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This may be the author’s version of a work that was submitted/accepted for publication in the following source: Hasan, Jafar, Roy, Anindo, Chatterjee, Kaushik, & Yarlagadda, Prasad (2019) Mimicking insect wings: The roadmap to bioinspiration. ACS Biomaterials Science and Engineering, 5(7), pp. 3139-3160. This file was downloaded from: https://eprints.qut.edu.au/131248/ c Consult author(s) regarding copyright matters This work is covered by copyright. Unless the document is being made available under a Creative Commons Licence, you must assume that re-use is limited to personal use and that permission from the copyright owner must be obtained for all other uses. If the document is available under a Creative Commons License (or other specified license) then refer to the Licence for details of permitted re-use. It is a condition of access that users recog- nise and abide by the legal requirements associated with these rights. If you believe that this work infringes copyright please provide details by email to [email protected] Notice: Please note that this document may not be the Version of Record (i.e. published version) of the work. Author manuscript versions (as Sub- mitted for peer review or as Accepted for publication after peer review) can be identified by an absence of publisher branding and/or typeset appearance. If there is any doubt, please refer to the published source. https://doi.org/10.1021/acsbiomaterials.9b00217 Page 1 of 57 ACS Biomaterials Science & Engineering 1 2 3 4 5 Mimicking Insect Wings: The Roadmap to 6 7 8 9 10 Bio-inspiration 11 12 13 14 15 Jafar Hasan1, Anindo Roy2, Kaushik Chatterjee2, Prasad KDV Yarlagadda1 16 17 18 1Science and Engineering Faculty, Queensland University of Technology, 2 George Street, 19 20 Brisbane, QLD 4001, Australia 21 22 23 2Department of Materials Engineering, Indian Institute of Science, C.V. Raman Avenue, 24 25 26 Bangalore 560012, India 27 28 29 30 31 32 Authors to whom all correspondence should be addressed: 33 34 35 [email protected] 36 37 38 [email protected] 39 40 41 42 43 44 45 46 47 48 49 50 51 52 53 54 55 56 57 58 1 59 60 ACS Paragon Plus Environment ACS Biomaterials Science & Engineering Page 2 of 57 1 2 3 Abstract 4 5 6 Insect wings possess unique, multifaceted properties that have drawn increasing attention in recent times. 7 8 They serve as an inspiration for engineering materials with exquisite properties. The structure–function 9 10 relationships of insect wings are yet to be documented in detail. In this review, we present a detailed 11 12 understanding of the multifunctional properties of insect wings including micro- and nano-scale 13 14 architecture, material properties, aerodynamics, sensory perception, wettability, optics and antibacterial 15 16 activity, as investigated by biologists, physicists and engineers. Several established modeling strategies and 17 18 19 fabrication methods have been reviewed to engender novel ideas for biomimetics in diverse areas. 20 21 22 23 24 Keywords: Biomimetics, insects, nanoscale architecture nanofabrication, surface science 25 26 27 28 29 30 31 32 33 34 35 36 37 38 39 40 41 42 43 44 45 46 47 48 49 50 51 52 53 54 55 56 57 58 2 59 60 ACS Paragon Plus Environment Page 3 of 57 ACS Biomaterials Science & Engineering 1 2 3 Introduction 4 5 6 Engineers and scientists have been studying and developing devices by borrowing ideas from nature 7 8 especially insects, owing to their diversity and abundance. Insects have evolved over millions of years to 9 10 overcome complex challenges, resulting in some unique properties that have helped them survive. The 11 12 origin of wings has been regarded as a key evolutionary change among insects, bats, birds and the extinct 13 14 pterosaurs and contribute towards the diversity of insects1. Insect wings are corrugated, membranous 15 16 outgrowths from the exoskeletons and primarily help insects in flight2. Largely, insects possess two pairs 17 18 19 of wings, namely, the forewings and hindwings. The wings are of different types such as membranous, stiff, 20 21 hard, scaled and fringed with hairs. The appearance, color and texture vary among different insects and 22 23 within species. In addition to flight capability, these wings impart several other abilities to insects such as 24 25 protection, thermal sensing, sound generation, mating, visual recognition, hydrophobicity and antibacterial 26 27 activity. The aerodynamics and recently-discovered bactericidal behavior of insect wings are some of the 28 29 key properties that have been investigated extensively. 30 31 32 Insects have fascinated philosophers since ages, as ancient Egyptians are known to have worshipped the 33 34 dung beetle between 1500 and 2500 B.C. Few of the earliest documented works on insect wings appear to 35 36 be initiated in the early nineteenth century3-4. The early investigations on insect wings were only performed 37 38 by entomologists and curators. But now, many engineers and scientists have been attracted to the wonders 39 40 of insect wings, especially the unique architecture at the micro- and nano-scales. 41 42 43 We analyzed the more than 2700 scientific publications (excluding book chapters and patents) on insect 44 45 wings with applications in different areas over the last seven years using the search engine tool Web of 46 47 48 Science (Figure 1). The publications were categorized into ten research areas, focusing on different 49 50 categories of insect wing inspiration. The first area with highest number of publications was flight 51 52 movements and wing aerodynamics; the second area was bioinspiration and biomimetics; the third area 53 54 focused on material properties, examining the stiffness and bending of insect wings and the fourth area was 55 56 57 58 3 59 60 ACS Paragon Plus Environment ACS Biomaterials Science & Engineering Page 4 of 57 1 2 3 antibacterial or bactericidal properties. Other areas such as wettability, sensing ability and reflectivity have 4 5 attracted increased interest probably due to the recent progress in characterization techniques. 6 7 8 However, the number of publications does not represent the scientific impact of the specific areas. The 9 10 Web of Science tool provides the h-index and average citation of all the searched publications. We 11 12 performed a citation report analysis of the number of publications in the last seven years on insect wings 13 14 15 and subject areas (Supporting Information Figure S1), chronicled by their year of discovery. Although 16 17 subject areas such as roughness, wettability and superhydrophobicity had fewer publications, they had 18 19 higher average citations. Notably, in the last seven years, 19 papers covering topics of bacteria and insect 20 21 wings have been cited at least 19 times (Supporting Information Figure S1). 22 23 24 The underlying theme of this paper is bioinspiration from insect wings. Most studies have endeavored 25 26 to understand wing behavior and characteristics whereas few have focused on actual mimicking vis-à-vis 27 28 modeling and fabrication. From an engineering perspective, mimicking of the wing or rather its unique 29 30 properties is as important as understanding the origin of the wing, evolutionary behavior, structure or 31 32 functions. In this paper, an extensive review on the origin, evolution, structure, composition, classification 33 34 and multifunctional properties of insect wings is presented. The different multifunctional properties are 35 36 grouped under bioinspiration sections including micro- and nano-scale topography, material properties, 37 38 39 aerodynamics, sensory perception, optics, wettability and antibacterial activity. Followed by bioinspiration, 40 41 biomimicry is discussed with sections on modeling, simulation and fabrication. In the final section, future 42 43 perspectives and concluding remarks are postulated. There has been no single commentary, analysis or 44 45 review of the cumulative work done on the unique and attractive properties of insect wings: this review is 46 47 an attempt to address that need. 48 49 50 51 Origin and evolution of wings 52 53 54 The origin of insect wings has been debated since centuries as contrasting theories have been put forth 55 56 based on the study of fossils. The problem lies in the absence of fossils detailing the transition between 57 58 4 59 60 ACS Paragon Plus Environment Page 5 of 57 ACS Biomaterials Science & Engineering 1 2 3 non-winged and winged insects5. Majorly, two theories have been proposed by biologists: one is the tergal 4 5 or paranotal hypothesis and the other is the pleural or gill hypothesis. In the paranotal hypothesis, which 6 7 was more accepted during the twentieth century6, the wings extended from the dorsal body wall or the 8 9 10 paranotal lobes to help the insects initially in gliding followed by flying in order to avoid falling from a 11 7-8 12 height . In the gill hypothesis, the wings extended from the leg segments and the branches or exites, which 13 14 helped the wings to show musculature and articulation9-10. The debate on the two hypotheses is essentially 15 16 based on the possibility of the insect wings to either develop from the pre-existing structures or to develop 17 18 new structures. Gegenbaur and Muller separately proposed in the 1870s6 that insect wings originated from 19 20 tracheal gills and tergal lobes respectively6, 11-12. Many scientists supported the gill theory or its variation 21 22 known as the pleural appendage theory in the latter half of the twentieth century6. However, in the absence 23 24 of transition fossils, neither of the theories can be rejected.

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