Materials Science and Engineering C 27 (2007) 941 – 946

www.elsevier.com/locate/msec

Living photonic crystals: Butterfly scales —

Nanostructure and optical properties
L.P. Biró a,⁎, K. Kertész a , Z. Vértesy a , G.I. Márk a , Zs. Bálint b , V. Lousse c , J.-P. Vigneron d
a
Research Institute for Technical Physics and Materials Science, H-1525, Budapest, POB 49, Hungary
b
Hungarian Natural History Museum, H-1088, Budapest, Baross utca 13, Hungary
c
Department of Electrical Engineering, Stanford University, Stanford, California 94305, California, USA and Facultes Universitaires Notre Dame de la Paix,
B-5000, Namur, Rue de Bruxelles 61, Belgium
d
Facultes Universitaires Notre Dame de la Paix, B-5000, Namur, Rue de Bruxelles 61, Belgium
Received 3 May 2006; received in revised form 22 September 2006; accepted 25 September 2006
Available online 15 November 2006

Abstract

The photonic crystal type nanostructures in the scales of male individuals of two butterfly species: Cyanophrys remus and Albulina metallica
were investigated by electron microscopy and reflectance measurements. While the colors of C. remus arise from structures with rigorous long
range (dorsal) or short range (ventral) three dimensional (3D) order, the colors of A. metallica are produced by quasi-ordered, layered structures.
Surprisingly, the most efficient photonic band gap reflector is the quasi-ordered structure giving the shiny, yellowish green color of the ventral
hind wings of A. metallica. All four investigated structures are based on a moderate refractive index contrast between chitin (n = 1.58) and air, the
various structures achieve a wide range of biological functions.
© 2006 Elsevier B.V. All rights reserved.

Keywords: Nanostructures; Butterfly wing scales; Photonic crystals; Electron microscopy; Reflectance

1. Introduction [5], more efficient lasers [6] and fibers for optical communica-
tions [7], less harmful pigments [8] to photonic paper [9] to
Photonic crystals [1, 2]] may be regarded as a special case of mention only a few.
composite, built from two materials with refractive indices n1 and While the manufacturing of large area photonic crystals
n2, characterized by a refractive index invariant under the spatial operating in the visible spectrum is still a somewhat challenging
translations of a crystalline lattice, Fig. 1. The periodicity of the and expensive task for laboratory techniques, as the result of
structure has to be comparable with the wavelength range in extremely refined biological evolutionary paths, periodic di-
which it will exhibit the photonic crystal type behavior. In well- electric structures which operate in this wavelength range, have
defined frequency ranges, called “stop bands”, these materials, evolved in living beings like certain butterflies, for example the
also called photonic band gap materials (PBG), can prohibit exclusively Neotropical butterfly genus Morpho [10–12], birds
electromagnetic wave propagation along specific directions, even [13], beetles [14], marine organisms [15] and even in plants
with the very moderate refractive index contrasts found with [16]. A more comprehensive overview was published recently
biological materials [3]. It should be emphasized, that for a by Welch [17], the palaeontological aspects were reviewed
complete photonic gap, usually more complex structures are recently by Parker [18].
needed than the structure shown in Fig. 1, which is only illus- In the present paper the characteristic nanostructures in the
trating the principle of a three dimensional PBG. wing scales, generating the blue and green colors of the lycaenid
PBG materials may have numerous applications ranging butterflies: Cyanophrys remus (Hewitson, 1868) and Albulina
from optical computing [4] through tunable photonic circuits metallica (Felder and Felder, 1865) (family Lycaenidae), will be
examined by transmission electron microscopy (TEM) and
⁎ Corresponding author. Tel.: +36 1 3922681; fax: +36 1 3922226. scanning electron microscopy (SEM), the reflectance of the
E-mail address: [email protected] (L.P. Biró). investigated structures and their biological role will be
0928-4931/$ - see front matter © 2006 Elsevier B.V. All rights reserved.
doi:10.1016/j.msec.2006.09.043
942 L.P. Biró et al. / Materials Science and Engineering C 27 (2007) 941–946

ing especially in the early morning hours, before the butterfly

starts flying. It is interesting to examine more closely in which
way evolution, using the same two materials: air and chitin
(n = 1.58) produced several different structures, which all exhibit
PBG behavior and have very different reflectance and different
roles in the survival of the individual and of the species.
The nano- and micro-structure of the butterfly scales are
revealed by SEM and TEM as shown in Figs. 3 and 4. From the
examination of the electron micrographs one may conclude that
the four structures represent four different cases, in the sequence
of the decreasing order in the structure: i) the dorsal wing
surface scales of C. remus are characterized by well developed
ridges, which are filled by the same nanostructure as the body of
Fig. 1. Schematic model of a 3D photonic crystal. As a rule of thumb the lattice the scale, as shown by the TEM image, the structure has long
parameter a has to be of the same order of magnitude as the wavelength for which the range order in the full three dimensions (3D), this observation is
PBG will form. Note that for a full PBG in practical cases, usually more complicated
quantitatively supported by detailed Fourier analysis of the
structures are needed than the simple cubic case used here for illustration.
images, published elsewhere [20]; ii) the ventral wing surface
scales of the C. remus exhibit locally in the grains a highly
discussed. Both butterfly species are colored by PBG ordered structure, a so called face centered cubic (fcc) inverse
nanostructures on both the dorsal and ventral sides and the opal, but there is no long range order as the orientation of the
nanostructures in the scales exhibit different degrees of order. grains is random; iii) the dorsal wing surface scales of A.

2. Experimental results and discussion

The butterfly samples used in the present work were obtained

from the collections of the Hungarian Natural History Museum,
Budapest, Hungary. All the specimens investigated were males.
The species A. metallica belongs to the subfamily Polyomma-
tinae and inhabits high altitude open habitats in the Himalayas.
The species C. remus belongs to the subfamily Theclinae and
occurs in the tropical and subtropical forest zone of south-
east Brazil, where it lives in forest edges at low or moderate
elevations.
For SEM examination pieces of wings were attached to the
sample holders and covered by 20 nm of sputtered gold to avoid
charging. A LEO 1540XB FESEM/FIB was used for SEM
investigations. The TEM samples were prepared by incorpora-
tion of wing pieces in plastic blocks, followed by ultramicro-
tome sectioning which resulted in 70 nm thick slices. The
samples were examined in TECNAI 10 transmission electron
microscope. Reflectivity measurements were carried out with an
Avaspec 2048/2 fiber-optic spectrometer, both in specular ar-
rangement under normal incidence and using a 3 cm integrating
sphere in order to collect all the light reflected under any angle
of emergence. An Avaspec diffuse, white standard was used as
comparison sample for reflectance measurements.
As seen in Fig. 2a and b, both butterfly species have blue
dorsal color (with role in sexual signaling) [19], while their
ventral coloration, used as cryptic color, to help avoiding the
attacks of predators, is greenish. The ventral wing surfaces of
the C. remus have a matt pea green coloration, while only the
ventral hind wing surface of A. metallica is shiny greenish-
yellow. It is worth pointing out that C. remus lives in forests and
the matt pea green color is helpful in hiding the butterfly against
the diffuse green background of the vegetation. On the other Fig. 2. Composed photographs of male butterfly individuals representing C. remus
hand A. metallica lives in a dew-rich, grassy environment at (a) and Albulina metallica (both Lepidoptera: Lycaenidae) (b). Left side shows the
high altitude, the shiny greenish color is useful for camouflag- dorsal surface of the wings, while the right side the ventral side, respectively.
 L.P. Biró et al. / Materials Science and Engineering C 27 (2007) 941–946 943

Fig. 3. Electron micrographs of the scales on the wings of the C. remus: (a) dorsal scale SEM micrograph, note the well developed ridges; (b) dorsal scale TEM
micrograph, note the filled ridges and long range order in the structure; (c) ventral scale SEM micrographs, note the granular filling below the plane of the thin ridges;
(d) ventral scale TEM micrographs, note the local order within each grain and the random orientation of neighboring grains. All scale bars correspond to 5 μm.

metallica show a characteristic, quasi-ordered structure, which producing the structural, or “physical color” [24] will cause that
is often called by the entomologists “pepper pot” structure [21]; in a certain wavelength region, the incoming light cannot
iv) the ventral wing surface scales of A. metallica also have a penetrate into the scale volume. The light will be reflected by the
quasi-ordered pepper pot type structure, but characterized by photonic crystal type structure (PBG), therefore it cannot be
different dimensions as compared with the dorsal side. As seen absorbed by the melanin distributed in the volume of the scale. In
from the TEM images, in fact both the dorsal and ventral scales a scale containing only melanin or other pigments and no PBG
of A. metallica exhibit a layered structure in which the thickness structure, the light may penetrate in the volume of the scale, due
of the chitin filled layers is different: 80 nm for the dorsal scales to the absorption its intensity will be reduced according to the
and 60 nm for the ventral scales. Additionally, within the air/ absorption coefficient of melanin (other pigment). Therefore,
chitin filled layers the effective refractive index depends on the when illuminated with white light, it will appear brown in
average size of the holes and the walls separating them, which is reflected light. In the region of the PBG a reflectance peak will be
again different for the dorsal and ventral scales. This quantity, superimposed on the reflectance curve characteristic for the
which we call filling factor, i.e., the ratio of hole diameter to the melanin, i.e., when a PBG is present, in the wavelength region of
width of the chitinous walls separating the holes is: 1.8 for the the photonic band gap, the reflectance will increase (from the
dorsal scales and 2.2 for the ventral scales. usually low value, characteristic for melanin) as the light is
The normal incidence specular reflectance measurements reflected before being absorbed by the melanin. The combined
(Fig. 5) revealed that for each of the above structures a char- reflectance due to the melanin and the PBG will produce together
acteristic reflectance peak can be found, Table 1. To allow the the blue or green coloration seen in Fig. 2 and the spectra in Fig.
comparison of the spectra measured, each spectrum was nor- 5. As a consequence, the color will depend on the melanin
malized to its maximum in the range of 250–850 nm. content, the efficiency of the PBG material in the scales – the
In fact, the spectral distribution of intensities in the light amplitude of the reflectance maximum – and on the bandwidth of
reflected from the scales of butterflies built of chitin – a trans- the photonic band gap – the full width at half maximum (FWHM)
parent bio-polymer – is determined by the content of pigment: in of the peak – these factors together will decide the intensity and
our case, brown melanin [3] (also a bio-polymer and a very the hue of the observed color. To facilitate the comparisons, all
efficient absorber in the UV and blue range of the visible [22, spectra in Fig. 5 were normalized to the maximum measured in
23]). A second factor is the structure itself when the scale the range of 250–850 nm, thus relative reflectances are given in
contains PBG material. Melanin alone would yield a continu- the figure. It is worth to point out that three of the four spectra,
ously increasing reflectance from 500 nm – the value of ab- although not all belong to the same butterfly species, show
sorption edge determined from Fig. 1 of Ref. [22] – towards relative reflectance of the order of 100% at 850 nm, while for the
800 nm, this would result in a brownish color. The PBG material ventral scales of A. metallica the relative reflectance is only 40%
944 L.P. Biró et al. / Materials Science and Engineering C 27 (2007) 941–946

Fig. 4. Electron micrographs of the scales on the wings of Albulina metallica: (a) dorsal scale SEM micrograph; (b) dorsal scale TEM micrograph; (c) ventral scale
SEM micrograph, note the similar but not identical structure with the SEM micrograph in (a); (d) ventral scale TEM micrograph, note similar but not identical structure
with the TEM micrograph in (b). The scale bars in (a) and (c) correspond to 2 μm; the scale bars in (b) and (d) correspond to 1 μm.

at this wavelength. This deviation from the general behavior is The two ordered structures, corresponding to the ventral (blue,
associated with a strong and broad maximum at 545 nm with the Fig. 3a and b) scales and to the dorsal (green, Fig. 3c and d) scales
relative amplitude of 100%. This indicates that the ventral scales of C. remus were modeled structurally and on the basis of the
of A. metallica contain an extremely efficient reflector, which is models numerical computations successfully reproduced the
in agreement with the observation by the naked eye, or the experimentally observed reflectance peaks. The model calcula-
photographic image in Fig. 2b. tion yielded: a strong blue peak at 450 nm for the dorsal scales,
while the green peak is composed of weaker blue (469 nm), strong
green (498 nm) and strong yellow (550 nm) reflections occurring
on the (110), (100) and (111) faces of the fcc inverted opal [20].
The modeling of quasi-regular structures is a more difficult task,
the same is valid for the numerical computation of the reflectance.
On the other hand the experimental reflectance curves shown in
Fig. 5, indicate that the quasi-regular, layered structures – which
may be less difficult to manufacture than the structures based on
three dimensional long, or short range order – are more efficient
when normal incidence specular reflectance is measured. A
similar behavior is found when the integrating sphere is used, the
PBG material from the ventral scales of A. metallica is the most
efficient one, but the differences are reduced as compared with the
specular case Table 1. Another interesting feature is that in these
layered structures the refractive index contrast that could be
achieved by sharply separated chitin/air layers is reduced by the
“mixed layers” of air and chitin, still the reflectance achieved in
the case of ventral scales of A. metallica is rather strong and has a
large bandwidth. To check for possible directional effects reflec-
Fig. 5. Relative reflectance data under normal incidence specular measurement tance measurements were carried out using an integrating sphere,
for the four butterfly wings. To facilitate comparison, each curve was normalized the peak positions and FWHM values are given in Table 1. The
to its maximum in the presentation window. comparison on specular and integrated values in Table 1 shows,
 L.P. Biró et al. / Materials Science and Engineering C 27 (2007) 941–946 945

Table 1
Reflectance peak positions and intensities as measured in normal incidence specular geometry and with the integrating sphere for the two butterflies under
investigation, λnormal is the peak position for normal incidence, λintegrated is the peak position for integrated measurements, NRnormal and NRintegrated are the normalized
reflectance intensities (see text for details) for specular and integrated measurements respectively, FWHMn and FWHMi are the full width at half maximum values for
the peaks for normal incidence and integrated measurements respectively
Butterfly Side λnormal (nm) λintegrated (nm) NRnormal (%) NRintegrated (%) FWHMn (nm) FWHMi (nm)
C. remus Dorsal 480 460 55 93 110 106
Ventral 545 541 64 58 87 91
A. metallica Dorsal 450 – 81 – 152 a
415 – 77 – 152 a
416 – 92 133
Ventral 560 545 100 100 185 227
a
Due to the close overlap of the two peaks the FWHM value is given for the two peaks together.

that although the relative amplitude of the blue maximum cor- comparison of the efficiency of different structures. The PGB
responding for the dorsal scales of C. remus increased signifi- material found in the ventral scales of A. metallica is the most
cantly when measured with the integrating sphere – indicating efficient reflector from the four investigated ones. It is worth
strong non-specular reflectance –, still its amplitude did not pointing out that it is not a rigorously ordered structure and it
increase over the amplitude of the green maximum of the A. is based on a moderate refractive index contrast. Such quasi-
metallica. The blue maximum of C. remus has a narrow band- ordered nanostructures, which may be more easily manufactured
width, while the green maximum of the A. metallica, has a very than the perfectly ordered 3D nanostructures could prove useful
large bandwidth which makes these structures suitable for dif- in various practical applications. The investigation of natural
ferent applications. designs may yield very useful templates for artificial structures.
As regards the biologic function of these colors, the blue
color of the dorsal scales has a role in sexual signaling [19], both Acknowledgements
in attracting the females and repelling other males. It is perhaps
more interesting here to concentrate on the very different, The work was supported by EU6 NEST/PATHFINDER/
cryptic green of the ventral scales. Two very different tasks were BioPhot-01915. The work in Hungary was partly supported by
achieved by appropriately modified PBG nanostructures built OTKA No. 042972. The work in Belgium was partly carried out
from the very same materials chitin and air. The species C. with support from EU5 Centre of Excellence ICAI-CT-2000–
remus, living in forests or at forest edges evolved a matt green, 70029 and from the Inter-University Attraction Pole (IUAP P5/1)
diffuse reflector built of randomly oriented photonic crystal on “Quantum-size effects in nanostructured materials” of the
grains with fcc inverse opal structure, thanks to which it may Belgian Office for Scientific, Technical, and Cultural Affairs.
blend very efficiently in the diffuse green background of the Correspondence and requests for materials should be addressed to
forest. The A. metallica, living in a high altitude, grassy habitat László P. Biró, [email protected].
with rich dew in the morning hours, developed a shiny cryptic
color, which may help it to blend efficiently in the glittering dew References
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