Bioinspired Micrograting Arrays Mimicking the Reverse Color Diffraction Elements Evolved by the Butterfly Pierella Luna

$Bioinspired Micrograting Arrays Mimicking the Reverse Color Diffraction Elements Evolved by the Butterfly Pierella Luna$

Bioinspired micrograting arrays mimicking the reverse color diffraction elements evolved by the butterfly Pierella luna

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Citation England, G., M. Kolle, P. Kim, M. Khan, P. Munoz, E. Mazur, and J. Aizenberg. 2014. “Bioinspired Micrograting Arrays Mimicking the Reverse Color Diffraction Elements Evolved by the Butterfly Pierella Luna.” Proceedings of the National Academy of Sciences 111 (44) (October 6): 15630–15634. doi:10.1073/pnas.1412240111.

Published Version doi:10.1073/pnas.1412240111

Citable link http://nrs.harvard.edu/urn-3:HUL.InstRepos:27417440

Terms of Use This article was downloaded from Harvard University’s DASH repository, and is made available under the terms and conditions applicable to Open Access Policy Articles, as set forth at http:// nrs.harvard.edu/urn-3:HUL.InstRepos:dash.current.terms-of- use#OAP 1 69 2 Bio-inspired micro-grating arrays: mimicking the 70 3 71 4 reverse color diffraction elements evolved by the 72 5 73 6 74 7 butterfly Pierella luna 75 8 * *†§ ‡ ‡ * * *‡§ 76 9 Grant England , Mathias Kolle , Philseok Kim , Mughees Khan , Philip Muñoz , Eric Mazur & Joanna Aizenberg 77 10 78 *School of Engineering and Applied Sciences, Harvard University, Cambridge, MA 02138 †Department of Mechanical Engineering, Massachusetts Institute of 11 Technology, Cambridge, MA, 02139 ‡Wyss Institute for Biologically Inspired Engineering, Harvard University, Cambridge, MA 02138 §Corresponding authors 79 12 80 13 Submitted to Proceedings of the National Academy of Sciences of the United States of America 81 14 82 15 Recently, diffraction elements that reverse the color sequence nor- tion effect results from the local morphology of individual scales 83 16 mally observed in planar diffraction gratings have been found in within the colored spot on the fore wings (12). The top parts 84 17 the wing scales of the butterfly Pierella luna. Here, we describe the of the scales are curled upwards, orienting lines of periodically 85 18 creation of an artificial photonic material mimicking this reverse arranged cross-ribs perpendicular to the wing surface and the 86 19 color-order diffraction effect. The bio-inspired system consists of wing surface normal. (Fig. 1C,D). Light incident at an angle onto 87 20 ordered arrays of vertically oriented micro-diffraction gratings. the curled parts of the scales is diffracted by the cross-rib structure 88 21 We present a detailed analysis and modeling of the coupling of acting as a diffraction grating, with a periodicity of ∼400nm. The 89 22 diffraction resulting from individual structural components and alignment of the grating perpendicular to the surface results in the 90 23 demonstrate its strong dependence on the orientation of the reverse color sequence that can be observed in angularly resolved 91 24 individual miniature gratings. This photonic material could provide reflection spectra and in the diffraction pattern (Fig. 1E,F). 92 25 a basis for novel developments in bio-sensing, anti-counterfeiting The identification of this unusual diffraction effect on the 93 26 and efficient light managementSubmission in photovoltaic systems and light wings of P. luna PDF(12) provided inspiration for the development 94 27 emitting diodes. of a bio-inspired photonic system that incorporates vertically 95 28 oriented micro-diffraction gratings with sub-micrometer peri- 96 | | 29 Bio-inspired optics Micro-gratings Biophotonics odicity analogous to the key features observed in the natural 97 30 structure. In addition, the artificial system displays a periodic 98 31 Three-dimensional photonic crystals (1-5), materials with arrangement of the individual vertical gratings in large arrays with 99 32 two-dimensional micro- or nano-sized periodic morphologies (6- two-dimensional micro-scale periodicity. This structural feature, 100 33 8) and one-dimensional multilayer configurations (9) have been which is not found in the natural organism, enriches the optical 101 34 identified as the primary cause of structural coloration in a wide signature of the artificial system via coupling of the diffractive 102 35 variety of non-related biological organisms. In contrast, surface- modes of the two present hierarchical morphologies. In the fol- 103 36 confined diffraction elements for the separation of incident light lowing, we discuss the optical properties of the artificial system 104 37 into specific colors are less abundant in nature and have only been and demonstrate that the modification of either one of the grating 105 38 discovered in a handful of organisms (10), including a fossil poly- morphologies changes the diffraction signature in predictable 106 39 chaete (7), the sea mouse Aphrodita sp. (6) and some flowering ways. 107 40 plants (11). Recently, diffraction elements that reverse the color 108 41 sequence normally observed in planar diffraction gratings have 109 42 been found in the scales of the butterfly Pierella luna (12). 110 43 Inspired by this biological light manipulation strategy, we de- Significance 111 44 vised an artificial material morphology mimicking the butterfly’s 112 45 diffraction effect by creating periodic arrays of vertically oriented In the course of evolution, many organisms have developed 113 46 individual micro-diffraction gratings. In addition to the butterfly- unique light manipulation strategies that rely on intriguing 114 47 inspired reverse color order diffraction arising from each in- combinations of a broad range of optical effects generated by 115 dividual micro-grating, the periodicity between the individual materials with sophisticated multi-scale hierarchical structural 48 arrangements. By exploiting the optical principles underly- 116 49 gratings causes diffraction on a different length scale, leading ing natural structural color, we can generate new photonic 117 50 to complex intensity distributions in experimentally measured materials. Researchers have only just begun to match na- 118 51 angularly resolved reflection spectra. An in-depth analysis of ture's morphological and compositional complexity in man- 119 the observed diffraction phenomenon complemented by optical made materials using nanofabrication. We present a bioin- 52 spired photonic material that mimics the reverse color order 120 53 modeling revealed a strong dependence of the optical signature diffraction found in the butterfly Pierella Luna. Exploiting and 121 54 on the orientation of the gratings. Such an effect can only be seen improving the butterfly's strategy, we create new photonic 122 55 because of the hierarchical nature of the superposed, orthogonal materials that increase our basic understanding of the optical 123 grating features. To further elucidate the role of the different interplay of hierarchical structures and provide a platform for 56 the development of novel photonic devices. 124 57 structural components for the emerging reflection spectra, the 125 58 initially vertically oriented individual micro-gratings were sub- Reserved for Publication Footnotes 126 59 jected to a tilt, resulting in a predictable change of the surface's 127 60 optical signature. 128 61 The dorsal side of the fore and hind wings of P. luna males 129 62 are dull brown in diffuse ambient illumination (Fig. 1A, left). 130 63 When exposed to directional illumination at grazing incidence, 131 64 a coin-sized spot on each forewing displays an angle-dependent 132 65 color variation across the whole visible spectrum (Fig. 1A, right). 133 66 The color changes from red to blue with increasing observation 134 67 angle unlike the variation from blue to red normally observed in 135 68 conventional diffraction gratings (13). This reverse color diffrac- 136

www.pnas.org ------PNAS Issue Date Volume Issue Number 1--?? 137 vidual plates well preserved. The silicon master is formed using 205 138 the Bosch process (15), in which multiple etching and passivation 206 139 steps give rise to the periodic undulations on the micro-plate 207 140 surface. The pitch and height of these grating structures can be 208 141 controlled by adjusting the etching parameters (16, 17). Here, 209 142 they are chosen to be comparable to the spacings and dimensions 210 143 of the diffraction-inducing micro-ribs on the P. luna scales (Fig. 211 144 2B), and hence are expected to cause a similar diffraction effect. 212 145 It is important to notice that in the biological system, the 213 146 periodicity of the diffraction grating-supporting scales is of the 214 147 order of 80 ± 10 µm along their length and 60 ± 10 µm perpen- 215 148 dicular to the scale axis (Fig. 1B). Due to these large distances 216 149 between diffraction elements and a non-negligible amount of 217 150 irregularity in the location of individual scales, no coherence is ob- 218 151 served for light diffracted from adjacent scales. The overall color 219 152 splitting only results from the diffraction caused by the cross-rib 220 153 gratings on the individual scales, which is confirmed by variable 221 154 angle spectroscopy and by diffraction microscopy measurements 222 155 (Fig. 1D). Unlike in the biological system, the individual micro- 223 156 diffraction gratings in the artificial system are intentionally ar- 224 157 ranged in a highly periodic manner, which is expected to result in 225 158 a richer diffraction signature and provide additional possibilities 226 159 of tailoring the interaction of light beyond the diffraction induced 227 160 by the scallops on the plates. 228 161 Variable observation-angle spectroscopy performed on the 229 162 Submissionartificial system servesPDF to spectrally and angularly resolve parts of 230 163 the complex diffraction pattern (Fig. 2C). For each measurement 231 164 the plane of light incidence is chosen to be perpendicular to the 232 165 surface of the individual micro-plates. The light incidence angle 233 166 θI is fixed and the observation angle θD is varied in the plane of 234 167 light incidence to capture light reflected in an angular range of 235 168 ±75° around the sample surface normal. Two main features are 236 169 observed in these measurements: 237 170 Fig. 1. Optical properties of the curled scales in buttery Pierella luna. A, (1) Straight lines of higher intensity resulting from diffraction 238 171 Optical image of P. luna under diffuse lighting (left) and directional lighting caused by the inter-plate periodicity represent the individual 239 172 at grazing incidence (right). Scale bar 10 mm. B, Optical micrograph of P. diffraction orders; the experimentally observed locations of these 240 173 luna scales under oblique illumination. Scale bar 50 µm. C, Scanning electron diffraction orders (shown in Fig. 2C,H) can be directly calculated 241 174 micrograph (SEM) of scales in the colored wing region. Scale bar 50 µm. using the grating equation (13). An example of such a calculation 242 175 White dashed boxes in (B) and (C) mark the curled tops of the scales from 243 which the color originates. D, Close-up image of the curled region of the can be seen in SFig. 1. Due to the large inter-plate pitch of 12 176 scale from which the color originates. Scale bar 20 µm E, Gray-scale encoded µm the angular separation between adjacent diffraction orders 244 177 reﬂection intensity as a function of wavelength and propagation direction and the free spectral range of each individual order are small. 245 178 showing the inverse color order diffraction pattern for 65° light incidence. For light incident at an angle θI = 45°, eight positive propagating 246 179 The red dashed line indicates the predicted location of the diffraction due to diffraction orders (left of the 0th order at sin(θ) = ‒0.71 in Fig. 247 180 the cross-rib structures for an orientation of the curled scale sections of -25° 2C) and 53 negative propagating orders are captured with the 248 181 relative to the surface normal and a cross-rib periodicity of 390 nm. The blue highest intensity in the direct reflection (0th order) and in the 249 182 shaded region signiﬁes the angle range for which the diffraction microscopy adjacent orders. 250 183 image of curled P. luna scales in (F) was obtained. The color bar under the (2) There is an arc-shaped distribution of intensity maxima 251 184 graph shows the human-eye perceived color for the spectra observed at the 252 corresponding angles calculated by the CIE 1931 standards [18]. F, Diffraction across different diffraction orders (emphasized by dashed red 185 microscopy image of the colored spot of a P. luna wing showing multiple lines in Fig. 2C). 253 186 diffracted orders in similar angular locations due to the variation in the This anomalous redistribution of light in the diffraction or- 254 187 position and angle of the diffracting scales. ders is caused by the scallops on each individual plate. To prop- 255 188 erly describe the diffraction resulting from the micro-diffraction 256 189 gratings oriented normally to the substrate, the grating equation 257 The artificial system consists of an array of individual 10 µm 190 (13) has to be reformulated taking into account their vertical 258 long, 2 µm wide and 18 µm high plates arranged in rows with an 191 orientation for diffraction in the plane of the scallops: 259 192 inter-plate spacing of 10 µm and a separation of 5 µm between 260 193 individual rows of plates (Fig. 2A). These parameters result in an [1] 261 194 overall periodicity of 12 µm in the direction perpendicular to the where d is the grating periodicity, m is the diffraction order, 262 195 plates and 15 µm in the direction collinear with the plane of the θI is the light incidence angle and θD is the diffraction angle. 263 196 plates and the sample surface. A periodic wave pattern—termed This equation describes the arc shape-like pattern observed in the 264 ∼ 197 “scallops”—of 500nm pitch runs along the sides of each individ- experiment under the assumption that the plates are vertical (Fig. 265 198 ual plate (Fig. 2B). 2C red shaded region). 266 199 The bio-inspired diffraction elements are fabricated in a Imaging of the diffraction patterns by diffraction microscopy 267 200 double-molding procedure. Starting from a silicon master, a peri- provides a direct visualization of the effects observed in the 268 201 odic array of scalloped micro-plates is first cast into polydimethyl- variable-angle spectroscopy measurements. The angle range that 269 202 siloxane to form a negative mold (14), which is then replicated can be visualized in these measurements is determined by the 270 203 with a UV-curable epoxy to produce a positive replica of the numerical aperture of the microscope objective. For a given light 271 204 master silicon structure with the original scallops on the indi- incidence angle θI the diffraction caused by the periodic ensemble 272

2 www.pnas.org ------Footline Author 273 341 274 342 275 343 276 344 277 345 278 346 279 347 280 348 281 349 282 350 283 351 284 352 285 353 286 354 287 355 288 356 289 357 290 358 291 359 292 360 293 361 294 362 295 363 296 364 297 365 298 Submission PDF 366 299 Fig. 2. Geometry and optical properties of the artificial photonic structure mimicking P. luna with vertically oriented (top row) and tilted (bottom row) 367 300 diffraction gratings. A, SEM of the array of scalloped microplates. Scale bar 5 µm. B, SEM of an individual plate with regular scallops. Scale bar 2 µm. C, 368 301 Variable angle spectroscopic data for 45° light incidence showing the arc-shaped diffraction pattern caused by the diffraction from the scallops coupled with 369 302 the diffraction due to the plates. The measurement geometry is shown in the top right inset. The red overlay displays where the first diffraction order of 370 303 the scallops based on the grating equation (eq. 2) is expected for tilt angles of ‒3° to 5°. The color bar under the graph shows the human-eye perceived 371 304 color for the spectra observed at the corresponding angles calculated by the CIE 1931 standards (18). D, Diffraction pattern caused by the periodic ensemble 372 305 of micro-plates for 45° light incidence. A choice of propagation angles is visualized by the white dashed lines. The diffraction orders within the blue frame 373 306 correspond to the diffraction observed in the angular range marked in blue in (C). E, Diffraction pattern resulting from the scallops on individual plates. The 374 307 diffraction orders within the yellow frame correspond to the diffraction observed in the angular range marked in yellow in (C). F-K, Same as (A-E), for tilted 375 gratings. Red overlay in (H) marks the range where higher intensities are predicted by the grating equation for tilt angles between 19° and 27°. 308 376 309 377 310 378 311 379 312 380 313 381 314 382 315 383 316 384 317 385 318 386 319 387 320 388 321 389 322 390 323 391 324 392 325 393 326 394 327 Fig. 4. Diffraction discretization. A,1 micron wide unit cell for diffraction 395 328 Fig. 3. Modeling of the expected diffraction patterns originating from the grating simulated via FDTD. B, Reflected spectra calculated from FDTD 396 329 ordered array of gratings with 45° illumination. A, Calculated diffraction simulation of (A) showing bright spots in each diffracted order with discrete 397 330 pattern for upright plates with scallops. B, Calculated diffraction pattern jumps in the diffracted wavelength. 398 331 for upright plates without scallops. C, Calculated diffraction pattern for 23° 399 332 tilted plates with scallops. D, Calculated diffraction pattern for 23° tilted 400 333 plates without scallops. on the sample through the microscope objective, allows for the 401 334 capturing of the diffraction component induced by the scallops 402 335 on the individual plates (Fig. 2E, with the signal in the yellow 403 336 of plates is most clearly observed when collecting light with the box corresponding to the yellow shaded spectral range in Fig. 404 2C). This feature is easily distinguished from the diffraction of 337 objective's axis aligned with the specular reflection direction θD = 405 the plate ensemble by the wider color spread. 338 ‒θI (Fig. 2D, with the signal in the blue box corresponding to the 406 339 blue shaded spectral range in Fig. 2C). Imaging of the sample's Overall, the measurements provide clear evidence of coupling 407 340 diffraction in the Littrow mounting (13), where light is incident between the first order mode of the scallop diffraction and the 408

Footline Author PNAS Issue Date Volume Issue Number 3 409 inter-plate periodicity based diffraction modes. The diffraction in photovoltaic systems (38-40), enhanced light extraction and 477 410 coupling can be controlled by adjusting the pitch of the scallops radiation profile shaping in light emitting diodes (41-43) and 478 411 on individual plates and the inter-plate geometry in the manufac- optically variable devices in consumer product design and anti- 479 412 turing procedure. Likewise, a change in inclination of the micro- counterfeiting (44-46). 480 413 diffraction gratings with respect to the substrate is expected to be Our results demonstrate the versatility of a bio-inspired ap- 481 414 reflected in a variation of the diffraction patterns. This change proach towards the creation of novel photonic systems. The 482 415 can indeed be observed by imposing a controlled tilt of ∼20° on unique diffraction-inducing nano- and micro-scale architecture 483 416 the micro-plates by shearing the sample (Fig. 2F,G). previously discovered in the scales of the male butterfly P. luna 484 417 The bending leaves the locations of the diffraction modes served as inspiration for artificial micro-diffraction grating arrays. 485 418 resulting from the inter-plate periodicity largely unaffected. Only While our photonic system mimics the reverse diffraction color 486 419 minor wavelength-dependent intensity variations in each diffrac- sequence found upon interaction of light with the butterfly's 487 420 tion mode are apparent (Fig. 2H,I). At large angles , measured scales, it also provides additional complexity in the diffraction 488 421 from the sample surface normal, a region of higher reflection patterns due to a periodic arrangement of the diffraction ele- 489 422 intensity appears, which is related to the inclination of the in- ments not found in the natural structure. Such arrays provide 490 423 dividual plates, i.e. the blaze of the grating array. By contrast, a platform for hierarchical photonic systems displaying unique 491 424 the diffraction caused by the scallops on the individual plates is diffraction coupling. A detailed optical analysis and modeling of 492 425 strongly influenced by the variation in plate tilt angle shifting the the diffraction patterns allowed us to observe, understand and 493 426 observed arc-shaped pattern in wavelength and angular position decouple diffraction effects induced by the plate ensemble and 494 427 (Fig. 2H,K). For micron-sized diffraction gratings which have a by the regular scalloping of individual plates. A variation of the 495 428 tilt angle, β, relative to the surface normal, the diffraction grating light incidence angle results in the expected shifting of the plate 496 429 equation can be reformulated as: ensemble diffraction modes but does not affect the diffraction 497 430 resulting from individual plates. On the other hand, a variation 498 [2] 431 in plate inclination leaves the inter-plate geometry diffraction 499 432 By calculating a fit for the arc-shaped intensity distribution modes untouched but has a strong influence on the scallop- 500 433 across the different diffraction orders in the variable angle spec- induced diffraction. 501 troscopic data (Fig. 2H, red shaded region), the tilt angle of the 434 SubmissionThe intensity PDF distribution of the diffraction induced by the 502 plates relative to the surface normal is found to be β ≈ 23°, in 435 scallops is modulated by the diffraction induced by the plate 503 agreement with the SEM image analysis. 436 ensemble. Where the scallop diffraction arc coincides with a 504 437 These findings are further supported by Finite Difference plate ensemble diffraction order a peak in intensity is observed. 505 438 Time Domain simulations (19). By comparing the plates with and A decrease in the plate ensemble period would result in fewer 506 439 without scalloping, the arc-shaped intensity distribution across propagating plate ensemble diffraction orders with a larger free 507 440 diffraction orders is clearly identified as the diffraction resulting angular range in between. This would lead to a discretization of 508 441 from the scallops (Fig. 3). Simulations of 23° tilted plates with the scallop diffraction pattern (seen in the FDTD simulation in 509 442 45° incident illumination show that this arc-shaped diffraction Fig. 4) inducing a discrete and easily perceivable color variation 510 443 pattern gets skewed and spectrally shifted as predicted by Eq. 2 with potential applications in the development of novel optically 511 444 and observed in the experiments; the influence of the blaze of variable devices in security printing and consumer product la- 512 445 the regular array of individual gratings, separate from the effect beling. Currently, efforts are underway to fabricate the diffrac- 513 446 of the scallops, can also be seen by closely examining Fig. 3 and tion structures in different material combinations that provide 514 447 noting that the two tilted plate simulations have regions of high a higher refractive index contrast, thereby strengthening the 515 448 intensity reflection at sin(θ) ≈ 0 where the upright plates do not. diffractive signal. 516 449 Furthermore, the simulations serve to predict and optimize the 517 450 influence of variations in inter-plate geometry, scallop grating Materials and Methods 518 451 pitch and shape and plate tilt angle prior to the manufacturing Manufacture of artiﬁcial diffraction structures 519 452 of the system. When Bosch etching (15) is used in conjunction with photolithography, 520 While the angular positions of the diffraction modes resulting the multiple etching and passivation steps give rise to a periodicity in 453 the sidewall of the structures due to the repeated underetching. While, 521 454 from the inter-plate periodicity only vary with the angle of light typically, the goal of this etching method is to create vertical sidewalls, these 522 455 incidence θI; for a given θI the diffraction pattern caused by undulations in the sidewall can form a diffraction grating similar to that on 523 456 the regular scallops on individual plates is strongly affected by the Pierella luna scales if the periodicities are chosen to fall within the range 524 a change in tilt of the plates relative to the sample normal. Con- of optical wavelengths. 457 Once structures with the correct geometry are created in silicon, they 525 458 sequently, a means of reversibly varying the plate tilt angle can can be replicated in other materials with better optical properties by using 526 459 provide the possibility to dynamically tune the diffraction pattern soft lithographic methods (14). By using soft, transparent materials instead 527 460 independent of light incidence. Possible means of achieving such of silicon, the structures can be bent much more easily and the optical 528 reversible actuation include embedding the plates in a stimuli- properties can be changed by applying metal coatings or doping the material 461 with pigments or other materials with interesting optical properties. The 529 462 responsive hydrogel (20-23), using a soft material negative of the replication is achieved by using a polydimethylsiloxane (PDMS) mold of the 530 463 structure and applying shear force to bend the micro-gratings, silicon master and curing an epoxy via UV light before removal from the 531 464 modifying the tips of the plates with ferromagnetic particles to mold. 532 allow for dynamic reconfiguration of the plate geometry using Structural and optical analysis 465 Once scalloped plate structures are made, optical characterization is 533 466 magnetic fields (24), or implementing tuning mechanisms shown performed for comparison of the structures observed on Pierella luna and 534 467 for simple planar diffraction gratings that rely on electric fields or the fabricated systems. Several different types of characterization were em- 535 468 mechanical deformation (25-28). ployed, including variable-angle spectroscopy, diffraction microscopy, and 536 Biological strategies for light manipulation have already been scanning electron microscopy. 469 For the variable angle spectrometry setup, an Ocean Optics DH-2000 537 470 successfully implemented in nanophotonic devices for applica- UV-VIS-NIR light source was used to illuminate a small spot (∼1 mm) of 538 471 tions in chemically selective vapor sensing, pH determination, the sample at a given incidence angle θI. For each angle of illumination, 539 472 infrared imaging, SERS-based chemical analysis, and localized light was collected at half degree increments for ‒75° to +75° relative to 540 473 heating from infrared absorption (29-34). The rich and tunable the sample normal and spectrally analyzed using an Ocean Optics Maya Pro 541 optical signature of our hierarchical bio-inspired diffraction- 2000 spectrometer. 474 For the diffraction microscopy images, a Bertrand lens was used to focus 542 475 based photonic material platform could provide a basis for novel on the back focal plane of the objective of an upright BXFM Olympus optical 543 476 developments in bio-sensing (35-37), efficient light management microscope. The sample was illuminated either from an external source 544

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