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| EXPLORING THE INTERFACE OF LIGHT AND BIOMEDICINE

  • Editor: Gregory W. Faris
  • Vol. 4, Iss. 10 — Oct. 2, 2009
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Structural color change in longhorn beetles Tmesisternus isabellae

F. Liu, B. Q. Dong, X. H. Liu, Y. M. Zheng, and J. Zi  »View Author Affiliations


Optics Express, Vol. 17, Issue 18, pp. 16183-16191 (2009)
http://dx.doi.org/10.1364/OE.17.016183


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Abstract

The elytra of longhorn beetles Tmesisternus isabellae show iridescent golden coloration which stems from long and flat scales imbricated densely on the elytral surface. The scales are able to change coloration from golden in the dry state to red in the wet state with water absorption. Structural characterizations revealed that the iridescent coloration of scales originates from a multilayer in the scale interior. Measurements on both water contact angle and chemical composition indicated that scales are hydrophilic. The change in scale coloration to red in the wet state is due to both the swelling of the multilayer period and water infiltration. The unraveled structural color change and its strategy may not only help us get insight into the biological functionality of structural coloration but also inspire the designs of artificial photonic devices.

© 2009 Optical Society of America

1. Introduction

In the biological world, many animals including amphibians [1

1. A. Rowlands, “The influence of water and light upon the color change of sightless frogs (Rana temporaria),” J. Exp. Biol. 1, 127–136 (1952).

, 2

2. G. J. Tattersall, P. C. Eterovick, and D. V. de Andrade, “Tribute to R. G. Boutilier: skin colour and body temperature changes in basking Bokermannohyla alvarengai (Bokermann 1956),” J. Exp. Biol. 209, 1185–1196 (2006). [PubMed]

], insects [3

3. N. F. Hadley, “Wax secretion and color phases of the desert Tenebrionid beetle Cryptoglossa verrucosa (LeConte),” Science 203, 367–369 (1979). [PubMed]

11

11. J. P. Vigneron, J. M. Pasteels, D. M. Windsor, Z. Vértesy, M. Rassart, T. Seldrum, J. Dumont, O. Deparis, V. Lousse, L. P. Biró, D. Ertz, and V. Welch, “Switchable reflector in the Panamanian tortoise beetle Charidotella egregia (Chrysomelidae: Cassidinae),” Phys. Rev. E. 76, 031907 (2007).

] and aquatic animals [12

12. R. T. Hanlon, K. M. Cooper, B. U. Budelmann, and T. C. Pappas, “Physiological color change in squid iridophores I. Behavior, morphology and pharmacology in Lolliguncula brevis,” Cell Tissue Res. 259, 3–14 (1990). [PubMed]

18

18. L. M. Mäthger, M. F. Land, U. E. Siebeck, and N. J. Marshall, “Rapid colour changes in multilayer reflecting stripes in the paradise whiptail, Pentapodus paradiseus,” J. Exp. Biol. 206, 3607–3613 (2003). [PubMed]

] can change their coloration in response to environmental stimuli. The adaptive values of color change are usually regarded as camouflage, signal communication, conspecific recognition, and reproductive behavior.

There are mainly two ways of coloration in the biological world: one is pigmentary color produced by the selective absorption of natural light and the other is structural color produced by the interactions of natural light with microstructures [19

19. A. R. Parker, “515 million years of structural colour,” J. Opt. A: Pure Appl. Opt. 2, R15–R28 (2000).

22

22. R. O. Prum, “Anatomy, physics and evolution of avian structural colours,” in Bird coloration, vol. I: mechanisms and measurements, edited by G. E. Hill and K. J. McGraw (Harvard University Press, Boston, 2006), pp. 295–353.

]. Thus, color change can occur via the change in pigment, microstructure, or their combination. Color change in most chameleons is due to pigment [23

23. P. de Grijs, “Notes on the faculty of changing colour in reptiles,” Ann. Mag. Nat. Hist. 3, 396–402 (1899).

]. The migrations and volumes change of pigment granules in the iris cells lead to reversible color change. An example of color change via microstructure is the blue damselfish Chrysiptera cyanea [24

24. H. Kasukawa, N. Oshima, and R. Fujii, “Control of chromatophore movements in dermal chromatic units of blue damselfish-II. The motile iridophore,” Comp. Biochem. Physiol. C 83, 1–7 (1986). [PubMed]

26

26. N. Oshima and R. Fujii, “Mobile mechanisms of blue damselfish (Chrysiptera cyanea) iridophores,” Cell Motil. Cytoskel. 8, 85–90 (1987).

]. It normally displays a characteristic blue color, produced by reflecting plates that make up the iridophores in the skin. During stressful conditions, the fish can change its blue coloration rapidly to ultraviolet. This color change is triggered by the simultaneous change in the spacing of adjoining reflecting plates. Tortoise beetles Charidotella egregia [10

10. P. Jolivet“Phsiological colour changes in tortoise beetles,”in Novel aspect of the biology of Chrysomelidae, P. Jolivet, edited by M. L. Cox and E. Petitpierre (Kluwer Academic, Netherland, 1994), pp. 331–335.

, 11

11. J. P. Vigneron, J. M. Pasteels, D. M. Windsor, Z. Vértesy, M. Rassart, T. Seldrum, J. Dumont, O. Deparis, V. Lousse, L. P. Biró, D. Ertz, and V. Welch, “Switchable reflector in the Panamanian tortoise beetle Charidotella egregia (Chrysomelidae: Cassidinae),” Phys. Rev. E. 76, 031907 (2007).

] possess a chirped multilayer in the cuticle and a pigmented red layer underneath. The presence of humidity in the porous patches within each layer makes the multilayer reflector in a perfect coherent state, resulting in golden coloration. When disturbed by stressful external events, liquid is expelled from the porous patches, turning the multilayer into a translucent slab and leaving an unobstructed view of the red pigmented layer. Hercules beetles Dynastes hercules [8

8. H. E. Hinton and G. M. Jarman, “Physiological colour change in the Hercules Beetle,” Nature 238, 160–161 (1972).

, 9

9. H. E. Hinton and G. M. Jarman, “Physiological colour changes in the elytra of the Hercules beetles, Dynastes hercules,” J. Insect Physiol. 19, 533–549 (1973).

] and beetles Coptocycla [27

27. C. W. Mason, “Transient color changes in the tortoise beetles (Coleoptera: Chrysomelidae),” Entomol. News 45, 52–56 (1929).

] can alter their coloration by varying the amount of water in the cuticle and thereby the physical characteristics of the thin films responsible for the interference color. Desert beetles Cryptoglossa verrucosa [3

3. N. F. Hadley, “Wax secretion and color phases of the desert Tenebrionid beetle Cryptoglossa verrucosa (LeConte),” Science 203, 367–369 (1979). [PubMed]

, 4

4. E. McClain, M. K. Seely, N. F. Hadley, and V. Gray, “Wax blooms in Tenebrionid beetles of the Namib desert: correlations with environment,” Ecology 66, 112–118 (1985).

] exhibit distinct colors from bluish-white to black in response to humidity, functionally in order to prevent water from evaporating.

In this paper, we studied the structural and optical properties of the elytra of beetles Tmesisternus isabellae. The elytral golden color is produced by a multilayer in scales which are densely imbricated on the elytra. This structural golden color can change to red in the dry state which is due to the water infiltration and swelling of the period of the multilayer.

2. Materials and Methods

Beetles Tmesisternus isabellae belong to a large family of longhorn beetles and live endemically in the tropical rainforests in Birdshead Peninsula of West Peninsula, Indonesia. Samples under study were obtained from the Shanghai Natural Museum, Shanghai, China. Beetles were observed and recorded using a digital camera (7.2 mega pixels, DSC-WS80, Sony, Japan). The microscopic images of elytra were observed and recorded using a LYNX stereo inspection optical microscope (Vision Engineering Co., UK) which is connected to a CCD camera and a desktop computer, under 80× magnifications.

The microstructures of scales were characterized by a scanning electron microscope (SEM) (Philips XL30 FEG, Philips, NL) and a transmission electron microscope (TEM) (JEM-1230, JEOL, Japan) after elytra were prepared following the similar methods of [28

28. M. D. Shawkey, A. M. Estes, L. M. Siefferman, and G. E. Hill, “Nanostructure predicts intraspecific variation in ultraviolet-blue plumage colour,” Proc. R. Soc. Lond. B 270, 1455–1460 (2003).

]. The change in the microstructures of scales in the wet state was observed using an environmental scanning electron microscope (ESEM) (Quanta 200 FEG, FEI Co., OR, USA).

Reflection spectra of elytra were measured by a micro-spectra analysis equipment which consists of a tungsten lamp light source, a microscope (Leica DM6000 M, Germany) with objective 10×, NA 0.3 and an optic spectrometer (range 200–1000 nm, SpectraPro 500i, Acton Research Co., USA). In our spectral measurements, a circular diaphragm with a diameter of 0.5 mm was used to create a narrow aperture that can enable measurements under nearly normal incidence (about 3 degrees). A broadband aluminium flat mirror standard (PYREX, Newport, USA) was used as the reference.

Fig. 1. Optical images of beetle Tmesisternus isabellae in the (a) dry and (b) wet states. The iridescent golden color in the dry state is able to change to red in the wet state. (c) Close-up image of the golden colored region of elytra in the dry state. In the colored region the elytral surface is densely imbricated with colored scales. (d) Same as (c) but in the wet state. The color of scales becomes red. (e) Underlying elytral surface with scales scrapped off. The darker spots are the stumps of scales and two golden strips on the left side are remaining scales. Scale bars: (a) and (b) 10 mm, (c) and (d) 100 µm, and (e) 50 µm.

Water contact angles of elytra were measured using an OCA20 Contact-Angle System (Data-physics, Germany) at room temperature. The volume of water droplets is about 2 µL. Measured water contact angle can provide qualitative information regarding the hydrophilic or hydrophobic character of a surface. X-ray photoelectron spectroscopy (XPS) data were obtained with an ESCALab220i-XL electron spectrometer (VG Scientific, UK) using 300 W Al-Kα radiation, from which the chemical composition of elytra can be analyzed.

The transfer matrix method [29

29. P. Yeh, Optical waves in layered media (Wiley, New York, 1988).

, 30

30. J. Zi, J. Wan, and C. Zhang, “Large frequency range of negligible transmission in one-dimensional photonic quantum well structures,” Appl. Phys. Lett. 73, 2084–2086 (1998).

] was used for the theoretical analysis of the revealed multilayer structure. Within the framework of the method it is possible to calculate reflectance, transmittance and absorptance of multilayer structures as a function of incident angle and wavelength.

3. Results

3.1. Color observation and spectral analysis

The elytra of beetles Tmesisternus isabellae in the dry state display an iridescent golden color marked with a black band in the middle and an irregular posterior black band [31

31. J. L. Gressitt, Systematics and biogeography of the longicorn beetle tribe tmesisternini (Bishop Museum Press, Honolulu, 1984).

], as shown in Fig. 1(a). With the view angle changing from normal to oblique, the golden colored region alters its coloration to green. This iridescent feature implies that the golden color should have a structural origin. With water dropped onto, the golden colored region can turn into red within a few minutes [Fig. 1(b)] while the black band coloration remains unchanged. The colored region of the elytra recovered to the golden color when the water evaporated and the elytra returned to the dry state. That is to say, the color change from golden in the dry state to red in the wet state is reversible.

Under an optical microscope, the colored region of elytra is composed of long and flat scales, imbricating on the elytral surface, as shown in Fig. 1(c). The iridescent golden color in the dry state is able to change to red in the wet state [Fig. 1(d)]. On the contrary, no scale exists in the black bands. It indicates that the elytra are basically black and the metallic golden color arises completely from the scales which could turn into red after water absorption. This can also be found by scraping off scales: the underlying elytral surface is black. From Fig. 1(e), we can also get the distribution density of scales, about 1500 per mm2.

Fig. 2. Measured reflection spectra of the colored region of elytra in the dry (solid blue line) and fully wet (solid red line) under normal incidence. The spectrum for the redried elytra is shown by a dashed blue line.

In the dry state the measured reflection spectrum of the colored region of elytra is characterized by a broad peak positioned at about 600 nm, displaying a golden color, shown in Fig. 2. In the wet state, however, the reflection peak is shifted to 662 nm, showing a red color. Its intensity undergoes a noticeable drop in wet state with respect to that in the dry state. The reversible color change from the wet to dry state could be observed: the reflection spectrum in the redried state coincides with that in the dry state. The measured reflection peaks are consistent with the color observation by the naked eye.

3.2. Structural characterization

The structures of scales in the dry state were characterized by SEM, shown in Fig. 3. Scales are about 140 µm long, 13 µm wide, and 3 µm thick, and become peaked at the end. From SEM images, the dorsal side of the scales is uneven, marked with a series of grooves. Grooves are not exactly parallel with each other. The spacing between two adjacent grooves is about 900 nm which is too large to produce diffracted colors in the visible range. Closer observations revealed that the groove ridges are further imposed by fine grooves spaced by a distance of about 45 nm. On the contrary, the ventral side of the scales is smooth without any ultrastructure. SEM cross section images revealed a multilayer structure in the interior of the scales, consisting of two alternating layers.

Fig. 3. SEM images of scales. (a) Dorsal side. (b) Ventral side. (c) Transverse cross section of a scale. A multilayer in the interior can be clearly seen. Scale bars: (a) and (b) 5 µm, and (c) 1 µm.
Fig. 4. TEM images of scales. (a) Transverse cross section of a scale. (b) Close-up view of the multilayer. The H and IH layers are labeled by H and IH, respectively. Scale bars: (a) 2 µm and (b) 0.5 µm.

TEM was also employed to get the detailed structural information of the scales, shown in Fig. 4. TEM cross section images support the observations of grooves in the dorsal side and the multilayer structure in the core region. As seen from both SEM and TEM images, the multilayer is composed of two alternating layers. The first one is a homogeneous (H) layer (dark regions) and the second one is an inhomogeneous (IH) layer. The IH layer consists of nanoparticles (grey regions) and air voids (bright regions) which can also be seen in SEM images. The number of periods of a multilayer in different regions is different. In the central region of a scale, it is about 10. By chemical treatments [32

32. T. D. Schultz and M. A. Rankin, “The ultrastructure of the epicuticular interference reflectors of tiger beetles (Cicindela),” J. Exp. Biol. 117, 87–110 (1985).

], we could determine that the constituent of scales might be melanoprotein. The thickness of the H layers is about 105 nm while it is about 70 nm for the IH layers.

3.3. Color change mechanism

In order to get insight into the color change of scales, ESEM was used to measure the change in the microstructure of scales in the wet state, shown in Fig. 5. Scales swell noticeably after water absorption. Close-up images show that both the cortex and the multilayer swell in the wet state. The swelling of both the cortex and multilayer is due to the water absorption by constituent melanoprotein. The period of the multilayer swells from about 175 nm in the dry state to about 190 nm in the fully wet state. From ESEM cross section images we can determine that the thickness of the H layers in the fully wet state swells to about 120 nm while the thickness of the IH layers remains nearly unchanged. The swelling of the period of the multilayer can cause color change from golden in the dry state to red in the wet state. In the wet state, from ESEM images it is hard to determine whether water infiltrates the air voids in the IH layers or not.

Fig. 5. ESEM images of scales. (a) Top view of the dorsal side in the dry state. (b) Top view of the dorsal side of the scale in the fully wet state. Transverse cross sections of the scale in the dry and fully wet states are given in (c) and (d), respectively. Scale bars: (a) and (b) 5 µm, and (c) and (d) 1 µm.
Fig. 6. Measurements of water contact angles for (a) the black band and (b) colored region of the elytra. Scale bars: 0.5 mm.

In order to explore the hydrophilic or hydrophobic character of the elytral surface, we conducted water contact angle measurements, shown in Fig. 6. The measured water contact angle in the colored region of elytra is 29.2° while in the black band region it is 150.7°. The small contact angle in the colored region indicates that scales are hydrophilic which is amiable for water infiltration and absorption. Oppositely, the large contact angle in the black bands implies a superhydrophobic character for the black bands [33

33. Capillarity and wetting phenomena: drops, bubbles, pearls, waves, edited by P.-G. de Gennes, F. Brochard-Wyart, and D. Quéré (Springer, New York, 2004).

].

We also measured the chemical components of both colored and black band regions of the elytra using XPS in order to find the chemical cause of the hydrophilic behavior of the scales. The two regions show similar compositions of carbon, oxygen and nitrogen. However, scales have an additional sodium component which leads to the hydrophilicity of scales [34

34. L. Xu, J. X. Wang, Y. L. Song, and L. Jiang, “Electrically tunable polypyrrole inverse opals with switchable stopband, conductivity, and wettability,” Chem. Mater. 20, 3554–3556 (2008).

, 35

35. L. B. Xu, W. Chen, A. Mulchandani, and Y. S. Yan, “Reversible conversion of conducting polymer films from superhydrophobic to superhydrophilic,” Angew. Chem. Int. Ed. 44, 6009–6012 (2005).

].

3.4. Modeling reflection spectra

To account for the color change quantitatively, we modeled the reflection spectra of the multilayer using the transfer matrix method [29

29. P. Yeh, Optical waves in layered media (Wiley, New York, 1988).

,30

30. J. Zi, J. Wan, and C. Zhang, “Large frequency range of negligible transmission in one-dimensional photonic quantum well structures,” Appl. Phys. Lett. 73, 2084–2086 (1998).

]. The model multilayer is composed of alternating high and low refractive index layers which mimic H and IH layers, respectively. The total number of periods is 10. The thickness of the H and IH layers in the dry state is assumed to be 105 and 70 nm, respectively, taken from the measurements. In the fully wet state the thickness of the H layer is 120 nm while that of the IH layer is 70 nm, taken from the ESEM measurements.

The refractive index of the H layers in the dry state is taken to be 2.0 [32

32. T. D. Schultz and M. A. Rankin, “The ultrastructure of the epicuticular interference reflectors of tiger beetles (Cicindela),” J. Exp. Biol. 117, 87–110 (1985).

]. In the wet state the H layer absorbs water which leads to its swelling. As a result, its refractive index should be different from that of pure melanoprotein. As a reasonable approximation, the dielectric constant (the square root of the refractive index) of the waterish melanoprotein layer can be effectively described by

ε1=εmfm+εwfw,
(1)

where εm and εw are respectively the dielectric constant of melanoprotein and water; fm and fw are the corresponding filling fraction in the waterish melanoprotein layer. We can determine the filling fractions approximately according to the thickness change of the H layer, namely fmdd/dw, where dd and dw are the thickness of the H layers in the dry and wet state, respectively. This leads to fm≈0.85 and fw≈0.15. With the refractive index of 1.333 for water we obtain a refractive index of 1.93 for the H layers in the fully wet state. Thus, the refractive index of the waterish melanoprotein layer can change from 1.93 in the fully wet state to 2.0 in the dry state.

Fig. 7. Simulated reflection spectra of the model multilayer at normal incidence. The black line represents the spectrum in the dry state. The spectra for the air voids with (without) water infiltrated are shown by blue (red) lines.

For the IH layers in the dry state its effective dielectric constant can be approximated by

ε2=εpfp+εafa,
(2)

where εp and εa are respectively the dielectric constant of melanoprotein nanoparticles and air; fp and fa are the corresponding filling fraction in the IH layer. From both SEM and TEM measurements, we can roughly obtain fp≈0.15 and fa≈0.85, leading to a refractive index of 1.2 for the IH layers in the dry state. In the fully wet state the refractive index of the IH layers can be estimated similarly, about 1.44.

With the values of layer thickness and refractive index, the reflection spectra of the model multilayer at normal incidence can be calculated by the transfer matrix method, shown in Fig. 7. In the spectra calculations, an imaginary value of 0.1 for the refractive index of the H layers is used in order to account for material absorption [36

36. M. F. Land, “The physics and biology of animal reflectors,” Prog. Biophys. Mol. Biol. 24, 75–106 (1972). [PubMed]

]. The estimated wavelength of peak reflection in the dry state at normal incidence is 601 nm, differing from the measured value only by 0.1%.

Since it is hard to determine whether water infiltrates into the air voids of the IH layers in the wet state, we consider two possible cases: i) the air voids are infiltrated with water and ii) the air voids remain unfilled. In the second case, the simulated reflection spectrum shows a broad peak positioned at 645 nm. The intensity of the reflection peak is a bit smaller than that in the dry state. On the other side, the reflection peak in the first case is located at 669 nm, in good agreement with the measured one of 662 nm. Its intensity is much smaller that that in the dry state which is consistent with the experimental results. We can thus conclude that the air voids in the dry state are filled with water.

4. Discussion

The elytra of beetles Tmesisternus isabellae are basically black. The perceived iridescent golden color in the elytra arises completely from long and flat scales which are densely imbricated on the elytral surface. This iridescent golden color originates from a multilayer in the scale interior. The multilayer was found to consist of two alternating layers. The first one is a nearly homogeneous melanoprotein layer while the second is an inhomogeneous layer consisting of melanoprotein nanoparticles and air voids. The constructive multilayer interference is the due cause of the golden coloration.

Scales are able to change their coloration from golden in the dry state to red in the wet state. This color change is reversible: the scales can change their golden color to red with water infiltration and recover the golden color by returning to the dry state via evaporation. In the wet state the period of the multilayer swells noticeably which is due to the water absorption by constituent melanoprotein. The color change to red in the wet state is due to both the swelling of the H layers and the infiltration of waver into the air voids in the IH layer.

Contact angle measurements indicate that scales are hydrophilic while black bands are hydrophobic. The ultrastructures on the upside of scales can further enhance their hydrophilicity [37

37. L. Jiang, R. Wang, B. Yang, T. J. Li, D. A. Tryk, A. Fujishima, K. Hashimoto, and D. B. Zhu, “Binary cooperative complementary nanoscale interfacial materials,” Pure Appl. Chem. 72, 73–81 (2000).

]. The hydrophilicity of scales is due to their sodium composition while in black bands there is no sodium composition, revealed by XPS measurements. The hydrophilic feature of scales is amiable for water infiltration and absorption.

As we know, structural coloration in the biological world is believed to have divers functionality such as camouflage, signal communication, conspecific recognition, and reproductive behavior [19

19. A. R. Parker, “515 million years of structural colour,” J. Opt. A: Pure Appl. Opt. 2, R15–R28 (2000).

22

22. R. O. Prum, “Anatomy, physics and evolution of avian structural colours,” in Bird coloration, vol. I: mechanisms and measurements, edited by G. E. Hill and K. J. McGraw (Harvard University Press, Boston, 2006), pp. 295–353.

]. Although the precise functionality of the dual structural coloration in beetles Tmesisternus isabellae is not clear, the reversible structural color change may certainly render more options for both adaption and function.

Owing to its unique properties, tunable structural color could open new avenue to the applications in display and imaging technology, printing and painting, textile industry, sensing, and photonic devices [38

38. A. C. Arsenault, V. Kitaev, I. Manners, G. A. Ozin, A. Mihi, and H. Míguez, “Vapor swellable colloidal photonic crystals with pressure tunability,” J. Mater. Chem. 15, 133–138, (2005).

42

42. J. J. Walish, Y. Kang, R. A. Mickiewicz, and E. L. Thomas, “Bioinspired electrochemically tunable block copolymer full color pixels,” Adv. Mater. 21, 1–4 (2009).

]. The revealed strategy of structural coloration may help us get deep insight into the biological functionality of structural color. On the other hand, it may also inspire the applications of structural color and the designs of artificial photonic devices as well.

Acknowledgments

This work was supported by the 973 Program (grant no. 2007CB613200). The research of X. H. Liu and J. Zi was further supported by the Shanghai Science and Technology Commission. F. Liu would like to thank Jingxia Wang of Laboratory of New Materials, Institute of Chemistry, CAS, Beijing for assistance.

References and links

1.

A. Rowlands, “The influence of water and light upon the color change of sightless frogs (Rana temporaria),” J. Exp. Biol. 1, 127–136 (1952).

2.

G. J. Tattersall, P. C. Eterovick, and D. V. de Andrade, “Tribute to R. G. Boutilier: skin colour and body temperature changes in basking Bokermannohyla alvarengai (Bokermann 1956),” J. Exp. Biol. 209, 1185–1196 (2006). [PubMed]

3.

N. F. Hadley, “Wax secretion and color phases of the desert Tenebrionid beetle Cryptoglossa verrucosa (LeConte),” Science 203, 367–369 (1979). [PubMed]

4.

E. McClain, M. K. Seely, N. F. Hadley, and V. Gray, “Wax blooms in Tenebrionid beetles of the Namib desert: correlations with environment,” Ecology 66, 112–118 (1985).

5.

K. H. L. Key and M. F. Day, “A temperature-controlled physiological colour response in the grasshopper Kosciuscola tristis sjöst. (Orthoptera: Acrididae),” Aust. J. Zool. 2, 309–339 (1954).

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9.

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10.

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11.

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12.

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K. M. Cooper, R. T. Hanlon, and B. U. Budelmann, “Physiological color change in squid iridophores II. Ultra-structural mechanisms in Lolliguncula brevis,” Cell Tissue Res. 259, 15–24 (1990). [PubMed]

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P. Vukusic and J. R. Sambles, “Photonic structures in biology,” Nature 424, 852–855 (2003). [PubMed]

21.

S. Kinoshita and S. Yoshioka, “Structural colors in nature: The role of regularity and irregularity in the structure,” Chem. Phys. Chem. 6, 1442–1459 (2005). [PubMed]

22.

R. O. Prum, “Anatomy, physics and evolution of avian structural colours,” in Bird coloration, vol. I: mechanisms and measurements, edited by G. E. Hill and K. J. McGraw (Harvard University Press, Boston, 2006), pp. 295–353.

23.

P. de Grijs, “Notes on the faculty of changing colour in reptiles,” Ann. Mag. Nat. Hist. 3, 396–402 (1899).

24.

H. Kasukawa, N. Oshima, and R. Fujii, “Control of chromatophore movements in dermal chromatic units of blue damselfish-II. The motile iridophore,” Comp. Biochem. Physiol. C 83, 1–7 (1986). [PubMed]

25.

H. Kasukawa, N. Oshima, and R. Fujii, “Mechanism of light reflection in blue damselfish motile iridophore,” Zool. Sci. 4, 243–257 (1987).

26.

N. Oshima and R. Fujii, “Mobile mechanisms of blue damselfish (Chrysiptera cyanea) iridophores,” Cell Motil. Cytoskel. 8, 85–90 (1987).

27.

C. W. Mason, “Transient color changes in the tortoise beetles (Coleoptera: Chrysomelidae),” Entomol. News 45, 52–56 (1929).

28.

M. D. Shawkey, A. M. Estes, L. M. Siefferman, and G. E. Hill, “Nanostructure predicts intraspecific variation in ultraviolet-blue plumage colour,” Proc. R. Soc. Lond. B 270, 1455–1460 (2003).

29.

P. Yeh, Optical waves in layered media (Wiley, New York, 1988).

30.

J. Zi, J. Wan, and C. Zhang, “Large frequency range of negligible transmission in one-dimensional photonic quantum well structures,” Appl. Phys. Lett. 73, 2084–2086 (1998).

31.

J. L. Gressitt, Systematics and biogeography of the longicorn beetle tribe tmesisternini (Bishop Museum Press, Honolulu, 1984).

32.

T. D. Schultz and M. A. Rankin, “The ultrastructure of the epicuticular interference reflectors of tiger beetles (Cicindela),” J. Exp. Biol. 117, 87–110 (1985).

33.

Capillarity and wetting phenomena: drops, bubbles, pearls, waves, edited by P.-G. de Gennes, F. Brochard-Wyart, and D. Quéré (Springer, New York, 2004).

34.

L. Xu, J. X. Wang, Y. L. Song, and L. Jiang, “Electrically tunable polypyrrole inverse opals with switchable stopband, conductivity, and wettability,” Chem. Mater. 20, 3554–3556 (2008).

35.

L. B. Xu, W. Chen, A. Mulchandani, and Y. S. Yan, “Reversible conversion of conducting polymer films from superhydrophobic to superhydrophilic,” Angew. Chem. Int. Ed. 44, 6009–6012 (2005).

36.

M. F. Land, “The physics and biology of animal reflectors,” Prog. Biophys. Mol. Biol. 24, 75–106 (1972). [PubMed]

37.

L. Jiang, R. Wang, B. Yang, T. J. Li, D. A. Tryk, A. Fujishima, K. Hashimoto, and D. B. Zhu, “Binary cooperative complementary nanoscale interfacial materials,” Pure Appl. Chem. 72, 73–81 (2000).

38.

A. C. Arsenault, V. Kitaev, I. Manners, G. A. Ozin, A. Mihi, and H. Míguez, “Vapor swellable colloidal photonic crystals with pressure tunability,” J. Mater. Chem. 15, 133–138, (2005).

39.

A. C. Arsenault, T. J. Clark, G. Von Freymann, L. Cademartiri, R. Sapienza, J. Bertolotti, E. Vekris, S. Wong, V. Kitaev, I. Manners, R. Z. Wang, S. John, D. Wiersma, and G. A. Ozin, “From colour fingerprinting to the control of photoluminescence in elastic photonic crystals,” Nat. Mater. 5, 179–184 (2006).

40.

K. Matsubara, M. Watanabe, and Y. Takeoka, “A thermally adjustable multicolor photochromic hydrogel,” Angew. Chem. Int. Ed. 46, 1688–1692 (2007).

41.

O. Sato, S. Kubu, and Z.-Z. Gu, “Structural color films with lotus effects, superhydrophilicity, and tunable stop-bands,” Acc. Chem. Res. 42, 1–10 (2009).

42.

J. J. Walish, Y. Kang, R. A. Mickiewicz, and E. L. Thomas, “Bioinspired electrochemically tunable block copolymer full color pixels,” Adv. Mater. 21, 1–4 (2009).

OCIS Codes
(310.6860) Thin films : Thin films, optical properties
(330.1690) Vision, color, and visual optics : Color

ToC Category:
Thin Films

History
Original Manuscript: May 22, 2009
Revised Manuscript: July 25, 2009
Manuscript Accepted: July 29, 2009
Published: August 27, 2009

Virtual Issues
Vol. 4, Iss. 10 Virtual Journal for Biomedical Optics

Citation
F. Liu, B. Q. Dong, X. H. Liu, Y. M. Zheng, and J. Zi, "Structural color change in longhorn beetles Tmesisternus isabellae," Opt. Express 17, 16183-16191 (2009)
http://www.opticsinfobase.org/vjbo/abstract.cfm?URI=oe-17-18-16183


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References

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  20. P. Vukusic and J. R. Sambles, "Photonic structures in biology," Nature 424, 852-855 (2003). [PubMed]
  21. S. Kinoshita and S. Yoshioka, "Structural colors in nature: The role of regularity and irregularity in the structure," Chem. Phys. Chem. 6, 1442-1459 (2005). [PubMed]
  22. R. O. Prum, "Anatomy, physics and evolution of avian structural colours," in Bird coloration, vol. I: mechanisms and measurements, edited by G. E. Hill and K. J. McGraw (Harvard University Press, Boston, 2006), pp. 295-353.
  23. P. de Grijs, "Notes on the faculty of changing colour in reptiles," Ann. Mag. Nat. Hist. 3, 396-402 (1899).
  24. H. Kasukawa, N. Oshima, and R. Fujii, "Control of chromatophore movements in dermal chromatic units of blue damselfish-II. The motile iridophore," Comp. Biochem. Physiol. C 83, 1-7 (1986). [PubMed]
  25. H. Kasukawa, N. Oshima, and R. Fujii, "Mechanism of light reflection in blue damselfish motile iridophore," Zool. Sci. 4, 243-257 (1987).
  26. N. Oshima and R. Fujii, "Mobile mechanisms of blue damselfish (Chrysiptera cyanea) iridophores," Cell Motil. Cytoskel. 8, 85-90 (1987).
  27. C. W. Mason, "Transient color changes in the tortoise beetles (Coleoptera: Chrysomelidae)," Entomol. News 45, 52-56 (1929).
  28. M. D. Shawkey, A. M. Estes, L. M. Siefferman, and G. E. Hill, "Nanostructure predicts intraspecific variation in ultraviolet-blue plumage colour," Proc. R. Soc. Lond. B 270, 1455-1460 (2003).
  29. P. Yeh, Optical waves in layered media (Wiley, New York, 1988).
  30. J. Zi, J. Wan, and C. Zhang, "Large frequency range of negligible transmission in one-dimensional photonic quantum well structures," Appl. Phys. Lett. 73, 2084-2086 (1998).
  31. J. L. Gressitt, Systematics and biogeography of the longicorn beetle tribe tmesisternini (Bishop Museum Press, Honolulu, 1984).
  32. T. D. Schultz and M. A. Rankin, "The ultrastructure of the epicuticular interference reflectors of tiger beetles (Cicindela)," J. Exp. Biol. 117, 87-110 (1985).
  33. Capillarity and wetting phenomena: drops, bubbles, pearls, waves, edited by P.-G. de Gennes, F. Brochard-Wyart, and D. Quéré (Springer, New York, 2004).
  34. L. Xu, J. X. Wang, Y. L. Song, and L. Jiang, "Electrically tunable polypyrrole inverse opals with switchable stopband, conductivity, and wettability," Chem. Mater. 20, 3554-3556 (2008).
  35. L. B. Xu, W. Chen, A. Mulchandani, and Y. S. Yan, "Reversible conversion of conducting polymer films from superhydrophobic to superhydrophilic," Angew. Chem. Int. Ed. 44, 6009-6012 (2005).
  36. M. F. Land, "The physics and biology of animal reflectors," Prog. Biophys. Mol. Biol. 24, 75-106 (1972). [PubMed]
  37. L. Jiang, R. Wang, B. Yang, T. J. Li, D. A. Tryk, A. Fujishima, K. Hashimoto, and D. B. Zhu, "Binary cooperative complementary nanoscale interfacial materials," Pure Appl. Chem. 72, 73-81 (2000).
  38. A. C. Arsenault, V. Kitaev, I. Manners, G. A. Ozin, A. Mihi, and H. Míguez, "Vapor swellable colloidal photonic crystals with pressure tunability," J. Mater. Chem. 15, 133-138, (2005).
  39. A. C. Arsenault, T. J. Clark, G. Von Freymann, L. Cademartiri, R. Sapienza, J. Bertolotti, E. Vekris, S. Wong, V. Kitaev, I. Manners, R. Z. Wang, S. John, D. Wiersma, and G. A. Ozin, "From colour fingerprinting to the control of photoluminescence in elastic photonic crystals," Nat. Mater. 5, 179-184 (2006).
  40. K. Matsubara, M. Watanabe, and Y. Takeoka, "A thermally adjustable multicolor photochromic hydrogel," Angew. Chem. Int. Ed. 46, 1688-1692 (2007).
  41. O. Sato, S. Kubu, and Z.-Z. Gu, "Structural color films with lotus effects, superhydrophilicity, and tunable stopbands," Acc. Chem. Res. 42, 1-10 (2009).
  42. J. J. Walish, Y. Kang, R. A. Mickiewicz, and E. L. Thomas, "Bioinspired electrochemically tunable block copolymer full color pixels," Adv. Mater. 21, 1-4 (2009).

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