Nanostructured Antireflective and Thermoisolative Cicada Wings

Apr 22, 2016 - Here, the temperature diffusivity of a cicada (Cyclochila australasiae) wing with nanotextured surfaces was measured using two compleme...
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Nanostructured Antireflective and Thermoisolative Cicada Wings Junko Morikawa,† Meguya Ryu,† Gediminas Seniutinas,‡,§ Armandas Balčytis,‡ Ksenia Maximova,*,‡ Xuewen Wang,‡ Massimiliano Zamengo,† Elena P. Ivanova,∥ and Saulius Juodkazis*,‡,⊥ †

Tokyo Institute of Technology, Meguro-ku, Tokyo 152-8550, Japan Centre for Micro-Photonics, School of Science, Swinburne University of Technology, John St., Hawthorn, VIC 3122, Australia § Melbourne Centre for Nanofabrication (MCN), Australian National Fabrication Facility (ANFF), Clayton, VIC 3168, Australia ∥ School of Science, Swinburne University of Technology, John St., Hawthorn, VIC 3122, Australia ⊥ Center for Nanotechnology, King Abdulaziz University, Jeddah 215589, Saudi Arabia ‡

S Supporting Information *

ABSTRACT: Inter-related mechanical, thermal, and optical macroscopic properties of biomaterials are defined at the nanoscale by their constituent structures and patterns, which underpin complex functions of an entire bioobject. Here, the temperature diffusivity of a cicada (Cyclochila australasiae) wing with nanotextured surfaces was measured using two complementary techniques: a direct contact method and IR imaging. The 4−6-μm-thick wing section was shown to have a thermal diffusivity of α⊥ = (0.71 ± 0.15) × 10−7 m2/s, as measured by the contact temperature wave method along the thickness of the wing; it corresponds to the inherent thermal property of the cuticle. The in-plane thermal diffusivity value of the wing was determined by IR imaging and was considerably larger at α∥ = (3.6 ± 0.2) × 10−7 m2/s as a result of heat transport via air. Optical properties of wings covered with nanospikes were numerically simulated using an accurate 3D model of the wing pattern and showed that light is concentrated between spikes where intensity is enhanced by up to 3- to 4-fold. The closely packed pattern of nanospikes reduces the reflectivity of the wing throughout the visible light spectrum and over a wide range of incident angles, hence acting as an antireflection coating.

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INTRODUCTION

bactericidal for common Gram-positive and Gram-negative bacteria as well as for spores.8 As an example of bioinspired design, black-Si surfaces were shown to be bactericidal as a result of a random pattern of nanoneedles of height similar to that of the ones observed on a cicada wing.9 However, the thermal and optical properties of a chitinous insect wing and a crystalline black-Si surface may vary significantly. Profound investigation of the functionality of the wing’s surface and its thermal and optical properties10 can make a significant contribution to the further development and improvement of cicada winglike surfaces and their introduction into manmade materials. For example, a possible enhancement of the bactericidal action could be attained by heat localization on the needles and light intensity redistribution leading to stronger light absorption and local heating on the surface of a bacterium at its contact point with the wing. These conjectures were the driving motivation behind this study to determine the thermal diffusivity of nanostructured wings for the first time.

Nature has created a plethora of micro- and nanostructured surfaces that exhibit outstanding properties, such as antireflection, antistick, self-cleaning, wetting properties, high surface tension, and so forth. And it is not surprising that the creation of biomimetic and bioinspired surfaces is currently a very active field of research,1,2 boosting the future development of new composite materials.3 Wings of some cicada species, e.g., Cyclochila australasiae used in this study, are sometimes even larger than the entire body footprint of the insect. The high-pitched, extremely loud sound that cicadas are known for is produced by a biconvex membrane bearing alternating long and short ribs that are located below a flexible cuticle under the wings.4 Veins on their wings serve as a hydraulic system to maintain the wing’s shape.5 The surface of the wing is covered by a random pattern of nanoneedles that are 200−400 nm tall with separations of 250− 300 nm in between them.6 Additionally, veins are covered with larger single spikes and hair sensors. It was recently demonstrated that nanospikes on the wings of cicadas and dragonflies contribute to the hydrophobicity of these surfaces and facilitate self-cleaning.7 Moreover, the nanospikes’ pattern on the cicada wings makes them © XXXX American Chemical Society

Received: March 14, 2016 Revised: April 18, 2016

A

DOI: 10.1021/acs.langmuir.6b00621 Langmuir XXXX, XXX, XXX−XXX

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Langmuir Here, thermal and optical properties of cicada wings are revealed by direct measurements and numerical modeling. It is shown that FTIR imaging in the IR spectral window using tabletop spectrometry provides imaging resolution comparable to that of earlier synchrotron experiments.11 Temperature diffusivity was directly measured by two methods: a contact method and IR imaging. The influence that nanotexturation has on the optical properties of the wing was numerically modeled using a finite-difference time domain (FDTD) Maxwell’s equation solver to obtain reflectivity spectra over a wide range of incident angles of light.

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EXPERIMENT AND MODELING

Thermal characterization of a cicada (Cyclochila australasiae) wing was carried out using several complementary methods: IR camera imaging, noncontact imaging mode analysis of thermal diffusivity under visible light excitation,12 Fourier transform infrared (FTIR) attenuated total reflection (ATR) mode spectrometry (alpha-Bruker), FTIR imaging spectrometry (Spotlight PerkinElmer), and a direct contact mode thermal wave diffusivity measurement method (ai-Phase Ltd.). Structural imaging and characterization of the wing surface was carried out using scanning electron microscopy (SEM) and focused ion beam (FIB) mode on the ion beam lithography (IBL) tool (Raith IonLiNE or FEI Helios NanoLab 600 Dual Beam FIB-SEM). FIB milling was required to obtain cross sections in order to make accurate estimates of the surface morphology of the needles and their height and shape as well as to measure the thickness of the wing membrane. Numerical simulations of light intensity distributions on the wing as well as the spectral/angular dependences of reflectance were carried out using a commercially available finite-difference time domain (FDTD)13,14 solver (Lumerical). The 3D rendering used in simulations as a representation of the wing (shown as an inset in Figure 5b) was obtained by first extracting the spike position coordinates from an SEM image of a wing segment and then at these predefined positions generating a randomized set of spikes with a normal distribution of parameters, likewise deduced from SEM data. The refractive index of the material was set to the value of n = 1.55, which is consistent with the average values reported for chitin and keratin.15 Simulations were conducted on a 3 × 3 μm2 nanotextured wing segment as well as on a flat surface for reference. Optical excitation was conducted using pulsed broadband plane wave sources at two perpendicular linear polarizations to simulate unpolarized solar radiation. The light angle of incidence was varied in the range of θ = 0−75° to account for the broad range of illumination conditions the wing is sure to experience in nature. The simulation region was terminated by Bloch boundary conditions at planes perpendicular to the wing surface and by perfectly matched layer boundaries at the two parallel planes. Broadband parameter sweeps of the source angle of incidence in FDTD are complicated by the fact that when using Bloch boundary conditions the angle of incidence changes as a function of frequency. Therefore, in order to obtain 2D spectral/angular dependence plots of reflectance, 100 broadband simulations at slightly different angles of incidence (varying from 0 to 75°) were performed, and the results were subsequently interpolated onto a common source angle/ wavelength grid. This is the standard procedure for obtaining a map of reflectivity at different angles of incidence versus wavelength.

Figure 1. (a) Optical image of a cicada (Cyclochila australasiae) wing. (b) IR image of vein and edge regions (marked in (a)), obtained over the 3−5 μm wavelength range. (c) SEM image of a broken section of the vein and wing with a close-up view of nanospikes on both sides of the wing. The layered wing structure is recognizable in the close-up image.

packed pattern of nanospikes that are up to 500 nm tall. The spikes make this surface not only antifouling and hydrophobic but also bactericidal.8 Thermal Imaging: Noncontact Method. First, the spatial map of IR absorption in the wing was measured at different IR wavelengths specific to the chemical constituents of the wing using a tabletop FTIR imaging spectrometer. The IR image of the wing in the 3−5 μm (3333−2000 cm−1) high transmission spectral window reveals an internal structure present in the thicker vein regions (Figure 1b). The IR absorption is governed not only by the material comprising the wing itself but also by surface coating layers that contain water-repellent wax that further supplements the hydrophobicity of a cicada wing arising from the nanospike pattern.11 A typical IR absorption spectrum of a cicada wing (Figure 2) reveals its chemical composition; in the visible spectral range, the wing is mostly transparent. (Wing transmittance spectra in the visible region are provided in the Supporting Information.) A clear amide I band of CO stretching around 1650 cm−1 is due to CO vibrations related to the proteins and chitin.16,17 The prominent 3290 cm−1 band is the amide A mode of N−H stretching (proteins and chitin), and the 2927 cm−1 band is due to C−H stretching and is characteristic of long-chain alkyls as a part of the lipids.18 The amide II band at 1514 cm−1 is attributable to N−H in-plane bending and indicates the presence of proteins and chitin.16,17 The overall spectral structure demonstrates the multicomponent chemical composition of the insect wings consisting of a chitin-based procuticle covered with epicuticle containing wax and proteins.5 The Fourier transform IR (FTIR) spectral measurements were carried out in imaging mode under tight focusing and using a detector with a 6.25 μm pixel size. Wing surface spectral maps obtained at two separate amide I absorption bands are presented (Figure 2). Similar spatial resolution of wing absorption has been previously demonstrated using IR beamlines at synchrotron light sources.11 Here we show that the chemical composition of the wing surface can therefore be mapped at the high resolution required for studies of the

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RESULTS AND DISCUSSION Most of a cicada (Cyclochila australasiae) wing (Figure 1) is composed of a transparent cuticle only 4−6 μm thick. Conversely, the supporting veins and edge regions of the wing have cross-sectional thicknesses of 60−150 μm. Sensory hairs that are typically 4 μm in diameter are also present on and near the veins. The transparent wing sections have a layered structure, as revealed by scanning electron microscopy (SEM) under higher magnification and are covered with a randomly B

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Figure 3 shows IR imaging data under optical excitation at 630 nm wavelength focused onto a vein which is considerably thicker than the cuticle it supports and has a stronger absorbance due to its green color (see Figure 1(a)). The central part of the tubular vein (Figure 3) appears more transparent on the IR image and has walls formed from a layered material. The image detected by the IR camera is proportional to the surface emissivity, ε, and temperature, T, which appear as a product and hence are undistinguishable according to the Stefan−Boltzmann law of gray body emission j = εσT4, where j is the emissive power and σ is the Stefan−Boltzmann constant. Emissivity is dependent on a multitude of physical factors and is also a function of surface texture. The vein was illuminated with a laser pulsed at low frequency, and the temperature distribution was calculated from the temperature transients at the same modulation frequency (details in ref 12). The corresponding amplitude and phase values of the first Fourier component are contour plotted, revealing isothermal regions and their diffusion from the vein structure to the nanoneedlecovered wing membrane region. The black and white stripes in the images Figure 3b,c show the same amplitude and phase regions that represent the temperature (emissivity) distribution with high precision. The thermal diffusivity and temperature of the vein are larger than those of the wing, as can be qualitatively deduced from the contour plots of phase and amplitude (Figure 3). The phase can be expressed as φ(x) = ω x + const ,

Figure 2. IR transmission spectrum of a cicada wing region near the vein (Figure 1) and the corresponding transmittance maps: all integrated, 1544 cm−1, and 1649 cm−1. CO amide I bands are marked by arrows (the intensity scale is in arbitrary units for better presentation). Spectra are collected by using FTIR (Spotlight, PerkinElmer) with a 6.25 μm pixel size detector matrix.

2α

where x is the propagation coordinate and ω is the driving cyclic frequency of the heat source.12 Hence, a variation of the slope, γ ∝ ω , in the phase plot represents a change in

bactericidal action of nanotextured surfaces for a typical bacterial size of a few micrometers using a simple tabletop setup.

2α

thermal diffusivity, α. From the γ slope on the phase

Figure 3. Thermal image in the pulsed optical excitation region (a) with amplitude (b) and phase (c) maps of the Fourier component corresponding to the excitation frequency. Contour plots reveal the gradients of temperature and emissivity (amplitude), with thermal diffusivity deducible from the phase slope shown in (d); lines are linear fits (details in the text). C

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also be influenced by the layered structure of the wing, which is recognizable in Figure 1c. Similarly, when SEM and optical imaging data are considered, the variations in the measured thermal diffusivity values can be explained by the nonuniformity in the thickness of the cuticle-layered membrane as well as the presence of microscopic blood vessels. Each of these membrane features depends on the proximity and size of the supporting veins in their immediate environment. When efficient cooling is required, a large surface contact area with air is a natural solution for biomaterials. Next, we inspect how the surface nanostructure of the cicada wing cuticle affects its optical properties, which in turn can influence the thermal, mechanical, and hydrophobic properties of the wing itself. Optical Reflectivity of a Wing. Light absorption can modify the surface temperature and water surface tension and could affect a wing’s functions. Here, numerical modeling of a realistic wing surface structure has been performed for the first time. SEM imaging was used to analyze the nanoscale surface pattern on the wing membrane and to create a representative model for simulating its optical properties. Nanospikes were shown to cover both sides of the wing membrane, which itself appears to have a laminar sheet structure. The nanospikes were closely packed and randomly arranged on the wing’s surface, with a nearest-neighbor separation of d = 175 ± 15 nm, as can be judged from the fast Fourier transform (FFT) shown in Figure 5a. The spikes have a rounded-tip cone shape, with an

dependence (Figure 3d), the in-plane thermal diffusivity values, α∥ = (3.6 ± 0.2) × 10−7 m2/s for the wing membrane, and (6.7 ± 0.2) × 10−7 m2/s for the vein, were obtained using this noncontact method. This imaging method for the determination of temperature diffusivity is inherently affected by heat transport at the air−wing interface because the thermal diffusivity of air is much higher. A more precise contact mode determination of temperature diffusivity through the wing that directly reflects the properties of the cuticle biopolymer is demonstrated next. Thermal Diffusivity: Contact Method. Measurements of thermal diffusivity along the thickness of the wing, in the direction perpendicular to its surface, were performed using a direct contact temperature wave (ai-Phase) method.19 The probes were applied at numerous different locations on the wing (Figure 4) and averaged over several separate

Figure 4. Thermal diffusivity measurement by means of a temperature wave method (ai-Phase) at different points, 1−7,on the wing. The average temperature diffusivity for the wing was α⊥ = (0.71 ± 0.15) × 10−7 m2/s (points 1−6), and that for the vein was (2.11 ± 0.15) × 10−7 m2/s (point 7). The inset shows a schematic representation of the contact method for measurements with the modulated temperature wave.

measurements. Such a procedure was essential because of the nanospikes present on both sides of the wing, which give rise to different contact conditions at each measurement location, mostly because of variations in the amount of trapped air, which can significantly influence (increase) the actual value of thermal diffusivity; the thermal diffusivity of air αair= 2.1× 10−5 m2/s is more than an order of magnitude larger than that of typical polymers.20 Temperature diffusivity of the thin wing cuticle regions was found to be α⊥ = (0.71 ± 0.15) × 10−7 m2/s (points 1−6), and for the thick supporting vein section, the value was α⊥ = (2.11 ± 0.15) × 10−7 m2/s (point 7). An inductive coil was used to simultaneously assess the thickness of the section through which heat transport was measured (ai-Phase). The transparent flat wing membrane sections were 5 ± 1 μm thick, and the veins were up to ∼250− 300 μm in diameter. These values are consistent with those obtained via optical imaging (Figure 3). The contact area over which the direct measurements (ai-Phase) were conducted was ∼250 × 150 μm2, larger than in the noncontact optical imaging case (Figure 3). Direct measurement is more precise, and its results are consistent with thermal diffusivity values obtained using the same method for a fibroin silk polymer film, ∼1.6× 10−7 m2/s, which has absorption properties comparable to those of a cicada wing. These direct measurements resolve a controversy regarding the high thermal conductivity of biomaterials such as silk,21 and reconfirm that lower values of biopolymer thermal diffusivity are to be expected.22 Low thermal diffusivity might

Figure 5. (a) SEM image of the cicada wing and its FFT map indicating the nearest-neighbor spacing of 175 ± 15 nm to be random. (b) Three-dimensional model of a wing segment with surface nanospikes, recreated from SEM images of the wing and used for FDTD simulations; the top SEM image shows a typical isometric view of spikes covering the wing.

average height of h = 240 ± 30 nm, an average tip diameter of dt = 70 ± 10 nm, and an average diameter at the base of dt = 200 ± 20 nm. For FDTD calculations, a 3D model of a representative 3 × 3 μm2 segment of the wing was rendered on the basis of an SEM image and was used to simulate the optical properties of a nanospike-decorated wing membrane in the visible spectral range (Figure 5b). Nanospikes on a cicada wing have spacing and height values similar to those that were found to reduce reflectivity and render wide-angle viewing on silica sheets.2,10 Hence, it is highly probable that the spikes serve an optical function of camouflage because analogous antireflective functionality is provided by the artificial spike-covered SiO2 surface. However, as an example of the multipurpose nature of biomaterials, the D

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Figure 6. (a) Angular reflectivity, R, spectra of a flat and nanoneedle-covered wing (the model is shown in Figure 5b; the actual wing is shown in Figure 1c). (b) Light E field, |E|, distribution at wavelengths of 400, 532, and 785 nm at normal θ = 0° incidence.

Morpho butterfly wings,24,25 is always accompanied by some presence of disorder (randomness) in the orientation and shape of the nanoscale structural features, together with some fixed parameters, e.g., the separation between the closest-neighbor spikes. High-efficiency visualization of IR light was enabled by harnessing the enhanced IR absorption between pillars of wing texturation structures.26 Also, the optical properties are highly dependent on the structural modifications; for example, the presence of chitin−melanin multilayered structure in the wing veins induces the significant color changes related to the variations in the reflectance and transmittance spectra.27

hydrophobicity of cicada and dragonfly wings is also partially defined by the nanotexture of their surfaces. The air pockets that get trapped between the spikes enable preferential Cassie− Baxter surface wetting, which, in addition to preventing the wing from becoming wet and causing encumbrance, also makes the surface self-cleaning when water droplets roll over it. Figure 6a clearly shows that, for light impinging at low-tomoderate angles of incidence, a wing surface covered with nanospikes has decreased the reflectivity by an order of magnitude over the entire visible spectral range when compared to a flat plane without such texture. Even at larger angles of incidence, including the Brewster’s angle, the reflectivity of the nanospike-decorated surface remains at least 4 times lower. Therefore, this provides a camouflage function for the cicada in the visible spectral range spanning 400−800 nm. The observed antireflective behavior is due to the spikes providing a gradual transition of the effective refractive index instead of a sharp boundary between air and biopolymer environments, thereby effectively coupling light into the bulk of the wing. This principle was previously demonstrated to be useful in solar-energy-harvesting applications.23 The aforementioned light-coupling behavior is further evidenced by the greatly increased intensity of light at visible wavelengths in the gaps between the spikes (Figure 6b). Typical averaged transmittance spectra of a cicada wing and a dragonfly wing in the visible spectral range are shown in Figure S1. Despite the biopolymer composition and the contributions from the opaque veins, the insect wings exhibit transmittance comparable to that of glass. However, pigmentation and strong Rayleigh scattering introduce strong transmission losses (accounted for partly as absorbance) scaling as λ−4. Optical functions of biomaterials is a fascinating multidisciplinary field of research that brings together concepts from photonic crystals, grating optics, materials science, and nanotechnology. The omnidirectionality of effects such as reflection/transmission or color appearance, as in the case of

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CONCLUSIONS

Cicada wings with nanospike surface texturation have a thermal diffusivity of α⊥ = (0.71 ± 0.15) × 10−7 m2/s across the thickness of the wing and α∥ = (3.6 ± 0.2) × 10−7 m2/s along its surface, as determined by contact and IR imaging methods, respectively. The layered structure of the wing contributes to the low thermal diffusivity along its thickness and facilitates a more efficient lateral spread of temperature, which is consistent with the experimental observations. An artificial silk film made from a fibroin water solution by drop casting has no laminar structure, and its temperature diffusivity across the film was approximately 2 times larger, ∼1.6× 10−7 m2/s.28 Nanospikes give rise to a light intensity distribution with higher intensity concentrated in between the spikes over the entire visible spectral range of λ = 400−700 nm. When compared to a flat plane of the same material, spike-covered cicada wings have a reflectivity reduced by roughly 1 order of magnitude over a large span of incident angles, providing camouflage functionality. E

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ASSOCIATED CONTENT

S Supporting Information *

The Supporting Information is available free of charge on the ACS Publications website at DOI: 10.1021/acs.langmuir.6b00621.

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Transmittance spectra of cicada and dragonfly wings in the visible spectral range (PDF)

AUTHOR INFORMATION

Corresponding Authors

*E-mail: [email protected]. *E-mail: [email protected]. Notes

The authors declare no competing financial interest.

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ACKNOWLEDGMENTS

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REFERENCES

J.M. acknowledges support by JSPS KAKENHI grant number 25420752. S.J. is grateful for partial support via the Australian Research Council DP130101205 Discovery project and a research stay supported by the Tokyo Institute of Technology and the Top Global University project of JSPS. We acknowledge support from the Bruker distributor in Japan with respect to testing the Alpha spectrometer. FDTD simulations were performed on the swinSTAR supercomputer at Swinburne University of Technology.

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DOI: 10.1021/acs.langmuir.6b00621 Langmuir XXXX, XXX, XXX−XXX