View metadata, citation and similar papers at core.ac.ukDownloaded from rsif.royalsocietypublishing.org on July 14, 2010 brought to you by CORE provided by University of Groningen Digital Archive J. R. Soc. Interface (2010) 7, 765–771 doi:10.1098 /rsif.2009.0352 Published online 14 October 2009 Reflectivity of the gyroid biophotonic crystals in the ventral wing scales of the Green Hairstreak butterfly, Callophrys rubi K. Michielsen 1, H. De Raedt 2, * and D. G. Stavenga 3 1EMBD, Vlasakker 21, 2160 Wommelgem, Belgium 2Department of Applied Physics, Zernike Institute for Advanced Materials, and 3Department of Neurobiophysics, University of Groningen, Nijenborgh 4, 9747 AG Groningen, The Netherlands We present a comparison of the computer simulation data of gyroid nanostructures with opti- cal measurements (reflectivity spectra and scattering diagrams) of ventral wing scales of the Green Hairstreak butterfly, Callophrys rubi . We demonstrate that the omnidirectional green colour arises from the gyroid cuticular structure grown in the domains of different orientation. We also show that this three-dimensional structure, operating as a biophotonic crystal, gives rise to various polarization effects. We briefly discuss the possible biological utility of the green coloration and polarization effects. Keywords: structural colour; butterflies; Lycaenidae; gyroid; photonic bandgap materials 1. INTRODUCTION remained elusive. Recently, we identified the cuticular structure in the ventral wing scales of C. rubi as a Butterflies are well known for their brilliant and often gyroid ( Michielsen & Stavenga 2008 ), a promising struc- iridescent colours ( Vukusic & Sambles 2003 ), but ture for biomimetic applications ( Parker & Townley some species have perfectly cryptic coloration to pro- 2007 ), such as replication ( Huang et al. 2006 ; Gaillot tect themselves from predators ( Kerte´sz et al. 2006 ). et al. 2008 ) into three-dimensional photonic structures. A striking example is the Green Hairstreak, Callophrys In this paper, we compare finite-difference time- rubi (Linnaeus 1758), a small butterfly that can be domain (FDTD) ( Taflove & Hagness 2005 ) simulation found in a wide range of habitats including rough data with the measured reflectivity spectra and scatter- shrubby grasslands, meadows, heathland, woodland ing diagrams of the ventral wing scales of C. rubi and and forest edges throughout Europe, Asia and Siberia demonstrate that its camouflaging omnidirectional (Asher et al. 2001 ). The sexes of C. rubi are very similar green colour arises from the gyroid cuticular structure in appearance: the wings are dull brown on the upper grown in the domains of different orientation. We also side (dorsal side) and bright matte-green on the under- show that this three-dimensional structure, operating side (ventral side). Under an Atlantic climate, one as a biophotonic crystal, gives rise to various polariz- generation is produced each year, but in many parts ation effects. In general, the response of insects to of the Palaearctic region C. rubi has two generations. polarized light may be direct, indirect via different pat- The flight period is concentrated between May and terns of reflection from a substrate, or both. We suggest early June or somewhat later, depending on the region that C. rubi may respond to (polarized) sunlight in the of origin ( Asher et al. 2001 ). During this time of the process of perching similar to the lycaenid Mitoura year, the vegetation still shows its bright spring green gryneus (Hu bne r 1819) ( Johnson & Borgo 1976 ), a but- coloration. The resting places and perching sites of ¨ terfly living in North America, closely related to and C. rubi are usually green leaves. While resting or perch- also having bright green ventral wings like C. rubi but ing, C. rubi closes its wings, so that the green-coloured with a variable amount of brown scaling. The ventral ventral sides of its wings make it virtually invisible. wing scales of M. gryneus have a gyroid structure The green coloration has been attributed to the pres- equivalent to that of C. rubi (Michielsen & Stavenga ence of a three-dimensional lattice structure organized 2008 ). Statistical data on the changes in the perching in irregular domains ( Morris 1975 ; Ghiradella & behaviour of M. gryneus with the time of day and on Radigan 1976 ; Jones & Tilley 1999 ; Tilley 2000 ), but perching postures support the assumption that the but- a quantitative analysis of the relation between the terfly orients with respect to the electric vector of reflectivity and the three-dimensional structure has the sunlight and the position of the sun ( Johnson & *Author for correspondence ( [email protected] ). Borgo 1976 ). As the perching sites of both M. gryneus Received 12 August 2009 Accepted 17 September 2009 765 This journal is q 2009 The Royal Society Downloaded from rsif.royalsocietypublishing.org on July 14, 2010 766 Reflectivity of biophotonic crystals K. Michielsen et al. and C. rubi are usually green leaves, we suggest that (a) their green colour allows them to find mates using polarization signals for intraspecific communication while remaining camouflaged to their predators, birds with polarization-insensitive eyes. 2. GREEN COLORATION The C. rubi butterflies we investigated were obtained from Dr I. Osipov ( http: // rusinsects.com /main.htm ). All specimens came from a Palaearctic region (South Ural) and were of the male sex. (b) (i) (ii) Butterfly scales are attached to the wing in rows like shingles on a roof, so that only the distal parts of the scales show. In reflected light, the resulting wing colour of C. rubi matches closely that of the plants on which the animal may rest or perch ( figure 1 a). A closer look at the scales reveals bright blue-, green- or yellow-coloured spots on their visible distal parts (figure 1 b). A similar coloration has been observed in the ventral wings of Cyanophrys remus (Kerte´sz et al. 2006 ), another lycaenid. The brownish proximal parts of the scales near the root with which the scale is c attached to the wing act as a dark background and ( ) hence have no direct influence on the overall colour appearance of the wing. The bright coloured spots on the distal parts of the scales vary in intensity and colour with the direction of illumination and obser- vation. This indicates that the origin of these local (d) (e) colours is structural ( Kinoshita et al. 2008 ). In transmitted light, the distal parts of the ventral scales clearly exhibit distinct irregular domains (figure 1 c) corresponding to the coloured spots observed in reflection ( Onslow 1923 ; Vukusic & Sambles 2001 ). Scanning electron microscopy (SEM) shows that the scale has the usual arrangement of ridges and crossribs and that the interior is packed with a three-dimensional Figure 1. ( a) C. rubi in the resting position on an oak leaf, ordered lattice of cuticle ( figure 1 d). Morris (1975) , who showing the green-coloured ventral face of its wings (pho- studied single wing scales, applying light microscopy tography Bea Koetsier). The green colour ensures excellent camouflage in its natural habitat. ( b) Optical micrograph of and transmission electron microscopy (TEM), con- a small region of ventral wing scales taken in reflection. b(i) cluded that they are composed of a mosaic of irregular Illumination with linearly polarized white light while the polygonal domains, with a mean grain diameter of image was captured through a parallel linear analyser; b(ii) 5.4 mm, and that the inside of the domains consists same as in b(i) but the image was captured through a crossed of a simple cubic network with lattice constant linear analyser. Green, blue and yellow spots can be identified. 0.257 mm and an average thickness of four lattice Scale bar, 100 mm. ( c) Optical micrograph of a single ventral units. Ghiradella & Radigan (1976) concluded from wing scale taken in transmission. Several domains are more detailed TEM studies that the internal cuticular observed across the distal part of the scale. The dark longi- lattice was face-centred cubic (FCC) and not simple tudinal lines are the ridges. Scale bar, 50 mm. ( d) Scanning cubic. They also noticed that the cuticular lattice in electron micrograph of part of a scale. Scale bar, 1 mm. Below the network of ridges and crossribs, a three-dimensional the proximal part of the scale is irregular, incomplete cuticular structure is seen. ( e) Gyroid structure modelling the and shallow, thus causing the lack of domains with cuticular structure (16 cubic unit cells). structured cuticle ( figure 1 c) and hence bright color- ation ( figure 1 b). We recently re-examined the TEM images and found that the cuticular lattice in the scales of C. rubi approximates a gyroid structure scales with gyroid structures similar to those of having a body-centred Bravais lattice symmetry, with C. rubi (Michielsen & Stavenga 2008 ). a cuticle volume fraction of 0.17 and a lattice constant For a large range of volume fractions, the gyroid of 363 nm ( figure 1 e) ( Michielsen & Stavenga 2008 ). structure acts as a three-dimensional photonic crystal Also, other recent structural studies have revealed when the refractive index contrast between the that the cuticular structure can be described by a two dielectric components becomes sufficiently large gyroid ( Hyde et al. 2008 ). We also suggested that (n/n0 2.5) ( Martı´n-Moreno et al. 1999 ; Babin et al. other lycaenids such as C. remus and M. gryneus have 2002 ; Maldovan et al. 2002 ; Michielsen & Kole 2003 ). J. R. Soc. Interface (2010) Downloaded from rsif.royalsocietypublishing.org on July 14, 2010 Reflectivity of biophotonic crystals K. Michielsen et al. 767 0.30 ( a) 0.7 0.25 0.6 0.20 0.5 0.15 0.4 reflectivity 0.10 0.3 reflectivity 0.05 0.2 0 0.1 350 400 450 500 550 600 650 700 wavelength (nm) 0 Figure 2. Reflectivity spectrum measured with a microspectro- (b) 0.7 photometer of a single scale of the ventral wing of C.