contact only at the tips of
asperities while being separated elsewhere by a film of
trapped air, which is known as the ‘Cassie state’ [35–37].
Superhydrophobicity and self-cleaning effect are typically
attained on the surfaces that combine roughness at both
the micro- and nanoscales [4–6,38 –40]; this principle of hierarchical roughness has increasingly been applied to the
design of artificial surfaces [34,37–44]. Similarly, in brochosomal coats, the microscale roughness formed by whole
particles and their ensembles is combined with the nanoscale
roughness created by the reticulate surface of individual
particles. In fact, the structure of brochosomal coats is
strikingly similar to that of artificial superhydrophobic
coats prepared from raspberry-like silica-based submicron
spheres [45,46], the main difference being that brochosomes have the concave and raspberry-like particles, the
convex sculpture. While technology is often inspired by
biology [34,47], in this particular case, the rapidly evolving
technology appears to have inadvertently reinvented an
organic solution.
The structure of brochosomal coats also resembles artificial
surfaces with re-entrant sculpture, unwettable by both highsurface-tension liquids and low-surface-tension liquids, such
as alcohols and alkanes, and therefore referred to as omniphobic [48,49]. However, we observed that brochosomal coats were
completely wettable with ethanol (surf. tension ¼ 22.3 mN m21
[50]). Wettability with low-surface-tension liquids has also been
observed on water-repellent plant surfaces [6].
Among related insects of the order Hemiptera, fine textures formed by close-set submicron processes on the wings
of some cicada species (Cicadoidea) produce water CAs of
up to 1468 [51] (for an unrelated potential function of these
processes, see Ivanova et al. [52]). By contrast, bare leafhopper
wings exhibit poorly developed microsculpture (figure 2d– l)
and moderately hydrophobic water CAs of 103 –1298. CAs in
that range have been recorded on other poorly sculptured
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