Biomechanics of a moth scale at ultrasonic frequencies Zhiyuan Shena, Thomas R. Neila, Daniel Roberta, Bruce W. Drinkwaterb, and Marc W. Holderieda,1 aSchool of Biological Sciences, University of Bristol, BS81TQ Bristol, United Kingdom; and bDepartment of Mechanical Engineering, University of Bristol, BS81TR Bristol, United Kingdom Edited by John B. Pendry, Imperial College London, London, United Kingdom, and approved October 9, 2018 (received for review June 13, 2018) The wings of moths and butterflies are densely covered in scales widens into a flattened blade (9). Each scale itself is a highly that exhibit intricate shapes and sculptured nanostructures. While sculptured porous structure, and scales show diverse morphol- certain butterfly scales create nanoscale photonic effects, moth ogies even on a single wing (10). The highly sculptured scale scales show different nanostructures suggesting different func- structure implies sophisticated evolutionary adaptations, analo- tionality. Here we investigate moth-scale vibrodynamics to un- gous to the highly organized nanoscale photonic structures for derstand their role in creating acoustic camouflage against bat visual signaling (11, 12). Across moths, scale morphologies are echolocation, where scales on wings provide ultrasound absorber diverse and hence provide a large candidate pool for biophysical functionality. For this, individual scales can be considered as adaptations. Previous studies have highlighted the role of moth- building blocks with adapted biomechanical properties at ultra- scale morphology in creating multiple functions of moth wings sonic frequencies. The 3D nanostructure of a full Bunaea alcinoe such as aerodynamics, thermal regulation, and wettability (13– moth forewing scale was characterized using confocal microscopy. 15). Additionally, moth wings have been hypothesized as Structurally, this scale is double layered and endowed with differ- the main organ bringing about acoustic camouflage. Micro- ent perforation rates on the upper and lower laminae, which are reverberation chamber testing revealed that scale-covered moth interconnected by trabeculae pillars. From these observations a wings are more absorbent at frequencies from 40 to 60 kHz than parameterized model of the scale’s nanostructure was formed wings with scales removed (7). There is, however, no explanation and its effective elastic stiffness matrix extracted. Macroscale nu- for how the moth wing, and more specifically its microstructure, merical modeling of scale vibrodynamics showed close qualitative creates this acoustic absorber functionality. and quantitative agreement with scanning laser Doppler vibrom- Lepidoptera wing scales are usually less than 0.25 mm wide, and etry measurement of this scale’s oscillations, suggesting that the thus always smaller than one-tenth of the smallest wavelength bats BIOPHYSICS AND governing biomechanics have been captured accurately. Impor- use for echolocation. Even the cross-section thickness of the wing COMPUTATIONAL BIOLOGY tantly, this scale of B. alcinoe exhibits its first three resonances including upper- and lower-scale layers is always below the rele- in the typical echolocation frequency range of bats, suggesting it vant wavelengths. Because wings are therefore ultrathin absorbers has evolved as a resonant absorber. Damping coefficients of the with subwavelength thickness, rigid porous absorption is in- moth-scale resonator and ultrasonic absorption of a scaled wing efficient, leaving the alternative of resonant absorber functionality were estimated using numerical modeling. The calculated absorp- (16). In resonant absorbers a resonant mass and spring system will tion coefficient of 0.50 agrees with the published maximum acous- provide maximum absorption at the frequency it is tuned to. Other tic effect of wing scaling. Understanding scale vibroacoustic resonant systems show maximum sound transmission at resonance behavior helps create macroscopic structures with the capacity (17). Both high absorbance and transmittance are viable strategies for broadband acoustic camouflage. Significance moth scale | acoustics | ultrasonics | vibration | porous materials Ultrathin sound absorbers offer lightweight solutions from he nocturnal acoustic arms race between moths and echo- building acoustics to sonar cloaking. The scales on moth wings Tlocating bats has been ongoing for 65 My. To defend them- have evolved to reduce the echo returning to bats, and we selves against the bats’ biosonar (most relevant frequencies from investigate their resonant sound-absorber functionality. Reso- 20 to 150 kHz, with wavelengths from 16.6 to 2.3 mm), different nant absorbers are most efficient at resonance, and laser moth species have evolved a wealth of active and passive defense Doppler vibrometry (LDV) revealed that an individual moth strategies. Several moth taxa have independently evolved ears scale’s three resonance modes indeed span the biosonar fre- that can detect the ultrasonic frequencies of the biosonar calls of quencies of bats. The porous anisotropic nanostructure of such an approaching bat (1), which allow them to respond with eva- scales was parameterized and its effective stiffness properties sive flight behaviors (2). In addition, Arctiinae, Geometridae, calculated. Modal analysis on a 3D model accurately predicts and some other moths produce loud ultrasound clicks when resonance modes and frequencies found by LDV, and confirms under attack, which can startle bats, alert them to the moths’ absorption performance-matching measurements. Our ability toxicity, or even jam the bats’ biosonar (1, 3, 4). Recent findings to model the absorbers contributing to evolved biosonar suggest some other moth species mimic such aposematic ultra- camouflage has implications for developing bioinspired thin sound clicks (5).* The many nontoxic moth species without and lightweight resonant sound absorbers. hearing capability, however, have to rely on passive acoustic Author contributions: Z.S., D.R., B.W.D., and M.W.H. designed research; Z.S. performed camouflage to avoid capture by bats (6, 7). research; Z.S., D.R., B.W.D., and M.W.H. contributed new reagents/analytic tools; Z.S. and Like in most flying insects, moth and butterfly wings consist of T.R.N. analyzed data; and Z.S., T.R.N., D.R., B.W.D., and M.W.H. wrote the paper. a solid thin chitinous membrane suspended between a network The authors declare no conflict of interest. of stiffer wing veins. In contrast to most other insects, however, This article is a PNAS Direct Submission. both the upper and lower wing surface of moths and butterflies Published under the PNAS license. are covered with arrays of overlapping scales, which has given the 1To whom correspondence should be addressed. Email: [email protected]. lepidos = order Lepidoptera its scientific name (Greek scale; This article contains supporting information online at www.pnas.org/lookup/suppl/doi:10. pteron = wing). The scales and wing membrane are part of the 1073/pnas.1810025115/-/DCSupplemental. insect exoskeleton consisting of a sclerotized biomaterial matrix of mainly chitin and protein (8). A typical moth scale is anchored *O’Reilly LJ, Neil T, Holderied MW, 16th International Meeting on Invertebrate Sound & into a socket in the wing membrane with a narrow pedicel and Vibration, September 14–17, 2017, Rauischholzhausen, Germany. www.pnas.org/cgi/doi/10.1073/pnas.1810025115 PNAS Latest Articles | 1of6 Downloaded by guest on September 26, 2021 to reduce backscatter and hence detectability to bat biosonar. Since scales are the basic elements of moth wings, their vibrational response is essential in understanding the acoustic behavior of entire moth wings and hence the acoustic camouflage effect in moth acoustic ecology and behavior. Moth-wing scales show a hierarchical design, with a scale tiling pattern at the large scale, scale shape at the next, and scale in- ternal structure of nanometer order. As a step to understanding this sophisticated natural structure, this paper focuses on ex- ploring the vibrational behavior of a single freestanding scale. Our prediction is that moth scales are resonant systems, and that their resonances are at biologically relevant frequencies used by bats for echolocation. We further provide an accurate numerical model of the dynamic behavior of a scale, which captures the governing physical phenomena at work. Numerical modeling is used to show that the scale resonator can achieve high absorp- tion coefficients at resonance. Existing resonant absorbers are made of solid materials. In some designs a layer of porous material is added to achieve higher absorption coefficients or a broadband performance (18). The moth scale represents a resonator design composed of res- onating microperforated scales. Elucidating the acoustic mech- anisms behind moth-wing sound absorbance aims at developing bioinspired sound-absorbing materials with a thickness below their functional wavelength for applications in noise control, architectural acoustics, and bioinspired radar and sonar target Fig. 1. Scale arrangement and structure. (A–C) SEM images of B. alcinoe concealment. scales: (A) Partly disrupted tiling of scales; (B) perforated top lamina of a scale; (C) cross-section of a fractured scale revealing the intertrabecular sinus Results between the two laminae. (D–F) Confocal microscopy of the scale: (D)Indi- Scale Shape and Structure. Scanning electron microscopy (SEM) vidual scale used for further analysis. (Magnification 20×.)