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

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2009 (2)

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).

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).

2008 (1)

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).

2007 (2)

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).

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

2006 (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]

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).

2005 (3)

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).

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).

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]

2003 (3)

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

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).

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]

2001 (1)

L. M. Mäthger and E. J. Denton, "Reflective properties of iridophores and fluorescent ‘eyespots’ in the loliginid squid Alloteuthis subulata and Loligo vulgaris," J. Exp. Biol. 204, 2103-2118 (2001).
[PubMed]

2000 (2)

A. R. Parker, "515 million years of structural colour," J. Opt. A: Pure Appl. Opt. 2, R15-R28 (2000).

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).

1998 (1)

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).

1990 (2)

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]

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

1989 (1)

J. N. Lythgoe and J. Shand, "The structural basis for iridescent colour changes in dermal and corneal iridophores in fish," J. Exp. Biol. 141, 313-325 (1989).

1987 (2)

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

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

1986 (2)

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]

K. M. Cooper and R. T. Hanlon, "Correlation of iridescence with changes in iridophore platelet ultrastructure in the squid Lolliguncula brevis," J. Exp. Biol. 121, 451-455 (1986).
[PubMed]

1985 (2)

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).

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).

1979 (1)

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

1974 (1)

J. E. N. Veron, "The role of physiological colour change in the thermoregulation of Austrolestes annulosus (Selys) (Odonata)," Aust. J. Zool. 22, 457-469 (1974).

1973 (1)

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).

1972 (2)

H. E. Hinton and G. M. Jarman, "Physiological colour change in the Hercules Beetle," Nature 238, 160-161 (1972).

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

1954 (2)

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).

K. H. L. Key and M. F. Day, "The physiological mechanism of colour change in the grasshopper Kosciuscola tristis sjöst. (Orthoptera: Acrididae)," Aust. J. Zool. 2, 340-363 (1954).

1952 (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).

1933 (1)

K. W. Foster, "Color changes in fundulus with special reference to the color changes of the iridosomes," Proc. Natl. Acad. Sci. 19, 535-540 (1933).
[PubMed]

1929 (1)

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

1899 (1)

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

Arsenault, A. C.

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).

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).

Bertolotti, J.

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).

Biró, L. P.

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).

Budelmann, B. U.

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]

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

Cademartiri, L.

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).

Chen, W.

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).

Clark, T. J.

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).

Cooper, K. M.

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]

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

K. M. Cooper and R. T. Hanlon, "Correlation of iridescence with changes in iridophore platelet ultrastructure in the squid Lolliguncula brevis," J. Exp. Biol. 121, 451-455 (1986).
[PubMed]

Day, M. F.

K. H. L. Key and M. F. Day, "The physiological mechanism of colour change in the grasshopper Kosciuscola tristis sjöst. (Orthoptera: Acrididae)," Aust. J. Zool. 2, 340-363 (1954).

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).

de Andrade, D. V.

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]

de Grijs, P.

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

Denton, E. J.

L. M. Mäthger and E. J. Denton, "Reflective properties of iridophores and fluorescent ‘eyespots’ in the loliginid squid Alloteuthis subulata and Loligo vulgaris," J. Exp. Biol. 204, 2103-2118 (2001).
[PubMed]

Deparis, O.

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).

Dumont, J.

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).

Ertz, D.

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).

Estes, A. M.

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).

Eterovick, P. C.

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]

Foster, K. W.

K. W. Foster, "Color changes in fundulus with special reference to the color changes of the iridosomes," Proc. Natl. Acad. Sci. 19, 535-540 (1933).
[PubMed]

Fujii, R.

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

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

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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).

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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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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).

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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).

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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).

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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).

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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).

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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).

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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).

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Figures (7)

Fig. 1.
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.

Fig. 2.
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.

Fig. 3.
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.
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.

Fig. 5.
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.
Fig. 6.

Measurements of water contact angles for (a) the black band and (b) colored region of the elytra. Scale bars: 0.5 mm.

Fig. 7.
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.

Equations (2)

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ε1 = εm fm + εw fw ,
ε2 = εp fp + εa fa ,

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