Over the course of their wildly successful proliferation across the earth, the insects as a taxon have evolved enviable adaptations to their diverse habitats, which include adhesives, locomotor systems, hydrophobic surfaces, and sensors and actuators that transduce mechanical, acoustic, optical, thermal, and chemical signals. Insect‐inspired designs currently appear in a range of contexts, including antireflective coatings, optical displays, and computing algorithms. However, as over one million distinct and highly specialized species of insects have colonized nearly all habitable regions on the planet, they still provide a largely untapped pool of unique problem‐solving strategies. With the intent of providing materials scientists and engineers with a muse for the next generation of bioinspired materials, here, a selection of some of the most spectacular adaptations that insects have evolved is assembled and organized by function. The insects presented display dazzling optical properties as a result of natural photonic crystals, precise hierarchical patterns that span length scales from nanometers to millimeters, and formidable defense mechanisms that deploy an arsenal of chemical weaponry. Successful mimicry of these adaptations may facilitate technological solutions to as wide a range of problems as they solve in the insects that originated them.

1 Introduction The central motivation behind the development of bioinspired materials—indeed, behind all biomimicry—is the idea that evolution by natural selection can be considered as a long‐running algorithm for developing solutions to the problem of survival in response to a wide variety of environmental pressures.1 Since life began in the oceans 4 billion years ago, living organisms have colonized almost every niche on the earth's surface using a diverse array of adaptations.2 Engineers seeking to develop solutions to problems with even remote analogues in nature do well to closely investigate the solutions developed by evolution. Insects are worth particular attention from a bioinspirational perspective given their astounding abundance and diversity; they arguably represent natural selection's wildest success. Around half of all known species of living organism are insects.3 Over one million species in the class Insecta have been described, with estimates of the total number of insect species ranging from three million to tens of millions. Beetles alone claim 240 000 known species (by comparison, there are around 6000 known species of mammals);3 a single tree in Peru was found to house 43 distinct species of ants.4 Insects are ubiquitous, having adapted to nearly all of the environments on earth, though only a handful of species live in the oceans or in polar regions.2 Some insects lead solitary lives, while others live in large groups with strict social hierarchies; a single “supercolony” of ants in Hokkaido contains over 300 million workers and 1 million queens.4 Insects' Latin‐origin namesake translates to “cut into pieces;” this theme extends throughout their body plan, which consists of a three‐part form (head, thorax, and abdomen), three pairs of jointed legs, compound eyes, and one pair of antennae. These cornerstone appendages, along with countless other structural adaptations such as wings or specialized organs, exist in all shapes and sizes. Adult insects range in length from 0.2 mm (fairyflies of the family Mymaridae)5, 6 to over 300 mm (stick insects of the family Phasmatidae);7 their mass varies 500 000‐fold. Accordingly, insects occupy many roles in the global food chain, eating living and dead plants, fungi, other insects, and vertebrates and serving as a common food source for higher animals, including Homo sapiens.2 A multitude of selective pressures accompany this diversity of lifestyle, and insects have evolved complex and effective solutions to the particular problems they face. Many of these solutions involve functional materials. Some adaptations, like the photonic structures that give butterfly wings their iridescence, are a part of the anatomy of the insects themselves. Some have their basis in biomaterials secreted from glands, like the wax that honeybees use to form their precisely hexagonal homes. Some insects, like the ants that cluster to form buoyant rafts and aerial bridges, aggregate to form functional materials with their bodies. Humans have been entranced by these creatures and their materials since the beginning of recorded history. The practice of beekeeping is at least 5000 years old,8 and it is said that the inventor of paper in China around 150 A.D. was inspired by watching vespid wasps make their nests.9 The history of scientific discovery owes a lot to insects, as well. The fruit fly, Drosophila melanogaster, has been an important model organism in the study of genetics and was the original subject of the studies that discovered sex‐linked inheritance and genetic mutation from exposure to radiation.10 More recently, studying social insects has led to insights about the nature of adaptive behavior in all social animals, including humans.11 Today there are over 100 active peer‐reviewed journals dedicated to field, applied, and experimental entomology. The range of adaptations in insects that have potential for translation to engineering problems is both wide and widely catalogued, but we wager that the majority of today's materials scientists and engineers spend little time reading entomology journals. We therefore intend to bridge an inspiration gap by showcasing some of the most notable ways in which insects have developed specialized anatomy, physiology, and behavior that exploit physical and material principles to ensure their survival (Figure 1). Even basic material adaptations in insects are potentially translatable. For instance, each creature is surrounded by an exoskeleton that imparts long‐term functionality and protection despite direct exposure to the stresses of the outside world; such a durable material with tunable mechanical, optical, and surface properties is attractive in a variety of contexts as wide as the insects themselves inhabit. Furthermore, specialized glands allow the emission of a wide variety of secretions, providing insects with the ability to deploy chemical adhesives, coatings, and signals on demand for shorter‐term use; this theme perhaps hints that engineered materials could benefit from similar active secretory capabilities. The exoskeleton and secretory glands appear in recurring structural motifs that provide insects with remarkable and diverse functional capabilities (Figure 1). Engineered systems ranging from miniature robots to specially designed functional surfaces to novel drug delivery schemes provide exciting opportunities to apply lessons learned from these creatures. Figure 1 Open in figure viewer PowerPoint The ability of insects to thrive in diverse environments is linked to two evolutionarily optimized systems: a cuticle‐derived exoskeleton with associated functional micro‐ and nanostructures, and glandular complexes that secrete chemically diverse substances. Most structures rely deeply on hierarchical organization, with structural ordering on length scales ranging from nanometers to millimeters. Insects' structural adaptations function to serve a broad set of insect needs including environmental sensing and control, protection, communication, and locomotion. Numbers in parentheses correspond to the section associated with the particular functionality. The sections that follow are organized by function, describing specialized structures for adhesion, movement, interaction with water, and for sensing and production of optical, thermal, vibrational, and chemical signals. Finally, we discuss the special capabilities of insect societies, which perform complex tasks involving specialized materials and often can be considered as materials unto themselves. Each (sub‐)section begins with a discussion or case study of the manners in which lessons from insects can be applied to engineering problems, then presents some of nature's most compelling solutions and discusses the physical principles relevant to the task at hand. An overview of insect adaptations arranged by material motif can be found in Table 1. Table 1. Insect adaptations sorted by material motif Material motif General functionality System of interest Insect and reference 3D nano and microstructures Adhesion Adhesive setae Colorado potato beetles, 42 606 47 43 Mechanical fasteners Dragonflies, 53 55 56 55 56 Chemical sensing and defense Anatomical allomone structures Bees, 486, 491 486 486 497 473, 499, 607 Defense spines Lepidopteran caterpillars, 485 485, 490 486 Built structures Caterpillars, 608-611 612 613-615 Projectile dispersal Bombardier beetles 467 Color vision and color manipulation 1D photonic structures Beetles, 289, 291 289, 291 Apposition eyes Ants, 361 361 Bioluminescence Fireflies 616 Color vision Honeybees, 617, 618 619 Disorder‐based color Butterflies, 320, 323, 324 329-331 332, 333 Photonic crystals Weevils, 290, 316, 319, 321 290, 316, 319, 321 Polarization vision Flies, 369, 374 379 380, 620 382, 383 Rhabdom Flies, 369 370 370 Locomotion Locomotive appendage Beetles 621 Locomotive setae Phantom midges, 128 129 127 134 Wing design Fairyflies, 6 124 Mechanosensation Campaniform sensilla Blowflies, 215 218 622 Hair plates American cockroaches, 217 623 209 Near‐field detectors Flies 226 Tactile hairs Desert locusts, 207 208 Sound production Scraper and file Grasshoppers, 264 264 624 624, 625 226, 256 Thermoregulation Cooling Butterflies, 626 416, 417, 512 Thermosensing Forest‐fire‐seeking beetles 2, 394 Water active properties Hydrophobic surface Termites 627 Sub‐aquatic exchange Cattail mosquitos, 628 180, 181 191 Branching and porosity Adhesion Adhesive pads Stenus beetles 70 Chemical sensing and defense Chemoreceptive sensilla Gypsy moths, 433-435 433 629 440, 441 Collective materials Building and fungus cultivation Termites 630 Built structures Honeybees 2 Group thermoregulation Termites, 528 512, 563 512, 563 Wind harvesting Termites 511, 631 Locomotion Locomotive appendages Jumping insects, 128 632, 633 634 Emulsions and biphasic solutions Adhesion Permanent adhesives Flies, 635, 636 68 637 57 Temporary adhesives Locusts, 58 59 65 65 Chemical sensing and defense Biphasic secretion True bugs, 469, 470 638 639 Built structures Green lacewings 640 Froths and foams Pyrgomorphid grasshoppers, 641 642 474 Hemolymph defense Sawflies, 643, 644 450, 645 645 646 Projectile dispersal Stick insects, 451, 459 647 Thermoregulation Cooling Honeybees, 410 411 412 Water active properties Surface excretion Leafhoppers 166, 167, 648 Layering Collective materials Built structures Social wasps 649, 650 Raft building to survive flooding Fire ants 580 Bivouac assemblies Army ants 512 Color vision and color manipulation Impedance matching Dragonflies, 337 339 338, 341, 342 342, 343 342 Water active properties Desiccation resistance Antarctic midges, 651 652 Regular repeated patterns Collective materials Defense swarming Japanese honeybees 574 Material‐like swarm Honeybees 573 Magnetic orientation Termites 631 Tree nesting Weaver ants 653 Water active properties Designed wettability Desert beetle 161 Hydrophobic surface Planthopper, 155 157 160 Thin flexible membranes Locomotion Locomotive method Mayflies 654 Wing design Bumblebees, 102-105 94, 106, 107, 112 Mechanosensation Subgenual organs Ground wetas 248, 249 Tympanum Cicadas 235 Sound production Tymbal sound production Tiger moths, 269 254, 266 Thermoregulation Thermosensing Dark‐pigmented butterflies 393, 655 Water active properties Hydrophobic surface Mosquitos 178 Water‐active behavior Termites 177, 656 Chemical/other Chemical sensing and defense Hemolymph defense Monarch butterflies, 448 641 657 Collective materials Group communication Honeybees 266, 550, 650 Swarm as organism Midges 587 Color vision and color manipulation Pigmentary coloration Swallowtail butterflies, 368 298, 299 Thermoregulation Cooling Moths, 408 658 Freeze resistance Spruce budworm, 423, 659 423, 659 Thermosensing Fruit flies 660

2 Adhesion Slippery surfaces and steep slopes are omnipresent in nature. To overcome these obstacles, organisms including (but not limited to) marine invertebrates, arthropods, and amphibians have developed organs that promote surface adhesion.12-17 Natural adhesives have been the subject of several hundred years of research,18, 19 and the adhesion techniques of mussels, barnacles, and tree frogs have garnered considerable attention, inspiring an array of synthetic mimics.20-22 Adhesives utilized by insects, however, have gone largely understudied when considering their diversity and abundance.23 These insect adhesive systems exist as two overlapping categories: physical adhesive structures that mechanically interlock or generate attractive force through van der Waals' interactions, and chemical adhesive secretions that act via molecular bonding, capillary forces, and viscous forces. Some insect adhesives generate impressive forces relative to body weight,24, 25 however, their strength alone is often outperformed by commercial adhesives which operate in a much different surface‐area‐to‐volume regime. They do, however, excel in rapidly attaching to (and often detaching from) surfaces with a variety of roughnesses and chemistries, and can self‐clean after encountering contaminants.26, 27 Fibrillar or branching structures are fundamental to many of the adhesive systems found in insects. In fact, variations of these nano‐ and microstructures exist in other areas of biology as well,28, 29 suggesting their geometry and mechanism of action are broadly beneficial. Researchers have spent considerable effort trying to replicate the van der Waals‐based dry adhesion of gecko foot pads,15, 29 but insects, none of which have been found to employ purely dry adhesion, indicate that other interactions like hydrogen bonding, viscous forces, and capillary forces can enhance or even dominate overall adhesion capability.23, 28-31 These additional forces are particularly relevant when adhering to wet substrates, as is necessary in wound dressing and tissue repair. Recent research reported a bioinspired “tough adhesive” designed to stick strongly to biological surfaces for medical applications.32 The adhesive is composed of two layers: a lower adhesive layer that binds to material through a combination of covalent bonds, electrostatic interactions, and interpenetration (material mixing), along with an upper matrix designed to dissipate energy when the contact interface is stressed. Here, as discussed in the insect adhesives below, a multifaceted adhesive approach leads to increased versatility and functionality. 2.1 Physical Adhesive Systems Insects' hardened exterior is made almost exclusively of cuticle: a versatile biomaterial that forms the rigid and multifunctional exoskeleton of all insects (Figure 2). Two types of cuticle microstructures help insect feet adhere to surfaces that have varying degrees of roughness.33 The first type, used primarily by flies and beetles, consists of arrays of small fibers (setae) ending in thin spatulas, disks, or points.34-36 The fibers are flexible and can bend extensively to accommodate large surface features, while the terminal tips fit within finer features to engage in close‐contact van der Waals' interactions.37 The second variety, found mainly in stick insects, ants, and cockroaches, are smooth pads with a soft cuticle capable of deforming in response to varied roughnesses. The cuticle has an internal branching structure consisting of rods directed perpendicular to the surface—an orientation thought to help increase contact area and thus strengthen surface‐area‐dependent attractive forces.38 Fuller and Tabor reported that densely arranged surface features smaller than 5 µm present major difficulties for climbing insects,39 and certain plant species take advantage of this effect. For instance, pitcher plants, from the carnivorous Nepenthes genus, have developed epicuticular wax crystals to serve a variety of purposes from increasing surface microroughness to contaminating adhesive structures with exfoliated crystals in order to capture and consume their insect prey.40, 41 Figure 2 Open in figure viewer PowerPoint 661 Ulomoides dermestoides. Scale bars: 20 µm. Adapted with permission. 662 Lamellar structure of the insect cuticle, which forms the majority of an insect's exoskeleton. Three distinct regions of nonliving layers rest on a living epidermal layer that houses various cuticle‐producing and microstructure‐related cells. The outermost epicuticle layer represents the first line of defense between the insect and its external environment. It often contains lipid secretions, waxes, or other coatings to manipulate wettability, perhaps the most intriguing of which are intricately structured nanoparticles, known as brochosomes, found on the leafhoppers of the family Cicadellidae (see Figure 10). Beneath this layer lies the exocuticle, which undergoes extensive crosslinking and has a relatively high rigidity. In many insects, it hardens rapidly to act as a protective envelope after molting for the prolonged development of softer and more hydrated endocuticle underneath. The exo‐ and endocuticular layers collectively form what is known as the procuticle, a composite material with protein, polyphenols, water, and lipids, along with crystalline arrangements of the important and abundant linear polysaccharide chitin. A) Cartoon of the structure of cuticle based on TEM images. Adapted with permission.Copyright 1982, Springer. B) Various morphologies of microtrichia (small stiff hairs) found in the Chinese beetle,. Scale bars: 20 µm. Adapted with permission.Copyright 2016, Springer. A curious example of physical adhesion has developed in the Colorado potato beetle, Leptinotarsa decemlineata, to suit its copulation posture.42 The tarsal microstructures on the beetles' legs exhibit sexual dimorphism—both male and female beetles have setae that terminate in points and spatulas, but only males have a third style of disk‐shaped setae.43, 44 These terminal disks allow the male to adhere strongly to the smooth back (elytra) of female beetles for extended periods of time during mating.45 Unsurprisingly, male beetles can adhere to smooth surfaces slightly better than female beetles, though females can adhere more than twice as strongly to rough, plant‐like surfaces.42 This observation provided a direct link between structure and function in tarsal adhesive structures. Disk‐shaped tips impart a larger surface contact area on smooth surfaces, leading to improved long‐term adhesion on those surfaces. Conversely, the flexibility of spear‐ and spatula‐shaped setae makes them well‐suited to rough surface adhesion on short time scales (e.g., for locomotion). As a passive form of defense, many different animals have developed hiding strategies that involve covering themselves with small materials and debris in their surrounding environments.46 The most well‐researched of insects with this behavior are reduviid nymphs and chrysopoid larvae (Figure 3).47 Both of these insect subsets rely on adhesive properties of physical microstructures for their camouflaging abilities. Chrysopoid larvae specifically are thoroughly covered in hair‐like setae that vary with body position and are specialized for different types of debris. Setae emerging from the back of the larvae are relatively long and flexible (often longer than body‐length), are hooked on the ends, and are well‐suited to carrying large, light objects.48 The setae found on the thorax or abdomen are densely packed and much shorter and stiffer than those on the back, typically have microtextured tips to increase contact area, and assist with carrying smaller objects like dirt or sand grains.48 Such selective adhesion properties may also be useful in engineered systems designed to perform a sorting function, e.g., devices that target specific particles or cells, or machines that separate differently sized parts along an assembly line. Figure 3 Open in figure viewer PowerPoint Apochrysa matsumurae carrying flocculence and cocoon material. B) Italochrysa italica disguised by pieces of woody material. Adapted with permission. 663 Lacewing larvae employ passive camouflage by carrying around detritus. A)carrying flocculence and cocoon material. B)disguised by pieces of woody material. Adapted with permission.Copyright 2014, Oxford University Press. 2.1.1 Anatomical Fastening A variety of different insects have convergently evolved physical methods to fasten two separate anatomical parts together.49 Nearly all of these techniques take advantage of complementary lock‐and‐key structures. Unlike other physical adhesive systems, these were not adapted to stick to generic rough or smooth surfaces, but rather are complete systems of reversible adhesion similar to Velcro. Dragonflies and damselflies (order Odonata) have a small and delicate connection between the head and the rest of the body (Figure 4A,B).50 This fragile joint is beneficial for its extreme flexibility, but poses a problem during relatively high‐force actions like feeding, perching, and mating.51, 52 To avoid potential damage during these activities, dragonflies and damselflies have developed a set of opposing frictional surfaces to provide support to the neck (Figure 4B,C). The system incorporates four components: arrays of epidermal microtrichia (small stiff hairs on the outer surface), muscles to orient the head and neck surfaces, sensory mechanisms to monitor surface contact, and cells to secrete adhesion‐promoting lipid‐based substances.49 Similar to locomotive setae, microtrichia can take on a variety of forms depending on the particular taxa of Odonata (Figure 4D).53 When placed into contact, the complementary surfaces do not fully interlock with one another. Instead, deformations of the microtrichia vastly increase surface contact area and prompt the release of wet adhesive secretions, both of which lead to relatively large adhesive forces.54 Figure 4 Open in figure viewer PowerPoint Ischnura senegalensis. B) Scheme of the damselfly head, neck, and head arrester system. C) Scanning electron microscopy (SEM) image of head‐arresting apparatus on the blue‐tailed damselfly, Ischnura elegans; MF = microtrichia field on back of head, NM = neck membrane, SPC = postcervical sclerite (movable pad covered in microtrichia complementary to MF). Scale bar: 10 µm. Reproduced with permission. 664 52 Dragonfly necks are fragile and require a reversible attachment system to secure them during high‐intensity maneuvers. A) The damselfly. B) Scheme of the damselfly head, neck, and head arrester system. C) Scanning electron microscopy (SEM) image of head‐arresting apparatus on the blue‐tailed damselfly,; MF = microtrichia field on back of head, NM = neck membrane, SPC = postcervical sclerite (movable pad covered in microtrichia complementary to MF). Scale bar: 10 µm. Reproduced with permission.Wiley. C) Diagrams of various frictional surface motifs found in different families of Odonates as indicated on the lower right of each panel. Reproduced with permission.Copyright 1999, The Royal Society. Examples of quick‐release adhesives can be found in many different flying insects that attach their wings to their bodies when not in use. These fastening mechanisms take on a variety of different forms, including snap‐like binders in aquatic true bugs (order Hemiptera),55 and the pointed, angled structures used by beetles (order Coleoptera).56 Aquatic Hemiptera secure their forewings tightly to the thorax while at rest using a knob‐and‐socket geometry similar to metal snaps used for fastening clothing, but much smaller.55 The thorax of these insects contains an array of knobs or button‐like protrusions, which are rounded, pear‐shaped, or dome‐like depending on the species. Each knob is entirely covered with small, densely packed tile‐like microtrichia. Some of the microtrichia contain ducts or pores to direct adhesive secretions into the contact zone. The wings contain complementary U‐shaped sockets with matching tile‐like microtrichia.55 2.2 Chemical Adhesive Systems The commercial adhesives industry has recently been affected by strict environmental and health regulations. These regulations, in combination with pressures from volatile oil markets, have driven adhesive manufacturers away from fossil‐fuel‐derived products and toward natural products.57 Insects present a multitude of biocompatible, biosynthesized solutions that could theoretically be mass‐produced using state‐of‐the‐art techniques including recombinant protein expression and microfabrication. 2.2.1 Chemical Adhesives for Stasis and Locomotion To complement their physical‐adhesion‐promoting architecture, each of the physical systems described previously also utilizes complementary adhesive secretions. Both fibrous and pad‐based tarsal structures secrete an epidermal fluid. This fluid is composed of three key parts: (i) an aqueous portion rich in amino acids and carbohydrates, (ii) oily nanodroplets containing hydrocarbons, and (iii) an emulsifier to stabilize the mixture (e.g., cholesterol, monoglycerides, etc.).58 A study of the chemical composition of the smooth pad secretions of the migratory locust, Locusta migratoria, revealed that there are discernible differences between the composition of the lipid membranes of the pad exterior and the adhesive residue that it leaves behind. The pad surfaces themselves have a much greater proportion of long chained (C 24 –C 32 ), saturated fatty acids in the form of wax esters, while the secretions contain short chained (C 16 –C 20 ) unsaturated fatty acids that exist either in their free form or as glycerol esters. Unlike the pads, the secretions also contain significant quantities of carbohydrates (40% of detectable organic components, mostly glucose), which are thought to play a key role in the fluid viscosity and overall adhesive function.58 Several theories attempt to explain the purpose of these locomotive secretions. First, they were thought to be used by insects as a glue‐like adhesive. However, Jiao et al. showed that the grasshopper Tettigonia viridissima could quickly attach and detach its pads because its adhesive secretions were not sticky in the traditional sense.59 An alternative explanation is that a thin film of fluid could facilitate stronger intermolecular forces by playing the role of a coupling agent, adapting to both hydrophobic surfaces and hydrophilic surfaces.60 Additionally, the fluid may promote capillary and/or viscous adhesion at the insect–surface interface. Emulsions and colloid‐rich solutions can exhibit non‐Newtonian behavior, so the oil/aqueous mixture may promote stronger viscous forces under shear stress in the contact region than the viscous forces of a pure aqueous solution.61 Another interesting property of adhesives intended for locomotion is their ability to self‐clean.26 Insects often travel along surfaces littered with small particles (e.g., dust, pollen, etc.). As with commercial adhesives, one might expect their adhesion ability to decline with time and walking distance, as epidermal surfaces and substances become contaminated. It has been shown, however, that insects retain approximately consistent adhesive strength throughout their lifespan.62 Both fibrillar and smooth pad structures are able to remove contaminating particles after only a few steps using several techniques. For example, many insects perform sliding movements while their feet are in contact with a surface in order to induce shear stresses that not only increase viscous adhesive forces, but help to dislodge contaminants.63, 64 Secreted adhesive fluid also plays a key role in self‐cleaning by making it possible to deposit contaminating particles with each step, essentially washing the epidermal layer.26 The ability of certain insects to strongly fasten themselves to a variety of surfaces is also remarkable. For instance, a leaf beetle, Chrysolina polita, can withstand drag forces from wind speeds of up to 48 m s−1 (170 km h−1), and branch accelerations that can impart forces of around 16 times greater than its body weight.34 The beetles are able to achieve this feat using feet with a fibrous exterior in combination with secreted adhesive. In a comparative study of adhesive secretion viscosities, Peisker et al. found that fly secretions (from Calliphora vicinia) have a much lower viscosity (10.9 mPa s) than secretions from beetles (Coccinella septempunctata, 21.8 mPa s).65 Both of these insects have fibrous adhesive feet, so the difference can be attributed to the composition of the fluid. This finding provides insight into the role that viscous forces play in general insect adhesion: fly secretions are suited for shorter detachment times to escape from predators, while beetles sacrifice rapid mobility for increased adhesive force.65 2.2.2 Permanent Insect Adhesives The manner in which female insects position and fasten their eggs on surfaces is critical to reproductive success. Insects accomplish this task by using a thick adhesive coating that can account for ≈20% of egg mass.66 The sticky substance is typically a permanent glue with the ability to join eggs to both hydrophobic and hydrophilic surfaces, as well as to surfaces covered in dirt or wax crystal contaminants.67 Physical properties of this substance vary widely across species, ranging from hydrogels to water‐soluble or insoluble liquid glues or light foams,66 but the majority share a predominantly (though surprisingly diverse) proteinaceous composition.57 For instance, praying mantises (order Mantodea) use a foam‐based egg coating that dries rapidly into a cement‐like casing and is primarily composed of proteins with α‐helical structural motifs in combination with various enzymatic crosslinkers.68 One of the strongest measured insect egg‐glues, a hydrogel from the gum moth Opodiphthera sp., consists of up to 50% protein by dry weight. (Here and throughout this review, “sp.” indicates a single nonspecific species in a genus, while “spp.” indicates multiple species.) Much of this protein has a strong over‐representation of glycine residues, which impart flexibility, and serine residues, which encourage hydrogen bonding; these are common characteristics of structural, adhesive, and elastic proteins.57 This glue has a dry shear strength of 1–2 MPa with high elastic extensibility and tack, which makes it a biocompatible alternative to currently available “permanent” synthetic adhesives.57, 69 2.2.3 Adhesive Prey Capture Insects also use adhesives to capture prey. A noteworthy example of this behavior is employed by rove beetles, Stenus spp. (Figure 5).70, 71 These beetles have developed a sticky, extensible labium (mouthpart) as a predatory weapon. With no prey present, the labium is stored within a membranous tube inside the beetle's head. To attack, the beetle rapidly extends its labium (typically on the order of 1–3 ms), drawing the prey into the beetle's jaw‐like mandibles for consumption. The labial structure is terminally tipped with a pair of adhesive pads, so‐called paraglossae, each with an intricate, outwardly branching structure.72 The surface area and branching extent of these pads differs widely with species and there is a positive correlation between greater surface area/branching and adhesive strength.70, 73 From an evolutionary perspective, enlargement of these paraglossae likely allowed beetles to target a niche of larger and faster fleeing prey.74 Figure 5 Open in figure viewer PowerPoint Stenus hunt with an extensible labium tipped with adhesive pads, the paraglossae (“pgl”). A) Extended labium of the Stenus beetle used for prey capture. 73 Stenus montivagus. Reproduced with permission. 73 Stenus clavicornis. D,E) Paraglossae of Stenus fossulatus. Note the differences in the extent of branching and spacing. Scale bars: A) 500 µm, B) 10 µm, D) 5 µm, C,E) 2 µm. B–D) Adapted with permission. 73 Rove beetles of the genushunt with an extensible labium tipped with adhesive pads, the paraglossae (“pgl”). A) Extended labium of thebeetle used for prey capture.Inset: the rove beetle,. Reproduced with permission.Copyright 2009, Udo Schmidt. B,C) Branching structure of paraglossae of. D,E) Paraglossae of. Note the differences in the extent of branching and spacing. Scale bars: A) 500 µm, B) 10 µm, D) 5 µm, C,E) 2 µm. B–D) Adapted with permission.Copyright 2017, Oxford University Press. Adhesive attack mechanisms of the Stenus beetles are suited to prey with many different physical and chemical surface properties.74 As with the locomotive adhesive systems, paraglossae combine a surface mapping microstructure (Figure 5B–E) with a viscous secretion that is produced by specialized glands within the membranous tube. The composition of this fluid, again similar to that found on insect feet, is a combination of two or more immiscible phases containing proteins, carbohydrates, and fatty acids in a viscous milieu.75 Two key aspects set the paraglossae apart from their locomotive counterparts. First, their microstructures are almost entirely immersed in secreted fluid. The viscosity of the fluid is therefore assumed to be the dominant adhesive force.73 Second, the adhesive strength of these pads is entirely independent of surface roughness. This independence is attributed to the relatively large amount of fluid in combination with the compressive forces generated from rapid protrusion which help to effectively fill voids in the surface.72

3 Specialized Structures for Movement When insects are not busy performing gravity‐defying adhesive walks, many of them also fly or swim to ensure their everyday survival, employing a broad array of physical structures with unique properties. Each structure is composed of cuticle arranged into macrolayers, thin membranes, porous architectures, or 3D protrusions (Figure 2). Insect appendages combine these material motifs in a way that precisely balances mass, elasticity, force output, and material cost to suit a particular need.76-78 Flying insects in particular have an obvious technological analogue in micro‐aerial‐vehicles (MAVs), which have generated tremendous buzz for their abundance of potential applications.79-81 Flying robots share many design constraints with insects, as their ability to fly relies on striking a delicate balance between the power output of their movement machinery, the amount of available energy, and mass constraints.82 Flying robot miniaturization is further complicated by the fact that large aircraft design motifs fail at small sizes due to differences in force scaling.80 Researchers recently developed a compelling solution to these problems in the form of a “robotic insect”—a small, battery‐powered flying robot with flapping wings.83 Its energy‐efficient locomotive design is derived directly from insects and it incorporates a switchable, electrostatics‐driven adhesive pad that allows it to perch underneath a variety of surfaces. We posit that robotic developments like this are not mere curiosities; they rather represent a shift toward engineered microsystems interacting with weak forces. This is a relatively new size regime for robots, but is one that insects have been inhabiting throughout their existence. 3.1 Insect Wing Morphology and Composition Nearly twelve thousand vertebrate species and more than one million insect species have developed wings for powered flight.84, 85 Flying vertebrates have wings containing embedded musculature which they use to actively manipulate wing shape in various flight styles.84 The span of an insect wing, however, is almost entirely passive and is controlled only by muscles localized to the wing base.86 Therefore, unique morphological and/or compositional features are responsible for any necessary deformations.87 Across all flying insect species, wings provide three key functionalities: (i) they act as levers, relaying force from muscles at the wing base to the surrounding air, (ii) they are oscillating airfoils that direct air through wing strokes to generate lift, and (iii) they act like cantilevered beams, deforming under a variety of forces.76, 88 To perform each of these tasks successfully, the wings must be lightweight, flexible, and strong, making them intriguing targets for material biomimicry. Quantifying these properties in insects is unfortunately nontrivial, as the delicacy and heterogeneity of wing material is not particularly suited to standard material characterization methods. In response, researchers have developed custom tensile testing apparatuses and have used other techniques like nanoindentation or static bending to measure flexibility descriptors such as Young's modulus.89-91 These systems have determined with reasonable consistency that the Young's modulus of an insect wing membrane is 2–5 GPa, which is comparable to that of nylon,92 though this value can vary with location on the wing, insect species, and general wing structure.91 As is the case for most other structures on insect exteriors, wings are made of cuticle. The cuticle is venated by branching hollow tubes of varying diameters and wall thicknesses, with elliptical, circular, or bell‐shaped cross sections to impart axial‐dependent bending stiffness.93-95 Generally, veins are larger in diameter and have thicker walls near the wing base where stresses are great, then taper moving out toward the wingtips to reduce inertial forces.96 Those veins spanning the leading edge of the wing are largest and carry oxygen, fluids, and neuronal connections. Other, smaller veins are only air‐filled and serve to either strengthen or promote bending in particular wing sections.76 Different insects have developed unique and diverse vein branching patterns.97 While all patterns tend to promote an exponential decay in bending stiffness from wing base to tip, spatial mapping of veins plays an important role in flexibility variation between the leading and trailing edges of wings (Figure 6).98, 99 As a method to promote further deformations within this relatively rigid venous structure, the cuticle of certain insect wings contains flexible linear segments, which act as fold lines.100 Such bands are distributed independently of support veins—those running radially (base to tip) mediate bending and twisting, while others oriented transversely (leading edge to trailing edge) act as one‐way hinges to help the wings bend and reset after the completion of a downstroke.100 Figure 6 Open in figure viewer PowerPoint Sympetrum vulgatum, with associated SEM images of the various structural wing features. Distribution of thicknesses of B) veins and C) membrane within the forewing. Scale bars: 1 mm. Reproduced under the terms of the CC‐BY license. 665 Dragonfly wings are advantageously venated and thickened to provide structural integrity and spatial variation in flexibility. A) Photograph of the forewing of the vagrant darter dragonfly,, with associated SEM images of the various structural wing features. Distribution of thicknesses of B) veins and C) membrane within the forewing. Scale bars: 1 mm. Reproduced under the terms of the CC‐BY license.Copyright 2010, Jongerius & Lentink. Other flex‐lines stay rigid during flight movements, but deform reversibly when the wings contact obstacles to prevent structural damage.101 A bumblebee is estimated to strike one obstacle per second while foraging for pollen,102 which means its wings will sustain ≈500 000 collisions over its lifespan of a month.103-105 After splinting the wings to prevent them from bending, researchers observed an order‐of‐magnitude increase in the rate of wing loss from collisions.101 These damage‐minimizing crumple zones are therefore essential to wing longevity, especially in foraging insects. Wing membranes not only serve as a deformable element, but may also contribute to overall flexural rigidity.93-95 Their thickness varies approximately four orders of magnitude across insect species, ranging from less than 500 nm in the delicate wings of fruit flies (Drosophila sp.) to thicker than 1 mm in the sturdy fore‐wings of beetles (order Coleoptera).76 Certain regions within an individual wing membrane can also vary in thickness and mass. The wings of dragonflies (order Odonata), for example, contain a region called a pterostigma. This dark‐pigmented spot sits adjacent to the leading wing edge and is thicker and denser than that of the surrounding cuticle, with a much coarser texture (Figure 6).106 It shifts the wing's center of mass toward the leading edge, which provides more gliding stability, helps to regulate wing pitch, and increases asymmetry between upstroke and downstroke in each flap.106, 107 Membrane composition also varies spatially within wings. The wings of certain beetles and earwigs specifically contain flexible regions rich in a protein called resilin that imparts elasticity.108, 109 These regions assist with wing folding for storage during rest and with general deformation by reducing the elastic modulus up to three orders of magnitude. Resilin also increases the elastic energy captured during wing movements for better flight efficiency.101, 110, 111 Unlike typical airfoils, which are smooth and aerodynamically streamlined, the wings of many insects are rough or textured. Some examples of this structuring include the cross‐sectional corrugations found in dragonfly wings (Figure 6) and scales on the wings of butterflies and moths.112, 113 In the dragonfly specifically, it is likely that corrugations improve rigidity between the wing base and tip to compensate for the ultralight and ultrathin membrane composition.94, 112 Some researchers argue that air vortices fill the voids created by these corrugations and effectively smooth the surface profile, while others assert that dragonfly‐wing corrugations trade aerodynamic performance for structural support.114, 115 Certain insect wings are also cambered near the wing base, meaning that the top (dorsal) side of the wing has a convex structure while the bottom (ventral) side is concave.116 This geometry adds an element of asymmetry to wing bending—downward force acting on the dorsal surface of a wing will result in more bending to reduce energy expended during an upstroke, while the wing resists bending under upward force on the ventral surface due to concavity to generate more lift from each downstroke.98 Curiously, fairyflies (family Mymaridae) and small flying insect species from at least six other families do not conform to the insect wing morphology described above, and instead have developed wings predominantly made up of long bristles (see Figure 7).6 The functional basis for this morphology is still up in the air, but likely involves some combination of weight reduction, electrostatic dispersal enhancement (a technique possibly used by ballooning spiders for flight),117 mechanosensation, improvement of wing folding, and/or flight efficiency.118-121 When moving an appendage through a fluid, the relationship between the velocity of that appendage and the force applied to it depends on the dimensionless Reynolds number, which represents the ratio of inertial forces to viscous forces and is calculated from the fluid's density, viscosity, and relative velocity as well as a characteristic dimension of the appendage. Most biological hairs are sized such that the force generated by their movement is independent of their spacing at relevant speeds.122 Fairyfly wings, however, have tiny hairs with diameters between 300 nm and 2.5 µm, expanding the range of velocities where hair spacing has a significant effect on the force generated through movement; the velocity of their wings falls within this range.6, 123 By actively controlling wing bristle spacing or attack angle, fairyflies are able to optimize their wingbeats to maximize lift and minimize work. In other words, fairyflies reduce their effective bristle spacing on downstrokes to make their wings behave like paddles, and increase this spacing on upstrokes to achieve a more rake‐like effect.122, 124 The force required to separate the wings, which clap together at the top of a wingbeat, also plays a role in this adaptation. Drag forces on one solid insect wing separating from another are more than three times greater than those on a wing translating independently, and this effect increases at lower Reynolds numbers.125 The bristled wings of a species of order Thysanoptera, Thrips physaphus, experience twelve times lower drag force while separating than solid wings.124 By improving flight efficiency, hair‐based wings allow smaller insects to fly for sustained periods of time without large, energy‐consuming musculature. A similar design approach may allow even the smallest of MAVs to fly using minimal battery power. Figure 7 Open in figure viewer PowerPoint Tinkerbella nana (Hymenoptera: Mymaridae), the wings are shown at the start of a downstroke. B) Dorsal angle SEM image of fairyfly Kikiki huna, the wings are shown at the finish of a downstroke. C) SEM image of a basal wing segment of the fairyfly Tinkerbella nana. Scale bars: A,B) 100 µm, C) 20 µm. Reproduced under the terms of the CC‐BY license. 6 Fairyflies have unique bristle‐based wings enabling efficient flight. A) Lateral angle SEM image of the fairyfly(Hymenoptera: Mymaridae), the wings are shown at the start of a downstroke. B) Dorsal angle SEM image of fairyfly, the wings are shown at the finish of a downstroke. C) SEM image of a basal wing segment of the fairyfly. Scale bars: A,B) 100 µm, C) 20 µm. Reproduced under the terms of the CC‐BY license.Copyright 2013, John T. Huber & John S. Noyes. 3.2 Swimming Adaptations Freshwater aquatic environments contain a disproportionately large amount of animal species. Despite covering only 1% of the surface of the Earth, they are home to more than 10% of taxonomically identified species, 80% of which (up to 200 000) are estimated to be aquatic insects.126 At least fourteen orders of insects contain aquatic species, and five of those orders consist mostly or entirely of aquatic insects.127 Insects have developed a variety of physiological systems to survive and thrive in water, including systems optimized for feeding, for respiration (discussed in Section 4.2), osmoregulation, and locomotion. Two notable solutions for aquatic movement have been developed by the phantom midge (Chaoborus crystallinus), and the mosquito (Culex pipiens). Both larvae and pupae of the phantom midge possess a tail fan, which is a structure containing an average of 26 cuticular filaments, ≈1 mm in length and 11 µm in diameter (at the base), with 10 µm of base‐separation when fully splayed.128 Each of these filaments has regions rich in the elastic protein resilin, which helps maintain a splayed state while resting.128 To move, the phantom midge curls up its body (fan actively retracted), and then rapidly straightens out while passively splaying the fan. Fan extension increases the surface area of the last abdominal segment by more than 500%, which provides paddle‐like thrust and potentially even steering/stability control.128 Similarly, mosquito larvae have a brush‐like structure emerging from their mouth that resembles a mustache.129 The hairs, which number around 1000 per larva and are each ≈400 µm long, are arranged in 20–30 rows with even spacing. They are actively swept back and forth at a rate of 11 Hz within a roughly 90° range of motion.129-131 This motion produces a one‐directional current that propels the larvae without producing any periodic disturbances, which would disrupt both vision (see Section 6) and vibrational sensation (see Section 5).129 Techniques that promote uniform (rather than periodic or random) and energy‐efficient locomotion are desirable from an engineering viewpoint as they provide maximum autonomy and power to other on‐board systems, e.g., cameras or flow sensors.132 Many of the best‐known aquatic insects come from the true bugs (order Hemiptera), which includes water striders, water boatmen, backswimmers, and shore bugs.126 Legs of insects in this order are well adapted to movement through water or on its surface. Gerromorphan bugs (water striders, shore bugs) have hairs on their legs and bodies that increase surface area and create trough‐shaped depressions on the surface of water.127 They move across the surface in three distinct fashions: (i) walking by moving three legs at a time as alternating tripods, (ii) rowing by moving the middle legs simultaneously while the hind legs lay flat on the water surface, and (iii) skating with powerful center leg strokes that look like a jump‐and‐slide.133 Water striders in particular are assisted by thin chitinous setae (hairs) 50 µm long that cover the surface of their legs.134 These setae are oriented at a 25° angle to the leg surface, which gives them interesting direction‐dependent surface‐adhesion properties stemming from the solid–liquid air contact line (see Section 4).135, 136 When the setae are directed opposite to the motion of the water (against the grain), fluid force pulls them away from the leg surface, increasing both the relative angle between the two and the water–hair contact area. This effect results in greater adhesion to the air–water interface, which the water strider uses both while drifting on the surface and for propelling motions.134 When the setae are oriented in the direction of water flow (with the grain), surface adhesion is reduced, which is beneficial for passive gliding after a leg stroke.134 In terms of fluid dynamics, the microhairs help water striders modulate the slip length, i.e., the amount of friction or drag force, between their legs and the fluid. Structured surface features that actively manipulate slip length have, for example, been applied in microfluidic and nanofluidic devices to control flow rates,137 and could inspire applications with larger size scales, e.g., to improve watercraft efficiency on the hulls of boats. Passive functional structures such as these have a range of applications limited only by the creativity of the engineer.

4 Water‐Associated Structures Insects have a number of nonlocomotive adaptations that relate to water, as well—they inhabit environments that range widely in terms of their humidity, access to moisture, and prevalence of interfaces, leading to a number of evolutionary pressures with material solutions. Some of these solutions are external: dragonflies, damselflies, and cicadas all have cuticular structures on their wings that protect against interference from raindrops and dirt.138-141 Others are internal: to avoid dehydration, various species of midges manipulate their systemic concentrations of osmolytes.142-144 Despite their functional and spatial differences, most water‐specific adaptations in insects share common mechanisms of action: they either modify wettability through a distinct air–water–surface interface, or they maintain specific osmotic or hydrostatic pressures. The concept of air‐gap‐based (super)hydrophobicity, since its introduction in the first half of the 20th century,145, 146 continues to be applied in new contexts. Advances in microfabrication and surface characterization have provided critical physical insight into how micro‐ and nanostructures modulate wettability.147 Aside from choosing substrate materials, engineers ultimately have three control parameters when designing a surface with roughness‐induced hydrophobicity: the size, the shape, and the density of fabricated surface features.148 As features become smaller and more densely packed, their ability to prevent condensation of fogs and fine mists improves. This effect is optimized when the features are shaped like cones (rather than cylinders), as is the case with the surface of lotus leaves.148, 149 These general trends represent a useful starting point for surface engineering, but intermediate parameters within each category and the various permutations found among the insect world have yet to be fully explored and may provide more optimized design approaches with advanced functionality. 4.1 Hydrophobic and Hydrophilic Surfaces Two groups of organisms have developed truly superhydrophobic (water contact angles greater than ≈150°) and self‐cleaning surfaces; plants and insects.150 Of the plants, lotus leaves have garnered considerable attention for their optimized hierarchical surface patterns that arise from micro‐ and nanostructured surfaces.151-153 Examining the hindwings of the planthopper, Desudaba danae, reveals apparent convergent evolution with the lotus (Figure 8).149 The surfaces of both planthopper wings and lotus leaves are dotted with tapered micropillars with base diameters between 4 and 10 µm and heights between 6 and 10 µm, spaced 15–30 µm apart.149 These pillars, and hydrophobic surfaces on insects in general, serve a variety of purposes. They: (i) prevent water (and thus weight) accumulation though antiwetting, (ii) exhibit low adhesion to foreign particles, (iii) promote droplet rolling to encapsulate and remove any contaminants that manage to stick to the surface, (iv) encourage droplet coalescence, which helps protect against the accumulation of water from fine mists, and (v) discourage bacterial growth.149, 154 Figure 8 Open in figure viewer PowerPoint 149 149 149 Planthoppers and lotus plants have developed remarkably similar superhydrophobic surface structures through convergent evolution. A–D) SEM images of the surface of the lotus leaf (inset) at varying magnifications. E–H) SEM images of the surface of the planthopper hindwing (inset) at varying magnification. I) SEM image of planthopper hindwing to highlight heterogeneous aspects of the protrusions and their spacing. Reproduced with permission.Copyright 2017, American Chemical Society. Inset of (A) Reproduced under the terms of the CC‐BY‐ND licence. Copyright 2011, Steve Corey;inset of (E) Reproduced under the terms of the CC‐BY licence. Copyright 2017, Katja Schulz. Broadly, these hydrophobic designs can be generalized into at least four groups: simple (e.g., pillar or dome‐shaped) micro‐ or nanostructures, complex (varied shape) micro‐ or nanostructures, scales (usually 2–3 µm in one dimension), hairs or setae much longer (typically more than 5 µm in length) than their diameters, and hierarchical organizations including any combination of these elements (Figure 9).155 Regardless of their design motif, hydrophobicity‐inducing structures in insects generally seek to maximize the air–water interface area while minimizing the solid–water contact area. This concept of air‐gap hydrophobicity, first put forth by Cassie and Baxter in 1944 to explain the hydrophobic nature of duck feathers and how they could serve as bioinspiration for water‐repellent clothing, is central to all surfaces in insects whose hydrophobicity is driven by structure rather than chemicals.146 The Cassie–Baxter theory describes hierarchical micro‐ and nanostructures as uniform curved surfaces with a heterogeneous composition (e.g., of air and solid), and posits that the air filling the space between these structures is essentially trapped and behaves like a nonwetting solid.146 Figure 9 Open in figure viewer PowerPoint Entomobrya intermedia and SEM images showing hexagonal and triangular motifs in P. flavescens. B‐B″) Image of Vertagopus arboreus, and SEM images showing irregular square and pentagonal motifs in I. viridus. C‐C″) Image of Kalaphorura burmeisteri, and SEM images showing secondary granular structures and hexagonal motifs in S. quadrispina. D‐D″) Image of D. ornata, and SEM images showing secondary granular structures and variable elliptical patterns in A. pygmaeus, Scale bars: A′–D′ = 2 µm, A″–D″ = 500 nm. Reproduced with permission. 666 Different orders and life stages of springtails (Collembola) have developed a variety of periodic, hierarchical surface structures with hydrophobic properties. A‐A″) Image ofand SEM images showing hexagonal and triangular motifs in. B‐B″) Image of, and SEM images showing irregular square and pentagonal motifs in. C‐C″) Image of, and SEM images showing secondary granular structures and hexagonal motifs in. D‐D″) Image of, and SEM images showing secondary granular structures and variable elliptical patterns in, Scale bars: A′–D′ = 2 µm, A″–D″ = 500 nm. Reproduced with permission.Copyright 2012, Springer. Fog forms on a surface when droplets larger than 190 nm in diameter (more than half the shortest wavelength of visible light) condense and accumulate.156 This phenomenon poses a challenge to insect vision, as insects lack eyelids and thus have no way to externally remove vision‐blocking moisture or other contaminants. Mosquitoes, family Culicidae, have superb vision that can function in poorly lit and damp environments to locate mates, oviposition sites, and blood sources.157 To maintain consistent sight and avoid fogging, the surface of each mosquito ommatidium (optical sensory unit, discussed in Section 6.4) is densely coated with nanoscale nipples. These nipples are around 100 nm in diameter and are spaced roughly 50 nm apart in a hexagonal non‐close‐packed array; they also provide refractive‐index matching for improved transparency (see Section 6.2). Their proposed mechanism of hydrophobicity mirrors that of the lotus leaf, planthopper wing, and water strider legs: the nanostructured array contains air gaps that effectively prevent water from contacting a large portion of the surface as in the Cassie–Baxter model of wetting.146, 149, 151, 158 In other words, the nanometer spacing of surface features creates a complex, nonplanar water–air–insect contact area, which makes it energetically less favorable for water droplets to wet the surface than to remain as spheres in the air.136 Additionally, theoretical studies show that it is unfavorable for water molecules to form a network of hydrogen bonds within nanostructured materials, and specifically between hydrophobic surfaces separated by a critical distance of 100 nm.159 Antifog eyes are not unique to mosquitoes; the green bottle fly, Lucilia sericata, has also developed a fog‐resistant eye surface structure thought to act in a similar manner, with well‐ordered bubble‐like protrusions ≈100 nm in diameter and packed in close proximity.160 Similar optical features have recently been found in many other insect species.148 Other insects including the desert beetle, Physaterna cribripes, use fog as an important source of moisture.161 When the desert humidity increases to a level where fog or dew can form, usually in the early morning, the beetle angles its elytra (protective wing cover) against the wind, causing droplets to condense on the upper cuticular surface.162 These droplets, which are tens of micrometers in diameter, would ordinarily detach from the surface under desert heat and wind conditions, but a specially developed elytral structure of hydrophilic islands on a hydrophobic substrate keeps them in place.163-165 The elytra's macroscopic structure is a random array of bumps of around 500 µm in diameter spaced between 0.5 and 1.5 mm from one another. The peaks of these bumps are smooth and hydrophilic, while the troughs between bumps are coated with wax and contain a hexagonal array of flattened, 10 µm hemispheres that render them hydrophobic. Droplets are attracted to the hydrophilic regions, where they spread to coat their “island” and begin growing upward until they have enough weight to overcome capillary adhesion to the bump.164 At this critical mass, they form large droplets that roll into the hydrophobic troughs where they are guided down the surface of the elytra to the beetle's waiting mouthparts.161, 164 Not all insects have developed cuticle nanostructures to produce specific interactions with water. Some, like the leafhopper, family Cicadellidae, achieve hydrophobicity by coating themselves in a nanosized proteinaceous powder.166, 167 The powder is composed of spherical honeycomb‐like particles called brochosomes, which have diameters between 200 and 700 nm and walls arranged in pentagonal and hexagonal shapes that open into a hollow center.167 Most of these particles have the same truncated icosahedral geometry also found in soccer balls, C 60 buckyballs, and viral capsids (Figure 10).168, 169 Their chemical composition is ≈60% protein and 40% lipids and/or other compounds; the exact composition varies with species.167, 170, 171 Within the proteins, there are higher than normal representations of glycine residues, which are often found in fibrous structural proteins, and tyrosine residues, which may play a role in polymeric hardening and crosslinking during wall formation.172, 173 The leafhopper applies these coatings shortly after molting by secreting a colloidal suspension of brochosomes from its hindgut onto its exoskeleton, then grooming itself with rapid leg strokes until the solvent evaporates.167, 174 Interestingly, the material composition of the brochosomes themselves is only moderately hydrophobic, but they are able to generate near superhydrophobicity when arranged in an ensemble layer by creating a complex water–air–insect interface rife with tiny air gaps (again approximating the Cassie–Baxter regime).167 Surprisingly, most leafhopper species actually live far away from water. While their brochosome coatings do defend against atmospheric moisture (e.g., rain), a more likely functionality can be traced to their own liquid excretions. Leafhoppers feed on phloem and excrete a sugar‐rich “honeydew,” which is sticky and provides an ideal growth substrate for pathogenic microbes.175 In dense populations of leafhoppers, hydrophobic coatings may serve largely to prevent insects from being coated in their own, or their neighbors', excrement.167, 176 Protective surface coatings made of actively secreted molecules and particles may also be useful in materials science as such surfaces could reduce biofilm formation or other fouling mechanisms. Figure 10 Open in figure viewer PowerPoint Athysanus agentarius. D) Touching brochosomes are connected on A. agentarius. E) Dense coating of brochosomes on the hind wing of A. alneti. F) Photograph of a green leafhopper. Scale bars: A,B) 50 nm, C,D) 100 nm, E) 1 µm. A–E) Adapted with permission. 667 667 The leafhopper (family Cicadellidae) coats itself with brochosomes—spherical, honeycomb‐like particles made of proteins and lipids and less than 1 µm in diameter—to achieve a nearly superhydrophobic exterior. Illustrative model of a typical brochosome with: A) general view and B) cross section. C) Individual brochosome on the surface of. D) Touching brochosomes are connected on. E) Dense coating of brochosomes on the hind wing of. F) Photograph of a green leafhopper. Scale bars: A,B) 50 nm, C,D) 100 nm, E) 1 µm. A–E) Adapted with permission.Copyright 2013, The Royal Society. F) Reproduced with permission.Copyright 2015, Bernard Dupont. Despite the highly optimized nanostructures on their eyes, both male and female mosquitoes of species Anopheles freeborni lack superhydrophobic wing surfaces to passively shed water, so their wings are susceptible to spontaneous capillary‐driven folding in high‐humidity conditions (e.g., heavy fogs).177 When this happens, their wings can become so tightly folded that they take a long time to dry, during which the mosquitoes are grounded. The mosquitoes have developed a modified wingbeat or “flutter stroke” to counter this effect.178 Normally, their wingtips oscillate at a frequency around 285 Hz, but when they sense moisture they will occasionally increase this beat rate more than threefold to 875 Hz and decrease its amplitude by nearly 90%.178 This flapping regime is poor for locomotion, but generates wing accelerations that are almost double those found in normal flight and sheds water droplets from the wing. Another adaptation, hard landing, is generally employed when the mosquito is hit by a raindrop in mid‐flight. When this happens, mosquitoes do not make any attempt to flap or clear their wings of water and instead begin a freefall dive reaching a terminal velocity of 0.44 m s−1, three times that of a falling dry, anesthetized mosquito.179 Upon hitting the ground, mosquitoes shed more than 75% of the associated water droplets, which allows them to resume flight and remove the remaining droplets via wing flutter.178 The concept of removing water through inertial forces may find uses in future large and small‐scale flying structures. 4.2 Systems for Sub‐Aquatic Exchange The primary survival challenge of aquatic insects (Section 3.2) is maintaining a consistent oxygen supply underwater. To this end, mosquito larvae from Aedes togoi float a snorkel‐like breathing apparatus on the surface of a body of water to maintain a steady oxygen supply. This appendage contains three main and two auxiliary “hydrofuge lobes” that are coated with oil secretions and arranged into the shape of a hollow cone.180, 181 The lobes converge to a single point containing an air hole (spiracle) that connects their conical structure to a tracheal trunk and the rest of the larval respiratory system.182 The floating mechanism is largely supported by surface tension, which holds the cone base at the water surface and pulls the lobes slightly apart. Lipid‐driven hydrophobicity prevents the air‐filled inverted cone from flooding and induces a negative water curvature in the gaps between lobes.183 When the larva moves downward to submerge itself (e.g., to avoid danger), hydrostatic pressure forces the lobes together, effectively sealing the spiracle until the lobes are again pulled apart by surface tension.182 Similar schemes have obvious applications as gas intake or outlet valves in the context of microfluidic actuators.184 Some insects maintain air bubbles within or nearby their exoskeleton for gas exchange (Figure 11). Known as “physical gills,” these bubbles can directly exchange oxygen and carbon dioxide with water and can either be supported by cavities of fixed volume (incompressible) or be nonsupported and free to expand and contract (compressible).185 Nonsupported air bubbles shrink as an insect dives: oxygen is used up through respiration, which increases the concentration of nitrogen in the bubble. The resulting gradient causes nitrogen to dissolve into the surrounding water.186 Any carbon dioxide produced and released by the insect quickly dissolves into the water as well. This balance of gas concentration and pressure results in a transient system where the insect must periodically return to the surface to replenish the bubble gasses.187 Figure 11 Open in figure viewer PowerPoint Gerris lacustris) showing size diversity. B) SEM image of the body of a backswimmer (Notonecta glauca), showing the microtrichia (m), as well as sharp‐tipped setae (st) and tapered‐rod setae (sb). C) SEM image of the waterlily leaf beetle (Galerucela nymphaea) showing the uniform orientation of water‐active setae on the insect's protective wing covers. All the arrows point toward the tail‐end (posterior) of the insect. A–C) Reproduced with permission. 189 194 Plastrons facilitate underwater gas exchange by using hydrophobic structures to maintain constant volume and equilibrium pressures. A) SEM image of the water‐repelling microtrichia (m) and setae (s) of the abdomen of the common pond skater () showing size diversity. B) SEM image of the body of a backswimmer (), showing the microtrichia (m), as well as sharp‐tipped setae (st) and tapered‐rod setae (sb). C) SEM image of the waterlily leaf beetle () showing the uniform orientation of water‐active setae on the insect's protective wing covers. All the arrows point toward the tail‐end (posterior) of the insect. A–C) Reproduced with permission.Copyright 2011, Wiley. D–F) Unsupported physical gills decrease in size as the insect uses oxygen, requiring the insect to return to the surface periodically. G–I. Supported physical gills allow insects to remain submerged indefinitely, provided they have low to moderate metabolic rates. D–I) Reproduced with permission.Copyright 2013, Company of Biologists. Supported physical gills, known as plastrons, are permanent fixtures that allow insects to remain submerged indefinitely in sufficiently oxygenated water.188 Unlike nonsupported physical gills, which shrink in response to pressure differences caused by respiration, plastrons have hydrophobic structures that counter the hydrostatic pressure of the water to keep the bubble volume relatively constant.189 As an insect absorbs oxygen for metabolic processes, its overall plastron pressure decreases, but the nitrogen partial pressure and plastron volume remain constant. Following this pressure decrease, oxygen diffuses from the water into the bubble, restoring overall plastron pressure and sustaining the resting metabolism of the insect.190 The river bug, Aphelocheirus aestivalis, is an aquatic insect that uses a plastron for gas exchange underwater and spends almost its entire adult life submerged. Its particular plastron is made up of cuticular hairs 0.4 µm in diameter and 3 µm long, spaced 0.5 µm apart.191 The hairs cover the entirety of the bug's highly flattened exterior, with a total surface area of ≈95 mm2 and an air volume of around 0.14 µL (with roughly a 1:1 hair to air volumetric ratio).192 This air pocket represents 8–9% of its body volume, which happens to be very similar to the proportion of lung capacity to body volume in humans.192, 193 Unlike vertebrates, however, insects employing plastron‐based respiration rely entirely on passive diffusion of oxygen through water into their breathing bubbles. These insects are therefore constrained in body size: metabolic rates in insects increase more steeply than surface area with increasing mass. Insects are also often constrained to highly oxygenated aqueous environments.194 It then follows that river bugs are likely one of the largest groups of plastron insects.192 They are shaped to have a high surface‐area‐to‐volume ratio, they have resting metabolic rates less than half of what is predicted for their size, and they are most commonly found in moving, well‐aerated streams.195 Organ‐on‐a‐chip systems have gained popularity for their potential to accurately replicate biological processes entirely in vitro.196 These systems, similar to the biological schemes they attempt to imitate, fully rely on controlled nutrient exchange between moving media and a cellular layer. Devices probing respiratory cells in particular could employ and benefit from a plastron‐based design to modulate exchange from the gas phase.

5 Sensing and Production of Mechanical Signals Insects navigate diverse and rapidly changing environments and do so while performing complex tasks like flying, mating, grooming, and foraging, among others. Making matters more difficult, all arthropods (including insects) are encased in a rigid exoskeleton similar to a medieval suit of armor. This exoskeleton provides essential benefits, but poses a major challenge in sensing and interacting effectively with the outside world. To solve these problems, insects have developed mechanosensory organs that provide spatial and force‐responsive feedback. These organs are similar to (and often complement) the appendages that insects use for locomotion; they are largely comprised of cuticle arranged in material motifs that impart various material properties like strength, elasticity, durability, and vibrational resonance. 5.1 Detection of Mechanical Signals in Insects The large majority of insect mechanosensory tools rely on approximately the same signaling mechanism based on ionic gradients, which is also employed by cochlear (hearing) hair cells in vertebrate organisms.197 The dendrite of a mechanosensory neuron sits within a highly resistant epithelial cell layer separating potassium‐rich endolymph from potassium‐deficient central hemolymph. Adenosine triphosphate (ATP) driven potassium pumps in the membranes of the epithelial cells maintain this transepithelial gradient and potential of 30 mV or more.198 When the dendrite is mechanically stimulated, mechanotransduction potassium channels open, rapidly depolarizing the associated neuron and alerting the insect to the presence of a stimulus. The large negative transmembrane resting potential of the neuron in combination with the large positive epithelial potential leads to signal transduction on the scale of microseconds, in accordance with the Hodgkin–Huxley model.199 Analogous to how signals from the human retinae are mapped into a complete visual image, insects are thought to process signals from mechanosensory arrays in aggregate, likely allowing them to interpret air currents, body movements, communication signals, and surface features as a “map” of their surroundings.200 Understanding mechanotransduction in biology requires thorough characterization of its fundamental components: the relationship between the physical properties of mechanosensory organs and their associated stimuli, and the ways in which signals from those organs are processed and subsequently influence an organism's behavior. The examples we present below aim to connect structural aspects of insect mechanosensors (e.g., morphology, elasticity, and anatomical position) with the forces they transduce. Such structure–force relationships are a central theme in the development of stretchable sensory electronics, which have applications in prosthetics, robotics, and biological monitoring.201, 202 Mechanical durability is critical in both manufactured and biological structures, as many of these devices and structures must last the lifetime of a product or insect despite exposure to wear and tear. Chortos et al. recently developed novel stretchable transistors by incorporating layers of carbon nanotubes within a polymeric material to measure stresses and strains applied to the material.203 The spatial orientation of the nanotube layers can be programmed to detect stretching or forces applied in desired directions, just as the orientation of cuticle microstructures of insects influences their specificity. The transistors themselves can be embedded into a variety of elastomer scaffolds; the composition of those scaffolds could potentially be optimized for durability or elasticity using various cuticle design principles found in insects. 5.1.1 Tactile Hairs The most prevalent organ morphologies used by insects for mechanical transduction are bristle‐like structures generally known as tactile hairs. These hairs consist of hollow shafts, each attached to a single sensory neuron, and act as lever arms that relay a mechanical force to corresponding mechanotransduction channels.204 Physically, they are thick, terminate in sharp points, and receive extra structural support from specialized cells.205 Each hair has directional selectivity that varies with aspects like hair morphology, shaft angle relative to the cuticle, and ion channel location and/or type.206, 207 Additionally, insects often possess two distinct types of associated sensory neurons: rapidly adapting (i.e., respond quickly to changes in stimuli) and slowly adapting (i.e., respond throughout the duration of the stimuli). Hair length varies between the two. Two‐spotted crickets, Gryllus bimaculatus, for instance, have tactile hairs ranging in length from 30 to 1500 µm.208 Long cricket hairs stimulate neuron dendrites, which are slowly adapting; these first‐order differentiators are sensitive to changes in displacement and generate action potentials over the duration of a stimulus. The neuron dendrites associated with shorter hairs are rapidly adapting second‐order differentiators that respond to changes in velocity.208 This difference stems mainly from the ion channels for mechanotransduction within the dendrites themselves rather than from the mechanical properties of the hairs—e.g., the short hairs of crickets remain pivoted past threshold under sustained stimulus, but their associated neurons do not transmit signals outside of the stimulus onset or offset. Together, these hairs allow the creatures to sense miniscule changes in air currents, including the wingbeats of predators in the presence of a steady wind. Studies on the desert locust, Schistocerca gregaria, revealed that in particular mechanical activation thresholds can vary considerably between the two types of mechanosensors, with roughly a 40° deflection threshold for rapidly adapting hairs and a 10° threshold for slowly adapting hairs.207 Head stabilization is essential to insect agility and visual navigation. Dragonflies accomplish this task by temporarily fastening their heads to their necks using an intricate, interlocking physical adhesive structure as discussed in Section 2. On the other hand, the hoverfly, Episyphrus balteatus, has a more developed structural and muscular head support than dragonflies, which it is able to manipulate with the help of tactile hair feedback.209 This feedback acts in combination with visual cues to orient both the head and body of the hoverfly in a horizon‐locked position. Head positioning is also important for walking insects, which face disruptions from step movements as well as inconsistent surface topographies. For example, in complete darkness, the bull ant, Myrmecia pyriformis, is able to maintain a consistent head position using feedback from joint‐positioned hairs, which monitor positions and forces on each ant limb to determine the direction of gravity.210, 211 There is little variability in the structure and ubiquity of tactile hairs between different insects,212-214 and the hairs play an integral role in the survival of insects. This convergent mechanosensory system is therefore thought to be extensively refined by evolutionary selection pressures.200 5.1.2 Campaniform Sensilla Another class of mechanosensory organ, known as campaniform sensilla, are dome‐shaped cuticle components that respond primarily to stress and strain.215 Similar to the tactile hairs, each sensillum is innervated by a single neuron, which rests within a socket underneath a dome composed of cuticle. Mechanotransduction channels in the dendrite of this neuron are activated when the dome flattens, caused either by compression or tension of the sensillum.216 The domes themselves are generally elliptical rather than circular, which imparts directional selectivity through axial orientation: a compression along the short axis or tension along the long axis will, for example, lead to dome flattening and thus neuronal activation.217 In the blowfly, Calliphora vicina, specifically, the average length of the long axis of a sensillum is about 9 µm, and the spacing between two sensilla is roughly 20 µm.215 Groups of sensilla also exist arranged side by side in close proximity, often forming structured rows.215 These groups are most commonly found in regions of the insect anatomy subject to larger strains (e.g., joints). Dendrites of each sensilla can be either rapidly or slowly adapting as well, allowing detailed sensory feedback.218 Like the tactile hairs, campaniform sensilla represent a mechanical force sensor with a unique morphology that may be replicated in next generation stretchable electronics. 5.2 Detection and Production of Vibrational Signals Hearing loss affects one in six adult humans,219 and is one of the most widespread chronic conditions in adulthood. With an aging population and increasing headphone use, the prevalence of hearing loss is expected to escalate in the coming years.220, 221 Current commercial hearing‐aids have low satisfaction rates:222 they are expensive, they are often energy inefficient, and they suffer from a poor signal‐to‐noise ratio, amplifying background noise and constraining their users to a voice‐volume comprehension threshold more than 30 dB greater than that of listeners who do not require a hearing‐aid.223 There is hence a need for miniaturized, biologically compatible systems that can efficiently detect, and also produce (see below), sounds in distinct frequency ranges. Insects are able to “hear” sounds through a variety of structures, very few of which resemble vertebrate ears. Sound is a vibration that propagates as a mechanical pressure wave through a transmission medium, such as air, water, or a solid substrate. As the majority of insects are land‐based animals, air is the most prominent carrier medium. It is, however, a compressible medium of low density. This means that although sound waves propagate a considerable distance through air, their intensity diminishes much faster than in solid or liquid media, and at an exponential rate described by Stokes' law of attenuation.224 Organs that can detect airborne sounds at a great distance (far‐field) are therefore much more sensitive than those that are only receptive to sounds or vibrations produced in their immediate vicinity (near‐field). Near‐field detectors are very common in the insect world, ranging from Johnston's organs at the base of mosquito antennae to rear‐projecting antennae‐like organs in cockroaches, even including the tactile hairs discussed previously.225 These detectors are used by flies (D. melanogaster) to sense the wingbeat frequencies of mates and by caterpillars to respond to the wingbeat frequencies of predators.226, 227 Near‐field detectors are most often found on rigid projections that resonate with ambient vibrations; their main limitation, apart from requiring close proximity to the source, is that they are generally only receptive to low frequencies (less than 500 Hz) with high intensities.228 Tympanal organs in insects—far‐field detectors—can sense the pressure wave of a sound field from more than 10 m away, and frequencies ranging from 2 to over 100 000 Hz.229 These organs are composed of three components: a tympanal membrane, an air‐filled sac pressed against the membrane, and a chordotonal sensory organ.230-232 The chordotonal organ is a cellular complex that ultimately houses a dendrite for the associated neuron(s), while the tympanum is a thin cuticle membrane similar to the head of a drum.229 Unlike vertebrate organisms, which have ears in close proximity to their cranial regions, insect ears exist at various positions on the body, including the head, wings, mouthparts, and legs.230-232 Such diversity in spatial distribution and frequency detection range is the result of imprecisely convergent evolution; insects have evolved tympanal hearing almost thirty independent times.233 By comparison, vertebrate hearing is thought to have evolved only once.234 The mechanics of insect hearing also vary considerably, from the intricate lever system joining thousands of auditory neurons in cicadas,235 to the simple, two‐auditory‐cell tympanum complex of Noctuid moths.236 Body size is a constraining factor in the evolution of tympanal organs, as the membrane requires either a minimum diameter or extreme tension to respond effectively to sound delivered at all but the very highest carrier frequencies. For example, a 0.5 mm diameter tympanum may respond maximally to 100 kHz sound delivered above a threshold amplitude of 60 dB sound pressure level (SPL) (= 20 mPa).237 Thus, the smallest insects generally do not possess tympanal organs and lack the ability to hear far‐field sound.238 5.2.1 Subgenual Organs The development of “smart material” systems with the ability to detect and locate self‐damage has garnered increasing interest in recent years. These kinds of systems offer the prospect of efficient and low‐cost monitoring of integrity in both microscale technological devices and macroscale civil structures.239 Vibration sensors can detect large changes in global vibration through a material that arise from a general loss of material stiffness. These sensors often struggle to detect small cracks that can quickly propagate beneath the surface and can lead to structural failure.240 Several potential solutions to this problem exist: (i) incorporating a massively parallelized array of microsensors, e.g., “sensory skin,” that provides a detailed force‐map of the entire structure;241, 242 (ii) improving upon the design of current vibrational sensors and their associated processing algorithms to locate cracks more effectively, or (iii) employing some combination of these first two strategies. Certain insects transmit and receive vibrational messages through the substrates they stand on for defense and other intraspecific purposes.243-245 Land bugs from more than ten families produce low‐frequency (50–200 Hz) vibrations using muscle contractions to rapidly percuss their hard abdominal (tergal) plate against a plant substrate.246, 247 The resulting vibrations travel well through the low damping substrate—measured intensity values of a 124 Hz signal through a cyperus stem were found to be consistent tens of centimeters from the source.243 Unsurprisingly, the organs that can detect these signals most sensitively, called subgenual organs, are located in the leg and are in direct contract with the substrate (subgenual means “below the knee”).198 Ground weta species from the genus of Hemiandrus do not have tympanal organs in the classic sense, and while they have tactile hairs that are receptive to near‐field vibrations, they are thought to be insensitive to far‐field airborne sound.248 They compensate for this deficiency with a sensitive intratibial structure known as a subgenual organ, which has different shapes and attachments depending on the desired physiological activation (e.g., frequency range).249 For instance, the subgenual organ in H. hemideina is pillow‐shaped and acts as a precisely sized inertial mass which resonates with vibrational stimuli.250 Alternatively, the organ of H. pillatarsis is wafer‐like, spanning the internal body fluid (hemolymph) channel in the tibia, with a thick attachment to one interior cuticle wall and a thinner attachment on the opposite side. This morphology allows it to function like a hinged plate: longitudinal waves traveling through the substrate, for example, act on the pliant region of the wafer, which swings back and forth stimulating the dendrites of sensory neurons.249 Other Hemiandrus species, as well as many other insects outside of that genus, have developed variants of these organs to perform the same function on different substrates at different frequencies and present intriguing targets for future morphological and biophysical investigation in the context of smart materials.249 5.2.2 Sound Production in Insects In acoustic communication, sound waves are generated specifically to be heard by the intended receivers.251 Hence, the sound needs to have sufficient acoustic power and has to be controlled to contain specific information. Sound production usually occurs by the active modification of specialized external organs. In a first approximation, the minimum source size for good source‐to‐medium matching has a radius of about 1/6 or 1/4 of the intended sound wavelength for a monopole or a dipole source, respectively.252-254 Due to their small size, invertebrates are therefore limited to producing sound either at high frequencies or at low acoustic power. As a consequence, noisy insects either are relatively big, use high frequencies or resort to other acoustic tricks.255 For instance, several species of mole crickets dig tunnels in the ground with megaphone‐shaped entrances.256, 257 When the males sing from just inside their burrow openings, the shape of the tunnel amplifies the sound. This strategy results in roughly a twenty‐fold increase in sound production, generating sounds that can be heard 600 m away.258 Evolution has brought forward two major mechanisms to produce sounds in large insects: stridulatory organs, in which two components are actively rubbed against each other, and sound‐radiating surface organs called tymbals. Small insects also produce sound by wing beating.259 Sound production in insects is often sexually dimorphic and restricted to the males. These sounds are often used in mating ritual or territorial behavior; however, some are used as a warning or defensive signal (so‐called acoustic aposematism). Excellent reviews have covered large areas of sound production251, 259, 260 and perception.261 Stridulation is the act of producing sound by rubbing together body parts that contain structured vibrational elements. Insects perform this task ad nauseam by rubbing one structure with a well‐defined lip (the so‐called “scraper” or plectrum) across a finely ridged surface (the “file”) or vice versa, generating vibrations in the process (Figure 12A–D). The sounds produced by stridulation are normally called “chirp” and “chirrup”. Insects are capable of generating a diverse range of songs that can be loud, musical, or highly patterned. This behavior is quite common in large insects and spiders, but is also found in some vertebrates such as fish and snakes. The position on the body and the anatomical features of the plectrum and the file can differ enormously in different invertebrates. What is largely conserved, however, is the mechanical durability of these organs, derived from the strength of their associated cuticular projections (Figure 2). Figure 12 Open in figure viewer PowerPoint 254 254 Gryllus bimaculatus cricket. Reproduced with permission. 668 669 669 Xosopsaltria thunberg, showing the position of the tymbal. Reproduced with permission. 670 Sound production in insects is due to two different mechanisms. A–D) Stridulation or E–H) tymbals. A–D) Crickets produce sound by stridulation, a scheme involving scraping a file along a ridged surface (plectrum). A) Habitat image of a cricket.B) Drawing of the underside of the wing showing the harp (the main resonator), the file, and the plectrum on the wing. C) Diagram explaining the main mechanism of excitation that results in sound production. B,C) Reproduced with permission.Copyright 1999, Company of Biologists. D) SEM image of the file of acricket. Reproduced with permission.Copyright 2009, Company of Biologists. E–H) Cicadas generate their characteristic sounds using tymbal organs, which produce sound via the dynamic buckling of a membrane. E) Habitat image of a cicada.F) Schematic drawing of a single tymbal organ showing the different components. G) Diagrams of the mode of excitation of sound resonances in the tymbal organs. As the membrane's ribs buckle inward, clicks are created. F,G) Reproduced with permission.Copyright 1995, Company of Biologists. H) Lateral view image of the pygmy bladder cicada,, showing the position of the tymbal. Reproduced with permission.Copyright 2016, Oxford University Press. The most common system, used by grasshoppers and many other insects, involves rubbing a scraper located on the leg (e.g., in beetles)257, 262, 263 or the trailing edge of the wings (e.g., mole crickets, Gryllus sp, and grasshoppers, Chortippus sp.)264, 265 against a hardened file on the underside of the adjacent wing. Both the scraper and the file are optimized for chirping and are coupled to thin, rigid parts of the wing (see Section 3.2) to promote acoustic coupling (Figure 12A–D). Each time the scraper passes over a tooth in the file, the thin, papery portions of the wings vibrate and amplify the sound. The nature of the sound that is produced depends on the resonance frequency of the wing determined by its cuticle rigidity, as well as the rate at which the teeth of the file are struck, which can vary from 7–65 Hz (bush crickets vs mole crickets).254 Tymbals, like wings, are corrugated exoskeletal membrane structures made of cuticle, but they are used to produce sounds rather than for locomotion. Insects generate clicking sounds by contracting and displacing these membranes, analogous to production of sound by an electronic loudspeaker. This mechanism is most prominently found in tiger moths (Arctiinae) and cicadas (Cicadoidea), producing deafening songs with peak intensities of over 100 dB.266 Cicadas have paired tymbals that are located on the sides of their abdominal base (Figure 12E–H). The tymbals are regions of the exoskeleton that are modified to form a complex membrane with thin, membranous portions and thickened ribs (Figure 1F,G). A contraction of the tymbal muscle causes the membrane to buckle inward, producing a loud click. As the membrane snaps back, it clicks again. Serial muscle contractions cause these membranes to vibrate rapidly; this vibration is transferred to enlarged air‐filled chambers derived from the tracheae, where it resonates and is amplified.254, 266-268 Tiger‐moth tymbals are modified regions of the thorax that produce high‐frequency, tuneable clicks in the 40–80 kHz range.269 Sounds from these clicks, unlike cicada songs, serve a dual purpose and are used both as mating signals and in acoustic aposematism against bats. The moths are advertising to bats that they are toxic and the sounds “jam” the sonar of moth‐eating bats to deter them.270, 271 Although placing a sound‐producing insect directly in your ear may not be a pleasant thought, insect‐sized and structured tymbals could be paired with insect‐inspired sound reception mechanisms to generate energy‐efficient and frequency‐targeted hearing assistance for humans.

6 Sensing and Manipulation of Light Most animals have used light as a primary information carrier for communication272 since the emergence of vision after the Cambrian explosion about 500 million years ago.273, 274 In particular, intricate optical structures deliver specialized signals that are processed into information by complex visual systems, the eyes.275, 276 The cuticle exoskeleton of certain insects contains ordered, quasi‐ordered or disordered nanostructures that reflect light in particular wavelength ranges and can produce vibrant colors, while cuticle on the exterior of other insects forms nanostructured layers that prevent light reflection entirely, rendering them transparent. Mechanisms to manipulate light have developed alongside those to detect it; the surface of some insect eyes is patterned with nanoscale features that promote efficient light transmission and also act as a hydrophobic deterrent for vision‐blocking condensation (Section 4). This light‐control toolkit is essential for insect survival, and has provided inspiration for engineered systems that harness fundamental physical phenomena to produce and detect visual signals. 6.1 Mechanisms of Color Production Insects have evolved a diversity of mechanisms that interact with incident light and allow them to create a dynamic form of information. The remarkable displays of insects have long fascinated biologists, physicists, and natural philosophers alike, including Newton, Darwin, and Rayleigh.277 Numerous recent reviews discuss the physical aspects of insect displays,273, 277-286 as well as their function in animal communication.275, 276, 287 In general, there are two main classes of animal coloration: pigmentary coloration due to the wavelength‐selective light absorption by chemical dyes and structural coloration due to the interaction of incident light with ordered, quasi‐ordered or disordered nanostructures causing interference.277, 288, 289 Both coloration mechanisms feature unique optical properties that can combine in nontrivial ways and modulate optical properties with potential applications ranging from displays, to brilliant durable paints, to adaptive camouflage and transparent materials.287, 290-293 Interferometric modulator displays are a low‐power microelectromechanical display technology based on structural coloration, enabling full visibility in direct sunlight, unlike conventional liquid‐crystal display screens.294, 295 The concept is relatively simple: each pixel in the display contains a fixed, semitransparent membrane separated a distance (air‐gap) of ≈1 µm above a reflective, moveable thin‐film stack. Both the membrane and stack reflect light, and their separation determines the relative phase of the aggregate light output. When the films are oriented at a distance such that all reflected light in the visible spectrum destructively interferes, the pixel is black, but when the stack is actuated to a distance that produces constructive interference of visible light, it takes on a color determined by its particular distance‐dependent phase shift.296 This “color” state is a direct analog to structural color in many insects, and represents just one of the many examples of potential light‐active microstructured devices that can incorporate insect‐inspired design. 6.1.1 Pigmentary Coloration Pigmentary coloration is the most abundant coloration principle found in animals. It is based on the deposition of different chemical pigments in the outer body layer that selectively absorb incident light. Pigments are responsible for most of the yellow, orange, red, and brown‐black colors observed in insects. It is curious to note that most insects are not capable of synthesizing green‐ or blue‐colored pigments (except for a few species, e.g., Graphium spp.297) and instead rely on nanostructural features to reflect these colors. The pigments are usually dispersed throughout randomly ordered structures so that any incident light that is not absorbed is scattered diffusely. Pigmentary colors hence appear identical in color from all viewing angles and are often described as dull and lusterless. Pierid butterflies are an exception to the dull appearance as they have evolved a way to create an intense pigment‐based color. In the wing scales of these butterflies, the pigments are condensed in randomly ordered rice‐grain‐shaped granules.298, 299 This arrangement greatly increases the effective refractive index of the granules, resulting in a much increased scattering strength and a higher reflectivity than if the pigment was randomly distributed throughout the wing scale.300 6.1.2 Structural Coloration Insects' most stunning visual displays arise from the interaction of light with nanostructures, resulting in structural coloration. To cause constructive interference of visible light, photonic structures must consist of at least two materials with different refractive indices (RI) and with periodicities on the mesoscale (i.e., ≈200 nm).277, 301 Such photonic structures are often assemblies of dielectric materials with negligible light absorption such as insect cuticle (RI ≈ 1.55)302 and air (RI = 1), but also feature assemblies of pigmented material, e.g., melanin‐containing layers, to achieve the desired refractive index contrast.286, 303, 304 Among insects, the striking palette of colorations is due to the plethora of nanomorphologies.305-307 Simply speaking, the photonic structures in insects can be treated as periodic optical materials (so‐called photonic crystals), and described using photophysical terminology.289, 301, 308 Morphologies can be categorized by their translational periodicity as 1D, 2D, and 3D photonic crystals, where the structure is locally periodic in one, two, and three dimensions, respectively. Each different morphology changes the way light interacts with the structure, as do local defects and disorder. Insect nanomorphologies range from ordered structures starting from thin films309-311 and multilayer structures277, 282, 304, 312, 313 to 3D photonic crystals to quasi‐ordered and fully disordered structures,314-320 each with different optical properties. 1D photonic structures, such as thin films or multilayer structures, are probably the most encountered nanostructure in nature.289, 291 These are responsible for the iride