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Shiny Wing Scales Cause Spec(Tac)Ular Camouflage of the Angled Sunbeam Butterfly, Curetis Acuta

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Shiny Wing Scales Cause Spec(Tac)Ular Camouflage of the Angled Sunbeam Butterfly, Curetis Acuta bs_bs_banner Biological Journal of the Linnean Society, 2013, 109, 279–289. With 8 figures Shiny wing scales cause spec(tac)ular camouflage of the angled sunbeam butterfly, Curetis acuta BODO D. WILTS1*, PRIMOŽ PIRIH2,3, KENTARO ARIKAWA4 and DOEKELE G. STAVENGA1 1Computational Physics, Zernike Institute for Advanced Materials, University of Groningen, Groningen NL-9747AG, The Netherlands 2Department of Biology, Faculty of Biotechnical Sciences, University of Ljubljana, Ljubljana SI-1000, Slovenia 3Department of Materials and Metallurgy, Faculty of Natural Sciences and Engineering, University of Ljubljana, Ljubljana,SI-1000, Slovenia 4Laboratory of Neuroethology, Sokendai-Hayama (The Graduate University for Advanced Studies), Hayama 240-0193, Japan Received 12 December 2012; revised 16 January 2013; accepted for publication 16 January 2013 The angled sunbeam butterfly, Curetis acuta (Lycaenidae), is a distinctly sexually dimorphic lycaenid butterfly from Asia. The dorsal wings of female and male butterflies have a similar pattern, with a large white area in the female and an orange area in the male, framed within brown–black margins. The ventral wings of both sexes are silvery white, which is caused by stacks of overlapping, non-pigmented, and specular-reflecting scales. With oblique illumination, the reflected light of the ventral wings is strongly polarized. We show that the silvery reflection facilitates camouflage in a shaded, foliaceous environment. The ecological function of the silvery reflection is presumably two-fold: for intraspecific signalling in flight, and for reducing predation risk at rest and during hibernation. © 2013 The Linnean Society of London, Biological Journal of the Linnean Society, 2013, 109, 279–289. ADDITIONAL KEYWORDS: camouflage – iridescence – Lycaenidae – polarization – scattering. INTRODUCTION a dull, inconspicuous colour, which then serves to camouflage the butterfly and decrease the risk of A tapestry of numerous small scales imbricates the predation: e.g. the ventral sides of I. io are brown– wings of butterflies, often causing strikingly colourful black, presumably rendering the butterfly inconspi- patterns (Nijhout, 1991). In many species, the pat- cuous against the background when they rest terns differ strongly between the dorsal (upper) and or hibernate. In the green hairstreak butterfly, the ventral (under) wing sides, because of opposite Callophrys rubi, the colour of the ventral wings biological functions. The dorsal wings, which are matches that of plant leaves (Michielsen & Stavenga, exposed in active butterflies, for instance during 2008; Michielsen, De Raedt & Stavenga, 2010; flight, are often brightly coloured. These markings Schröder-Turk et al., 2011). function in intra- and interspecific signalling: for The colour of the wing scales can be mainly pigmen- example, in the radiant blue male Morpho butterflies tary (as in I. io), as a result of pigments deposited in and in the elaborately coloured peacock butterfly, the wing scale structures, or can have a structural Inachis io (Nijhout, 1991; Srinivasarao, 1999; basis (as in C. rubi), when the structure of the scales Kinoshita, 2008). In most butterflies, the ventral have periodicities in the nanometer range. Butterfly wings, exposed when the butterflies are at rest, have wing scales commonly consist of two layers: a flat basal lamina and a structured upper lamina. The two layers are joined by pillar-like trabeculae (Ghiradella, 1984; *Corresponding author. E-mail: [email protected] Ghiradella, 1998; Ghiradella, 2010). When the upper © 2013 The Linnean Society of London, Biological Journal of the Linnean Society, 2013, 109, 279–289 279 280 B. D. WILTS ET AL. lamina is irregularly structured, the scale acts as a angle-dependent reflectance measurements. We diffuser, and, in the absence of a light-absorbing discuss the biological function of the silvery-white pigment, thus becomes a white light reflector coloration as an adaptive coloration strategy, serving (Stavenga et al., 2004; Morehouse, Vukusic & for camouflage in a foliaceous environment and as an Rutowski, 2007). For example, the wing scales of white intraspecific signal during patrolling flights. pierids (cabbage butterflies) have highly elaborate, granular structures, which effectively scatter broad- band light (Giraldo, Yoshioka & Stavenga, 2008). MATERIAL AND METHODS These granules contain a pterin pigment, leucopterin ANIMALS (Yagi, 1954), which absorbs light in the ultraviolet Specimens of Curetis acuta Moore, 1877 (Lycaenidae) wavelength range (invisible for humans, but visible were captured near Sokendai, Shonan Village, Kana- for insects). Xanthopterin and erythropterin, other gawa Prefecture, Japan. Micrographs of wing patches pterins common in pierid butterflies, also absorb in the were taken with a Zeiss Universal Microscope (Carl blue and green wavelength ranges, respectively, and Zeiss AG, Oberkochen, Germany) and an Olympus thus the wings have a yellow, orange, or red colour SZX16 stereomicroscope (Olympus, Tokyo, Japan), (Wijnen, Leertouwer & Stavenga, 2007). equipped with Kappa DX-40 (Kappa Optronics Structural coloration occurs when periodic struc- GmbH, Gleichen, Germany) and Olympus DP70 tures enhance light reflection in a specific wavelength digital cameras, respectively. range by constructive light interference and suppress light reflection at other wavelengths by destructive interference (Vukusic & Sambles, 2003; Kinoshita, SCANNING AND TRANSMISSION Yoshioka & Miyazaki, 2008). The periodicity can be ELECTRON MICROSCOPY one-dimensional, as in the multilayers of the blue- coloured wing scales of various lycaenids (Wilts, The ultrastructure of the wing scales was investi- Leertouwer & Stavenga, 2009), or three-dimensional, gated with an XL-30 ESEM scanning electron micro- as in the gyroid-type photonic crystals in the green- scope (Philips, Eindhoven, Netherlands). Prior to coloured wing scales of the papilionid Parides imaging, the wing scales were sputtered with palla- sesostris (Land, 1972; Vukusic & Sambles, 2003; dium. For transmission electron microscopy (TEM) of Michielsen & Stavenga, 2008; Wilts et al., 2012a). In the scales, wing parts were prefixed in 2% parafor- 1 many butterfly species the structural colours are maldehyde and 2.5% glutaraldehyde in 0.1 mol l- tuned by filtering pigments: that is, pigmentary and sodium cacodylate buffer (CB, pH 7.3) for ~45 min, structural colorations are combined, for instance in then post-fixed in 2% osmium tetroxide in 0.1 M CB the green scales of P. sesostris (Wilts et al., 2012a) and for 2 h at room temperature (25 °C), and further in the purple wing tip scales of the male pierid Colotis block-stained in 2% uranyl acetate in 50% EtOH for regina (Wilts, Pirih & Stavenga, 2011). 1 h. After dehydrating with a graded series of ethanol Structural coloration commonly refers to reflections and infiltration with propylene oxide, the tissues were in a restricted wavelength band. Some structurally embedded in Spurr’s resin. The tissues were cut into coloured butterfly species, however, have wing scales 40–50-nm ultrathin sections, which were observed reflecting broadband light, for example the nymphalid using a Hitachi H7650 (Tokyo, Japan) transmission Argyrophorus argenteus, where the wings are fully electron microscope. covered by silvery reflecting scales (Vukusic, Kelly & Hooper, 2009). Silvery reflecting wing scales also occur in patches at the ventral wings of several fri- SPECTROMETRY tillary butterflies (Simonsen, 2007; Giraldo, 2008). Reflectance spectra of the wings were measured with Another prominent example is the angled sunbeam a bifurcated probe (Avantes FCR-7UV200; Avantes, butterfly Curetis acuta, which is a widespread Asian Eerbeek, the Netherlands) and with an angle- butterfly (Eliot, 1990). In central Japan, its flying dependent reflectance measurement (ARM) set-up, period is between May and November, with a peak in using an Avaspec 2048-2 CCD detector array spec- the autumn on warm and sunny days. The ventral trometer. The procedures were performed as wings of both sexes of C. acuta are almost fully described previously (Pirih, Wilts & Stavenga, 2011; covered by silvery coloured scales, but the coloration Stavenga et al., 2011). Transmittance spectra of single of the dorsal wings is sexually dimorphic (see Fig. 1). scales were measured with a microspectrophotometer To unravel the spectral and spatial reflection proper- (MSP), consisting of a Leitz Ortholux microscope, ties of C. acuta wings and wing scales, we have with an Olympus 20¥ objective (NA 0.46), connected applied a variety of optical methods: among others with the Avantes spectrometer. The reference was a microspectrophotometry, imaging scatterometry, and diffuse white reflectance tile (Avantes WS-2). © 2013 The Linnean Society of London, Biological Journal of the Linnean Society, 2013, 109, 279–289 SHINY CAMOUFLAGE OF CURETIS ACUTA 281 Figure 1. Sexual dichromatism of the angled sunbeam butterfly, Curetis acuta, and reflectance spectra. A, dorsal side of the female C. acuta with large, white-coloured areas on the fore- and hindwing, framed by brown–black borders. B, dorsal side of the male, with large, orange–red-coloured areas. C, brilliant-white ventral side of the female. (The ventral wing side of the male is identical.) D, reflectance spectra measured with a bifurcated probe of the numbered wing areas in (A–C). Scale bar: 1 cm. IMAGING SCATTEROMETRY sets. The dorsal fore- and hindwings in both sexes are For investigating the spatial reflection characteristics framed within brown–black
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