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Journal of the Optical Society of America B

Journal of the Optical Society of America B

| OPTICAL PHYSICS

  • Editor: Henry van Driel
  • Vol. 29, Iss. 5 — May. 1, 2012
  • pp: 1104–1111
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Angular dependence of structural fluorescent emission from the scales of the male butterfly Troïdes magellanus (Papilionidae)

Eloise Van Hooijdonk, Carlos Barthou, Jean Pol Vigneron, and Serge Berthier  »View Author Affiliations


JOSA B, Vol. 29, Issue 5, pp. 1104-1111 (2012)
http://dx.doi.org/10.1364/JOSAB.29.001104


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Abstract

This paper reveals an enhanced fluorescence in the hindwings of the male Troïdes magellanus, due to the confinement of fluorophores in a three-dimensional photonic structure. It is characterized by a spatial variation of the emission intensity and coloration. It also reveals the role of the structure on the emission and reflection complementary processes. We focus on the experimental analysis of these phenomena by means of a morphological study, a reflection characterization, and an emission characterization. Collecting and analyzing data over every emerging direction was important in this work. A theoretical approach is proposed to explain the experimental observations.

© 2012 Optical Society of America

1. INTRODUCTION

The control of light emission with a high extraction efficiency has proven to be important in many applications, such as solar cells [1

1. J. C. Goldschmidt, M. Peters, J. Gutmann, L. Steidl, R. Zentel, B. Blasi, and M. Hermle, “Increasing fluorescent concentrator light collection efficiency by restricting the angular emission characteristic of the incorporated luminescent material: the ’Nano-Fluko’ concept,” Proc. SPIE 7725, 77250S (2010). [CrossRef]

], light-emitting diodes [2

2. D.-H. Kim, C.-O. Cho, Y.-G. Roh, H. Jeon, Y. S. Park, J. Cho, J. S. Im, C. Sone, Y. Park, W. J. Choi, and Q.-H. Park, “Enhanced light extraction from GaN-based light-emitting diodes with holographically generated two-dimensional photonic crystal patterns,” Appl. Phys. Lett. 87, 203508 (2005). [CrossRef]

], DNA microarrays [3

3. P. C. Mathias, S. I. Jones, H. Y. Wu, F. Yang, N. Ganesh, D. O. Gonzalez, G. Bollero, L. O. Vodkin, and B. T. Cunningham, “Improved sensitivity of DNA microarrays using photonic crystal enhanced fluorescence,” Anal. Chem. 82, 6854–6861 (2010). [CrossRef]

], biosensors [4

4. R. P. Tompkins, J. M. Dawson, L. A. Homak, and T. H. Myers, “Optofluidic photonic crystals for biomolecular fluorescence enhancement : a bottom-up approach for fabricating GaN-based biosensors,” Proc. SPIE 7056, 70560J (2008). [CrossRef]

], laser scanning confocal microscopy [5

5. J. Y. Ye, M. T. Myaing, T. P. Thomas, I. Majoros, A. Koltyar, J. R. Baker, W. J. Wadsworth, G. Bouwmans, J. C. Knight, P. S. J. Russell, and T. B. Norris, “Development of a double-clad photonic-crystal-fiber based scanning microscope,” Proc. SPIE 5700, 23–27 (2005). [CrossRef]

], etc. The condition for this enhanced fluorescence is a strong source confinement in one or more spatial directions. The photonic crystal has been demonstrated to be a good candidate. This structured material exhibits a periodic spatial variation of the refractive index. Its particularity is the existence of photonic band gaps, inhibiting the light propagation and making possible the perfect control of the photons. Since the two major articles of Yablonovitch [6

6. E. Yablonovitch, “Inhibited spontaneous emission in solid-state physics and electronics,” Phys. Rev. Lett. 58, 2059–2062 (1987). [CrossRef]

] and John [7

7. S. John, “Strong localization of photons in certain disordered dielectric superlattices,” Phys. Rev. Lett. 58, 2486–2489(1987). [CrossRef]

], the photonic crystal has become a well-understood concept fruitfully integrated in many applications.

Manufacturers want produce new devices presenting well-targeted features. They have at their disposal a wide range of materials. The difficulty is to imagine which photonic structure is able to produce a desired optical effect. On the other hand, living organisms offer a wide assortment of natural photonic architectures. The biophotonic tends to combine both fields in order to create devices inspired from our environment. But before artificially transposing the observations of the nature, it is important to understand the underlying physics.

This work aims to exhibit an enhanced fluorescence in the hindwings of the male butterfly Troïdes magellanus and to understand its physical origin. We suggest that the natural three-dimensional photonic structure present in the butterfly’s scales, close in size to the involved wavelength, influences the spatial distribution of the emitted intensity and coloration. As a result of the source confinement in the particular geometry, fluorescent emission is reinforced or attenuated according to the observation direction. A relationship between reflection and emission phenomena is also perceptible.

Our experimental analysis was carried out in three steps. The first step was an examination of the natural photonic structure by means of optical and electron microscopes images. The second step was the reflection characterization using a high performance viewing angle instrument. The result, called a bidirectional reflectance distribution function (BRDF) map, was a representation of the reflected flux with the observation direction. The last step consists in a fluorescence properties investigation. In order to obtain a representation of the emitted flux according to the observation direction, a flexible setup consisting in an ultraviolet source coupled to a gonio-spectrofluorometer was employed. In order to explain our observations, we performed numerical simulations predicting the emission spatial distribution when a planar source is embedded in a Troïdes-like structure. The computational code was based on the scattering-matrix formalism.

2. STATE OF THE ART

A member of the large Papilionidae family, the butterfly Troïdes magellanus is found in Australia and Indonesia. With a wingspan from 16 to 18 cm, their forewings are black with veins bordered by white color. By contrast, hindwings present a very bright uniform yellow coloration under daylight [Fig. 1(a)]. The veins and the wing’s edge are black. Surprisingly, when the observer and the light source are collocated in a grazing direction to the wing, a bright glint with blue-green hues is perceptible [Fig. 1(b)]. Moreover, under an ultraviolet illumination, a yellow-green coloration is produced. The abdomen is yellow, while the head and the thorax are black.

Fig. 1. (a) Photographs of the dorsal view of the male Troïdes magellanus [10]. (b) At grazing illumination and observation, a bright glint with blue-green hues is perceptible on the hindwings [10]. (c) Orientation of the hindwing in an axis system. The sample is placed in the xy plane, the z-axis being normal and the y-axis pointing from the termen to the base of the wing. The light propagation direction, represented by the red arrow, is defined by two angles: the polar angle θx and the azimuth angle φx. The index “x” is “i” in the case of the incident beam and “d” in the case of the detected beam.

Since its discovery in 1862 by Felder [11

11. G. W. Beccaloni, M. J. Scoble, G. S. Robinson, and B. Pitkin, eds., “The Global Lepidoptera Names Index (LepIndex),” http://www.nhm.ac.uk/entomology/lepindex.

], little descriptions have been conducted on this butterfly. The first article we can mention dates back to 2002. Lawrence et al. [12

12. C. Lawrence, P. Vukusic, and R. Sambles, “Grazing-incidence iridescence from a butterfly wing,” Appl. Opt. 41, 437–441 (2002). [CrossRef]

] observed the photonic structure of the scales by means of electron microscope images and analyzed their optical properties—especially the bright glint—by measuring ultraviolet-visible reflection spectra. They concluded that this glint found its origin in an iridescence phenomenon. In 2008, Vigneron et al. [13

13. J. P. Vigneron, K. Kertesz, Z. Vertesy, M. Rassart, V. Lousse, Z. Balint, and L. P. Biro, “Correlated diffraction and fluorescence in the backscattering iridescence of the male butterfly Troides magellanus (Papilionidae),” Phys. Rev. E 78, 021903 (2008). [CrossRef]

] realized an upgraded study of this feature and, in parallel, were interested in the fluorescence of the wing. They brought a first theoretical explanation of the physical origin. One year later, Lee and Smith [14

14. R. T. Lee and G. S. Smith, “Detailed electromagnetic simulation for the structural color of butterfly wings,” Appl. Opt. 48, 4177–4190 (2009). [CrossRef]

] used a finite-difference time-domain (FDTD) method to simulate the structural coloration of the wing. However, they did not consider in their numerical simulations the presence of fluorophores embedded in the natural photonic structure.

The papiliochrome II is the molecule at the origin of the fluorescence in the male Troïdes magellanus. The pigment was first isolated by a Japanese team in the wings of some Papilionidae members. This studious work was successful in 1970 with the publication by Umebachi and Yoshida [15

15. Y. Umebachi and K. Yoshida, “Some chemical and physical properties of papiliochrome II in the wings of Papilio xuthus,” J. Insect Physiol. 16, 1203–1228 (1970). [CrossRef]

] of a very detailed article on the chemical and the physical properties of the papiliochrome II in the scales of the Papilio xuthus. In the following decades, other scientists refined and broadened this subject [16

16. S. J. Saul and M. Sugumaran, “Quinone methide as a reactive intermediate formed during the biosynthesis of papiliochrome-II, a yellow wing pigment of papilionid butterflies,” FEBS Lett. 279, 145–148 (1991). [CrossRef]

,17

17. P. B. Koch, B. Behnecke, M. Weigmann-Lenz, and R. H. French-Constant, “Insect pigmentation: activities of β-alanyldopamine synthase in wing color patterns of wild-type and melanic mutant swallowtail butterfly Papilio glaucus,” Pigment Cell Res. 13, 54–58 (2000). [CrossRef]

]. They isolated various components of the pigment and described its formation.

The population of the Troïdes magellanus is severely restricted by the pressure on its living environment, and all specimens are classified as vulnerable or endangered [18

18. Convention on International Trade in Endangered Species of wild fauna and flora (CITES), “Appendices I, II, and III,” http://www.cites.org/eng/app/Appendices-E.pdf.

]. Hence, the specimens used for the present studies were all certified to have been obtained through commercial breeding.

In comparison to all these publications, relating either the enhanced fluorescence in butterfly wings or the Troïdes magellanus optical properties, the present paper exposes an original contribution interesting for two aspects. Firstly, we investigated the influence of a more complex three-dimensional photonic structure on the emission process, while other publications involved two-dimensional structures. Secondly, we brought a refined theoretical approach of the emission properties, directly comparable to our experimental data.

3. MATERIALS AND METHOD

To help the understanding of the following discussion, an axis system is defined [Fig. 1(c)]. The Lepidoptera’s wing is located in the xy plane, the y-axis pointing from the termen to the base of the wing and the z-axis being normal to the sample. The red arrow, representing a light propagation direction, is defined by two angles: θx is the polar angle measured from the normal to the sample, while φx is the azimuth angle measured counterclockwise in the xy plane, the x-axis being the origin. The index “x” is “i” in the case of an incident flux or “d” in the case of a detected flux.

The architecture of an individual scale was described in the works of Lawrence et al. [12

12. C. Lawrence, P. Vukusic, and R. Sambles, “Grazing-incidence iridescence from a butterfly wing,” Appl. Opt. 41, 437–441 (2002). [CrossRef]

] and Vigneron et al. [13

13. J. P. Vigneron, K. Kertesz, Z. Vertesy, M. Rassart, V. Lousse, Z. Balint, and L. P. Biro, “Correlated diffraction and fluorescence in the backscattering iridescence of the male butterfly Troides magellanus (Papilionidae),” Phys. Rev. E 78, 021903 (2008). [CrossRef]

]. However, it seems indispensable to achieve new observations, at all levels of complexity, in order to confirm the implicated photonic structure and to extract with a better accuracy the geometric parameters. These data are essential for further numerical simulations. Practically, small pieces were cut in an uniform yellow area of the hindwings. An Olympus BX51 optical microscope allowed us to approach the scale disposition on the wing’s membrane and the color properties of an isolated scale. A Jeol 7500 FESEM and a LEICA S 440 scanning electron microscope (SEM) were used to approach the nanoscale.

The second step of this experimental analysis was the reflection characterization. For this purpose, a high performance viewing angle instrument (Eldim Co.) was employed. The result, called a BRDF map, gave the spatial variation of the luminance, expressed in units of candela per square meter (cd/m2).

A high flexible setup was used to characterize the emission properties of the Troïdes magellanus. Composed of various modules, they were adjusted to perform a large variety of fluorescence measurements [Fig. 2(a)]. Firstly, it allowed the acquisition of excitation spectra, i.e., the variation of the emitted intensity at a fixed analysis wavelength λanalysis according to the excitation wavelength. Secondly, it allowed the acquisition of emission spectra, i.e., the variation of the emitted intensity with the wavelength for a fixed excitation wavelength λexcitation. The boundaries of the emission band were noted λmin and λmax. An adapted filter was placed before the detector in order to eliminate the excitation component from all the measurements. A simultaneous examination of both excitation and emission spectra allowed us to select the appropriate excitation wavelength and filter, in order to reach a compromise between the emission efficiency and the non disruption of the emission band. A specific example will be examined in Section 4. Finally, this setup allowed us to gain the spatial distribution of the emitted flux, the main concern of this work. The result gave two diagrams: (i) the variation of the emitted energy with the collection direction (defined by the θd and φd angles), and (ii) the variation of the median wavelength with the collection direction. An example of the emitted energy (the area under an emission band) and the median wavelength (the wavelength separating this emission band into two equivalent parts) is given in Fig. 2(b).

Fig. 2. (a) Schematic representation of the emission experimental setup. Two types of measurements are possible: excitation spectrum and emission mapping. (b) Emission spectrum performed at the normal to the sample under an excitation of 325 nm. In dark is represented the emitted energy, i.e., the area under the emission band. In light gray is represented the median wavelength, i.e., the wavelength separating the curve into two parts of an equivalent area.

4. EXPERIMENTAL APPROACH

A. Morphological Investigation

Viewed by an optical microscope, the dorsal side of the hindwings of the male Troïdes magellanus is composed of a membrane transparent to visible light, covered by a set of scales. For a butterfly, two kinds of scales coexist: the ground and the cover scales. In the Troïdes magellanus, the latter seems atrophied. Under a visible illumination, the coloration of the ground scales is yellow [Fig. 3(a)]. By contrast, it is yellow-green under an ultraviolet illumination, as shown in Fig. 3(b). Fixed by a pedicel, the scales are ordered on the membrane like tiles on a roof. With a width close to 65 µm and a length close to 95 µm, they present an inclination of about 9° relative to their support.

Fig. 3. Optical microscope view from the dorsal side of a hindwing fragment of the Troïdes magellanus (a) under a visible source and (b) under an ultraviolet source.

With electron microscopes, the micro- and nanoarchitectures of an isolated scale can be reached. It can be compared to a flattened bag with adjoining surfaces (called the lower and upper laminae). With a thickness of 1400 nm, the lower lamina has no important roughness. On the other hand, the upper lamina consists of a sheet folded on itself to draw the ridges [Fig. 4(a)]. Running from the petiole to the apex of the scale, the ridges are periodically distributed with a lattice parameter close to 1500 nm. A cross section view of a scale fractured across a plane parallel to the xz plane and rotated 90° [Fig. 4(b)] reveals the crossribs binding the ridges at their junctions. The ridge sections are triangular (base1500nm and height4000nm). A lateral view of a scale [Fig. 4(c)] reveals the presence of lamellae distributed on both sides of the ridges. They are periodically distributed along the length of the ridges with a lattice parameter close to 250 nm. They are strongly inclined: the angle between the lamellae and the scale bottom is close to 60°. Note that the yellow scales’ structure is similar for the dorsal and the ventral sides of the wing (SEM images not shown).

Fig. 4. (a) SEM image of the top view of a ground scale of the Troïdes magellanus showing the ridges. They form a diffraction grating with a lattice parameter of 1.5 µm. Each ridge bears a set of lamellae. They form a multilayer with a smaller lattice parameter of 250 nm. (b) Cross section view of a scale fractured across a plane parallel to the xz plane and rotated 90°. The upper lamina is formed by crossribs [C] and ridges [R], each bearing the lamellae [*]. The section of the ridges is triangular. (c) Lateral view of a scale. The lower lamina [L] has no significant rumpling. The lamellae are tilted at about 60° relative to this one.

We made the approximation that there was no statistical disparity of all geometric parameters (interridges distance, interlamellae distance, lamellae inclination, etc.). We qualified the geometry of these scales as a three-dimensional photonic structure, while there was a periodic variation of the refractive index in the three spatial directions. The set of ridges could be approached by a diffraction grating with a lattice parameter of 1500 nm. Moreover, the lamellae could be approached by a multilayer if the scale is viewed in a grazing direction, i.e., a stack of air and chitin layers. The periodicity was smaller: 250 nm.

B. Reflection Characterization

Figure 5(a) is the BRDF map of the dorsal side of the hindwing. The dotted-dashed line is an axis perpendicular to the length of the ridges, and the red star indicates the incident direction. This diagram presents a mirror symmetry according to the y-axis. Moreover, three main reflection spots are perceptible in the observation directions (θd, φd) being respectively (25°, 150°), (25°, 90°), and (25°, 30°). Fig. 5(b) is a spatial schematic representation of the incident and main reflected beams. By comparing this diagram with the SEM images of the structure [Fig. 4(a)], we can see that the reflection occurs preferentially in directions perpendicular to the length of the ridges.

Fig. 5. (a) BRDF map for the dorsal hindwing measured by a viewing angle instrument. The diagram represents the luminance (cd/m2) according to the detection angles θd and φd. The red star is the incident direction (θi=25°, φi=90°). The light is reflected in the direction of the dotted-dashed line, an axis perpendicular to the length of the ridges. (b) Schematic representation of the reflection process. In magenta is the incident beam, and in green are the main reflection spots.

The behavior of this map is typical for scientists working on the optical properties of butterflies [22

22. S. Berthier, Photonique des Morphos (Springer-Verlag, Berlin, 2010).

]. The set of regularly spaced ridges can be approached by a diffraction grating. An electromagnetic wave falling on this device is diffracted by the ridges, each one acting as a secondary source. The outgoing waves will interact together and interfere constructively in directions perpendicular to the length of the ridges and destructively in other directions.

C. Emission Characterization

Optical images presented previously showed that the yellow parts of the hindwings are fluorescent. What are the membrane and the scales contributions? To give an answer, we performed emission spectra measurements on (i) the membrane alone, (ii) the membrane with the scales on the ventral side of the wing, and (iii) the membrane with the scales on both sides of the wing. The illumination and detection conditions remained constant between the three acquisitions. A soft brush was used to remove the scales when required. The results [Fig. 6(a)] show that the fluorescence is concentrated in the scales. Although the membrane exhibits a fluorescent signal, it is very weak in comparison to the scales’ signal. In the rest of this paper, we will focus only on the scales of the dorsal side. But results are similar for the scales of the ventral side (results not shown).

Fig. 6. (a) Emission spectra for (1) the membrane alone, (2) the membrane with the ventral scales, and (3) the membrane with the ventral and dorsal scales (i.e., the whole wing). The membrane presents a weak fluorescent signal in comparison to the dorsal and ventral scales’ signal. (b) Excitation spectrum carried out at λanalysis=535nm and emission spectrum performed with λexcitation=325nm. The boundaries of the emission band are noted λmin and λmax. 325 nm is the best compromise, giving a good fluorescent efficiency without disrupting the emission band.

Figure 6(b) is the excitation and emission spectra. Emission spectrum was performed at the normal collection direction to the sample with an excitation wavelength of 325 nm. The emission band is narrow (λmin=460nm and λmax=760nm) with a maximum of intensity at 535 nm. The excitation spectrum, performed for an analysis wavelength of 535 nm, shows three zones: (i) an increase (in average) of the intensity with the wavelength, (ii) a plateau between 425 and 490 nm (the perturbations coming from the xenon lamp), and (iii) a sharp decrease. Both curves were preliminaries needed to set the best working parameters. We saw that excitation wavelengths between 425 and 490 nm gave the best fluorescence efficiency and should be preferred. Unfortunately, these wavelengths were very close to the minimum of the emission band, and the filter, used to eliminate the excitation component from the measurements, disturbed the emission band. In consequence, a smaller excitation wavelength (325 nm) had to be chosen for the following, with an adapted filter.

Fig. 7. (a) Diagram of the emitted energy with the detection angles θd and φd. The red star is the incident direction (θi=25°, φi=90°), the white disk is a nonsignificant area, and the dashed line is an axis parallel to the length of the ridges. The emitted energy is maximal in the direction (50°, 280°). Dividing each value of the emitted energy by the cosine of the polar angle θd gives a luminance value. (b) is the resulting diagram showing the variation of the luminance according to the detection angles θd and φd. A logarithmic representation was chosen. The emission is attenuated in a direction perpendicular to the length of the ridges. (c) Schematic representation of the emission process. In magenta is the incident beam, and in green are the main emission spots.

By comparing Fig. 5(a) and Fig. 7(b), we can advance that reflection and emission are complementary processes. In a collection direction, if the reflection is important, the emission is attenuated, and vise versa. Moreover, the light is reflected in directions perpendicular to the ridges, while the emission is attenuated in these same directions. We propose that the photonic structure is the central element of this observation, acting as a diffraction grating in the case of the reflection and as a waveguide in the case of the emission.

Let us analyze now the diagram for the median wavelength [Fig. 8(a)]. As previously, the red star is the incident direction, the white disk is a nonsignificant zone, and the dashed line is an axis parallel to the length of the ridges. Please note that the color scale has no meaning in terms of colorimetry. A variation of the median wavelength with the collection direction is visible. It matches to a variation of the emission band shape with the collection direction, i.e., of the emitted coloration. The behavior of this diagram is very similar to that of Fig. 7(b): two mirror symmetries (according to the x- and y-axes) and two main spots at the (60°, 90°) and (60°, 270°) directions are perceptible. In other words, when the butterfly is observed in a direction where the fluorescence is reinforced, the median wavelength is displaced to the most important values. Conversely, when the butterfly is observed in a direction where the fluorescence is attenuated, the median wavelength is displaced to the less important values. We focus on eight emission spectra corresponding to particular collection directions: φd is maintained at 270°, while θd varies from 0° to 70°. Their translation into the CIE 1931 chromaticity diagram [Fig. 8(b)] shows a modification of the emitted coloration from green (when the collection is normal to the sample) to turquoise if the collection is grazing to the sample. The redistribution of the fluorescence by the scales of the Troïdes magellanus is clearly demonstrated, in terms of the emission directionality and in terms of the median wavelength modification.

Fig. 8. (a) Diagram of the median wavelength with the detection angles θd and φd. The red star is the incident direction (θi=25°, φi=90°), the white disk is a nonsignificant area, and the dashed line is an axis parallel to the length of the ridges. The map presents two mirror symmetries according to the x- and y-axes. (b) We select particular collection directions represented by the dashed arrow. We translate the corresponding emission spectra in the CIE 1931 chromaticity diagram. A variation of the emitted coloration from green (when the observation is normal to the sample) to turquoise (when the observation is grazing to the sample) is observed.

5. THEORETICAL APPROACH

A. Optical Model Of The Wing

The scattering-matrix treatment is adapted to a stratified medium presenting a lateral periodicity of the refractive index. For numerical simulations, the wing model was divided into layers. The refractive index is maintained uniform across one layer thickness. In each layer, a unit cell is repeated periodically according to the lateral directions. This cell is formed by a host medium containing one or more inclusions. This concept was described with more details by Deparis and Vigneron [24

24. O. Deparis and J. P. Vigneron, “Modeling the photonic response of biological nanostructures using the concept of stratified medium: the case of a natural three-dimensional photonic crystal,” Mater. Sci. Eng., B 169, 12–15 (2010). [CrossRef]

].

Based on the morphological data, we elaborated an idealized model of the wing [Fig. 9(a)]. The lower lamina is represented by a 1400 nm homogeneous slab. The ridges were represented by a central trunk, decorated on both sides by homogeneous slabs of various sizes (lamellae). For each layer, the unit cell presents an asymmetric character, the lamellae being alternatively distributed on both sides of the ridges. For the sake of the simplicity, the lamellae were considered parallel to the lower lamina and not inclined 60° as in reality. The section of the ridges had a triangular shame (base=1500nm and height=4000nm). As required by the computational code, both the lower slab and the ridges extended to infinity in the lateral dimensions. We assumed that the wing is formed by a unique biological material exhibiting no absorption: we chose chitin. Its refractive index is set at n=1.56, a value commonly accepted by the scientists [25

25. I. Sollas, “On the identification of chitin by its physical constants,” Proc. R. Soc. B 79, 474–481 (1907). [CrossRef]

].

Fig. 9. (a) Optical model of the ultrastructure found in the Troïdes magellanus. The lower lamina was modeled by a homogeneous slab (thickness: 1400 nm), whereas the corrugated wing surface was modeled by a central trunk decorated on both sides by homogeneous slabs of various sizes (the lamellae). The section of the ridges was triangular (base: 1500 nm, height: 4000 nm). (b) The polar and azimuth angle distribution of normalized emission (log. scale) for an idealized Troïdes-like structure containing an infinitely plane source. Dotted-circles indicate the area of important emission, i.e., at grazing emergence directions, globally parallel to the length of the ridges.

We considered this idealized photonic structure in which an internal radiation plane is inserted. We located this infinitely thin planar source at the boundary between the lower lamina and the ridges, as illustrated in Fig. 9(a). This source was supposed to emit at 535 nm. This wavelength corresponds to the maximum of the experimental emission band.

B. Simulation Results

In order to quantify the optical response of a such system, the emitted light flux was calculated at various collection directions (characterized by the polar angle θd and the azimuth angle φd) using the 3D scattering-matrix computational code mentioned above. The values of emission are then normalized using values calculated from an equivalent unstructured material, the emission and collection conditions remaining identical. A logarithmic scale is preferred in order to emphasize the contrasts.

The theoretical azimuth and polar angular distribution of coupling emission is shown in Fig. 9(b). Two mirror symmetries are perceptible: according to the x-axis and the y-axis. Besides, we notice that emission is attenuated according to the x-axis, i.e., in directions perpendicular to the length of the ridges. Emission is more important at grazing emergence directions, globally parallel to the length of the ridges. It is highlighted by the dotted-circles on Fig. 9(b).

6. CONCLUSION

The yellow scales of this butterfly bear a basal membrane, covered by high parallel ridges running along the length of the scale and presenting a triangular section. Ridges form a diffraction grating. Sides of these triangles named lamellae form a multilayer and are tilted at about 60° relative to the basal membrane.

The analysis reported in this paper underlines the enhanced fluorescence occurring in the yellow scales of the Troïdes magellanus. This process is characterized by (i) an emission reinforcement or attenuation according to the observation direction and (ii) a spatial dependence of the emission band shape, i.e., of the emission coloration. More, the analysis underlines the correlation between the reflection and emission processes. The origin seems to be the natural photonic structure of the scales, leading to a preferential direction of light propagation. In the case of the reflection, the structure acts as a diffraction grating, dispersing light according the x-axis, i.e., in directions perpendicular to the length of the ridges. By contrast, the structure acts as a waveguide in the case of the emission, attenuating the light according the x-axis.

A method adapted to angular measurements was important in this experimental analysis. BRDF mapping was performed by a viewing angle instrument, while emission mapping was performed by a goniometer coupled to a spectrofluorometer. Morphological investigation was realized by means of optical and electron microscopes.

Theoretical results of the spatial distribution of the emitted flux agree well with the reported experiment results. Theoretical predictions were obtained by numerical simulations based on the scattering-matrix method. The insertion of an infinitely thin planar source in a Troïdes-like photonic structure was considered. This theoretical approach provides a deep physical understanding of the enhanced fluorescence occurring in the hindwings of the butterfly Troïdes magellanus.

ACKNOWLEDGMENTS

The authors gratefully thank S. Borenstajn (LISE, Paris, France) and J. F. Colomer (PMR, Namur, Belgium) for realizing some SEM images. They also thank F. Breton (INSP, Paris, France) for contributing to the development of the experimental setup. They acknowledge C. Vandenbem (PMR, Namur, Belgium) for contributing to the theoretical approach. They also acknowledge the use of Namur Interuniversity Scientific Computing Facility “Namur-iSCF,” a common project between the Belgian Fund for Scientific Research (F.R.S.—FNRS) and the University of Namur (FUNDP, Belgium). E. Van Hooijdonk is supported as a research fellow by the F.R.S.—FNRS.

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R. P. Tompkins, J. M. Dawson, L. A. Homak, and T. H. Myers, “Optofluidic photonic crystals for biomolecular fluorescence enhancement : a bottom-up approach for fabricating GaN-based biosensors,” Proc. SPIE 7056, 70560J (2008). [CrossRef]

5.

J. Y. Ye, M. T. Myaing, T. P. Thomas, I. Majoros, A. Koltyar, J. R. Baker, W. J. Wadsworth, G. Bouwmans, J. C. Knight, P. S. J. Russell, and T. B. Norris, “Development of a double-clad photonic-crystal-fiber based scanning microscope,” Proc. SPIE 5700, 23–27 (2005). [CrossRef]

6.

E. Yablonovitch, “Inhibited spontaneous emission in solid-state physics and electronics,” Phys. Rev. Lett. 58, 2059–2062 (1987). [CrossRef]

7.

S. John, “Strong localization of photons in certain disordered dielectric superlattices,” Phys. Rev. Lett. 58, 2486–2489(1987). [CrossRef]

8.

P. Vukusic and I. Hooper, “Directionally controlled fluorescence emission in butterflies,” Science 310, 1151 (2005). [CrossRef]

9.

E. Van Hooijdonk, C. Barthou, J. P. Vigneron, and S. Berthier, “Detailed experimental analysis of the structural fluorescence in the butterfly Morpho sulkowskyi (Nymphalidae),” J. Nanophoton. 05, 053525 (2011). [CrossRef]

10.

T. Neubauer, “Butterflycorner—butterfly from all over the world,” http://en.butterflycorner.net.

11.

G. W. Beccaloni, M. J. Scoble, G. S. Robinson, and B. Pitkin, eds., “The Global Lepidoptera Names Index (LepIndex),” http://www.nhm.ac.uk/entomology/lepindex.

12.

C. Lawrence, P. Vukusic, and R. Sambles, “Grazing-incidence iridescence from a butterfly wing,” Appl. Opt. 41, 437–441 (2002). [CrossRef]

13.

J. P. Vigneron, K. Kertesz, Z. Vertesy, M. Rassart, V. Lousse, Z. Balint, and L. P. Biro, “Correlated diffraction and fluorescence in the backscattering iridescence of the male butterfly Troides magellanus (Papilionidae),” Phys. Rev. E 78, 021903 (2008). [CrossRef]

14.

R. T. Lee and G. S. Smith, “Detailed electromagnetic simulation for the structural color of butterfly wings,” Appl. Opt. 48, 4177–4190 (2009). [CrossRef]

15.

Y. Umebachi and K. Yoshida, “Some chemical and physical properties of papiliochrome II in the wings of Papilio xuthus,” J. Insect Physiol. 16, 1203–1228 (1970). [CrossRef]

16.

S. J. Saul and M. Sugumaran, “Quinone methide as a reactive intermediate formed during the biosynthesis of papiliochrome-II, a yellow wing pigment of papilionid butterflies,” FEBS Lett. 279, 145–148 (1991). [CrossRef]

17.

P. B. Koch, B. Behnecke, M. Weigmann-Lenz, and R. H. French-Constant, “Insect pigmentation: activities of β-alanyldopamine synthase in wing color patterns of wild-type and melanic mutant swallowtail butterfly Papilio glaucus,” Pigment Cell Res. 13, 54–58 (2000). [CrossRef]

18.

Convention on International Trade in Endangered Species of wild fauna and flora (CITES), “Appendices I, II, and III,” http://www.cites.org/eng/app/Appendices-E.pdf.

19.

D. M. Whittaker and I. S. Culshaw, “Scattering-matrix treatment of patterned multilayer photonic structures,” Phys. Rev. B 60, 2610–2618 (1999). [CrossRef]

20.

Y. Zhao, G. Wang, and X. H. Wang, “Light emission properties of planar source in multilayer structures with photonic crystal patterns,” J. Appl. Phys. 108, 063103 (2010). [CrossRef]

21.

M. Luscidini, M. Gerace, L. C. Andreani, and J. E. Siper, “Scattering-matrix analysis of periodically patterned multilayers with asymmetric unit cells and birefringent media,” Phys. Rev. B 77, 1–11 (2008).

22.

S. Berthier, Photonique des Morphos (Springer-Verlag, Berlin, 2010).

23.

J. L. Meyzonnette, “Notions de photométrie,” in Radiométrie et Détection Optique (EDP Sciences, 1992), pp. 3–92.

24.

O. Deparis and J. P. Vigneron, “Modeling the photonic response of biological nanostructures using the concept of stratified medium: the case of a natural three-dimensional photonic crystal,” Mater. Sci. Eng., B 169, 12–15 (2010). [CrossRef]

25.

I. Sollas, “On the identification of chitin by its physical constants,” Proc. R. Soc. B 79, 474–481 (1907). [CrossRef]

OCIS Codes
(160.4760) Materials : Optical properties
(260.2510) Physical optics : Fluorescence
(330.1690) Vision, color, and visual optics : Color
(350.4238) Other areas of optics : Nanophotonics and photonic crystals

ToC Category:
Physical Optics

History
Original Manuscript: November 22, 2011
Revised Manuscript: January 23, 2012
Manuscript Accepted: February 10, 2012
Published: April 30, 2012

Virtual Issues
Vol. 7, Iss. 7 Virtual Journal for Biomedical Optics

Citation
Eloise Van Hooijdonk, Carlos Barthou, Jean Pol Vigneron, and Serge Berthier, "Angular dependence of structural fluorescent emission from the scales of the male butterfly Troïdes magellanus (Papilionidae)," J. Opt. Soc. Am. B 29, 1104-1111 (2012)
http://www.opticsinfobase.org/josab/abstract.cfm?URI=josab-29-5-1104


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References

  1. J. C. Goldschmidt, M. Peters, J. Gutmann, L. Steidl, R. Zentel, B. Blasi, and M. Hermle, “Increasing fluorescent concentrator light collection efficiency by restricting the angular emission characteristic of the incorporated luminescent material: the ’Nano-Fluko’ concept,” Proc. SPIE 7725, 77250S (2010). [CrossRef]
  2. D.-H. Kim, C.-O. Cho, Y.-G. Roh, H. Jeon, Y. S. Park, J. Cho, J. S. Im, C. Sone, Y. Park, W. J. Choi, and Q.-H. Park, “Enhanced light extraction from GaN-based light-emitting diodes with holographically generated two-dimensional photonic crystal patterns,” Appl. Phys. Lett. 87, 203508 (2005). [CrossRef]
  3. P. C. Mathias, S. I. Jones, H. Y. Wu, F. Yang, N. Ganesh, D. O. Gonzalez, G. Bollero, L. O. Vodkin, and B. T. Cunningham, “Improved sensitivity of DNA microarrays using photonic crystal enhanced fluorescence,” Anal. Chem. 82, 6854–6861 (2010). [CrossRef]
  4. R. P. Tompkins, J. M. Dawson, L. A. Homak, and T. H. Myers, “Optofluidic photonic crystals for biomolecular fluorescence enhancement : a bottom-up approach for fabricating GaN-based biosensors,” Proc. SPIE 7056, 70560J (2008). [CrossRef]
  5. J. Y. Ye, M. T. Myaing, T. P. Thomas, I. Majoros, A. Koltyar, J. R. Baker, W. J. Wadsworth, G. Bouwmans, J. C. Knight, P. S. J. Russell, and T. B. Norris, “Development of a double-clad photonic-crystal-fiber based scanning microscope,” Proc. SPIE 5700, 23–27 (2005). [CrossRef]
  6. E. Yablonovitch, “Inhibited spontaneous emission in solid-state physics and electronics,” Phys. Rev. Lett. 58, 2059–2062 (1987). [CrossRef]
  7. S. John, “Strong localization of photons in certain disordered dielectric superlattices,” Phys. Rev. Lett. 58, 2486–2489(1987). [CrossRef]
  8. P. Vukusic and I. Hooper, “Directionally controlled fluorescence emission in butterflies,” Science 310, 1151 (2005). [CrossRef]
  9. E. Van Hooijdonk, C. Barthou, J. P. Vigneron, and S. Berthier, “Detailed experimental analysis of the structural fluorescence in the butterfly Morpho sulkowskyi (Nymphalidae),” J. Nanophoton. 05, 053525 (2011). [CrossRef]
  10. T. Neubauer, “Butterflycorner—butterfly from all over the world,” http://en.butterflycorner.net .
  11. G. W. Beccaloni, M. J. Scoble, G. S. Robinson, and B. Pitkin, eds., “The Global Lepidoptera Names Index (LepIndex),” http://www.nhm.ac.uk/entomology/lepindex .
  12. C. Lawrence, P. Vukusic, and R. Sambles, “Grazing-incidence iridescence from a butterfly wing,” Appl. Opt. 41, 437–441 (2002). [CrossRef]
  13. J. P. Vigneron, K. Kertesz, Z. Vertesy, M. Rassart, V. Lousse, Z. Balint, and L. P. Biro, “Correlated diffraction and fluorescence in the backscattering iridescence of the male butterfly Troides magellanus (Papilionidae),” Phys. Rev. E 78, 021903 (2008). [CrossRef]
  14. R. T. Lee and G. S. Smith, “Detailed electromagnetic simulation for the structural color of butterfly wings,” Appl. Opt. 48, 4177–4190 (2009). [CrossRef]
  15. Y. Umebachi and K. Yoshida, “Some chemical and physical properties of papiliochrome II in the wings of Papilio xuthus,” J. Insect Physiol. 16, 1203–1228 (1970). [CrossRef]
  16. S. J. Saul and M. Sugumaran, “Quinone methide as a reactive intermediate formed during the biosynthesis of papiliochrome-II, a yellow wing pigment of papilionid butterflies,” FEBS Lett. 279, 145–148 (1991). [CrossRef]
  17. P. B. Koch, B. Behnecke, M. Weigmann-Lenz, and R. H. French-Constant, “Insect pigmentation: activities of β-alanyldopamine synthase in wing color patterns of wild-type and melanic mutant swallowtail butterfly Papilio glaucus,” Pigment Cell Res. 13, 54–58 (2000). [CrossRef]
  18. Convention on International Trade in Endangered Species of wild fauna and flora (CITES), “Appendices I, II, and III,” http://www.cites.org/eng/app/Appendices-E.pdf .
  19. D. M. Whittaker and I. S. Culshaw, “Scattering-matrix treatment of patterned multilayer photonic structures,” Phys. Rev. B 60, 2610–2618 (1999). [CrossRef]
  20. Y. Zhao, G. Wang, and X. H. Wang, “Light emission properties of planar source in multilayer structures with photonic crystal patterns,” J. Appl. Phys. 108, 063103 (2010). [CrossRef]
  21. M. Luscidini, M. Gerace, L. C. Andreani, and J. E. Siper, “Scattering-matrix analysis of periodically patterned multilayers with asymmetric unit cells and birefringent media,” Phys. Rev. B 77, 1–11 (2008).
  22. S. Berthier, Photonique des Morphos (Springer-Verlag, Berlin, 2010).
  23. J. L. Meyzonnette, “Notions de photométrie,” in Radiométrie et Détection Optique (EDP Sciences, 1992), pp. 3–92.
  24. O. Deparis and J. P. Vigneron, “Modeling the photonic response of biological nanostructures using the concept of stratified medium: the case of a natural three-dimensional photonic crystal,” Mater. Sci. Eng., B 169, 12–15 (2010). [CrossRef]
  25. I. Sollas, “On the identification of chitin by its physical constants,” Proc. R. Soc. B 79, 474–481 (1907). [CrossRef]

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