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Coloration Principles of the Great Purple Emperor Butterfly (Sasakia Charonda) Doekele G

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Coloration Principles of the Great Purple Emperor Butterfly (Sasakia Charonda) Doekele G Stavenga et al. Zoological Letters (2020) 6:13 https://doi.org/10.1186/s40851-020-00164-6 RESEARCH ARTICLE Open Access Coloration principles of the Great purple emperor butterfly (Sasakia charonda) Doekele G. Stavenga1* , Hein L. Leertouwer1 and Kentaro Arikawa2 Abstract The dorsal wings of male Sasakia charonda butterflies display a striking blue iridescent coloration, which is accentuated by white, orange-yellow and red spots, as well as by brown margins. The ventral wings also have a variegated, but more subdued, pattern. We investigated the optical basis of the various colors of intact wings as well as isolated wing scales by applying light and electron microscopy, imaging scatterometry and (micro)spectrophotometry. The prominent blue iridescence is due to scales with tightly packed, multilayered ridges that contain melanin pigment. The scales in the brown wing margins also contain melanin. Pigments extracted from the orange-yellow and red spots indicate the presence of 3-OH-kynurenine and ommochrome pigment. The scales in the white spots also have multilayered ridges but lack pigment. The lower lamina of the scales plays a so- far undervalued but often crucial role. Its thin-film properties color the majority of the ventral wing scales, which are unpigmented and have large windows. The lower lamina acting as a thin-film reflector generally contributes to the reflectance of the various scale types. Keywords: Wing scales, Iridescence, Thin films, Structural coloration, Spectrophotometry, Scatterometry Introduction ridges made up of narrow piles of partly overlapping Sasakia charonda, the national butterfly of Japan since lamellae that are connected by crossribs [5–7]. 1957, is locally known as oh-murasaki, or the great The scale structures scatter incident light, which, in purple emperor. Indeed, the dorsal wings of the male the absence of pigment, results in white-colored scales. display a striking, blue-purple central wing area, which is In the presence of pigments, the scattered light is fil- accentuated by a surrounding brown margin dotted with tered, dependent on the pigment’s absorption spectrum, orange-yellow spots. A prominent red spot exists basally thus resulting in a pigmentary (or chemical) color. The on the hindwings. The species is distinctly sexually di- pigments expressed in the scales are rather characteristic morphic, as the dorsal wings of the (slightly larger) female for the various butterfly families [14]. For instance, lack the brilliant blue-purple iridescence of the male [3]. pterins are the dominant pigments in Pieridae [2, 31], As holds universally for butterflies, the color pattern is ommochromes and their precursor 3-OH-kynurenine created by a lattice of scales that covers the wings like color the wings of Nymphalidae [4, 10, 15, 19], and mo- tiles on a roof. The scale material, chitin, is structured lecular compounds of kynurenine bound to N-β-alanyl- into a thin, plate-like lower lamina and an elaborate dopamine (NBAD) create the papiliochromes found in upper lamina. The latter consists of numerous parallel Papilionidae [16, 17, 27]. All butterfly families employ mel- anin in brown and black scales. When the scales contain regular-arranged, nanosized structures, light interference creates a structural (or * Correspondence: [email protected] 1Surfaces and thin films, Zernike Institute for Advanced Materials, University physical) color. Notably, the lower lamina, because of its of Groningen, Nijenborgh 4, NL-9747, AG, Groningen, the Netherlands thickness being on the order of 100–300 nm, always acts Full list of author information is available at the end of the article © The Author(s). 2020 Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article's Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article's Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creativecommons.org/licenses/by/4.0/. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated in a credit line to the data. Stavenga et al. Zoological Letters (2020) 6:13 Page 2 of 10 as a thin-film reflector [18, 22]. By adjusting the actual of S. c. charonda. Additional specimens captured in thickness, the color of the reflected light can be finely China and Korea were purchased from a commercial tuned [22, 30]. Another structural coloration is well supplier (The Bugmaniac). Close-up photographs of known from the iconic Morpho butterflies; their scales small wing areas and isolated scales of both the abwing have ridges folded into chitin-air multilayers, which cre- (upper) side and adwing (under) side (i.e., facing the ate intensely blue wings [7, 28]. Further tuning of the wing) were made with a Zeiss Universal microscope scale color can occur by combining the structural color- using a Zeiss Epiplan 16x/0.35 objective (Zeiss, Oberko- ation with wavelength-selective absorbing pigments [32, chen, Germany). 33], but when the scale contains a high melanin concen- tration, its color is lost [25, 29]. Spectrophotometry Pigmentary coloration is generally diffuse and nondirec- Wing reflectance spectra were measured with a bifurcated tional, while structural coloration is often called metallic probe connected to a halogen/deuterium light source and because the reflected light strongly depends on the direc- an Avantes AvaSpec-2048-2 CCD detector array spectrom- tions of illumination and viewing. The two coloration eter (Avantes, Apeldoorn, Netherlands). The angle of illu- mechanisms, which thus can be easily distinguished, are mination was approximately normal with respect to the both applied in the wings of male S. charonda. The brown, wing surface. A microspectrophotometer consisting of a yellow and red scales are found to be colored by pigments Leitz Ortholux microscope and the Avantes spectrometer deposited in scales having the basic butterfly scale struc- was used to measure the reflectance spectra of individual ture, where the ridges are made up of a few (at most 2–3) scales, which were removed from the wing and glued to overlapping lamellae. By contrast, the blue-purple scales the tip of pulled-glass pipettes. The reference for all reflect- of the central wing area have enhanced ridges with up to ance measurements was a white diffuse standard (Avantes seven overlapping lamellae, which thus create a multilayer WS-2). The absorbance spectra of the pigment extracts, causing a distinct iridescent coloration [11, 12]. obtained by immersing small yellow and red wing areas in Medina et al. [13] studied the spatial and spectral a solution of 50:1 methanol: 1 M hydrochloric acid, were characteristics of the iridescent wings of S. charonda, measured with a setup consisting of the halogen/deuterium but the applied spectral analysis focused on human col- light source, optical fibers, and the detector array. orimetry and thus was restricted to wavelengths above 400 nm. The visual system of S. charonda includes ultra- Anatomy of the wing scales violet light, as the photoreceptors have peak wavelengths To examine the scales’ anatomy, wing pieces were sput- at ~ 340, 430 and 550 nm [9]; therefore, the wing reflect- tered with platinum and observed with a JSM-6490LV ance spectra should also be measured in the short wave- scanning electron microscope (JEOL, Tokyo, Japan). For length range. transmission electron microscopy, wing parts were pre- Here, we present a more comprehensive analysis of fixed in 2% paraformaldehyde and 2.5% glutaraldehyde − the spectral properties of the variously colored wing in 0.1 mol l 1 sodium cacodylate buffer (CB, pH 7.3) areas together with the anatomy and spatial reflection overnight at 4 °C. Embedding in Spurr was followed by characteristics of their scales. We confirm that the dehydration with a graded series of acetone and infiltra- prominent blue wing coloration is caused by scales with tion with propylene oxide. Tissue sections with a thickness multilayered ridges, but we find that the thin-film reflec- of 50 nm were observed with an H-7650 transmission tors of the scales’ lower laminae, often combined with electron microscope (Hitachi, Tokyo, Japan) equipped different pigments, importantly determine the coloration with a CCD camera (Quemesa, Seika Digital Image Corp., of S. charonda. The optical mechanisms determining Tokyo, Japan), and the images were analyzed with iTEM butterfly coloration appear to be quite universally applic- software (Olympus, Tokyo, Japan). able to other nymphalid butterflies [8, 25]. Imaging scatterometry Materials and methods Imaging scatterometry was applied to visualize the far-field Specimens and photography angular distribution of the light scattered from single scales A mounted male S. charonda charonda (Japanese sub- gluedattheendofpulled-glassmicropipettes.Thesample species) of the Sokendai-Hayama butterfly collection was was positioned in the first focal point of the scatterometer’s photographed with a Nikon D70 digital camera equipped ellipsoidal mirror, which collects light from a full hemi- with an F Micro-Nikkor macro objective (60 mm, f/2.8; sphere. A narrow aperture beam (5°) provided by a xenon Nikon, Tokyo, Japan). UV images were made by using a lamp illuminated a small area of a scale (diameter ~ 13 μm). blacklight lamp and the camera’s red channel. We ap- A piece of magnesium oxide served as a white diffuse refer- plied normally incident, obliquely incident and transmit- ence object.
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