High light absorption properties and optical structures in butterfly Heliophorus ila Lvcaenidae wing scales

Abstract

When the sunlight irradiates the surface of butterfly wings, it can be absorbed by the microstructures in the wings scales and converted into heat to maintain the butterfly’s metabolism. This phenomenon is an inspiration which is facilitating the scientific research in solar energy utilization. In this study, the absorption characteristics of seven species of butterfly were investigated using a spectrometer. It was found that the butterfly Heliophorus ila Lvcaenidae showed more efficient absorption capability (absorptivity was about at 85%) compared with other species in the wavelength range from 230 nm to 850 nm. Then, the morphology and structures of the butterfly Heliophorus ila Lvcaenidae wing scales were examined by Scanning Electron Microscope (SEM) and Transmission Electron Microscope (TEM). The results showed that there were two kinds of scales distributed on the wing surface of the butterfly Heliophorus ila Lvcaenidae. Finally, the optical mechanisms were revealed by theories of multiple reflection and resonance. It was confirmed that the hierarchical hollow nano-architectures of the scales were responsible for the high-efficiency absorption behaviour. This study could be used as a theoretical reference for subsequent bionic design of structural materials for solar energy utilization.

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1. Introduction

As a typical hotspot in the bionics field recently, butterfly wings are endowed with a diverse set of excellent properties.¹ In recent years, scholars have done a lot of research on the species, warning colorations and scales microstructure.^2–4 The organized distribution of the scales can be observed under quite low magnification. These scales are composed of a chitin materials.⁵ Due to different optical effects, for example anti-reflection, diffraction, light scattering as photonic crystal structure,^6–11 scales appear in many colors which can be employed for signal transmission, mimicry, alerting and other purposes.^12–14 In terms of applications, bionic products originated from butterfly have been used on various occasions. For example, the polarization-sensitive characteristic inspired by butterfly structural colors can be used for anti-counterfeiting and decoration techniques.¹⁵ By simulating scales optical characteristics in a different spectrum, stealth skills^16–18 and thermal or gas sensors were developed.^19,20 Super black carbon films were manufactured by imitating scales microstructure.^21,22 Also, the butterflies scales have been adopted as templates for fabricating light trapping specimen^23,24 and other special function devices^25–28 by scholars all over the world.

Recent studies showed that there were certain species appearing in very early spring (April or May) at high altitude mountainous areas, where energy was used to protect their body from cold climate, which depended on the efficient sunlight absorption of their wing surface scales (Fig. 1). In addition, during the breeding season, more energy was needed to gestate eggs, while the energy could not be provided by their body due to the decline of its mobility. Therefore, more solar energy should be obtained for energy demand during this period. The efficient absorption relied on not only the arrangement format, but also mainly the delicate nano-architecture inner scales.

Fig. 1 Image of butterfly Heliophorus ila Lvcaenidae and distribution of the scales on its wing surface.

In this work, a spectrometer was employed to test optical characteristics of 7 kinds of butterflies. The results illustrated that the butterfly Heliophorus ila Lvcaenidae scales had the best sunlight absorbing effect with absorptivity reaching up to 85%. The microstructures of butterfly Heliophorus ila Lvcaenidae scales were studied with SEM and TEM and simplified models were then built up. The cross section image of butterfly Heliophorus ila Lvcaenidae scales had two hierarchies of microstructures. The upper part had a hollow trianglar form that resulted in multiple reflections and refractions. The bottom hollow layer formed a rectangular resonant cavity model which had light trapping effect. The solar energy was absorbed efficiently due to the integrated function of these two mechanisms. This study demonstrated an enlightening way to exploit bionic designing of structural materials for solar heat utilization.

2. Materials and methods

2.1 Spectrometer

Seven species of butterfly were studied: Papilio machaon, Parnassius stubbendorfii, Papilio maackii, Brenthis daphne, Apatura ilia, Heliophorus ila Lvcaenidae and Troides brookiana.

Test specimens were taken from single pure color areas of abdomen wings and with complete scales to avoid influence on the optical measurements by any eyespot or other colors. Tests were carried out under the same conditions: trial wavelength range within 230–800 nm with 0° incident angle. Reference light with an incident angle of 8°. The temperature of the laboratory was at 15–30 °C. Relative humidity was less than 65%. Finally, the absorption curves were obtained and the scales with best absorption effect were selected to be examined further.

2.2 SEM observation

Specimens for SEM were taken from the butterfly Heliophorus ila Lvcaenidae, which showed the lowest reflectivity. The first step was a degreasing process: Specimens were rinsed in normal saline solution (0.65% NaCl) and ether for 10 min respectively to get rid of mucus, fat and protein. The second step was dehydration: The degreased specimens were immersed into a series of ethanol solutions with concentrations of 40%, 50%, 70% and finally pure ethanol, 10 min in each solution before natural dehydration. The third step was to paste samples on a metallic substrate with double-sided conductive tape, making sure not to damage the specimens surface during the whole process. The final step was sputtering: all specimens were sputtered with 15–20 nm gold powder within 40° rotating angle and examined under field emission scanning electron microscope (FESEM; FEI SIRION 200).

2.3 TEM observation

TEM photos were taken with a JEOL-100 microscope system. The specimens were also taken from wings of the butterfly Heliophorus ila Lvcaenidae dorsal. The specimens were prepared by the following steps: (1) immersed in 4% glutaraldehyde for 2 hours to avoid structure change following evaporation of water; (2) placed in sodium cacodylate buffer solution for 1.5 hours; (3) kept in 1% osmic acid for 1.5 hours and dehydrated with ethanol; (4) embedded in epoxy resin, and solidified for 4 hours with an oven; (5) sliced into lamellas with thickness of 70 nm.

3. Results and discussion

3.1 Spectrometer results

Reflectivity curves of all samples are shown in Fig. 2. The wavelengths ranged from 230 nm to 850 nm and the y-axis shows the reflectivity (R%).

Fig. 2 Spectral curves of several butterfly wings. (a) I Butterfly Papilio maackii shining area, II butterfly Parnassius stubbendorfii, III butterfly Papilio machaon, IV butterfly Heliophorus ila Lvcaenidae. (b) V butterfly Apatura ilia, VI butterfly Brenthis daphne, VII butterfly Troides brookiana, VIII butterfly Papilio maackii black area.

Three optical effects may occur when light reaches the wing surface, namely, reflection, transmission and absorption. The sum of the three portions of light should be 100% as shown in eqn (1). When the transmission was at a certain level, a lower reflectivity means a higher absorptivity. The absorption capacity could be evaluated by calculating the absorptivity based on the formula.

Reflectivity (R%) + Absorbtivity (A%) + Transmissivity (T%) = 100% (1)

For clear comparison, the curves were displayed in Fig. 2a and b separately. In the full trial spectrum, Papilio maackii shining area and Apatura ilia exhibited higher reflectance, shown as Fig. 2-I and V. This meant their absorptivities were lower. Furthermore, these two curves demonstrated steady tendency and had not any peak value within the whole spectrum. Reflectivity of Papilio machaon, Parnassius stubbendorfii, Brenthis daphne, Troides brookiana increased with wavelength obviously, shown as Fig. 2-II, III, VI and VII. The reflectivity value reached its highest point in the red spectrum. Butterfly Heliophorus ila Lvcaenidae (Fig. 2-IV) had the lowest reflectivity among all the samples. The minimal value plunged to 15%. It meant the absorptivity of butterfly Heliophorus ila Lvcaenidae could be as much as 85%. Furthermore, its absorptivity almost remained at a constant level within the entire trial spectrum without any obvious peak.

The reflectivity of the black area of butterfly Papilio maackii (Fig. 2-VIII) reached 50%, which was higher than that of butterfly Heliophorus ila Lvcaenidae and a spectral peak emerged at 650 nm. After the primary optical testes and analysis, butterfly Heliophorus ila Lvcaenidae scales were selected to be further observed at a micro level with SEM and TEM.

3.2 SEM and TEM results

The overlapping arrangement and morphology of scales could be observed at lower magnification, shown in Fig. 3a. Scales imbricated on the wing surface. There were two types of scales on butterfly Heliophorus ila Lvcaenidae wing surfaces. The cover ones (type 1) had regular through-holes structure, through which the incident light passed directly and shone on the ground ones (type 2). The type 2 scales could be observed quite clearly although they hid under the cover ones. This confirmed the existence of through-holes of type 1 scales further.

More micro details of a single scale were obtained at higher magnification. Shown in Fig. 3b, there were parallel ridges distributing from front to end on every scale. There were also many short ribs (the length varied at 100–200 μm) connecting each two adjacent ridges. The distances between each two ribs were almost same, and therefore some rectangular lattices were formed which looked like thousands of windows. The regular through-holes structures of the cover scales (type 1 scales) in this manuscript could scatter the incident light, resulting in more and more incident light irradiating on the surface of the ground scales (type 2 scales). Finally, most of the light energy could be absorbed by the ground scales. The role of the cover scales (type 1 scales) was mainly diffracting light. So, they were largely conducive to absorption instead of direct absorption. There were other kinds of disordered nano-hole structure like this were also found in other butterflies.^29,30

Fig. 3 Images of SEM and TEM. (a) Images of two kinds of scales. The cover ones were type 1 and the ground ones were type 2. (b) Holes in type 1 scales surface. The ridges together with ribs formed holes which the incident light could pass through. (c) Morphology of type 2 scales, where ridges occupied a large proportion of the lit area. (d) Cross section image of type 2 scales. Type 2 scales were cut down along the arrows direction in order to obtain the cross section details.

Details of type 2 scales also had ridges (Fig. 3c). However, the difference was that the ridges were more densely distributed and had a greater width. Spacing between two ridges was about 0.5–0.8 μm. Therefore, ridges occupied a larger proportion of the lit area and played a main role in sunlight absorption.

Therefore, even though there were two kinds of scales on butterfly Heliophorus ila Lvcaenidae wings, the upper scales had a holes structure and rarely absorb sunlight. The underlying scales with ridges have absorption capability.

3.3 Optical mechanism analysis

Based on the TEM image of a cross section, the optical model of type 2 scales of butterfly Heliophorus ila Lvcaenidae were divided into two parts, and the different optical effects of each part were discussed (Fig. 3d). The simplified model was built as shown in Fig. 4.

Fig. 4 Microstructure model of scales with absorption function. (a) TEM image of scale microstructure. (b) 3D simplified model.

3.3.1 Multiple reflection and refraction. The upper part was shown in Fig. 5. When sunlight travelled through air (refractive index n₁) to scale chitin material (refractive index n₂) which constitutes original butterfly wing,^31,32 reflection and refraction would happen on the interface at the same time. Some conclusions can be obtained according to geometrical optics principles: (1) the refraction light exists in the plane of incident light and interface normal; (2) refraction and incident light are separated at each side of the normal; (3) the incidence angle α and refraction angle γ accords with the law as eqn (2).

n₁ sin α = n₂ sin γ (2)

Fig. 5 Schematic of the multiple reflection and refraction occurred on the upper part of the structures of the scale surface.

In this case, n₂ > n₁. So, γ < α. The refraction light travelled across the materials and entered into the hollow zone. Then, refraction and reflection occurred at any interface. After multiple reflections and refractions, light travelled for a longer distance, and only a small part of light was reflected back to the air, resulting in most of the incident light being effectively adsorbed within the structure eventually.

3.3.2 Optical resonator effect of bottom part. The resonant cavity was made up of two parallel planes. The light was trapped in this cavity by being reflected back and forth (Fig. 6). In an ideal resonant cavity, any electromagnetic disturbance behavior would not stop. The electro-magnetic field was calculated by solving Maxwell’s equations according to the boundary conditions. The electromagnetic field was considered as a wave bouncing back and forth between cavity walls and resulting in a standing wave field.

Fig. 6 Schematic of the light absorption occurred on the bottom part of the structures of the scale surface.

In this case, the bottom part of the scales could be optimized as a rectangular cavity of six planes as shown in Fig. 6. The coordinates of the inner surface are shown as eqn (3).

The electric field of the electromagnetic wave inside the cavity is E and magnetic field is H. Any rectangular components of E and H should meet the Helmholtz equation. For any component of u(x,y,z), there was ∇²u + k²u = 0,³³ based on separation of variables method. If it is supposed that u(x,y,z) = X(x)Y(y)Z(z), then

k_x² + k_y² + k_z² = ω²με (5)

So, the result of u(x,y,z) was

u(x,y,z,) = (C₁ cos k_xx + D₁ sin k_xx)(C₂ cos k_∂yy + D₂ sin k_yy)(C₃ cos k_zz + D₃ sin k_zz) (6)

Established boundary conditions were n⇀ × E⇀ = 0,∂E_n/∂_n = 0 and x = 0, y = 0, z = 0. The arbitrary constant C_i and D_i can be defined, and as a result u(x,y,z) can be specified as a component of E⇀.

In terms of boundary conditions on planes of x = L₁, y = L₂, z = L₃, it is true that k_xL₁, k_yL₂, k_zL₃ must be an integer times π, namely

In eqn (8), m, n, p represent numbers of half-wave contained in each rectangle side.

After substituting eqn (7) into ∇E⃑ = 0, the three arbitrary constants A₁, A₂, A₃ must fit the relation shown in eqn (9).

k_xA₁ + k_yA₂ + k_zA₃ = 0 (9)

It can be concluded from eqn (9) that two out of the constants A₁, A₂, A₃ were independent. After satisfying eqn (8) and (9), eqn (7) could be considered as one sort of region oscillation of the electromagnetic field inside the rectangular hollow structure.

For each group of m, n, p, there are two independent polarized wave modes, and the resonant frequency ω can be obtained from eqn (5) and (10).

ω_mnp is the resonant frequency of resonant cavity. The resonance oscillation mode of lowest frequency was wave (1,1,0) with wavelength λ shown by eqn (11).

Above was the ideal mode of resonant cavity. In this study, of the butterfly Heliophorus ila Lvcaenidae, the scale material consisted of a rectangular cavity. L₁ = 580 nm, L₂ = 130 nm, L₃ ≫ L₁, L₂, the materials had a certain energy consumption. The light wave bounced back and forth on the cavity wall. In this process, a portion of light was consumed and absorbed by the materials. Certain light with wavelength λ₁₁₀ was strengthened and reflected back to the air from certain flaws position and produced the wings structural color of butterfly Heliophorus ila Lvcaenidae. In this case, the calculation result was λ₁₁₀ = 253.7 nm, that is why there was an non-obvious peak nearby 250 nm spectrum region of curve-IV in Fig. 2a.

4. Conclusions

In this study, the absorption efficiency of seven species of butterflies was tested. It was found that the wings of butterfly Heliophorus ila Lvcaenidae had the highest absorption capability (with absorptivity of 85%) among all samples in spectrum 230–850 nm.

SEM results showed that butterfly Heliophorus ila Lvcaenidae had two kinds of scales. Sunlight passed through the holes in the scales on the surface and irradiated on the underlying scales. The underlying scales played a main role in the absorbing behavior.

TEM analysis illustrated the cross section microstructure of scales type 2. There were two parts of optical delicate nano-architectures. The top part was simplified to a hollow triangle model. Sunlight was repeatedly reflected and refracted on the slope surface. In this way, the light travelled a longer path length in the scale materials. Therefore, more energy was consumed. The bottom part was simplified to a rectanglar resonator model. Incident light was reflected back and forth repeatedly. Energy was absorbed gradually and saved during this endless reflecting process. Only light with wavelength λ₁₁₀ = 250 nm could be reflected out to show the structural color of butterfly Heliophorus ila Lvcaenidae.

This study focuses on the absorption mechanisms for the inner microstructures of the scales. The contents of this paper have an important reference value for solar heat utilization research via bionic design.

Acknowledgements

This work was supported by funds of the Specialized Research Fund for the Doctoral Program of Higher Education. (no. 20102103120012), the National Natural Science Foundation of China (no. 51305282, 51175220, 51325501, 51290292) and Postdoctoral Science Foundation of China (no. 2015M571360).

References

1. S. C. Niu, B. Li, Z. Z. Mu, M. Yang, J. Q. Zhang, Z. W. Han and L. Q. Ren, Journal of Bionic Engineering, 2015, 12, 170–189.
2. S. Zhan, W. Zhang, K. Niitepold, J. Hsu, J. F. Haeger, M. P. Zalucki, S. Altizer, J. C. de Roode, S. M. Reppert and M. R. Kronforst, Nature, 2014, 514, 317–321.
3. X. S. Li, Y. L. Zhang, J. H. Fang, O. Schweiger and J. Settele, Journal of Insect Conservation, 2011, 15, 617–632.
4. K. Kertesz, G. Piszter, E. Jakab, Z. Balint, Z. Vertesy and L. P. Biro, Appl. Surf. Sci., 2013, 281, 49–53.
5. K. L. Yu, S. Lou, J. Ding, D. Zhang, Q. X. Guob and T. X. Fan, Soft Matter, 2013, 9, 2614–2620.
6. R. H. Siddique, S. Diewald, J. Leuthold and H. Holscher, Opt. Express, 2013, 21, 14351–14361.
7. V. Saranathan, C. O. Osuji, S. G. J. Mochrie, H. Noh, S. Narayanan, A. Sandy, E. R. Dufresne and R. O. Prum, Proc. Natl. Acad. Sci. U. S. A., 2010, 107, 11676–11681.
8. C. Mille, E. C. Tyrode and R. W. Corkery, Chem. Commun., 2011, 47, 9873–9875.
9. L. Y. Wu, Z. W. Han, Y. Q. Song, S. C. Niu and L. Q. Ren, Chin. Sci. Bull., 2012, 57, 4525–4528.
10. J. Han, H. L. Su, D. Zhang, J. J. Chen and Z. X. Chen, J. Mater. Chem., 2009, 19, 8741–8746.
11. C. Mille, E. C. Tyrode and R. W. Corkery, RSC Adv., 2013, 3, 3109–3117.
12. A. Sweeney, C. Jiggins and S. Johnsen, Nature, 2003, 423, 31–32.
13. K. Kunte, W. Zhang, A. Tenger-Trolander, D. H. Palmer, A. Martin, R. D. Reed, S. P. Mullen and M. R. Kronforst, Nature, 2014, 507, 229–242.
14. Y. M. Zheng, X. F. Gao and L. Jiang, Soft Matter, 2007, 3, 178–182.
15. K. Zhang, Y. W. Tang, J. S. Meng, G. Wang, H. Zhou, T. X. Fan and D. Zhang, Opt. Express, 2014, 22, 27437–27450.
16. Z. W. Han, S. C. Niu, L. F. Zhang, Z. N. Liu and L. Q. Ren, Journal of Bionic Engineering, 2013, 10, 162–169.
17. Z. W. Han, S. C. Niu, C. H. Shang, Z. N. Liu and L. Q. Ren, Nanoscale, 2012, 4, 2879–2883.
18. Z. W. Han, S. C. Niu, M. Yang, Z. Z. Mu, B. Li, J. Q. Zhang, J. F. Ye and L. Q. Ren, RSC Adv., 2014, 4, 45214–45219.
19. A. D. Pris, Y. Utturkar, C. Surman, W. G. Morris, A. Vert, S. Zalyubovskiy, T. Deng, H. T. Ghiradella and R. A. Potyrailo, Nat. Photonics, 2012, 6, 195–200.
20. T. Jiang, Z. C. Peng, W. J. Wu, T. L. Shi and G. L. Liao, Sens. Actuators, A, 2014, 213, 63–69.
21. Q. B. Zhao, T. X. Fan, J. A. Ding, D. Zhang, Q. X. Guo and M. Kamada, Carbon, 2011, 49, 877–883.
22. Z. Jaksic, D. Pantelic, M. Sarajlic, S. Savic-Sevic, J. Matovic, B. Jelenkovic, D. Vasiljevic-Radovic, S. Curcic, S. Vukovic, V. Pavlovic, J. Buha, V. Lackovic, M. Labudovic-Borovic and B. Curcic, Opt. Mater., 2013, 35, 1869–1875.
23. Z. W. Han, S. C. Niu, M. Yang, J. Q. Zhang, W. Yin and L. Q. Ren, Nanoscale, 2013, 5, 8500–8506.
24. Z. W. Han, S. C. Niu, W. Li and L. Q. Ren, Appl. Phys. Lett., 2013, 102, 233702.
25. H. Mei, D. Luo, P. Guo, C. Song, C. C. Liu, Y. M. Zheng and L. Jiang, Soft Matter, 2011, 7, 10569–10573.
26. J. Tang, S. M. Zhu, Z. X. Chen, C. L. Feng, Y. J. Shen, F. Yao, D. Zhang, W. J. Moon and D. M. Song, Mater. Chem. Phys., 2012, 131, 706–713.
27. S. H. Kang, T. Y. Tai and T. H. Fang, Curr. Appl. Phys., 2010, 10, 625–630.
28. F. Liu, Y. P. Liu, L. Huang, X. H. Hu, B. Q. Dong, W. Z. Shi, Y. Q. Xie and X. A. Ye, Opt. Commun., 2011, 284, 2376–2381.
29. P. Vukusic, J. R. Sambles and C. R. Lawrence, Proc. R. Soc. B, 2004, 271, S237–S239.
30. W. Wang, W. Zhang, X. Fang, Y. Huang, Q. Liu, M. Bai and D. Zhang, Opt. Lett., 2014, 39, 4208–4211.
31. L. Ding, H. Zhou, S. Lou, J. Ding, D. Zhang, H. X. Zhu and T. X. Fan, Int. J. Hydrogen Energy, 2013, 38, 8244–8253.
32. H. L. Leertouwer, B. D. Wilts and D. G. Stavenga, Opt. Express, 2011, 19, 24061–24066.
33. J. J. Mao, Y. Liu and J. Q. Zhu, Fundamentals for Electromagnetic Fields & Micro-Wave Engineering, Publishing House of Electronics Industry, Beijing, 2004, pp. 179–182, (in Chinese).

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