Structural coloration in nature

Abstract

Nature’s color has three main sources: pigments, structural colors, and bioluminescence. Structural color is a special one, which is the color produced by micro- or nano- structures, and is bright and dazzling. The most common mechanisms of structural colors are film interference, diffraction grating, scattering, and photonic crystal. The biological colors are mainly derived from film interference which includes thin-film and multi-film interference. The diffraction grating mechanism is found in, for example, seed shrimp, mollusk Haliotis Glabra, and flower of Hibiscus trionum). Scattering includes coherent and incoherent scattering. Well-known examples of coherent scattering include colors produced by brilliant iridescent butterfly wing scales and avian feather barbules such as the peacock’s tail. Examples of colors produced by photonic crystal structures include opal color in the beetle and iridescent spines in the sea mouse. Coloration changes occur through the structural changes for camouflage, predation, signal communication, and sex choice. This paper presents an overview of lessons from nature and various relevant mechanisms. Examples of bioinspired fabrication methods and applications are also presented in the paper.

Full text

Cite this: RSC Advances, 201 3, 3, 14862
Structural coloration in nature
Received 6th March 2013,
Accepted 10th May 2013
DOI: 10.1039/c3ra41096j
www.rsc.org/advances
Jiyu Sun,*
ab
Bharat Bhushan*
b
and Jin Tong
a
Nature’s color has three main sources: pigments, structural colors and bioluminescence. Structural color is a
special one, which is the color produced by micro- or nano-structures, and is bright and dazzling. The most
common mechanisms of structural colors are film interference, diffraction grating, scattering and photonic
crystals. Biological colors are mainly derived from film interference, which includes thin-film and multi-film
interference. The diffraction grating mechanism is found in, for example, seed shrimp, mollusk Haliotis
Glabra and the Hibiscus trionum flower. Scattering includes coherent and incoherent scattering. Well-
known examples of coherent scattering include colors produced by brilliant iridescent butterfly wing scales
and avian feather barbules, such as the peacock’s tail. Examples of colors produced by photonic crystal
structures include opal in beetles and iridescent spines in the sea mouse. Coloration changes occur
through structural changes for camouflage, predation, signal communication and sex choice. This paper
presents an overview of lessons from nature and various relevant mechanisms. Examples of bioinspired
fabrication methods and applications are also presented in this paper.
1. Introduction
We live in a colorful world, and always feel the colors bring
beauty and pleasure. What is color? It contains many profound
topics. Light source, object and the viewer are three parts that
make a color perceived system, and modifications of one or
more will change color perception. Color has three main
attributes: hue, saturation and brightness. Considering that
color depends on both the color of the object itself and the
perception of the observer,
1
the perception of color is
determined by both subjective attributes of a viewer’s visual
receptors and objective physical attributes of the reflected light
and orientation of the colored structure.
2
Fig. 1 illustrates the
special cases of light reflection. If a flower reflects all
wavelengths of light it is perceived as white (top panel), in
reverse it is perceived as black (second panel), and in the in
between situation (it absorbs and reflects some wavelengths) it
has a color (third panel). However, the real color also depends
a
Key Laboratory of Bionic Engineering (Ministry of Education), Jilin University,
Changchun, 130025, P. R. China. E-mail: sjy@jlu.edu.cn
b
Nanoprobe Laboratory for Bio- & Nanotechnology and Biomimetics (NLB2), The
Ohio State University, 201 W. 19th Avenue, Columbus, OH 43210-1142, USA.
E-mail: bhushan.2@osu.edu
Dr. Jiyu Sun is an Associate
Professor in the College of
Biological and Agricultural
Engineering and The Key
Laboratory for Bionic
Engineering, Jilin University,
China.
Dr. Bharat Bhushan is an Ohio
Eminent Scholar and The
Howard D. Winbigler Professor
and the Director of the
Nanoprobe Laboratory for Bio- &
Nanotechnology and Biomimetics
at the Ohio State University, USA.
He holds two M.S., a Ph.D., an
MBA, and two honorary and two
semi-honorary doctorates. He has
authored 8 scientific books, 90+
handbook chapters, 800+ scienti-
fic papers (h index–66+; ISI
Highly Cited Researcher in
Materials Science since 2007
and in Biology and Biochemistry since 2013. He has also edited
50+ books and holds 19 U.S. and foreign patents.
Bharat Bhushan
Jiyu Sun
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on whether the observers have the color-light receptors, such
as for vertebrate eyes the flower appears red, but for bee eyes
the flower appears a dull green (bottom panel).
1
Different animals can have different color perception cells,
as shown in Table 1.
2
Ones which do not have color vision may
still detect differences in brightness. Diurnal birds have more
color perception cell types than nocturnal ones. Most
mammals detect less color types than humans. Some animals
can feel the invisible colors, such as the bee can perceive ultra-
violet (UV).
1
For the objective physical attributes: (1) most
objects’ color result from the selective reflectance and
absorption of incident light; (2) the angle of light incidence
on the structures may affect the resulting color, and some
structures can change from transparent to brightly colored
simply by a change in viewing angle;
2–4
(3) as the angle of the
incident light changes, the observed color also changes.
5
Nature does not have sophisticated technologies, such as
electron beams that can etch thin layers of material, so it has
relied on ingenuity instead.
6–8
There are three main ways in
which animals produce color: through pigments, structural
colors or bioluminescence.
2
Except for animal pigments and
bioluminescence (or ‘cold light’ resulting from a chemical
reaction), another major category of color/light displayed in
animals, structural coloration, has recently received more
scientific attention.
5
The relatively bright, directional effect of
most optical reflectors in nature (including their ultraviolet
component) is termed structural color,
9
shown in Fig. 2.
Structural color is the result of selective light reflection while
pigmentary color originates from selective light absorption by
the electrons of pigments.
10
Fig. 2c–i show various examples of
structural colors in nature which appear in a number of
animals, including insects, birds, mollusks, sea mice and
fish,
11–15
and a number of plants shown in Fig. 2a and b,
16,17
which separate from the comparatively duller, diffuse effect of
chemical pigments.
18
In some cases, structures can change the
pigment colors.
5,19
As an example, peacock tail feathers are
pigmented brown, but their structure makes them appear
blue, turquoise, and green, and often they appear iridescent
(Fig. 2d).
20
Color is not only caused by the structural color and
is sometimes combined with pigment.
10
Although Hooke
20
and Newton
21
correctly explained the
structural colors of silverfish (insect) and peacock feathers,
Fig. 1 Color is a property of the light reflected by an object and the visual
system of the animal observing it as illustrated by three special cases of light
reflection. The bottom panel shows the human and bee eyes.
1
Table 1 Phylogenetic distribution of color vision. Generalizations are based on
various levels of evidence and a different number of species are sampled
2
Taxa Color vision
Mollusks
Gastropods None
Bivalves None
Cephalopods None
Arthropods
Crustaceans In most
Insects In most
Fish In most
Amphibians In some
Reptiles
Snakes, crocodilians None
Turtles, lizards In most
Birds
Nocturnal None
Diurnal In most
Mammals
Non-primates None
Primates
Prosimiae None
Simiae In most
Dr. Jin Tong is a professor in the
College of Biological and
Agricultural Engineering and
the Key Laboratory of Bionic
Engineering, Jilin University,
China, a Cheung Kong Scholar
of Cheung Kong Scholars
Program, Ministry of Education,
China and Li Ka Shing
Foundation, Hong Kong, China
in 2000. He is an adjunct pro-
fessor of Kansas State University
since 2004. A project was sup-
ported by the National Science
Fund for Distinguished Young Scholars of China in 2000. He
obtained the John Deere Industrial Prize from the International
Society for Agricultural Engineering (CIGR) in 2004. Vice-president
of the Asian Association for Agricultural Engineering from 2006 to
2007.
Jin Tong
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respectively, it was not until the introduction of the electron
microscope to biology in the 1940s that structural colors in
animals became a subject of study,
5,23
as commenced by
Anderson and Richards.
22
Structural color can also be categorized as either iridescent
or non-iridescent.
24
Most of our current knowledge regarding
the development of iridescent structures comes from work on
insects.
25
Broadly defined, surfaces of which the color changes
with the viewing angle are called iridescent colors,
26
while
non-iridescent colors remain similar in appearance regardless
of the angle of observation.
27
From the view of physical
mechanisms, both interference and diffraction can produce
iridescent colors, and some forms of scattering produce non-
iridescent structural colors because they originate from the
irregularity of the structure.
9
Flowers are different–they appear as bright colors because
they selectively reflect certain wavelengths of light, which are
perceptible to pollinating animals, and usually to humans as
well (Fig. 2a).
1,10
Blue iridescence is prevalent in fern-like
tropical understory plants of the genus Selaginella (Fig. 2b).
17
The scales on the wings of many butterflies and moths
(Lepidoptera) produce striking iridescent colors by interfer-
ence, diffraction, scattering or 3-D photonic crystals, and have
been the focus of many studies on the mechanisms and
relationship to iridescence.
13,15,24,28–47
For example, the
famous blue butterflies of the genus Morpho have wing scales
which selectively reflect a narrow bandwidth of blue light by
multilayers, allowing other wavelengths to be transmitted
through the wing (Morpho rhetenor as shown in Fig. 2e).
13
The
elytra of many beetles (Coleoptera) are famous for their
iridescent properties, including those of jewel-like scarab
beetles.
5,48–52
Fig. 2c shows the diamond weevil beetle, Entimus
imperialis, with the black elytra where numerous pits are
studded with yellow-green scales.
15
By varying photonic
structure characterizations, incident light angle, or the
refraction index contrast of the color-produced optical system
via the environmental stimuli, reversible coloration changes,
which are basically passive, are revealed in fish, insects and
birds.
53
Some beetles’ elytra colors change with the absorption
of moisture based on humidity, temperature and environ-
ment.
54–60
Fig. 2f shows the greatly enlarged composite image
of Closterocerus coffeellae (Hymenoptera insect), which illus-
trates the dramatic effect of changing the background
reflections on wing interference pattern visibility.
14
The left
side wing displays its pigmentation pattern against a light
reflecting white background, whereas the right side wing
Fig. 2 Structural colorations in nature. (a) Base of H. trionum petal, showing iridescence overlying the red pigment , shown in the inset;
16
(b) blue iridescence is
prevalent in the fern-like tropical understory plants of the genus Selaginella;
17
(c) the diamond weevil beetle, Entimus imperialis, with the black elytra where
numerous pits are studded with yellow-green scales;
15
(d) the brilliant iridescent colors of the male peacock’s tail feathers are created by structural coloration, as first
noted by Isaac Newton and Robert Hooke; (e) broad blue dorsal wing color of the blue butterfly Morpho rhetenor;
13
(f) this greatly enlarged composite image of
Closterocerus coffeellae (Hymenoptera insect) illustrates the dramatic effect of changing the background reflections on wing interference pattern visibility.
14
The left
side wing displa ys its pigmentation pattern against a light reflecting white background, whereas the right side wing displays its wing interference pattern reflection
against a light absorbing black background; (g) the polished shell of a mollusk, the nacre of Haliotis glabra has beautiful iridescent colors;
11
(h) hollow nanofiber
bristles of Aphrodita aculeata (a species of sea mouse) reflect light in yellow, red and green to warn off predators;
12
(i) siamese fighting fish (Betta splendens), the
males have more attractive colors and fins.
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displays its wing interference pattern reflection against a light
absorbing black background. In mollusks, the nacre of Haliotis
glabra has beautiful iridescent colors (Fig. 2g).
11
Cephalopoda
(squid, cuttlefish and octopi) are well known for brilliant
colorations that change dynamically across social and beha-
vioral contexts.
26
In birds, the nanostructural organization of
keratin, melanin and air in feather barbules can produce
iridescent coloration through thin-film, multi-film interfer-
ence or photonic crystals.
61–65
The brilliant iridescent colors of
the male peacock’s tail feathers are created by structural
coloration (Fig. 2d). The sea mouse, Aphrodita aculeata,is
partly covered with long, felt like threads (spines) that produce
a brilliant iridescence (Fig. 2h).
12
The generation of blue
coloration in siamese fighting fish (Betta splendens, Fig. 2i) is
predominantly structural and manifested by motile irido-
phores through a multilayered thin-film interference phenom-
enon of the non-ideal type.
66
Nevertheless, it is sometimes
difficult to distinguish between iridescent and non-iridescent
colors, since structural colors often involve multiple scales of
organization.
67
Nature learned relatively early about the way light interacts
with periodic structures due to the evolutionary selection
advantages it offers.
68
Structural colors may provide several
functions, such as conspicuousness (such as efficiency of
reflection, warning and attractant to conspecifics), camou-
flage, thermoregulatory mechanisms, and mirror/antireflec-
tion functions in photophores or eyes.
3,5
In turn, structural
colors with special functions inspire reflector designs and
commercial applications. Structural colors have been closely
connected with human life since the dawn of civilization, they
have often been used for ornaments and decoration of
accessories and furniture, for example that use of the lamina
of mother-of-pearl of ear shell or turban shell to decorate
lacquerware was brought from China in the 8th century.
67
Structural color in nature have attracted much attention
recently due to their potential for applications in technol-
ogy–none more so than those of butterflies, since this group
displays the widest diversity of structures, resultant colors and
visual effects of any living organism.
13
Structural coloration
may be especially crucial for future color and the related
industry because of the non-fading feature and environmental
friendliness.
5,10,53
One approach to optical biomimetics focuses on the use of
conventional engineering methods to make direct analogues
of the reflectors and anti-reflectors found in nature, the other
is merely mimicking what happens in nature, leading to a
thriving new area of research involving biomimetics through
cell culture.
68
There are already some bioinspired fabrications
and products available that have replicated the surface
structure of animals, such as textiles,
56
cosmetics,
69
vehicle
shells,
23
anti-counterfeiting technologies (on banknotes, credit
and debit cards and branded goods),
70–72
optical filters
35,73–75
and optical security devices.
76,77
The strategy of structural
colors may not only help us get insight into the biological
functionality of structural coloration but also may inspire the
design of novel artificial optical devices.
78
Inspired by the
humidity-dependent color change observed in the cuticle of
the Hercules beetle, a biomimetic thin-film-type humidity
sensor with nanoporous structures (3-D photonic crystals) was
designed.
60
The visible color of the fabricated humidity sensor
changed from blue-green to red as the environmental
humidity increased.
In this paper, the mechanisms of structural color and
functions are discussed. Examples of bioinspired fabrication
and applications are also introduced. Section 2 presents a
primer on various physical mechanisms of structural color
which include film interference, diffraction gratings, scatter-
ing, photonic crystals and coloration changes. Section 3
presents various examples of structural colors in nature based
on various mechanisms presented in section 2. Section 4
introduces the examples of bioinspired fabrications and
applications, which mainly focus on mimicking iridescent
effects, polarization effects and color changing.
2. Physical basis of structural colors
In general, biologists have found helpful the classification of
structural colors into the categories of thin-film and multi-film
reflections (interference), diffraction gratings, scattering and
photonic crystals.
5,9,18,26,79,80
Fig. 3 shows the schematics of
the physical mechanism of structural colors in nature, thin-
film and multi-film interference, diffraction grating, scattering
(coherent and incoherent scattering) and photonic crystals
(one-dimensional (1-D), two-dimensional (2-D) and three-
dimensional (3-D)). Sometimes the actual appearance of the
natural structural color can be made by combining different
physical mechanisms.
9
For example, in the Morph butterfly a
multi-film interference was found in the vertical direction and
diffraction grating in the horizontal direction.
8,33,35,38
The
mechanisms responsible for producing structural colors have
been summarized in several excellent
reviews.
5,9,18,24,25,52,55,63,65,79–85
We next present a primer on various mechanisms.
2.1 Film interference
Film interference in nature includes thin-film and multi-film
interference. The well-known example color caused by thin-
film interference is the iridescent soap bubble. Thin-film
interference is found in nature, where light is reflected and
interferes from the upper and lower boundaries.
5
The
reflectivity of a thin, non-absorbing layer of thickness d
1
with
refractive index n
1
, bound by two semi-infinite media with
refractive indices n
0
and n
2
, can be determined theoretically by
summation over the amplitudes of all the light beams which
leave the layer in reflection, and those beams might have
incurred multiple reflections within the layer (Fig. 3a).
86
In the soap-bubble case, the condition for constructive
interference becomes
9
2n
1
d
1
cosh
1
=(m 2 1/2) l
(1)
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where l is the wavelength giving the maximum reflectivity, m
is a positive integer, d
1
is the thin-film thickness, n
1
is the
refractive index and h
0
and h
1
are the angles of incidence and
refraction, respectively. When used with anti-reflective coat-
ings, the constructive interference thin-film equation becomes
2n
1
d
1
cos h
1
= ml.
Multi-film interference is qualitatively understood in terms
of a pair of thin layers piling periodically.
9
The regular multi-
film stack is also called a Bragg mirror, and the infinite version
of this structure is a 1-D photonic crystal.
80
Multi-film
interference is common in animals.
5
The multi-film structures
encountered in the living world can be quite complex: in the
beetle Chrysina resplendens, for instance, no less than 120
layers are stacked to produce a vivid metallic gold color.
80
Consider two layers designated as A and B with thicknesses d
1a
and d
1b
, and refractive indices n
1a
and n
b
, respectively, as
shown in Fig. 3b.
9
For n
1a
. n
1b
, constructive interference
occurs when,
9
2(n
1a
d
1a
cosh
1a
+ n
1b
d
1b
cosh
1b
)=ml (2)
or
ml =2n
j
d
j
(3)
where j stands for the respective layer.
If the optical path difference is equal to (m9 + 1/2) l when
constructive interference occurs, then eqn (3) becomes,
(m9 + 1/2) l =2n
j
d
j
(4)
where m9 is a positive number.
At a normal incidence of light and m9 = 0, eqn (4) simplifies
to l/4 = n
j
d
j
, hence the quarter-wave stack is ideal for
multilayer arrangements.
86
That is, when the layer thicknesses
are approximately greater than l/4 of the measurement beam
and the films are transparent, it is called an ideal multilayer.
87
If the spacing of these layers approaches one-quarter of the
wavelength of the visible light (y380–750 nm), one or more
colors will be produced by constructive interference.
52
If the
dimensions of the system deviate from the quarter-wave
condition (i.e. nd is not equal for all layers), then the reflector
is known as a non-ideal multilayer
63
in a theoretical sense
(may be ‘ideal’ for some natural situations).
5
So, compared to
thin-film interference, colors produced by the multi-film
interference are brighter, more colorful and saturated, as well
as the forms have more variety. For example, green beetle
Calloodes grayanus shows a strong reflection of the green
wavelength because of the uniform periodic multi-film
interference.
88
2.2 Diffraction gratings
In 1818, another type of physical structure with reflective
properties was developed in a physics laboratory–diffraction
grating, and until 1995, it was not known to exist in nature.
79
It
is a surface which is periodically corrugated in some direction
along the surface.
80
Diffraction gratings became major players
in the scientific and commercial worlds of optics, and have
become refined and varied to produce an array of optical
effects.
23
They are responsible for the metallic-like colored
holograms found on credit cards or foil-type wrapping paper,
and they are now appearing on stamps and banknotes since
they can be difficult to forge.
79
The basic physics of the grating is just the same as that
involved in a periodic multilayer stack, except for the
orientation of the periodicity.
80
In Fig. 3c,
18
two parallel rays,
labeled 1 and 2, are incident on the grating with one groove
spacing, d, and are in phase with each other at wavefront A.
Fig. 3 Structural colors arise via (a) thin-film interference, many of the light beams that contribute to the overall reflectivity of the thin-film have incurred multiple
reflections in the layer, which det ermine their final amplitude when they leave the layer, based on Fresnel’s reflection and transmission coefficients;
72
(b) multi-film
interference;
9
(c) diffraction grating dividing white light into spectra, rays scattered from different points on the grating interfere either constructively or
destructively;
18
(d and e) scattering (coherent and incoherent scattering)
93
and (f–h) photonic crystals (one-, two- and three dimensional photonic crystals (1-D, 2-D,
3-D)).
94
The colors correspond to materials with different refractive indices.
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Upon diffraction, the principle of constructive interference
implies that these rays are in phase at diffracted wavefront B if
the difference in their path lengths, dsinh
0
+ dsinh
3
,isan
integral number of wavelengths; this in turn leads to the
grating equation,
89
ml = d (sinh
0
+ sinh
3
) (5)
where h
0
and h
3
are angles of incidence and diffraction,
respectively, and which govern the angular locations of the
principal intensity maxima when light of wavelength, l,is
diffracted from a grating of groove spacing d. Here m is the
diffraction order (or spectral order), which is an integer. d =
175 nm is a critical period for the human color vision range:
for periods smaller than this, there is a zero-order grating, with
a period too short to produce diffraction orders other than the
specular order m =0.
80
When m = 0, the grating acts as a
mirror, and the wavelengths are not separated.
89
It leads to the
law of reflection h
3
= h
0
and eqn (5) changes to,
ml =2d sinh
0
(6)
Along a particular direction on the plane of the light field is
the superposition of the coherent light emitted from each slit.
When interference occurs, due to the light emitted from each
slit in the interference phase of points that are different
between them, and thus will be partially or fully destructive
interference. However, the path difference between the light
from adjacent slits is equal to the integral multiple wave-
length, the phases will add together and constructive
reinforcement will occur. For larger values of the period,
diffraction occurs, first at large incidence angles, emitting a
violet color.
80
2.3 Scattering
Light scattering is commonly used in nature in the production of
blue coloration. The term scattering in general means the
interference of light with different wavelengths reflected from
scattering objects either in a constructive or destructive way.
90–92
The simplest classification of mechanisms for the production of
structural color uses the terms of either coherent scattering of
light (interference, reinforcement, thin-film reflection and
diffraction, Fig. 3d) or incoherent (Rayleigh, Tyndall, Mie
scattering, Fig. 3e).
63,83,93–95
In coherent scattering there is a
definite phase relationship between incoming and scattered
waves, whereas in incoherent scattering this is not the case.
Traditionally, Tyndall scattering has been used to refer to
incoherent scattering by small particles near the size of visible
wavelengths, whereas Rayleigh scattering is used to refer to
incoherent scattering by all small particles down to the size of
a molecule.
95,96
Mie scattering, which is a mathematically
correct description of light scatter, more precisely describes
small particle size scattering.
83
Iridescent colors are produced
by coherent scattering, but coherent scattering does not always
produce iridescent colors.
97
There are three main classes of
coherently scattering nanostructures: laminar, crystal-like, and
quasi-ordered; laminar and crystal-like nanostructures com-
monly produce iridescence, which is absent or less conspic-
uous in quasi-ordered nanostructures.
93
By contrast,
incoherent scattering does not yield iridescence.
94
2.4 Photonic crystals
Organismal structural colors can also be produced by photonic
crystals.
82
Photonic crystals are another important source of
structural colorations, they are structures periodic in 1-D, 2-D,
or 3-D ordered, sub-wavelength lattices that can control the
propagation of light in the manner that atomic crystals control
electrons (Fig. 3f–h).
94,98,99
The most general concept of
photonic crystals, covering all cases, is the graded-index
periodic optical structure, which can be defined as any non-
absorbing medium which is invariant under the translations
of a crystal lattice.
100
Photonic crystals may be regarded as a
special case of composite, built from two materials with
refractive indices n
1
and n
2
, characterized by a refractive index
invariant under the spatial translations of a crystalline lattice,
while a 1-D photonic crystal is merely the thin-film inter-
ference (Bragg mirrors) described earlier.
80
2.5 Coloration changes
A change in structures will result in coloration changes found
in organisms for camouflage, predation, signal communica-
tion and sex choice. For example, fish, cephalopods, birds,
beetles and butterflies go through color change based on
multi-film interference and photonic crystals.
54–60,71,80,101–114
For the underlying mechanism of multi-film interference,
the angle of refraction at different layers h
1a
and h
1b
in eqn (2)
can be obtained from Snell’s law n
1a
sinh
1a
= n
1b
sinh
1b
= n
0
sinh
0
, where h
0
is the incident angle from air, n
1a,b
are
refraction indexes and h
1a,b
are angles of refraction (the
subscripts represent the layer index). The peak reflectance
wavelength l
max
at an angle h
0
can be expressed as,
115
ml
max
~2 d
1a
ffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffi
n
2
1a
{n
2
0
sin
2
h
0
q
zd
1b
ffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffi
n
2
1b
{n
2
0
sin
2
h
0
q

(7)
When a substance is illuminated with white light, we see a
specific color if the reflected light of only a particular
wavelength range is visible to our eyes (380 nm–770 nm).
9
The different wavelengths of the electromagnetic waves result
in the different color perception of the human eye, such as
770–622 nm perceiving in red; 622–597 nm orange; 597–577
nm yellow; 577–492 nm green; 492–455 nm indigo color; and
455–350 nm purple. So the change of l will lead to the
perception of color change. From eqn (7), it is easy to elucidate
that either n, d,orh
0
is related to the optical path in the
multilayer and thus leads to shifting interference peaks at
different wavelengths l.
53,115
Fig. 4a–c illustrates the variation
of d, h and n, which results in color changes in cephalopods
(expansion and compression of extracellular space between
protein platelets), neon tetra fish (tilting protein platelet), and
beetle cuticle (changing refractive index of a porous layer by
absorbing liquid), respectively.
115
For the underlying mechanism of 3-D photonic crystals, the
color also depends on the refractive index, tilting angle and
distance between the cubic close packing (CCP) (111) planes.
The reflected wavelength l is expressed by the combining the
Bragg equation with Snell’s law,
116
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ml~2d
111
ffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffi
n
2
eff
{ sin
2
h
0
q
(8)
Here, m is a positive integer, d
111
is the distance between the
CCP (111) planes, n
eff
is the average refractive index and h
0
is
the angle of incidence. From eqn (8), the structural color can
be changed by controlling three parameters: d
111
, n
eff
and h
0
.
Actually, in 3-D photonic crystals, the easiest method for color
change to occur is by changing d
111
. Fig. 4d–f shows three
structure types of colloid-based soft materials which exhibit
tunable structural color by diffracting visible light: opal
composite (3-D close-packed) (Fig. 4d), inverse opal (Fig. 4e)
and non-close-packed colloidal crystal embedded in a soft
material, typically a hydrogel (Fig. 4f), they all can change color
by adjusting the value of d
111
.
115
The elastomer in the opal
composite plays an important role in the reversible tuning of
the colloidal crystal lattice as shown in Fig. 4d. Using opal as a
template, an inverse opal structure can be produced, which
exhibits porous morphology and tunable color as shown in
Fig. 4e. In Fig. 4f, which is a colloidal crystal embedded in a
poly(N-isopropylacrylamide) hydrogel, its lattice spacing is
tuned by the temperature-induced phase transition in the
hydrogel.
3. Lessons from nature
The array of structural colors found in animals and plants
today results from millions of years of evolution.
5
Structural
color is a significant feature of a number of animals and
plants.
11–17
The micro- or nano- structures are responsible for
the color in form, such as hair, fur, scales, filaments, skin,
barbules, shells and exoskeletons.
We next present various lessons from nature based on
various physical mechanisms.
3.1 Film interference
Film interferences are most common in nature (Table 2). The
color caused by the thin-film interference exits in the
transparent wings of Closterocerus coffeellae (Hymenoptera
insects) (Fig. 2f).
14
The wings of some houseflies act as a
single thin-film and appear to have different colors as a result
of differences in the thickness of the layer that provides a
change in the color observed from unidirectional polychro-
Fig. 4 Color ation chang es mechanisms in living creatures: multi-film interference (a–c): (a) expansion and compression of extracellular space between protein
platelets in cephalopods, (b) tilting protein platelet in the iridophore of neon tetra fish, (c) changing refractive index of a porous layer by absorbing liquid onto the
beetle shell; photonic crystals structures by diffracting visible light (d–f): (d) opal composite made of 3D close-packed colloidal spheres bonded by an elastomer, (e)
inverse opal made of a soft-material frame structure–here opal acts as a template for the soft material, (f) non-close-packed colloidal crystal embedded in a soft
material, typically a hydrogel.
115
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matic light.
5
Some birds’ iridescence originates from thin-film
reflectors, such as satin bowerbirds,
117
rock dove
147
and blue-
black grassquit.
119
The two-color (green and purple) switching
iridescence of the neck feather of the rock dove occurs very
suddenly by only slight shifting of the viewing angle.
148
The
iridescent blue color leaf is caused by a physical effect, thin-
film interference.
120,121
The ultrastructural basis for the film in
blue leaves of neotropical ferns D. nodosa is multiple layers of
cellulose helicoidal microfibril arrangements, and in T. elegans
it is the remarkably uniform thickness and arrangement of
grana in specialized chloroplasts adjacent to the adaxial wall
of the adaxial epidermis.
121
The swimming crab (Ovalipes molleri, decapoda), the
amphipod crustacean (Danaella sp.) and fish skin all bear
multi-film interferences in their cuticles in different forms
(Fig. 5a–c).
79
A broadband reflector is any multilayer structure
that reflects most or all wavelengths of light simultaneously,
hence a broadband of the visible spectrum.
52
A broadband
wavelength-independent reflectance, appearing pure gold or
silver (mirror-like) to the human eye, can be achieved in a
multilayer stack in at least three ways: (1) regular multilayer
stacks (each tuned to a specific wavelength, Fig. 5d I), (2)
‘chirped’ stack (a stack with systematically changing optical
thicknesses, Fig. 5d II), and (3) ‘chaotic stack’ (a disordered
arrangement of layer thicknesses about a mean value, Fig. 5d
III).
5,88
Chirped broadband reflectors have been mostly
reported in beetles.
88
Multi-film interferences of beetles can be located at different
layers within the integument: epicuticle, exocuticle and
endocuticle (Fig. 6).
52
For the epicuticular reflector, notable
examples are the highly iridescent green Chrysochroa beetles,
no less than 120 layers are stacked to produce a vivid metallic
broadband gold color.
126
Multi-film interferences also occurs
in tiger beetles (Cicindelinae),
103
the iridescent chrysomelid
beetle, Plateumaris sericea
50,125
and jewel beetle.
67
In the case of the jewel beetle and leaf beetle where the
epicuticle region consists of a high reflector due to a
multilayer, the outer epicuticle mainly contributes to the
reflection, which is essentially insensitive to the polarization
(Fig. 7a).
67
For the exocuticular reflector, it occurs in many
scarabs beetles that layers of chitin fibrils laminated with
protein, structured as parallel bars and stacked with a rotation
of each layer, resulting in a helical structure that only reflects
circular waves of inverse chirality, as in flower beetle Chrysina
resplendens, unpolarized illuminating light is reflected circu-
larly polarized.
122,123,131
For the endocuticular reflector, it
occurs in the gold beetle Anoplognathus parvulus.
124
Moreover,
the scale of male beetle Hoplia coerulea can appear blue-violet
iridescence which is caused by the presence of an interesting
photonic structure inside the scales whith stacking of chitin
plates supporting arrays of parallel rods.
58,130
The distance
between two consecutive rods (or voids) is too small (175 nm)
to produce diffraction for visible light, so that the layer
appears as an effective medium of reduced refractive index,
mixing air and chitin, as a result this provides the refractive
index contrast to turn the structure into a color-selective Bragg
mirror.
During development, insect cuticles are secreted in phases,
which easily gives rise to nanostructured multilayers that
create brilliant body colors.
149
Butterflies and moths are a
Table 2 Some film interference in nature
Variety Species Color References
Thin-film interferences Bird Satin bowerbirds Iridescent color 117
Rock dove Green and purple 118
Blue-back grassquit UV-reflecting iridescent color 119
Marine animal Fish Blue, turquoise, green,
copper, gold, or platinum
66
Plant Leaves Iridescent blue 120,121
Insect Butterflies Iridescent color 31
Months Iridescent color 31
Hymenoptera Vivid color interference 14
Diptera Vivid color interference 14
Multi-film interferences Insect Beetles Iridescent green; blue-violet
iridescence; gold; jewel;
50,58,67,103,108,122–131
Dragonflies Blue 95
Bees Blue 132
Damselfly Green 70
Moths Iridescent color 29,133,134
Butterflies Iridescent color; reflect yellow
and blue light to combine green
31,82,135–137
Plant Fruits Iridescent blue color with green
and purple/red speckles.
138
Marine animal Fish Silver; red; iridescent color 139–142
Mollusk Iridescent color 143,144
Sapphirinid copepods Iridescent color 145
Decapods Iridescent color 146
Clam, shrimps Iridescent color 5
Tanaidacea Iridescent color 5
Squid Iridescent color 85,147
Bird Male Lawes’ parotia Yellow-orange, blue-green 111
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treasure chest for multi-film interference.
148
Similar multi-film
interferences were found in dragonflies,
95
blue banded
bees,
132
damselflies
70
and moths.
29,133,134
The broad-band
green wings of the lycaenid Chrysozephyrus aurorinus butterfly
have scales where the lumen consists of a stack of chitin layers
and for the so-called Morpho, each ridge is elaborated into
lamellae, which together act as a multi-film reflector.
82,136,137
All the general mechanisms used by animals to produce
structural colors are also used by plants,
1
such as marble berry
Pollia condensata fruits (Fig. 7b),
138
where the striking
pixelated or pointillist appearance color is caused by Bragg
reflection of helicoidally stacked cellulose microfibrils that
form multilayers in the cell walls of the epicarp.
138
In plants,
multilayers are found predominantly in shade-plant leaves,
suggesting a role either in photoprotection or in optimizing
capture of photosynthetically active light.
1
The multi-film interferences widely exist in fish,
67,113,139–144
mollusks,
143,144
sapphrinid copepods,
145
swimming crab
Ovalipes decapods,
146
Limnadia clam shrimps (Spinicaudata)
and Tanais tennicornis (Tanaidacea)
5
and squid.
85,147
Fig. 7c
shows iridescent cells under a blue stripe in neon tetra fish,
each cell contains two rows of parallel platelets of guanine
crystals which move like a Venetian blind. A few stacks of
periodically arranged light-reflecting platelets result in multi-
layer optical interference phenomena.
67,113
The breast-plate plumage of male Lawes’ parotia birds
(Parotia lawesii) produces dramatic color changes during its
courtship displays thereby achieving much larger and more
abrupt color changes than is possible with ordinary iridescent
plumage (Fig. 8a–b).
111
The combination of thin-film inter-
ference and multi-film interference within a single feather is
unique to the parotia breast-plate plumage. Melanin multi-
layers within the barbules give a yellow-orange reflection,
while the cortex acts as an enveloping thin-layer reflector
producing bluish side beams. The unique property of the
parotia barbules is their boomerang-like cross section (Fig. 8c).
This allows each barbule to work as three colored mirrors
(Fig. 8d): a yellow-orange reflector in the plane of the feather,
and two symmetrically positioned bluish reflectors at respec-
tive angles of about 30u. This makes it possible for the parotia
to achieve much larger and more abrupt color changes than
under static conditions, when they keep moving during their
courtship displays, which can increase its competitiveness.
Currently the best studied structural color is the butterfly
scale, with exemplary optics in nature. Fig. 9 presents a
diagrammatic view of a fragment of a more or less
unspecialized scale, together with some of the more common
variants on this form.
31
As shown in Fig. 9a, the ridges can be
taller so that their lamellae form a stack of thin-films that
collectively form a multi-film interference mirror or ‘‘multi-
film reflector’’. This mechanism is responsible for such
structural colors as the brilliant blues of the genus Morpho
and others, for the ultraviolet reflection in certain male Pierid
butterflies, and for the greens in some Papilionid butterflies
(Euploea desfresnes, Colias eurytheme male). In Fig. 9b, the
scale lumen forms a 2-D photonic crystal that may channel or
direct incoming light to, for example, reflective structures
within the interior of the scale (that acting as a long-pass
optical filter, together with variable multi-film reflection
determines the blue-green wing coloration of Papilionid
butterflies of the nireus group, such as Papilio bromius, P.
epiphorbas, P. nireus, P. oribazus and P. zalmoxis).
31,75
Fig. 9c
shows the reflective system on the ridges can ‘‘rock back’’ so
that it is the microribs that are serving as the multi-film
Fig. 5 Examples of multi-film interference. The transmission electron micro-
graphs (TEM) of (a) a quarter-wave stack with corrugations in the swimming
crab Ovalipes molleri. The corrugations, not considered in physics, provide
interesting variations to the reflector. The branchin g of the layers are also
interesting, introducing stability and robustness to the stack. (b) A ‘chirped’
broadband reflector, or mirror, in an amphipod crustacean (Danaella sp.). This
mirror is positioned on the antenna and is employed to redirect biolumines-
cence produced from the body. (c) A ‘chaotic’ broadband reflector in fish skin.
79
In (a) all high-index layers (dark) are equal in thickness; in (b) and (c) the high-
index layers (dark and light, respectively) vary in thickness. All layers are of the
order of 100 nm thick. (d) A schematic of three ways of achieving a broad-band
wavelength-independent reflector in a multilayer reflector (high refractive index
material is shown shaded).
87
(I) Three-quarter wave (narrow band) stacks, each
tuned to a different wavelength, such as a ‘‘red’’, ‘‘green’’ and ‘‘blue’’. (II) A
‘chirped’ stack, where layer thickness, and consequently the wavelength
reflected in phase, decreases systematically with depth in the stack. (III) A
‘chaotic’ stack, where layers of different thickness are arranged randomly within
the stack.
Fig. 6 Schematic of the (a) epicuticular reflector, (b) exocuticular reflector and
(c) endocuticular reflector in beetle elytron.
52
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interference; the lamellae may or may not still be present
(Trogonoptera brookianus). The microribs can run from ridge to
ridge, essentially obliterating the scale lumen; such scales
typically have a ‘‘satiny’’ sheen (Lamproptera curiosa), as shown
in Fig. 9d. Fig. 9e shows that the window structure can be
modified into ‘‘pores and plates’’, although not so regularly as
to qualify as a 2-D photonic crystal (Colias eurytheme male,
Colias eurytheme butterflies). As shown in Fig. 9f, the scale
lumen may be filled with laminae that act as thin-film mirrors
(Urania ripheus, Papilio sp. butterflies). In Fig. 9g, the scale
lumen may contain iridescent 3-D photonic crystals reflectors
(Thecla herodotus, Mitoura grynea, Parides sesostris, Teinopalpus
imperialis butterflies). Any of these structures may be modified
in any of several ways to produce variants to suit the
functions.
31
Moreover, the natural nanoarchitectures combine
regularity and irregularity in clever ways, giving interesting
optical effects that would not be possible with a completely
regular structure.
67
While some striking iridescence caused by special micro-
structure integrate with multi-film interference to produce
new mechanism, Vukusic et al.
135
showed light-bouncing
bowls in wing scales for color mixing in the swallowtail
butterfly (Papilio palinurus) that reflect yellow and blue light to
combine as green, as shown in Fig. 10a. Scanning electron
microscopy (SEM) images show that the scale surface
comprises a regular 2-D array of concavities, and the
transmission electron microscopy (TEM) images of these
scales in cross-section reveal the multilayering that causes
Fig. 7 Some samples of multi-film interference in nature. (a) Dorsal and ventral views of the Japanese jewel beetle (Chrysochroa fulgidissima) at various viewing
angles, and microstructures of the surface and cross-section by SEM (scanning electron microscopy) and TEM.
67
(b) Photographs of marble berry Pollia condensata
fruits, which blue color is not uniform, have a brilliant pixelated iridescent appearance with green and purple/red speckles. The diameter of each fruit is about 5 mm.
TEM of a single thick-walled cell multilayer structure and the cellulose microfibrils that constitute the thick cell wall. The red line highlights the twisting direction of the
microfibrils.
131
(c) Iridescent cells under a blue stripe in neon tetra fish (body length = 30 mm). Each cell contains two rows of parallel platelets of guanine crystals
which move like a Venetian blind. An iridophore of the neon tetra contains a few stacks of periodically arranged light-reflecting platelets, which can cause multilayer
optical interference phenomena, RP: reflecting platelet.
67,113
Fig. 8 The breast-plate plumage of male Lawes’ parotia bird (Parotia lawesii)
produces dramatic color changes from (a) yellow-orange to (b) blue-green
when viewed from fron-to-parallel-to- oblique by altering the positioning of
barbules on the feather tips. (c) A transverse section shows the ridged structure
of the top surface of the barbule with two faces enclosing an angle of about
120u. About 15 melanin layers border the left-hand slope over a span of 8 mm.
(d) Diagram of the barbule cross section, assuming an effective refractive index
of 1.56. When the multi-layer inside the barbule is tilted at an angle of 11.3u
with respect to the horizontal plane on both sides of the symmetry plane, a light
beam incident normal to the horizontal plane hits the multi-layers normally, and
thus will be reflected back along the line of incidence. Part of the incident light
is, however, reflected at the surface. The angle between the incident and
reflected beam then is 60u, because of the 30u slant of the upper surface of the
barbule segments.
111
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the iridescence as well as a modulation that leads to retro-
reflection (Fig. 10b).
135
In reflection, for normally incident
light, concavity and its inclined sides appear yellow and blue,
respectively, polarization is converted through double reflec-
tion from orthogonal sides of a concavity, which finally
combine into green (Fig. 10c). It is termed orthogonal-surface
retro-reflection.
Scales from the wing of the Madagascan sunset moth show
iridescence caused by the deep groove structure formed
between two adjacent rows of regularly arranged scales, and
together with multi-film interference produces an inter-scale
reflection mechanism; the wing color changes depending on
light polarization.
118
The similar bowls found in the swallow-
tail butterfly has been found in beetles where the elytra surface
comprises an array of hexagonal pits which cause color
mixing.
103,108,127–129
Beetle Plusiotis boucardi has an array of
‘bowl-shaped’ recesses on the elytra that are formed from a
dual-pitch helicoidal layer, and reflectivity spectra collected
from the beetle have been compared to theoretical data
produced using a multi-layer optics model for modeling chiral,
optically anisotropic media, such as cholesteric liquid crys-
tals.
127
In particular, the reflectors are shown to have the form
of small concave pits and troughs that are filled with
contouring chiral material.
108
The presence of chiral reflectors
with two different pitches satisfying Bragg reflection was cited
as responsible for color.
129
3.2 Diffraction gratings
Diffraction gratings are particularly common in invertebrates.
5
The notable sample is Morpho , this genus is perhaps one of the
most strikingly colored butterflies. Most species have two
distinct layers of different scales: larger cover scales and
smaller ground scales arranged alternately in rows.
100,114
One
layer is made of basal scales which form multi-film inter-
ferences vertically (arrays of chitin that are shaped like
Christmas trees and sprout at the scales’ outward surface)
and a diffraction grating horizontally (the parallel branches of
each ‘‘tree’’ act as another kind of diffraction grating which
may reflect up to 80% of the incident blue light); the other
layer is made of ridges of cover scales which are wider than
those of the basal scales and serve to diffract and broaden the
angle over which the blue color is visible, its function is
synergistically to produce novel visual effects.
8,35,36,38
Moreover, butterflies exhibits sexually dimorphic iridescence,
such as the butterfly Lamprolenis nitida, which is capable of
emitting two distinct patterns of iridescence in different
directions by separate components on the same scale, which
were found to originate from first order blazed diffraction
gratings formed by different scale nanostructures angled with
respect to the scale surface (Fig. 11a).
13,148
Some polychaete worms also produce iridescence through
diffraction gratings.
5
Iridescence is particularly common on
the setae or setules (hairs) of Crustacea, such as on certain first
antennal setules of male ‘seed shrimps’ (Myodocopina ostra-
cods, Crustacea).
151
Here, the grating is formed by the external
surface of juxtaposed rings with walls circular in cross section,
the width of the rings, and consequently the periodicity of the
grating, is about 700 nm in Azygocypridina lowryi (a species of
ostracod crustacean) (Fig. 11b).
79,146,151
The ostracod
Euphilomedes carcharodonta (Crustacea; Ostracoda;
Myodocopida), for example, additionally houses a diffraction
grating on the rostrum, a continuous flattened area of the
Fig. 9 Possible structural variations on a generic scale in butterflies. (a) The
ridges can become taller than usual and their lamellae stack up to produce a
series of thin-films that act as multi-film interference mirrors. (b) The window
regions may display a series of fine alveoli that form in essence a 2-D photonic
crystal with associated optical properties. (c) The ridge structure can ‘‘rock back’’
so that the lamellae are now vertical and it is the microribs that are acting as the
reflective multilayers. (d) The microribs can extend across from ridge to ridge
and essentially close the windows. (e) The region between the ridges may be
filled with a ‘‘plates and pores’’ structure that we take to be essentially a variant
of the 2-D photonic crystal structure shown in (b). (f) The scale interior, or lumen,
can be filled with stacks of laminae that form a second type of multi-film
interference mirror. (g) The scale interior can be filled with a lattice that is
effectively a form of 3-D photonic crystal, again with associated optical
properties.
31
Fig. 10 Color-mixing mechanism due to concavities in a scale of (a) Papilio
palinurus butterfly (wingspan = 100 mm). Modulated multilayering leads to dual
color in P. palinurus. (b) TEM image showing a cross section through one
concavity on a P. palinurus butterfly iridescent scale; inset, SEM image of the
surface of an iridescent scale. (c) Real-color image showing the dual-color nature
of the reflectivity from the surface of the P. palinurus butterfly iridescent scale,
taken using unpolarized light in an optical microscope. Top inset, image of the
same region taken with crossed polarizers. Bottom inset, illustration of the
mechanism by which polarization is converted through double reflection from
orthogonal sides of a concavity.
135
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carapace that is corrugated to form periodic ridges.
79
The
mollusk Pinctada Margaritifera shows very strong iridescence
colors that are caused by diffraction,
152
while Tan et al.
11
thought the iridescent colors of mollusk Haliotis Glabra were
caused by both diffraction and interference, because there
were found to have a fine-scale diffraction grating structure
and stacks of thin crystalline nacreous layers or platelets below
the surface. The dark brown beetle Serica sericea bears gratings
on its elytra with 800 nm periodicity, which causes a brilliant
iridescence in sunlight.
22
The diffraction grating is also found in plants. The
iridescence in flowers of the Hibiscus trionum, Tulipa species
(Fig. 11c)
17
and Mentzelia lindleyi, comes from the overlying
cuticle of the petal epidermal cells which produces a series of
long, ordered ridges with a periodicity that acts as a diffraction
grating and splits the light reflecting from the surface into
component wavelengths.
1,17
3.3 Scattering
The special white colors in beetles’ cuticle were discovered.
153–155
All whites in beetles are structural, arising from non-ordered,
broadband, or Mie scattering of incident light by nanoscale
particles.
52
Structural whiteness is created by having a light
scattering material that scatters all incident wavelengths
equally.
155
Examples of incoherent scattering include blue sky, blue
smoke, blue ice, and blue snow.
93
For example, ‘‘so called’’
Rayleigh scattering results in a blue color and red color when
the system is viewed in transmission.
5
Although most
structural color in animals is produced by coherent light
scattering, the blue coloration in many amphibians is
attributed to incoherent scattering (Fig. 12a).
83
Fig. 12b
illustrates the basis of green coloration in amphibians and
other vertebrates. As light strikes the surface of an animal like
a frog, short wavelengths of light (blue-violet) are largely
absorbed by the filtering xanthophore or yellow pigment layer,
the rest are scattered by the iridophore or scattering layer.
Long wavelengths (red-orange) largely pass through the
filtering and scattering layers of the skin and are absorbed
by the melanophore or melanin layer. Intermediate wave-
lengths (yellow-green) pass through the filtering layer and are
scattered from the surface of the iridophore layer and pass
back through the filtering layer. Thus, the light reflected from
the surface contains a high proportion of yellow-green
wavelengths and the animal appears green.
The blue color in some animals has been thought to be
caused by incoherent scattering, such as the giant blue
swallowtail butterfly (Papilio zalmoxis),
90
dragonflies and
damselflies (Odonata),
156
and avian skin, while recently they
were disputed as a result of coherent scattering.
The color of the blue scales of the Papilio zalmoxis butterfly
have been found to be mainly of structural origin, due in part
Fig. 12 Blue coloration in amphibians.
83
(a) Young sibling male frogs of P. dacnicolor. The green individual is normal for the species, while the blue frog is one of only
a few that was produced from this spawning. Blue individuals are rare. (b) Diagrammatic interpretation for the basis of green coloration in amphibians and other
vertebrates.
Fig. 11 Examples of diffractive structures in nature. (a) A photograph showing
the violet observable when illuminating the male Lamprolenis nitida butterfly
hindwing at 60 degrees (left), an SEM showing that the cross-ribs are roughly
rectangular slabs, making an angle of approxim ately 30u with the plane of the
scale indicating the position of the cross ribs and flutes (middle), model of the
blazed grating (right);
150
(b) a diffraction grating in the seed-shrimp (ostracod
crustacean) Azygocypridina lowryi, all spectral colors can be observed with
varying angle, periodicity is 600 nm;
79,151
(c) base of Hibiscus trionum flower
petal, showing iridescence overlying red pigment (left), SEM of H. trionum
flower petal, half spanning the pigmented (heavily striated longitudinally
toward the petal base) epidermis (middle), top view showing striations on the
petal surface of Tulipa. kolpakowskiana flower, resembling a line grating with a
periodicity of 1.2–0.3 m (right).
17
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to incoherent scattering (Tyndall scattering) by a layer of air-
filled alveoli and in part to thin-film interference in a
basement lamella.
90
Prum et al.
91
found that the scales of
the P. zalmoxis butterfly are not appropriately nanostructured
for incoherent scattering, alternatively the blue color was
caused by coherent scattering. Other blue, non-iridescent,
integumentary structural colors of dragonflies and damselflies
(Odonata) have been attributed to incoherent Tyndall or
Rayleigh scattering.
156
Prum et al.
95
investigated a damselfly
(Enallagma civile) and a dragonfly (Anax junius) and found the
observed reflectance spectra do not conform to the inverse
fourth power relationship predicted for Tyndall/Rayleigh
scattering. So he supposed that coherent light scattering could
be occurring both from the surfaces and from structures at the
center of the spheres. Structural colors of avian skin have long
been hypothesized to be produced by incoherent (Rayleigh/
Tyndall) scattering.
157
While Prum et al.
158
revealed that non-
iridescent green and blue skin colors are produced by coherent
scattering from hexagonally organized arrays of dermal
collagen fibers. Coherent scattering models take into account
the phases of different scattered waves.
159
Fig. 13 shows the
structurally colored facial caruncles and the TEM micrograph
of the male yellow-bellied asity bird, Neodrepanis hypoxantha,
Fig. 13a and b, respectively; Fig. 13c is a two-dimensional
Fourier power spectrum through Fig. 13b, which shows that all
the tissues are substantially nanostructured at the appropriate
spatial scale to scatter visible light coherently.
159
These results
confirm that the nanostructure of the collagen arrays
determines the colors that are coherently scattered by these
tissues.
Coherent scattering includes several important optical
phenomena, notably diffraction or interference.
82
Well-known
examples of coherent scattering include the structural colors
produced by brilliant iridescent butterfly wing scales and avian
feather barbules such as the peacock’s tail.
81,160,161
Iridescence
occurs if changes in the angle of observation or illumination
affect the mean path length of scattered waves, such a change
will affect the phase relationships among the scattered waves
and change which wavelengths are constructively reinforced
after scattering.
93
The fluorescent blue colors seen in many
Fig. 13 (a) Structurally colored facial caruncles of male asities bird (Neodrepanis hypoxantha); (b) TEM micrograph shows the nanostructure of a nearly hexagonal
array of collagen fibers in light blue caruncle tissue; (c) two-dimensional Fourier power spectrum of the N. hypoxantha tissue.
159
Table 3 Some photonic crystals in nature
Variety Species Color Structure References
2-D photonic
crystal
Marine
animal
Marine worm Iridescent color Tubular structures containing hexagonally
packed hollow cylindrical channels
163,170
Comb-jellyfish Iridescent Tightly packed arrays of cilia 42,171,172
Brittlestar Color-change Double-lens arrays 166,173
Glass sponge Fiber-optical characteristics Lattice-like skeleton of fused siliceous
spicules and a crown-like organization
of basalia at the base.
174,175
Bird Peacock Iridescent Lattice arrays of solid rods 64,176,177
Magpie Black, yellowish-green iridescent Air-filled circle melanin granules 178,179
Crow Black Solid circle melanin granules rods 179,180
3-D photonic
crystal
Insect Beetle White; opal; orange
scale; green iridescence;
rows of brilliant spots;
yellow and blue bands;
greenish-white;
mixed blue and violet
colors; bright white
Solid array of transparent spheres with
hexagonal close-packing order; face-centered
cubic; concave spots with diamond-type scale;
ordered periodic 3D-lattice; face-centered-cubic
array of spheres; bags containing agglomerated
spheres; random network of interconnecting
cuticular filaments
51,131,153,154,
164,169,181–186
Butterfly Blue dorsal color, matt
pea green ventral
color; black matt
with blue shining
Gyroid-type; a chitinous matrix with regularly
arrayed air-holes; shingles on a roof; elongated;
deep zigzag ending
15,29–31,38,
40,42,43,45,47
Plant Edelweiss
flowers
White Hollow tubes with a series of parallel
striations around the external surface
187
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fish, for example, the coral reef damselfish and surgeonfish
Paracanthurus hepatus, are the products of coherent light
scatter.
83
Similar phenomena were also found in plants. The
iridescent blue leaf coloration is found to comes from a
physical effect, constructive interference of reflected blue
light.
16,162
3.4 Photonic crystals
Natural photonic crystals are defined as a medium with a
refractive index that varies in space periodically.
131
The typical
samples of 2-D and 3-D photonic crystals were first found in the
sea mouse Aphroditidae Polychaeta
163
and opal in the weevil,
164
respectively. And now, photonic crystals have been revealed in
marine animals, insects and birds.
9,56,101,102,107,165–169
2-D and
3-D photonic crystals were more common in marine animals,
birds, insects (beetle, butterfly) and plants, respectively
(Table 3). Similar photonic crystal-type structural colors have
been discovered one after another from various ranks of the
animal world, and it has become one of the common
expressions for structural color.
67
Decades before the synthesis of fabricated photonic struc-
tures, studies were revealing the complex and elegant way in
which it was accomplished naturally, while aquatic systems
were the subject of many of the earliest studies.
82
The sea
mouse (Aphrodita aculeata) is distinguished by an amazing
iridescence along the lower sides of the body, associated with
both hairs and spines (Fig. 2h).
12,188
The iridescence of spines
is caused by the regularity of the structure resembling that
being developed for photonic crystals, and the sea mouse
exploits a partial photonic band gap to achieve its remarkable
coloration effects.
163,188
The 2-D photonic crystals with tightly
packed arrays of cilia close to hexagonal were found in
Ctenophora (commonly known as comb jellies).
42,171,172
The
ctenophore Beroe
¨
cucumis is a transparent marine animal with
comb rows that are iridescent with rainbow colors passing
down the length of the animal as it swims, the regular packing
of the cilia is apparent, each one being found at a node of an
orthorhombic lattice, its model set as the reflectance of the
tightly packed cilia (Fig. 14a).
172
Other examples of 2-D
photonic crystal structures can be found in the dorsal arm
plate of the brittle star Ophiocoma wendtii.
166,173
The analysis
of arm ossicles in brittle star Ophiocoma showed that in light-
sensitive species, the periphery of the labyrinthic calcitic
skeleton extends into a regular array of spherical microstruc-
tures that have a characteristic double-lens design which
minimizes spherical aberrations and birefringences and
detects light from a particular direction.
166
The spicules of
the deep-sea ‘glass’ sponge Euplectella have remarkable fiber-
optical properties which can provide a highly effective fiber-
optical network, its lattice-like skeleton of fused siliceous
spicules and a crown-like organization of basalia at the base
which may be useful in distributing light in its deep-sea
environment.
174,175,189
The beautiful iridescent feathers of some birds are indeed
due to 2-D photonic crystals incorporated on the surfaces of
their barbules, for example peacocks (Fig. 2d).
64,176,177
It was
found that the cortex in differently colored barbules of
peacock feathers is responsible for coloration which contains
a 2-D photonic crystal structure: in the blue, green, and yellow
barbules, the lattice structure is nearly square, whereas in the
brown barbule it is a rectangular lattice; the only differences
are the lattice constant (rod spacing) and the number of
periods (melanin rod layers) along the direction normal to the
cortex surface.
64
The black-billed magpie bird Pica pica is not
exactly a black-and-white bird, in fact yellowish-green irides-
cent feathers forming a long tail, and bluish reflections on the
dark areas of the wings (Fig. 14b).
178,179
Their barbule cross
section shows the cortex surrounding the central core, while
Fig. 14 (a) The ctenophore Beroe
¨
cucumis is a transparent marine animal whose comb rows are iridescent, with rainbow colors passing down the length of the animal
as it swims (left), the regular packing of the cilia is apparent, each one being found at a node of an orthorhombic lattice (middle), model for the reflectance of the
tightly packed cilia (right);
172
(b) The black-billed magpie bird Pica pica has in fact yellowish-green iridescent feathers forming a long tail, and bluish reflections on the
dark areas of the wings (left), cross section of a barbule of a yellowish-green tail feather showing the cortex surrounding the central core, the cortex is a thin-film of
keratin and melanin containing cylindrical air holes, regularly distributed (middle), model of the structure (right).
178
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the cortex is a thin-film of keratin and melanin containing
cylindrical air holes, regularly distributed.
178
For a yellowish-
green feather, the structural model is actually an homoge-
neous block of keratin and melanin (refractive index 2) which
contains an hexagonal lattice of parallel air channels, the
distance of neighboring holes is 180 nm, while the size of the
holes is 50 nm (50 nm 6 50 nm for a square section).
178
Relatively, the jungle crow showed a simple structure of
melanin granules.
179,180
The 2-D photonic crystal structure,
stack of repeated corrugated layers, also has been found in the
blue scales of the male Hoplia coerulea butterfly which are
mentioned in section 3.1.
58
Chitin materials can be shaped into very complex forms and
3-D photonic crystals have been shown to occur in many
insects.
80
The 3-D photonic crystals in beetles were more
common in the weevil beetle (Pachyrhynchus argus,
Pachyrrhynchus congestus pavonius, Lamprocyphus augustus,
and Entimus imperialis)
51,131,164,181,183
and the longhorn beetle
(Calothyrza margaritifera, Pseudomyagrus waterhousei, and
Prosopocera lactator).
169,185,186
The Pachyrhynchus argus weevil
beetle has a metallic coloration that is visible from any
direction owing to a photonic crystal structure analogous to
that of opal.
164
The elytra surface has scales (0.1 mm in
diameter), the inner structure of the scales is a solid array of
transparent spheres (each with a 250 nm diameter) which are
arranged in flat layers and have a precise, hexagonal close-
packing order, as a result the lattice constant of the crystal
approaches half the wavelength of light, it acts as a 3-D
diffraction grating, forming optical domains within a single
scale. The other nice example of 3-D photonic crystals
structures in weevils is provided by the Brazilian ‘diamond
weevil’ beetle, Entimus imperialis, the special arrangement of
the scales in the concave pits significantly broadens the
angular distribution of the reflections, as a result, the virtually
angle-independent green coloration of the weevil closely
approximates the color of a foliaceous background.
131
The
3-D photonic crystal grains were found in the scales of the
longhorn beetle Prosopocera lactator (Cerambycidae).
169
The
local geometric structure can be described as a face-centered-
cubic array of spheres, connected by short rods, reminiscent of
the ‘‘ball-and-stick’’ models used by solid-state chemists to
visualize atomic structures. Another white beetle Cyphochilus
spp. also has 3-D photonic crystals structure, which originates
from the arrangement of white scales that imbricate above its
elytra, the scales fractured edge is composed of a random
network of interconnecting cuticular filaments with diameters
of about 250 nm.
53,154
The 3-D photonic crystals have been found in some beetle
species as well as in butterflies.
15,29–31,38,40,42,43,45,47
Structurally colored butterfly scales are extremely diverse in
nanostructure and in optical functions.
47
Butterfly photonic
crystals, as typified by the structure found in Parides seostris,
Thecla sp. or Vaga sp., respectively, have a so-called ‘‘inverse
opal’’ structure, which can be described as a chitinous matrix,
in which there are regularly arrayed air-holes.
42
The structural
colors of a number of papilionid and lycaenid are produced by
3-D biological photonic crystals, which were recently identified
as single-network gyroid-type photonic crystals comprised of a
complex network of the dielectric cuticular chitin (refractive
index, n = 1.56+ i0.06) and air in the cover scales of the
wing.
15,47
The gyroid also has a body-centered cubic lattice, but
it has a locally threefold-coordinated topology.
43
Photonic structures are also found in plants.
16,187,190
The
hairs of edelweiss flowers (Leontopodium nivale subsp. alpinum)
are hollow tubes with a series of parallel striations around the
external surface that acts as a 3-D photonic crystal, through
diffraction effects, the hairs absorb the majority of the UV
light, effectively acting as an efficient sun-block that shields
the covered living cells from harmful ultraviolet radiations.
187
Structurally colored natural photonic crystals (found in
butterflies, beetles, and other insects) are made of ordered
porous chitin structures.
191
In addition to these highly ordered
structures, biological photonic nanostructures also include
amorphous, or quasi-ordered, dielectric nanostructures where
there are local correlations but little long-range order.
192
Ordered photonic structures can produce iridescent structural
colors due to their direction-dependent partial photonic band
gaps, relatively amorphous photonic structures that can
produce non-iridescent coloration.
193
In well-defined fre-
quency ranges, called ‘‘stop bands’’, these materials, also
called photonic band gap materials, can prohibit electromag-
netic wave propagation along specific directions, even with the
very moderate refractive index contrasts found with biological
materials.
40,194
3.5 Coloration changes
The adaptive values of color change are usually regarded as
camouflage, predation, signal communication, conspecific
recognition, and reproductive behavior.
59
That is color
changes are triggered by excitement, stress, mate choices or
to prevent water from evaporating which is found in fish,
cephalopods and insects (Table 4).
Coloration change includes reversible and non-reversible.
52
The former can occur via the change in pigment, micro-
structure, or their combination (pigmentary color produced by
the selective absorption of natural light and the structural
color produced by the interactions of natural light with
microstructures).
59
Non-reversible structural color change co-
occurs with ageing,
52
such as pupa of a large tree nymph
butterfly (Idea leuconoe) whose color changes from yellow to
gold within two days after pupation.
67
Some reversible coloration changes are caused by selective
reflections of structural colors.
94,100
Like many scarab beetles,
the manuka beetle Pyronota festiva selectively reflects chiral
light, which is usually green, presumably for camouflage, but
can be purple, blue, orange, red or brown, related to hydration
of a cuticular multilayer reflector.
109
The color changes of the
wings of several Lepidoptera butterfly species are caused by
photonic nanoarchitectures, as a result incident light is partly
combined with polarized and reflected more than once.
114
This ability to change color quickly makes them difficult for
predators to pursue.
71,109,110,114
Or with changing viewing
angle, the butterfly changes color, while the degree of color
change is dependent on the species, for example, in Morpho
cypris, the wing color changes very quickly into black, while in
M. didius, its change is rather dull.
9
The breast-plate plumage
of the male bird of paradise, Lawes’ parotia bird Parotia
lawesii, can abruptly switch between yellow, blue, and black
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during the parotia’s courtship displays because the boomerang-
like cross section of parotia barbules works as three colored
mirrors, as described above.
111
Because the surface micro-
sculpture affects the intensity and wavelength content of the
additive mixing of interference colors, most tiger beetle
(Cicindelinae) species show an inconspicuous dorsal coloration
that provide crypsis either by matching the general color of the
substrate, by mimicking the color of small stones or by
correlating with the color of soils on which they occur.
101,196–198
There is another mechanism of coloration changes, the level
of hydration cause a variation in the thickness of the
multilayer stack, thus changing the refractive index of porous
layers.
52
In ordered photonic crystals, color changes can be
induced by relative gas/vapor concentration variations in a
mixed atmosphere.
191
There are color changes in the elytra of
some species of beetles that related with humidity and
microstructures, such as nanosized holes in the layer (3-D
porous structure) of Hercules beetles, Dynastes hercules,
54,57,60
a chirped multilayer reflector in tortoise beetles Charidotella
eregia,
56
multilayer in the scale interior of the longhorn beetles
Tmesisternus isabellae,
59
a stack of repeated corrugated layers
(a 2-D photonic crystal) of beetles Hoplia coerulea,
58
and the
"wax filaments" meshwork in desert beetles Cryptoglossa
verrucosa (LeConte).
101
It is desirable for beetles to change
color reversibly and rapidly to serve for species and sex
recognition, and also for camouflage and mimicry.
199
It was
also found that Morpho butterfly scales change color in
response to water, ethanol and methanol vapor.
200
Some
cephalopod species, such as squid, cuttlefish and octopus, can
almost instantaneously change body color for camouflage and
signaling.
84,107
Fish are another group of animals that show
physiological color changes during excitement or under
stress.
106,113
Thus the structural color in those cases should
be called a dynamical one, whose selected color change is
according to the change in the environment.
9
By contrast,
feather colors have been generally assumed to be relatively
static, changing by small amounts only over periods of
months, while recent research showing that iridescent
plumage color changes are also in response to water in the
feathers of the mourning dove, Zenaida macroura.
112
4. Bioinspired fabrication and applications
Structural color has high brightness and does not fade, while
the iridescent effect, polarization effect, and UV effect, that
pigment colors, do not have these characteristics. It can greatly
enrich the biological use of color to achieve the requirements
of the various types of biological functions, we can explore the
use of the structure to achieve a lot of complex functions from
the study of the living nature of structural color optics. The
understanding of their mechanisms of production have
inspired biomimeticists to develop various optical coatings,
paints, cosmetics, textiles, and anti-counterfeiting
devices.
56,68,201
For example, the structural coloration created
by butterfly wings has been used by L’Oreal for cosmetics.
69
There are two ways, one is reproducing the natural structure
with the highest possible degree of fidelity, and the other is
extracting new principles from structures found in the living
world and implement those using different materials and
different structural solutions.
100
Thus those design concepts
and reproducing methods have been conducted in various
nonmetallic materials and polymers for enhancing or improv-
ing their original mechanical properties. While multiple
colors, contrast, polarization, reflectance, diffusivity, and
Table 4 Some color changes found in biological animals
Species Normal color Changed color Trigger reasons References
Fish Damselfish Chrysiptera cyanea Blue Ultraviolet Stressful conditions 105–107
Paradise whiptail Pentapodus
paradiseus
Blue Red Stress 108
Neon tetra Paracheirodon innesi Blue Violet, yellow Excited or under stress 113
Cephalopod Squid Loligo pealeii Iridescence Disruptive pattern Agonistic encounters,
camouflage
85
Bird Mourning dove Zenaida macroura Iridescence More chromatic Water 112
Male bird of paradise Lawes’
parotia Parotia lawesii
Yellow-orange Blue-green Attract female 111
Beetle Tortoise beetles Charidotella egregia Red Golden Stress 56
Hercules beetles Dynastes hercules Khaki-green Black With humidity
level increases at night
for better camouflage;
thermoregulation
54,57,60
Desert beetles Cryptoglossa verrucosa Bluish-white Black Prevent water from
evaporating
101,102
Beetles Tmesisternus isabellae Golden Red Not clear 59
Beetles Hoplia coerulea Blue Green Conspecific sex
choice recognition
58
Manuka beetle Pyronota festiva Green Purple, blue, orange,
red or brown
Camouflage 108
Tiger beetle Cicindela Interference colors Nearly to rock or soil
condition
Camouflage 103
Butterfly Lepidoptera Iridescence Camouflage 71,109,110,114,195
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texture must all be controlled simultaneously without optical
losses in order to fully replicate the appearance of natural
surfaces and vividly communicate information.
202
4.1 Mimic iridescent effects
The butterfly has iridescent blue wings that have inspired
scientist and engineers to reproduce it.
68,203,204
Reproductions
of the butterfly Morpho ‘Christmas tree’ structures,
73
the quasi-
structure, using focused ion beam chemical vapor deposition
(FIBCVD) was fabricated (Fig. 15a) and the brilliant blue
reflection from the quasi-structure for a wide range of incident
light angles was observed (Fig. 15b).
73
The quasi-structure was
2.60 mm in height, 0.26 mm in width, 20 mm in length, and
had a 0.23 mm grating pitch. The shape and size were nearly
the same as the Morpho butterfly scales. Another fabrication of
Morpho-butterfly-blue was obtained by producing a dielectric
multilayered nanostructure on the stepped quartz by electron
beam lithography and dry etching, a simple and conventional
technique in the semiconductor industry (Fig. 15c and d).
205
To produce the desired surface pattern, conventional electron
beam lithography and dry etching were applied to quartz
substrates (Fig. 15c). The distance between the rectangular
units was determined by a random number generated by a
computer program. The process was finalized by step-by-step
electron-beam-assisted deposition of seven bilayers of TiO
2
(high refractive index layer, y40 nm thickness) and SiO
2
(low
refractive index layer, y75 nm thickness, Fig. 15d). There is
another completely replicated approach to reproduce the
butterfly’s scale by a uniform Al
2
O
3
coating through a low-
temperature atomic layer deposition (ALD) process.
206
A
similar method was used to replicate nanostructures of
butterfly Morpho menelaus with ALD and the comprehensive
features inherited from the bio-templates may be especially
crucial in practical applications.
207
In addition to the
structural blue color, the wing of the Morpho butterfly has a
waterproof character, so by preparing inverse opal films using
Fig. 16 Structural color printing using ‘M-Ink’.
210
(a) The superparamagnetic core and ethanol solvation layer allow the stable dispersion of the colloidal nanocrystal
clusters (CNCs) in the M-Ink. A strong repulsive force can be generated when two solvation layers overlap. (b) Upon the application of an external magnetic field,
CNCs are assembled to form a chain-like photonic nanostructure. This chain-like photonic nanostructure acts as a coloration unit of M-Ink, the color of which can be
tuned by varying the interparticle distance by modulation of the external magnetic field intensity. (c) SEM image of a cross-section of the color fixed structure. The
dimpled structures are the traces of the chain-like aligned CNCs. (d) Upper: reflection micrographs of multicolored structural color generated by gradually increasing
magnetic fields. Microstructure i is generated under the influence of no magnetic field. Microstructures ii–viii are generated by gradually increasing the magnetic field
strengths from 130 G to 700 G; down, TEM micrograph of the same sample. (e) Multicolored bar codes. (f) Photonic crystal film with anti-transmission black tape as
the transferred substrate, which blocks transmission light from the backside.
Fig. 15 Morpho-butterfly-scale quasi-structure fabricated by FIB-CVD (a and b): (a)
secondary-ion microscopy image of the imitation of the Morpho-butterfly scale
fabricat ed by FIB-CVD; (b) optical microscopy images of the structure of (a) observed
with a 5 to 45u incidence angle of white light.
73
Reproduction process of the
Morpho-blue (c and d): (c) SEM image of a quasi 1-D pattern on a quartz substrate,
fabricat ed by electron beam lithography and dry etching. (d) Morpho structure
emulated by deposition of TiO
2
/SiO
2
multilayer on the nano-pattern in (c).
205
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TiO
2
the bioinspired colloidal crystal films even had super-
hydrophobic properties.
208
By mimicking the structural colors found in butterfly wings,
a system was developed in color wring and printing with the
use of colorless materials, that is photonic papers and inks:
the ‘‘paper’’ is a 3-D crystal of polymer beads embedded in an
elastomer matrix made of poly(dimethylsiloxane) (PDMS) and
the ‘‘ink’’ is a liquid (e.g. a silicone fluid or organic solvent)
capable of swelling the matrix, changing the lattice constant
and hence wavelength of the light diffracted.
209
This system
may provide an alternative route to the realization of reusable
papers or recording media where no pigment will be required
for color display. Researchers have developed a high-resolu-
tion patterning technique that produces multiple structural
colors within seconds, based on successive tunings and fixings
of color using a single material (called ‘M-Ink’, the color of
which is tunable by magnetically changing the periodicity of
the nanostructure and fixable by photochemically immobiliz-
ing those structures in a polymer network) along with a
maskless lithography system (Fig. 16).
210
M-Ink is a three-
phase material system consisting of asuperparamagnetic
colloidal nanocrystal clusters (CNCs), a solvation liquid and
a photocurable resin (Fig. 16a). The combination of attractive
and repulsive forces determines the interparticle distance, and
the interparticle distance in a chain determines the color of
the light diffracted from the chain, which can be explained by
Bragg diffraction theory (Fig. 16b). Thus, the color can be
tuned by simply varying the interparticle distance using
external magnetic fields. Using this system, the chain-like
structure can be preserved without distortion (Fig. 16c).
Fig. 16d presents a reflective optical microscope image and
the corresponding spectrum data for each microstructure,
showing gradual color changes from red to blue as the applied
magnetic field strength is gradually increased. This gradual
increase in the external magnetic field induces an increasing
attractive force between the induced magnetic dipole moment
of the CNCs, thereby decreasing the interparticle distance in
the chains. By controlling the UV exposure pattern and
magnetic field strength, the bar-coded microstructures
(Fig. 16e), composed of 16 colorful strips, were fabricated by
16 sequential color tuning and fixing steps. The structural
color of the film is clearly seen by blocking the transmitted
light from the backside by transferring the film to a black
substrate (Fig. 16f). M-Ink can produce colorful patterns
conveniently from a single ink instead of using many different
inks for different colors, and also M-Ink-based systems can be
used in forgery protection, structurally colored design materi-
als and printing technology. Further studies have used self-
assembled colloidal photonic crystal substrates to support
high resolution, multicolor, stable but erasable images printed
with transparent silicon oils of varying molecular weight, and
the erasing of the images is done simply by adding a low vapor
pressure oil which dissolves the image, returning the substrate
to its original state.
211
Based on the model of scales of the lycaenid butterflies
Albulina metallica, which are quasi-ordered, perforated layer-
type nanoarchitectures, a quasi-ordered composite (SiO/(In &
SiO), well-separated indium (In) nanoparticles with near-
spherical shape and diameters close to 50 nm on SiO and
the mixed SiO–In layers were separated by pure SiO layers)
multilayer structure using standard thin-film deposition
techniques was reproduced with potential of the bioinspired
designs for various coatings and possibly for other fields like
colorants, paper and textile industry.
212
Similar composites
may lead to inexpensive ways of producing bioinspired
coatings with tunable properties.
100
One of the most well-known examples of direct biomimetic
applications is adding luster to fibers derived from the multi-
film interference of the Morpho butterfly, and this is the first
application of the Morpho butterfly’s coloration.
205
For
instance, a cloth formed by two layers is now currently
manufactured: in this device, a back substrate, opaque and
colored, is covered by a porous layer that strongly diffuses
light, so that the primary dry aspect of the surface is white, as
water is applied to fill in the pores, the refractive index
contrast with air is cancelled and the cover layer becomes
translucent enough to leave a view on the substrate color (U.S.
Patent 6953345).
58
A non-circular structurally colored fiber
fabricated by conjugated melt spinning had a multilayer core
covered by polyester, resulting in structural blue, green, or red
colors owing to light interference.
205
The unusual multilayer structure of the beetle Chrysochroa
vittata has been successfully reproduced, using SiO and nickel
for the alternating layers instead of chitinous ingredients.
74
Only the principle of construction of the multilayer was
extracted from the biological structure; very different materials
were used to realize its artificial counterpart.
100
The chitin
plate (refractive index of 1.56) was replaced by a layer of silicon
oxide (SiO; refractive index of 1.9). Inspired by multilayer
structures of iridescent Coleoptera in which iridescence takes
different aspects by tuning the layer thicknesses, periodic
TiO
2
–SiO
2
multilayer films were fabricated in order to
demonstrate the concept of structurally tuned iridescent
surfaces.
213
The weevil and longhorn beetles’ families
(Curculionidae and Cerambycidae, respectively) possess a range
of interesting three-dimensional photonic crystal structures
operating at visible wavelengths, including non-close-packed
lattices of cuticular spheres and diamond-based architectures.
A low temperature sol–gel biotemplating method was devel-
oped, to transform bio-polymeric photonic crystals into heat
and photo-stable silica and titania inorganic structures. The
fabricated oxide-based structures display good structural and
optical properties.
214
The ultra-bright whiteness of certain
beetle scales has inspired the development of optimization
principles for the manufacture of white paper where it is
normal to coat paper with nanoparticle scatterers, but typically
the whiteness, and therefore the apparent ‘‘quality’’ of the
paper falls short of the whiteness in the beetle Cyphochilus.
215
And also an extremely white fabric using electrospun
nanofiber webs have been created.
216
A simple, novel method
for obtaining structurally colored films consisting of poly (1,2-
butadiene) (PB) and Os multi-layers that mimic the surface
structure of jewel beetle elytra.
217
The elytra of the Taiwanese
beetle Trigonophorus rothschildi varians consists of a multilayer
structure intercalated with a random distribution of cylind-
rical holes normal to the plane of the multilayer, bioinspired,
artificial nanoarchitectures of similar structure and with
similar properties were realized by drilling holes of submicron
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size in a multilayer structure, showing that such photonic
nanoarchitectures of biological origin may constitute valuable
blueprints for artificial photonic materials.
218
Mimicking bird feathers brilliantly colored without the use
of pigments, the self-assembly of biomimetic isotropic films,
with a characteristic length-scale comparable to the wave-
length of visible light that can produce structural color when
wavelength-independent scattering is suppressed,
201
has been
motivated by the production a photonic band gaps.
9,68,79,94
The self-organizing biomineralization in deep-sea glass
sponges, which produces a unique nonlinear-optical biomin-
eral nanocomposite material combining the flexibility and
strength of a protein with the elasticity and strength of silicon
dioxide, is promising for applications in photonics.
219
4.2 Mimic polarization effects
As learned from butterfly scales, small fragments of thin-films
that cause colored reflections were mixed within a matrix of
transparent paint, which caused the vehicle to appear blue and
green when viewed the front and behind, respectively.
23
Mimicking the color mixing effect found on the wings of the
Indonesian butterfly Papilio blumei a combination of layer
deposition techniques, including colloidal self-assembly,
sputtering and atomic layer deposition, was used to fabricate
photonic structures (Fig. 17).
72
Firstly, polystyrene colloids
with a diameter of 5 mm are assembled on a gold-coated silicon
substrate. A 2.5 mm thick layer of platinum or gold is then
deposited to fill the interspaces of the colloids by electro-
chemical approach, creating a negative replica. After the
removal of the polystyrene spheres colloids by ultrasonic waves
and a sputtering thin carbon film, a multilayer of quarter-wave
titania and alumina films is grown by ALD (Fig. 17a),
inheriting the morphology of the hexagonally arranged pits
of the negative replica (Fig. 17b). The sample exhibits similar
color mixing with that of Papilio blumei butterflies (Fig. 17c
and d). Moreover, by modifying the surface morphology of the
imitation (Fig. 17e), even visual information, e.g. a picture, can
be encoded into the photonic structures which display a
striking appearance change from pale blue in the specular
direction to red in retro-reflection (Fig. 17f and g). This
bioinspired work is expected to find applications in the
security labeling field or in the color industries, such as
painting and coating.
72
The polarization effects found in the curved scales of the
male butterfly Suneve coronata may be of use in protecting
banknotes against counterfeiting (Fig. 18).
71
With a combina-
tion of multilayered planes and grooves, an infinity of devices
can be imagined that produce colored effects linked to the
Fig. 17 Mixed structural coloration and applications inspired by the colorful wing scale structure of the Papilio blumei butterfly.
72
(a) Schematic diagram of artificial
samples mimicking the scale structures of P. blumei; (b) SEM photographs in top view show the concavities on the surface of the replica which is (c) green
macroscopically but it reflects blue at grazing incidence (d), showing some iridescence; (e) modifications of the concavities’ morphology by melting colloidal spheres
embedded in the concavities, which leads to a striking change in color of the sample from blue to red viewed (f) in direct specular reflection and (g) in retro-reflection.
Fig. 18 Two kinds of anti-fake or encryption designs for banknote are inspired,
which apply (a) a colored effect or (b) a grey level change linked to the
polarization and the broken surface symmetry.
71
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polarization. For instance, by etching periodic triangular-like
grooves on the surface of a flat multilayer, the film displays a
coloration of green, which is actually a mixed color from
yellow in the flat region and blue in the grooves in normal
incidence, as shown in Fig. 18a. When one uses ridged areas
only, the surfaces present the same color under natural light
and it is impossible to distinguish any pattern. The ridge areas
become apparent by using a polarizer letting the reflected
component penetrate. Transverse electric (TE) and transverse
magnetic (TM) are relative to the central motif structures,
Fig. 18b.
Learning from the chiral films in manuka beetle cuticles,
specialized coatings have been replicated in titania.
109
From
studying cephalopods, two main outcomes about adaptive
reflectance can be derived: (1) one is that the best method for
changing coloration is by compacting and spreading out
pigments; (2) the other is that efficient reflection and
wavelength modulation can be achieved by thin-film inter-
ference.
202
4.3 Mimic color changing
4.3.1 Color-tunable devices. In order to mimic those color
changes, scientists have been working on realizing the color-
tuning mechanism found in nature in synthetic materials.
According to eqn (7), the variation of d, h and n results in color
changes.
115
Due to the obvious appearance changes which are
easy to be picked up with the naked eye, color-tunable devices
are explored to identify the status changes by temperature,
vapor, solvent, humidity in ambience, the applied mechanical
force, electric field, magnetic field, etc.
53
By mechanical stretching, a soft opal film on a PDMS rubber
sheet changes color from red to green upon stretching and the
color is restored by releasing the strain, behind it is the
variation of d.
220
Such opal composite films can be used in
practical devices such as a color indicator, tension meter or
elongation strain sensor.
A bioinspired material, inspired from the self-assembling
protein structures of squid Loligo pealeii (Fig. 19a and b),
designed from a self-assembled block copolymer, lamella, for
an electrically tunable full color device, is expected to bring a
new design approach to photonic crystals with tunable colors
(Fig. 19c).
221
As seen in Fig. 19c, the pixel comprises an
electrochemical cell consisting of top and bottom electrodes
(indium tin oxide (ITO)-coated glass) separated by an inert 200
mm fluoropolymer spacer. The bottom electrode is coated with
a block copolymer film and the cell is filled with an electrolytic
fluid (2, 2, 2-trifluoroethanol (TFE)). The resulting film has
well aligned lamellar domains as evidenced by inspection of
the cross-section using TEM (Fig.