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Abstract
Nature produces some of the most striking optical effects through the combination of structural and chemical principles to give rise to a wide range of colors. However, creating non-spectral colors that extend beyond the color spectrum is a challenging task, as it requires meeting the requirements of both structural and pigmentary coloration. In this study, we investigate the magenta non-spectral color found in the scales of the ventral spots of the Lyropteryx apollonia butterfly. By employing correlated optical and electron microscopy, as well as pigment extraction techniques, we reveal how this color arises from the co-modulation of pigmentary and structural coloration. Specifically, the angle-dependent blue coloration results from the interference of visible light with chitin-based nanostructures, while the diffused red coloration is generated by an ommochrome pigment. The ability to produce such highly conspicuous non-spectral colors provides insights for the development of hierarchical structures with precise control over their optical response. These structures can be used to create hierarchically-arranged systems with a broadened color palette.
© 2023 Optica Publishing Group under the terms of the Optica Open Access Publishing Agreement
1. Introduction
In nature, coloration serves various functions that aid in the survival of the species, including communication [1], light harvesting [2,3], thermal regulation [4], and concealment [5]. Coloration is typically classified into two categories: pigmentary and structural. Pigment-based colors have a chemical basis, are angular-independent and usually result in an opaque optical appearance. Structural colors, on the contrary, have a physical basis, can be angle-dependent, and appear either opaque or very brilliant depending on the presence of either short-range or long-range order, respectively. Pigmentary coloration results from selective absorption processes, while structural coloration [6] occurs when visible light interferes with a structure with either short- or long-range variation of the refractive index at the nanoscale, usually achieved by the alternation of two different materials [7].
Animals and plants often combine these two color-producing mechanisms to achieve more brilliant colors, through the absorption of scattered light [8,9], or to obtain a broader palette [1,10,11]. This latter case allows for the generation of non-spectral colors, which result from the combination of multiple, nonadjacent wavelengths. Examples of non-spectral colors include white, black, grey, magenta, and brown [12]. In nature, non-spectral colors originating from the co-modulation of pigmentary and structural elements have been observed in various natural systems and can serve specific biological functions [6,13–15].
Butterflies are known to use a combination of pigmentary and structural coloration to achieve a wide range of colors [16–23]. Butterflies living in remote and endangered places are still being investigated to determine the origin and the role of their coloration. Lyropteryx apollonia [24] (Westwood, 1851) is a butterfly species belonging to the Riodinidae family and is distributed across the Neotropics [25–27]. The Riodinidae family is commonly known for the metallic luster of their wings and the Lyropteryx genus has been, so far, poorly documented with the few existing records reporting only on these butterflies being rapid fliers, with high wing beat frequencies, and moving in erratic patterns [28]. So far, little is known about the coloration of their wings, despite being often mentioned for their metallic marks.
Here, we investigate the spectral behavior of the Lyropteryx apollonia wings, with a particular focus on their distinctive magenta ventral spots. Through correlated optical micro-spectroscopy and electron microscopy, we characterize the structural and pigmentary mechanisms that produce the non-spectral magenta color on the scales of the butterfly's ventral spots. The magenta color arises from the modulation of pigmentary red and structural blue, which combine following the additive color mixing principle. The pigment responsible for the red coloration has not been reported previously in literature and is identified as likely belonging to the ommochrome pigment family, with a cinnabarinic acid core. Upon pigment removal, the scales display only blue structural color, generated by the interference of the regularly arranged chitin multilayered ridges with visible light. This study sheds light on a color-producing strategy developed by a natural system. The ability to generate non-spectral colors through the combination of different coloration mechanisms has important implications for the development of artificial materials and devices with fine control over their optical response.
2. Results and discussion
The Lyropteryx butterfly’s wings are characterized by a simple stripes-and-spots pattern with bright magenta spots on the ventral side (Fig. 1(a), (b), Fig. S1, Fig. S2). The optical appearance of these spots is uniformly red/magenta, when viewed macroscopically. Interestingly, the color of the spots appears to change with the observation angle (Fig. 1(a), Fig. 2(c)), which suggests that nano- or microstructures may play a role in their generation or modulation. Each magenta spot is formed by the regular arrangement of tightly packed specialized scales (Fig. 1(c), d). Specifically, an outer layer of cover rounded scales (Fig. 1(c), (d), Fig. S3) partially covers a layer of serrated red cover scales (Fig. 1(c), (d), Fig. S3). The tip of each cover scale is bent towards the wing lamina (Fig. S3), as observed in other butterfly species [29,30]. When analyzing the magenta scales with an optical microscope in bright field reflection, the cover scales appear uniformly red, except for a narrow strip that shows a bright metallic blue appearance (Fig. 1(d)). This blue strip runs perpendicularly to the length of each scale and appears located close to the tip due to the intrinsic curvature of each scale.
Fig. 1. Combined pigmentary and structural color in the magenta spots of Lyropteryx apollonia butterfly. Macroscopic photograph of a specimen of Lyropteryx apollonia butterfly from the (a) ventral and (b) the dorsal side. (c) Schematic representation of the color formation mechanism responsible for the magenta spots on the butterfly wings. The scales forming the spots are uniformly red with blue stripes running along the length of each scale; the blue is caused by the nanostructuring of the upper lamina of each scale into ridges formed by lamellar multilayers, while the red is caused by the presence of a pigment distributed throughout the scale. (d) Bright field reflectance micrograph of a magenta spot of the butterfly showing scales with pigmentary red and structural blue color.
Fig. 2. Optical analysis of the scales in the magenta spots. (a) Normalized reflectance spectra as a function of wavelength collected at normal incidence on regions of the scales showing blue stripes (blue area) and bright red coloration (red area). Spectra are normalized with respect to the reflectance of a silver mirror. (b) Bright field reflection (BFR, left) and corresponding dark field reflection (DFR, right) of the scales of the magenta spots. (c) Macroscopic pictures of the spots on the ventral forewings taken normally to the wing (θ=0°) and at an angle θ=70° with respect to the normal to the scale. (d) CIE chromaticity chart showing the color transition upon variation of the angle from θ=0° to θ=70°. (e) Bright field reflection images acquired with a stereo microscope for various angles. White dashed regions highlight the extent to which the blue stripes are visible. (f) Contour plot of the normalized reflectance spectra as a function of wavelength from θ=-40° to θ=70° angular range, demonstrating the iridescent behavior of the blue color and the angular independence of the red color. Spectra are normalized with respect to the reflectance of a silver mirror.
The optical appearance of these scales varies depending on whether they are observed with the naked eye or measured using an optical microscope. While the scales appear uniformly magenta or red when viewed with the naked eye, the microscope reveals that the scales are actually red with distinctive blue stripes. This discrepancy in optical appearance can be explained by the additive color mixing principle. According to this principle, the limited size of the blue-generating elements on each scale prevents them from being macroscopically resolved separately from the red-generating elements. As a result, the overall optical appearance of these scales is determined by the combination of red and blue elements, resulting in the scales appearing magenta when viewed with the naked eye for specific angles. This type of color generation mechanism has also been documented for other butterflies and for some plants [31–34].
To further investigate the response of the magenta scales, optical microscopy coupled with spectroscopy and multispectral imaging was carried out (Fig. 2(a), Fig. 3). Analysis using bright field reflectance imaging coupled with spectroscopy showed two main spectral responses. The red portion of the scales exhibited strong reflectance for λ> 600 nm, with a constant intensity above this wavelength, as typical for pigmentary red elements [16]. In contrast, the spectral feature collected from the blue stripes showed a more narrowband reflectance peak centered around λ∼ 450 nm with a shoulder for λ> 600 nm. This suggests that a portion of the reflected light responsible for the red coloration is also collected by the optical fiber, which might imply that the blue and red colors are colocalized in the plane of the scale. The presence of two separated spectral responses within each magenta scale was confirmed by performing bright-field multispectral imaging. By spectrally separating the blue and red components (Fig. 3), the spatial location of the elements responsible for those colors can be clearly seen on each scale.
Fig. 3. Multispectral analysis of the magenta spots. (a) Schematic representation of the three-dimensional map that can be acquired using a multispectral camera. The spectroscopic information of the sample is collected for each pixel at every wavelength defined by the range λstart-λend and by the step size Δλ within the spatial domain defined by the coordinates x and y. The stack of these images creates the three-dimensional map. (b) Reflectance spectra as a function of wavelength corresponding to the blue and red reflecting regions on the magenta spots of the Lyropteryx butterfly wings. The reported blue spectrum was obtained by subtracting the red spectrum from the raw blue spectrum. (c) Bright field reflection (BFR) and corresponding dark field reflection (DFR) multispectral analysis of a magenta spot. The RGB images show the location of the blue ridges in BFR and DFR; the false-color red and false-color blue images highlight the spatial position of the regions of the scales reflecting either red or blue light; the false-color recombined multispectral map is obtained by combining the false-color individual red and blue images.
Optical microscopy techniques, including bright field (BFR) and dark field reflection (DFR) microscopy were employed to investigate the mechanisms underlying the blue and red coloration (Fig. 2(b), Fig. 3). The analysis revealed that the red color is independent of the angle of incidence and is distributed across the entire scale (Fig. 2(b), Fig. 3). Conversely, the blue color is angle-dependent, and its location and intensity vary depending on the imaging mode used. Specifically, bright field reflection micrographs show a narrow bright blue strip located close to the tip of each scale while dark field reflection micrographs show lower intensity blue strips distributed over a larger area of the scales (Fig. 2(b), Fig. 3). Due to the intrinsic curvature of the scales (Fig. S3) only a small portion of the blue light is collected by the microscope objective in BFR, while most of it is scattered at higher angles and is thus not collected; this scattered light can, instead, be collected by analyzing the same scale in DFR. Thus, correlated BFR and DFR microscopy suggests that the structure responsible for the blue strip is not limited to the tip of the scale but is distributed across the entire scale.
To further investigate the angular dependence of the scales’ color, custom-made setups were used both macroscopically and microscopically (Fig. 2(c)-(f), Fig. S4, S5). Macroscopically, when the wings of the Lyropteryx butterfly were tilted, the color of the spots varied from magenta at normal incidence (θ= 0°) to bright red for higher angles (θ= 70°) (Fig. 2(c)). By extracting the RGB values associated with each spot and by converting those values to CIE 1976 L*a*b* color space [35], the transition from the non-spectral magenta color to red color was observed (Fig. 2(d)). Higher magnification angular resolved imaging of the ventral spots was then carried out using a bright field stereo microscope equipped with a dovetail goniometric platform (Fig. 2(e), S4, S5). By changing the relative angle between the scales and the detector (θmin = - 23°, θmax = - 23°, as measured normally to the stage) the location of the blue strips was observed to be either extended to most of the scale (for θ < -7°) or to be localized to just the tip (for θ > 3°) (Fig. 2(e), Fig. S5). However, no significant variation of the red color was observed upon changing the tilting platform angle. To further study the iridescence of the spots, angular resolved spectroscopy was carried out using a custom-made goniometer [36] (Fig. 2(f), S4). Spectrally, an increase in the incident and collection angle θin = θout with respect to the normal to the red spot caused a spectral variation of the blue signal, while the reflectance generated by the red pigment was angle-independent.
The morphology of the scales in the magenta spots and the nanostructure responsible for the blue color were investigated by isolating and imaging a single scale from one of the spots in bright field reflection optical microscopy, followed by correlated scanning electron microscopy (Fig. 4). Optically, the scale appeared uniformly red except for the metallic blue strip (Fig. 4(a)). Correlated scanning electron microscopy (SEM) of that same scale in top view shows parallel ridges running along the entire length of the scale’s upper lamina (Fig. 4(b)). Higher magnification imaging in top view revealed the crossribs connecting the ridges and their hierarchical arrangement, which is typical of some butterfly scales (Fig. 4(c)). The longitudinal ridges are each formed by a multilayer reflector of alternating chitin scutes [37] and air gaps, as confirmed by Fourier Transformed Infrared Spectroscopy (FTIR) (Fig. S6). Each ridge is formed by approximately 10 scutes, alternating with respect to the longitudinal ridges (Fig. 4(c), d) consistently with what seen in other butterfly scales having a similar structure [38–40]; the multilayers are slightly tilted with respect to the scale lamina, such that their number is constant across the ridges length [40,41]. The thickness and the spacing of the scutes in each ridge falls within the range of a few hundreds of nanometers (t = 118 ± 13 nm, average ± standard deviation, N = 30), which is sufficient to interfere with visible light and produce structural coloration through multilayer interference; the spacing between each ridge is, instead, at the micrometer level (1.1 ± 0.1µm, average ± standard deviation, N = 30), thus capable of producing diffractive effects. This suggests that the observed blue coloration could originate from a combination of multilayer reflectors and diffracting elements as also observed for other butterfly species [6,40].
Fig. 4. Morphological characterization of combined pigmentary and structural scales. (a) Focused-stacked bright field optical micrograph of a single scale showing both structural blue (upper strip) and pigmentary red (across the scale). (b) Corresponding scanning electron image of that scale showing the presence of regular ridges running along the length of the scale on the upper lamina. (c) Top-view high magnification scanning electron image of the scales showing ridges formed by scutes’ multilayers. (d) High magnification scanning electron cross-sectional image of scale showing the nanostructured upper lamina formed by alternating scutes.
To investigate the chemical nature of the red color observed in the scales forming the magenta spots and to identify the pigment present, an extraction procedure was carried out following an established protocol [16]. The optical appearance of the scales was studied before and after the extraction in bright and dark field reflection (Fig. 5(a), Fig. S7, S8). Before the extraction, the scales appear diffusely red with structural blue color along the blue strips visible both in bright and in dark field reflection. After the extraction, the scales still retain the blue strips, but appeared to have completely lost the red coloration. This experiment thus suggests that the red color is of chemical nature and shows that the blue strips’ optical appearance is minimally affected by the used extraction treatment.
Fig. 5. Pigment isolation and characterization. (a) Bright field reflection (top row, BFR) and corresponding dark field reflection (bottom row, DFR) of a spot of magenta scales before (left column) and after (right column) pigment extraction. (b) Absorbance as a function of wavelength of phenoxazinone-based pigments characteristic of ommatin-like compounds. Inset shows the chemical structure of the ommochrome pigment core. (c) Normalized reflectance as a function of wavelength of red areas of the magenta spots (scales) and of the solidified extracted pigment (extracted pigment). Reported values are average ± standard deviation for Nextracted pigment = 21 and Nscales = 19. (d) Bright field reflection micrograph and (e) corresponding scanning electron micrograph of extracted solidified pigment. (f) Liquid chromatograph of extracted pigments detected at λ = 440 nm showing multiple peaks, labeled A-J and (g) corresponding UV-Vis spectra for each labeled peak; the peaks labeled A, B, F, G and H show the expected double peak typical of ommochrome pigments.
Bright field reflection of the extracted pigment shows amorphous dark red granules (Fig. 5(d)) and SEM analysis did not reveal any crystalline structure (Fig. 5(e)). The reflectance spectra of the extracted dried pigment granules and of the pigment within the scales were compared, showing comparable behavior in terms of spectral shape. A stronger reflectance was measured for the isolated granules compared to the ones within the scales for λ<600 nm, possibly due to the presence of a strong reflecting substrate. However, by considering the baseline difference between the pigment as measured on the scales and the pigment after extraction, a smaller reflectance intensity of the latter is observed for λ>600 nm, along with a broadening of the reflectance peak (Fig. 5(c)). These spectral variations are possibly caused by the presence of interferents introduced during the extraction step, pigment degradation upon extraction, or the variation of the chemical environment surrounding the pigment [42].
To investigate the nature of the red pigment observed in the magenta spots, an extraction procedure was carried out. The resulting pigment was analyzed using high-performance liquid chromatography (HPLC) and liquid chromatography-mass spectrometry (LC-MS) following established protocols [42] and compared to the HPLC of xanthommatin, one of the most common and well-known ommochromes in invertebrates (Fig. 5). Red pigmented spots were isolated and extracted with acidified methanol, and the resulting orange-red solution was analyzed by liquid chromatography-mass spectrometry (LC-MS), detected by UV-Vis absorption and time-of-flight mass spectrometry immediately after extraction to minimize any alteration of the pigment due to degradation (Fig. 5(b), (f), (g), Fig. S9-S14).
The extracted pigment was found to exhibit absorption peaks at λ1= 422 nm and λ2= 439 nm, which closely match the peaks characteristic of ommochrome pigments based on a differentially substituted cinnabarinic acid core [22,42,43] (λmax = 420-450 nm) (Fig. 5(b)). The pigment is tentatively identified as having a phenoxazinone core which is characteristic of the yellow-to-red ommatin pigments [44], which is consistent with the presence of ommochrome pigments observed in other insect species [42,44] and with red-sensitive pigments in the Riodinidae butterfly family [45,46]. HPLC analysis revealed the presence of eluted peaks, which may represent different pigments or degradation products of a single pigment (Fig. 5(f), g). Despite poor ionization and a large number of interferents (Fig. S9), tentative ion candidates for the pigment were identified (Table S1).
3. Conclusion
In conclusion, this study provides insights into the optical properties of the Lyropteryx apollonia butterfly wings, specifically the magenta color observed on the scales that form the ventral spots. By combining optical micro-spectroscopy, electron microscopy, and chemical extraction techniques, the study shows that the magenta color results from a combination of structural blue and pigmentary red coloration mechanisms. The blue reflectance is caused by visible light interference with chitin-based nanostructured ridges on the upper lamina of the scales, while the diffuse red coloration is likely due to an ommochrome pigment with a cinnabarinic acid core distributed across the scale. The blue and red domains can be individually resolved at the microscale, but not at the macroscale, in accordance with the additive color mixing principle. This study provides inspiration for the fabrication of materials with non-spectral colors that are angle-dependent and can be achieved through the combination of pigmentary and structural design principles.
Funding
Office of Naval Research (N00014-22-1-2429).
Disclosures
The authors declare no competing interests.
Data availability
All data sets are available in the main text, in the supplementary materials, or from the corresponding author upon reasonable request.
Supplemental document
See Supplement 1 for supporting content.
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