Photonic Crystal Structure of Wing Scales in Sasakia Charonda Butterﬂies

Materials Transactions, Vol. 51, No. 2 (2010) pp. 202 to 208 Special Issue on Development and Fabrication of Advanced Materials Assisted by Nanotechnology and Microanalysis #2010 The Japan Institute of Metals

Jirˇina Mateˇjkova´-Plsˇkova´1, Dalibor Jancˇik1, Miroslav Masˇla´nˇ1, Satoshi Shiojiri2 and Makoto Shiojiri3;*

1Centre for Nanomaterial Research, Faculty of Science, Palacky University in Olomouc, Slechtitelu 11, 783 71 Olomouc, Czech Republic 2Matsubara Junior High-school, Kyoto 604-8812, Japan 3Professor Emeritus of Kyoto Institute of Technology, 1-297 Wakiyama, Kyoto 618-0091, Japan

The hindwings of the male Sasakia charonda charonda butterflies comprise iridescent purple-blue areas, iridescent white-pearl areas, yellow spots and red spots as well as brown background. We have examined the microstructure of their scales by scanning electron microscopy, for applying their photonic crystal structures to fine light manipulators such as reflection elements in laser diodes. The scales in the yellow spots, red spots and brown background have almost the same structure, which is an optical diffraction grating made of ridges with two cuticle layers. Their difference comes from the contained pigments. The scales in the iridescent purple-blue and white-pearl are also the same in structure. They have seven tilted cuticle layers lapped on the ridges, which also constitute a grating. The widths of the ridge and groove in the grating are different between scales of the two kinds. It is shown that the vivid iridescence is mainly attributed to multiple interferences caused between rays reflected from the seven cuticle layers with air gaps. [doi:10.2320/matertrans.MC200903]

(Received July 6, 2009; Accepted September 28, 2009; Published November 18, 2009) Keywords: butterﬂy, wing scale, Sasakia charonda, great purple emperor, photonic crystal, ﬁeld-emission scanning electron microscopy

1. Introduction using three lycaenid subfamilies; the Coppers (Lycaeninae), the Hairstreaks (Theclinae) and the Blues (Polyommatinae), The characteristic patterns and vivid coloration of wing that the hue of the various blue colors is characteristic scales of butterflies have lately attracted considerable for the microstructure and nanostructure of the body of the attention as photonic crystals for an excellent tool to scales.6) Prum et al.,7) who have investigated the physical manipulate light. Vukusic et al.1,2) studied the origin of the mechanisms of structural color production in twelve bright green coloration of the wing scales of an Indonesian Lepidopteran species from four families, reported that all male Papilio palinurus butterfly, and revealed that the dual the species are appropriately nanostructured to produce color arises from modulated multilayers, producing the blue visible colors by coherent scattering, indicating that only component as the result of an orthogonal-surface retro- the blue of P. Zalmoxis is a fluorescent pigmentary color. reflection process. They also studied the coloration of a Costa However, Lepidoptera, which is the generic name for Rica male Ancyluris meliboeus Fabricius butterfly, called a butterflies and moths, has about 180000 species in the world, ‘living jewel’, and found highly tilted, multilayered arrange- and only a few species have been investigated on the ment that produces a bright iridescence of broad wavelength structure of wings. range.3) Biro´ et al.,4) who investigated the role of photonic- Recently, we have investigated the microstructure of crystal-type structures in the thermal regulation of a lycaenid scales in male wings of Sasakia charonda charonda butterfly sister species pair, showed that the blue color can be (S. charonda) butterfly.8) It is a species in Apaturinae attributed unambiguously to the fine, sponge-like medium, subfamily of Nymphalodae and is called ‘the great purple called ‘pepper-pot structure’, which appears between the emperor’ in English and ‘ohmurasaki’ in Japanese. Adults ridges and the cross ribs in the scales of the colored butterfly. have dark brown wings with white patches and a small red- Only traces of this structure were found on the scales of the orange spot on each of the hindwings. Male generates purple- discolored butterfly. They also revealed from the thermal blue iridescence in the forewings and hindwings, while the measurements that the high-altitude butterfly reaches a female lacks. We identified and named six types of scales; temperature 1.3–1.5 times the temperature reached by the B1, W1, and R1 in brown background, yellow spots, and red low-altitude butterfly, and then concluded that this is spots, respectively, B2 in iridescent purple-blue and W2 in attributed to the photonic crystal-like behavior of the white-pearl, both of which characterize the male, and B3 in pepper-pot structure, which significantly reduces the pene- the wing edges. The B1, W1, and R1 scales are almost the tration of blue light into the body of the scales. Ve´rtesy same in structure, and the B2 and W2 scales are almost the et al.5) examined the dependence between color and scale same. The difference among the B, W, and R scales is in morphology in species belonging to the cosmopolitan tribe species and content of pigment. The B1, W1, and R1 scales Polyommatini representing Lycaenidae, showing that the have only two layers of cuticle lapped on the ridges. In pepper-pot structure operates as a natural photonic band- contrast with them, the B2 and W2 scales have seven gap material causing increased reflectance in the spectral multilayers of cuticle piled on the ridge. The characteristic range from blue to near ultraviolet (UV). They demonstrated, purple-blue of the male wings was ascribed to the com- bination of the structural and chemical coloration in the B2 *Corresponding author, E-mail: [email protected] scales with melanin. Photonic Crystal Structure of Wing Scales in Sasakia Charonda Butterflies 203

Fig. 1 (a) Photograph of a hindwing of a male S. charonda butterﬂy. (b) SEM image of B2 scales arranged in the iridescent purple-blue on the wing. (c) Optical microscopy (OM) image of B2 and W2 scales around the boundary between the iridescent purple-blue and iridescent white-pearl areas. (d) OM image of B1 and W1 scales around the boundary between the yellow spot and the brown background. (e) OM image of R1 and B1 scales around the red spot and the brown background. (f) SEM image of B2 scales separated from the wing. Removed scales were observed in this experiment.

The structures of the photonic crystals of these scales layer about 10 nm thick to avoid charging effects, similar to would be applicable to fine light manipulators such as our previous observation.8) Scales separated from an un- reflection elements in laser diodes, especially in blue, purple, coated wing were also prepared in the present experiment. and ultraviolet laser diodes. In fact, some investigators have The removed wing scales were not coated with any gold layer produced replicas of the photonic structures of butterfly to observe them in authentic intact natural state. Little scales using atomic layer deposition technique (ALD),9,10) charging effect was present. The hue of the scale’s colors was which is a surface-controlled process of depositing materials examined in an optical microscope (OM). with atomic-layer accuracy.11,12) More structural investiga- tions of the butterfly scales are still required for achieving 3. Results and Discussion tunable photonic properties in the artificial scales. The present paper reports on further observations of the wing Figure 1(a) shows a photograph of a hindwing of a male scales in a male S. charonda butterfly following our previous S. charonda butterfly. Iridescent purple-blue area, iridescent one,8) and discusses their microstructures causing the bright white-pearl area, yellow spots and red spot can be seen as iridescence. well as brown background. In a previous paper,8) the scales in these parts were named B2, W2, W1 and R1, respectively, 2. Experimental Procedure and the scales in the brown background B1. These scales are arranged on the wing as shown in Fig. 1(b). Each scale The male S. charonda used in the present experiment was comprises many ridges which run parallel to each other. The sampled in July, 2008 in Nagano Prefecture in the middle B2 and W2 scales taken with OM are shown in Fig. 1(c), of Japan. Scanning electron microscopy (SEM) observations the B1 and W1 scales in Fig. 1(d) and the R1 and B1 scales were performed in secondary electron detection mode in a in Fig. 1(e). The W1 and W2 scales are semi-transparent, range of 2–15 kV of the accelerating voltage, using a Hitachi the B1 and B2 scales are semi-transparent brown and the SU6600 with a Shottky field-emission gun. The microscope R1 scales are semi-transparent red. In the present SEM guarantees a resolution of 1.2 nm at 30 KV and 3.0 nm at experiment we observed scales removed from the wings, 1 kV. We observed the wing coated with a sputtered gold as shown in Fig. 1(f). Figure 2 shows a SEM image of the 204 J. Mateˇjkova´-Plsˇkova´, D. Jancˇik, M. Masˇlańˇ, S. Shiojiri and M. Shiojiri

Fig. 2 SEM image of a W2 scale separated from the wing. The scale is bent and broken during preparation so that allows us to observe the side view and broken cross-sectional view as well as the top view of the cuticles piled on the ridges.

Fig. 3 Computer diﬀractogram and enlarged SEM images of some areas of the W2 scale in Fig. 2. (a) Computer diﬀractogram from the area enclosed by the square. (b) The side view and top view of the cuticles piled on the ridges. (c) The cross-sectional view of a ridge with cuties. (d) Edge of the scale.

W2 scale. It was bent and broken during preparation. Thus, Figure 3(a) reproduces the computer diffractogram or fast this sample preparation allowed us to observe the side and Fourier transform (FFT) image from the area enclosed by a broken cross-section as well as the top of the cuticles lapped square in Fig. 2. This area views the top surfaces of the on the ridges. cuticles on the ridges. Strong diffraction spots in Fig. 3(a) Photonic Crystal Structure of Wing Scales in Sasakia Charonda Butterflies 205

Fig. 4 SEM images of ridges in a B2 scale separated from the wing. (a) The top surfaces of the ridges. (b and c) The top and side surfaces of the cuticles on the ridges. (d) Schematic of the piled cuticles.

come from the ridges, parallel to the length of the scales, Table 1 Diffraction grating in the wing scales in the male S. charonda with almost equal spacings of 0:9 mm. The ridges, thus, butterfly. may be regarded as an effective diffraction grating for the d d d D t Scale 1 2 n B B incident light. In fact, we observed the corresponding (mm) (mm) (mm) (mm) (mm) () (nm) reflection spots through the wing in the optical diffraction B1, W1 & R1 0:4 1:1 1:5 0:8 2 0:8 10 280 experiment using a laser beam. The grating comprises ridges B2 & W2 0:6 0:3 0:9 1:0 7 1 8 280 0:6 mm wide and grooves 0:3 mm wide between the d , d , d, D and t are indicated in Fig. 4(d). n is the number of cuticle ridges. The cross ribs in the grooves are not regularly spaced 1 2 layers piled on the ridge. B is the angle between the cuticle and scale as seen in Fig. 2, and then cause only diffuse intensity on surfaces, and corresponds to the blaze angle for the blazed grating. B is the lower-order layer lines in the diffractogram. Neither the the blaze wavelength. pepper-pot4) nor modulated multi-layers causing the dual color1) exist in the grooves in the scales of the S. charonda butterfly. Therefore, the iridescence of the wings is y-axis normal to the x-z plane. From the top view images attributed only to the diffraction grating of the ridges in as shown in Fig. 4(a) we measured the width of the ridges the scales. The side of a ridge as well as the top of two d1, the width of the grooves d2 and the spacing between the ridges can be seen in Fig. 3(b), indicating that cuticles are cuticles D. The number n and total thickness t of the piled piled on the ridges. Figure 3(c) reveals the multilayered cuticle layers were also estimated. They are summarized in arrangement of the cuticles, which are spaced out with a thin Table 1. air gap. Figure 3(d) shows how the cuticle layers terminate The highly tilted, multilayered arrangement in the W2 and at the edge of the scale. They are bent at a right angle B2 scales is very resemble to that in the scales of the male toward the back surface, keeping the strength of the scale, Ancyluris meliboeus Fabricius butterfly (living jewel) found accordingly. by Vukusic et al.3) They addressed that the diffraction Figure 4(a) shows a top view of the cuticles on the ridges component appears to combine additively with the interfer- in a B2 scale. Figures 4(b) and (c) disclose the multilayered ence from the underlying multilayer to produce a broad range arrangement of cuticle. The B2 scales are the same in of coloration, as well as a limited reverse color change with structure as the W2 scales, although they are different in angle compared to that associated with conventional flat color and hue of the iridescence due to melanin pigment multilayering. They illustrated that 30 layer tilt causes a 60 contained. Figure 4(d) illustrates the schematic projections portion of the wing’s ‘observation hemisphere’ not to appear of the ridge with cuticles. In the figure, we take the x-axis iridescent ‘dark zone’. For the present W2 and B2 scales, along the rides run the length of the scale from the root, however, the tilt angle of cuticles layers was estimated to the z-axis normal to the surface of the scale and the be B ¼8 . Therefore, the dark zone where the mirror 206 J. Mateˇjkova´-Plsˇkova´, D. Jancˇik, M. Masˇlańˇ, S. Shiojiri and M. Shiojiri

Fig. 5 (a) Bright and dark zone for the observation of the iridescence. nG is the normal of the grating or surface of the scales and nS is the normal of cuticle surface tilted at B ¼8 . (b and c) Photograph of the hindwing of a male S. charonda butterfly, taken at a low glancing angle under sunlight and at a high glancing angle under a fluorescent light, respectively. reflection does not occur by any incident light is within grooves. We, however, observed sometimes the background 2B ¼16 , as shown in Fig. 5(a). In fact, when we shining in green under a fluorescent light, as shown in observed the wing at a glancing angle smaller than 16, the Fig. 6(b), which is a result of significant diffraction by the purple-blue area appeared dark without hue of iridescence, grating. as seen in Fig. 5(b). However, since this dark zone is quite The reflection of the incident light from the scales is narrow the male butterflies can always display the bright complicated due to the three-dimensional gratings. The light wings characteristic of them. reflects on the upper and bottom surfaces of each cuticle SEM images of B1 scales are shown in Fig. 6. Figures 6(a) layer, propagating the layer and air gap. These multiple and 6(b) indicate the front and the back of the scales. The reflected rays interfere with each other and consequently back is covered with a thin layer, exposing the ends of the generate the hue of iridescence. Besides the dark zone cuticles around the edge, which is supposed in Fig. 3(d). mentioned above, we here touch upon another effect caused Figures 6(c) and (d) reveal a grating of the ridges on which by the highly tilted, multilayered arrangement in W2 and B2 only two cuticle layers are piled. The grating parameters scales. The top surface of the ridge, schematically shown in estimated from SEM images are tabulated in Table 1. It was Fig. 4(d), may constitute a blazed grating with a saw-tooth also confirmed that those values are common among the B1, profile. The blazed diffraction gratings were designed to W1 and R1 scales. The difference may be ascribed to the obtain high diffraction efficiency for certain order m and species and quantity of the contained melanin; perhaps a wavelength .13) When the incident light and the m-th order brown-black dihydroxyindole eumelanin and a red-brown of diffracted light are related by mirror reflection with each benzothiazine pheomelanin. other on the facet surfaces as indicated in Fig. 5(a), most Thus, it is revealed that the wings of the male S. charonda of the incident energy is concentrated into the m-th order butterfly have two kinds of scales with three-dimensional diffracted light. This satisfies ¼ð2D=mÞ sin B cosð BÞ, grating. Each grating is composed of the grid of the ridges where D is the spacing or the grating period and is the with the spacing d in the y direction, the arrangement incident light angle made with the normal to the grating. B is of cuticles spaced out by D in the x direction, and the called blaze angle. The wavelength for m ¼ 1 and ¼ B, multilayered arrangement of cuticles with air gaps nearly in where the 1st-order diffracted light returns along the same the z-axis. In the grating with the spacing of d, the surfaces path as the incident light, is called the blaze wavelength B of the ridges with the width of d1 contribute effectively to and B ¼ 2D sin B. The blaze wavelength represents the the reflection of light, and d2 is the width of the grooves not blaze characteristics of the grating. For the W2 and B2 to contribute to the reflection intensity. The ratio of d1=d2 scales with B ¼8 and D ¼1:0 mm, the blazed wave- for the grating in the B1, W1 and R1 scales is 0:4 which length is estimated to be B ¼280 nm. This means the is much smaller than the ratio of d1=d2 ¼ 2 for grating in relative high efficiency is expected for shorter wavelength. the B2 and W2 scales. This is a reason why the iridescence Incidentally, the brazed diffraction gratings with B ¼ hardly occurs on the brown background, yellow spots and 300 nm are commercially recommended for monochro- red spot in the wing, while the vivid iridescence appears on mators and spectrographs used in an optimum range of the purple-blue and white-pearl areas. The color of the B1, operation of 200 nm450 nm. Thus, the vivid purple-blue W1 and R1 scales may come from simple absorption and iridescence on the male butterfly wing can be ascribed scattering of the light by the scales and substance in the to this wavelength-selective reflection of the light on the Photonic Crystal Structure of Wing Scales in Sasakia Charonda Butterflies 207

Fig. 6 SEM images of B1 scales separated from the wing. (a) The fronts of scales where the ridges can be seen. (b) The back of a scale, which is covered with a thin layer. (c) The top surfaces of cuticle layers on the ridges. (d) The side surfaces of the cuticles on the ridges. surfaces of the piled semi-transparent cuticles layers. Light areas, and the other is in W1, R1 and B1 scales at yellow absorption of melanin in the cuticles may also complement spots, red spots and brown background. The difference the exposure of purple-blue. The revealed photonic structure between the W, B and R scales is ascribed to species and of the butterfly scales, thus, give us a very helpful hint quantity of contained melanin. The W2 and B2 scales have to manipulate light in photoelectric devices such as blue seven wide cuticle layers lapped on the ridges, while the or UV light emitting diodes, fabricated particularly by W1, R1 and B1 scales have only two narrow cuticle layers. ALD.11,12) The vivid iridescence from the W2 and B2 scales, which The B1, W1, and R1 scales have only two cuticles piled is characteristic of the male butterflies, is attributed to the on the narrow ridge so that the reflected light is too weak interference of incident light reflected by the grating in to exhibit any iridescent hue on these areas. Rather, the these scales. The grating in the scales looks like a blazed incident light, particularly UV radiation may be absorbed diffraction grating with the blaze angle of B. The blazed and converted to heat energy by melanin. The female grating with observed tilting angle B and spacing D in the butterflies have bigger brown wings without iridescent scales has high efficiency in a shorter wave length range of scales which significantly reduce the penetration of light 200 nm450 nm, which may be the origin of purple-blue due to the reflection. The females thereby can get more iridescence wing together with adsorption in melanin. The heat energy, to be used for breeding, from sunshine than the B1 scales do not reflect much light but rather may absorb male butterflies. Thus, the wing structure of the butterflies to convert it to heat energy due to melanin. Hence, the may give us another suggestion which is a hint to design photonic and photochemical structures of the wing scales in photochemical crystal devices for internal conversion or the S. charonda would be applicable to fine light elements radiationless de-excitation where the UV radiation is trans- in the photo-electro devices especially in blue, purple, and formed into heat. ultraviolet regions.

4. Conclusion Acknowledgements

The wing scales of the male S. charonda have been We thank Professor H. Saijo, Kinki University, for useful observed by FE-SEM. The scales form a three-dimensional discussion with him about the blazed diffraction grating. The optical diffraction grating, which is composed of the grid of present paper would be dedicated to the memory of Prof. the ridges with the spacing d, the multilayered arrangement Rudolf Autrata, Institute of Scientific Instruments of the of cuticles lapped on the ridge, and the surface arrangement ASCR, v.v.i., Academy of Sciences of the Czech Republic, of cuticles tilted at B and spaced by D. Two kinds of three- who passed away on January 12, 2006. Our successive and dimensional diffraction gratings are recognized; one is in successful scientific collaboration are thanks to the late Prof. W2 and B2 scales at iridescent white-pearl and purple-blue Autrata. 208 J. Mateˇjkova´-Plsˇkova´, D. Jancˇik, M. Masˇlańˇ, S. Shiojiri and M. Shiojiri

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