Bio-Optics and Bio-Inspired Optical Materials - ACS Publications

Review Cite This: Chem. Rev. 2017, 117, 12705-12763

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Bio-Optics and Bio-Inspired Optical Materials Sirimuvva Tadepalli,† Joseph M. Slocik,‡ Maneesh K. Gupta,‡ Rajesh R. Naik,*,§ and Srikanth Singamaneni*,† †

Department of Mechanical Engineering and Materials Science and Institute of Materials Science and Engineering, Washington University in St. Louis, St. Louis, Missouri 63130, United States ‡ Materials and Manufacturing Directorate, and §711th Human Performance Wing, Air Force Research Laboratory, Wright-Patterson Air Force Base, Dayton, Ohio 45433, United States ABSTRACT: Through the use of the limited materials palette, optimally designed microand nanostructures, and tightly regulated processes, nature demonstrates exquisite control of light−matter interactions at various length scales. In fact, control of light−matter interactions is an important element in the evolutionary arms race and has led to highly engineered optical materials and systems. In this review, we present a detailed summary of various optical effects found in nature with a particular emphasis on the materials and optical design aspects responsible for their optical functionality. Using several representative examples, we discuss various optical phenomena, including absorption and transparency, diffraction, interference, reflection and antireflection, scattering, light harvesting, wave guiding and lensing, camouflage, and bioluminescence, that are responsible for the unique optical properties of materials and structures found in nature and biology. Great strides in understanding the design principles adapted by nature have led to a tremendous progress in realizing biomimetic and bioinspired optical materials and photonic devices. We discuss the various micro- and nanofabrication techniques that have been employed for realizing advanced biomimetic optical structures.

CONTENTS 1. Introduction 2. Optical Materials and Optical Engineering in Biology and Nature 2.1. Absorption and Bulk Transparency 2.1.1. Absorption 2.1.2. Biological Transparency 2.2. Photonic Structures 2.2.1. Photonic Structures in Nature 2.2.2. Phenomena Responsible for the Formation of Photonic Crystals 2.3. Reflective and Antireflective Structures 2.3.1. Reflective Structures 2.3.2. Antireflective Structures 2.4. Scattering 2.5. Polarized Light in Nature and Helicoidal Structures 2.5.1. Polarized Light 2.5.2. Helicoidal Structures 2.6. Tunable Color and Dynamic Camouflage 2.7. Waveguiding and Lensing 2.8. Light Harvesting and Light Generation 2.8.1. Light Harvesting 2.8.2. Bioluminescence 3. Bioinspired Optical Materials and Devices 3.1. Molecular Biomimetics 3.1.1. Pigment-Based Materials 3.1.2. Protein-Based Materials 3.1.3. Optically Active Nonprotein Biological Materials

© 2017 American Chemical Society

3.2. Bioinspired Periodic/Aperiodic Structures 3.2.1. Photonic Crystals 3.2.2. Helicoidal Structures 3.2.3. Opal/Inverse Opal Structures 3.2.4. Antireflecting Surfaces 3.3. Responsive Materials 4. Conclusions and Outlook Author Information Corresponding Authors ORCID Notes Biographies Acknowledgments References

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1. INTRODUCTION Over millions of years, through natural selection, nature has optimized materials, structures, models, systems, and processes for a broad range of functions and serves as a valuable “solution manual” for addressing some of the most critical global challenges. Nature demonstrates highly complex and sophisticated engineering models at various length scales that have inspired mankind throughout history. Biomimicry or bioinspiration involves learning nature’s design principles and developing sustainable solutions for challenges faced by

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Special Issue: Bioinspired and Biomimetic Materials Received: March 17, 2017 Published: September 22, 2017

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DOI: 10.1021/acs.chemrev.7b00153 Chem. Rev. 2017, 117, 12705−12763

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Figure 1. Schematic showing the process of biomimicry in optical materials: material−structure−function relationship and bioinspired optical materials. Reprinted with permission from ref 3 (copyright 2001 University of Chicago Press), ref 4 (copyright 2014 National Academy of Sciences), ref 5 (copyright 2004 Optical Society), ref 6 (copyright 2014 National Academy of Sciences), ref 7(copyright 2004 The Royal Society), ref 8 (copyright 2012 National Academy of Sciences), ref 9 (copyright 2015 American Chemical Society), ref 10 (copyright 2015 Nature Publishing Group), ref 11 (copyright 2009 The Royal Society), ref 12 (copyright 2005 John Wiley and Sons), ref 13 (copyright 2006 American Chemical Society), ref 14 (copyright 2009 SPIE), ref 15 (copyright 2005 Japanese Society of Applied Physics), ref 16 (copyright 2002 American Chemical Society), and ref 17 (copyright 2007 Nature Publishing Group).

humanity. Considering that natural materials and systems have evolved to perform various functions, including structural support, signal transduction, actuation, sensing, catalysis, trafficking, gating, light harvesting, charge transfer, molecular recognition, self-assembly, self-organization, and self-replication, or combinations of two or more of these functions, the structures and properties of these materials and systems are extremely diverse. Learning from nature and applying nature’s

engineering principles is a promising approach not only to sustainable solutions for various critical global challenges such as food, water, homeland security, public health, and clean energy but also to achieve revolutionary advances in the design and fabrication of novel functional materials and systems (e.g., responsive, autonomous, self-healing, and self-replicating).1 Amazingly, biomaterials are able to achieve complex (multi)functionality utilizing a limited materials/chemistry palette. 12706


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the optimized designs of optical materials and systems in nature and underscore the importance of consulting this comprehensive library for expediting the design of synthetic materials with desired optical properties (Figure 1). In this review, we attempt to provide a detailed account of the various optical effects found in nature and biology with a particular emphasis on the materials and optical design aspects responsible for their optical functionality. The review is divided into four sections. The current section provides an introduction to the importance of bioinspired design and sets the stage for a comprehensive overview of bioinspired optical engineering in the subsequent sections. The first step toward biomimicry and bioinspired design is a comprehensive understanding of “nature’s way” of solving the problem followed by the rational selection of adaptable design principles. Following this brief introduction, a broad range of optical phenomena, including absorption and transparency, photonic structures based on diffraction and interference, reflection and antireflection, scattering, light harvesting, wave guiding and lensing, camouflage, and bioluminescence, are described in section 2. The objective of the second section is to serve as an abridged version of nature’s optical engineering manual, describing some of the key findings of nature’s design principles. In section 3, we provide a number of examples of synthetic optical materials and structures that either are outright replicas of natural optical structures or are based on design principles adapted by nature to achieve desired optical properties. Both of these approaches can lead to synthetic optical materials that can outcompete natural materials and structures by taking advantage of the rich palette of synthetic materials available and the broader processing windows accessible (e.g., temperature, pH, and organic solvents) in synthetic manufacturing processes. Section 3 also aims to provide an overview of the wide variety of microand nanofabrication techniques that can be employed for the fabrication of biomimetic optical structures. We finish the review with a few concluding remarks in section 4. Although the review is aimed to be a comprehensive account of optics in nature and bioinspired optics, considering the breadth of the topic and the large body of literature in the field, it is impossible to exhaustively cover all aspects of this topic. We hope that the review will serve as a comprehensive summary for researchers in this field and stimulate interest for those new to this topic. The readers are also referred to other reviews for extensive discussion of certain topics related to bioinspired and biomimetic optical materials.18−20

This rather humble materials approach to solve some of the most stringent functional requirements makes biomimicry all the more attractive for sustainable and scalable solutions. In the course of natural selection, optical materials and systems designed and optimized by nature for efficient light harvesting, manipulation, management, and production are truly exceptional. In fact, efficient light harvesting and management mechanisms are of fundamental importance to biological systems for their survival by enabling coloration/ camouflage, photoprotection, photosynthesis, light-driven radiative heating of biological tissues and bodies of water, regulation of circadian rhythms, and vision/light detection. One can find remarkable examples of optical materials and structures in nature and biology that render unique and well-defined optical properties through efficient manipulation of light through absorption, reflection, scattering, diffraction, interference, transmission (bulk transparency), wave guiding, and lensing, and combinations of two or more of these effects (Figure 1). In fact, it is often difficult to tease out the various optical phenomena responsible for the unique optical effects observed in natural materials. The beauty of optical engineering in nature is epitomized in the effective use of a limited set of materials, which often carry out other functions (e.g., structural support and wettability), for various optical processes. Except for a few materials such as guanine crystals with a large refractive index (1.86), most of the materials in optical structures found in natural systems are rather ordinary (Table 1). Thus, it is the extraordinarily precise Table 1. Common Biomaterials Found in Biophotonic Structures biomaterial chitin

biological occurrence

keratin

insect cuticles, wings, and corneal structures avian feathers

cellulose guanine reflectin aragonite

plants fish scales cephalopods mollusk shells

collagen

avian and mammalian skin

material type polysaccharide

protein polysaccharide organic crystal protein inorganic mineral protein

optical properties waveguiding, transparency, photonics, structural coloration photonics, structural coloration structural coloration broad-band reflection dynamic reflection thin-film interference structural coloration

2. OPTICAL MATERIALS AND OPTICAL ENGINEERING IN BIOLOGY AND NATURE

optical engineering of these ordinary materials that is responsible for their unique and often exceptional optical properties (Figure 1). For example, the bright blue color of the Morpho butterfly wings over wide viewing angles is due to the constructive interference of light reflecting from densely packed nanoscale ridges on the wings of the butterfly. The optimization of these naturally engineered structures is evidenced by the utilization of diamond- and tetragon-shaped structures, which are recognized to be ideal geometries for the highest band gap width-to-frequency ratio at lowest refractive index contrast. Yet another example is the more than 90% efficiency of light harvesting during photosynthesis (light conversion to electrochemical potential) with a quantum yield that approaches unity.2 Essentially, if the efficiency were any lower, there would not be enough energy for downstream photochemical redox reactions that are responsible for the production of chemical energy (carbohydrates and sugars). These examples highlight

2.1. Absorption and Bulk Transparency

2.1.1. Absorption. The absorption of light dominates all aspects of nature and accompanies a multitude of biologically important light-dependent functions and photochemical reactions. These include coloration/camouflage, photoprotection, light harvesting, photosynthesis, light-driven radiative heating of biological tissues and bodies of water, regulation of circadian rhythms, and enabling vision/light detection.21 Generally, everything in nature absorbs some spectral form of light at a specific wavelength (ultraviolet (UV) to infrared (IR)), and without this ability to selectively absorb light, there would be no color, vision, heat, and/or light-derived energy and biomass production. Of all the possible light absorption events occurring in nature, photosynthetic organisms/plants have 12707


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perfected the process of light harvesting/absorption for photochemical production by achieving the highest quantum yields known to exist in nature (see also section 2.8.1). In essence, light-based interactions promote electronic, rotational, and vibrational transitions upon absorption of photons. Absorption is characterized by the interaction of different wavelengths of light with biological matter and is represented at the atomic, molecular, cellular, and macroscopic levels. At the molecular level, biomolecules such as protein and DNA strongly absorb UV radiation, photoactive pigments, biological chromophores, and metal−protein complexes (i.e., enzymes) selectively absorb different forms of visible light, and water molecules preferentially absorb IR light. While most of these light−biomaterial interactions are beneficial, the absorption of UV radiation exerts damaging effects on proteins and DNA in the form of bond breakage/rupture and UV-initiated photocross-linking of DNA and proteins.22,23 For biomolecules, peptide bonds within proteins absorb light at 180−230 nm, aromatic-containing amino acid residues absorb at 260−280 nm, and DNA absorbs from 240 to 275 nm due to π → π* transitions of the nucelobases.24 To minimize the detrimental effects of UV on these biomolecules, sacrificial UV-absorbing molecular pigments are utilized (i.e., melanin and carotenoids). At longer wavelengths, IR radiation is selectively absorbed by water molecules and is rapidly converted into thermal energy. Importantly, radiative heating of water from IR absorption is responsible for generating heat within water-containing biological tissues and for producing heat from large bodies of water. At the cellular level, biological cells contain mostly proteins and nucleic acids, where each component additively contributes to broad spectrum absorption, while, at the macroscale and beyond, structures are best exemplified by the multicompositional nature of biological tissues. For instance, a generic biological tissue contains many different types of lightabsorbing pigments/chromophores that include the heme groups of hemoglobin in blood, melanin pigments, water molecules, adipose, and various yellow pigments.25 2.1.1.1. Light-Absorbing Pigments. Pigments Composed of Organic Molecules. Carotenoids are an important class of molecular pigments with high absorption coefficients. For this reason, they mainly function as light-harvesting molecules and for UV protection in photosynthetic plants and microorganisms (discussed in more detail in section 2.8.1), but are also admired for their contributions to biological coloration. Consequently, carotenoids produce orange coloration by strongly absorbing 500−600 nm light. On the macroscale, orange coloration originating from carotenoid absorption is evident in autumn leaves changing color and varieties of animal coloration. Notably, pink flamingos must acquire dietary supplements of carotenoid-rich shrimp to retain their characteristic color. Similarly, melanin is another universal light-absorbing pigment with many different functions in nature. These pigment-based functions include UV protection, coloration/ camouflage, increased mechanical properties, increased virulence in yeastlike fungus, and metal binding/sequestration.26,27 In nature, melanin is a major component of mammalian and cephalopod skin, cephalopod ink, microorganisms, retinas, and bird feathers. Melanin is biochemically synthesized and deposited in specialized organelles of pigment-generating melanosomes.28 Optically, melanin exhibits broad-band absorption that covers wavelengths from UV to visible light (Figure 2). In its native chemical form, melanin is a high molecular weight, complex polymer derived from sources of tyrosine,

Figure 2. (a) Absorbance spectrum of melanin granules from Sepia officinalis (Sigma, M2649). (b) SEM micrograph of melanin granules. The scale bar is equal to 10 μm.

dihydroxyphenylalanine (Dopa), 5,6-dihydroxyindole, and 5,6dihydroxyindole-2-carboxylic acid monomers. As a result, depending on the biochemical pathway, degree of oxidized components, combination of monomers, and extent of crosslinking, melanin pigments can exist in the different forms of eumelanin (black-pigmented melanin) or pheomelanin (orange-red melanin).29 Because of its complexity and variability and a lack of detailed structural information on biologically derived melanin, the biomimetic synthesis of a biological equivalent to natural melanin in vitro is challenging and to date has been unachievable. Melanin plays a major role in the determination of color by strongly absorbing visible light. The amount and type of melanin pigment ultimately determines color by absorbing more or less visible light, while also protecting cells against UV damage. For example, skin and hair color are largely attributed to differing amounts of melanin, while the defensive and chemical properties of cephalopod ink are maximally enhanced at high melanin concentrations. In the latter example, cephalopods eject melanin-rich ink in response to the presence of a predator or imminent attack. Compositionally, squid ink contains ∼1 g of eumelanin, which makes up ∼15 wt % of the total ink composition and is ∼100−200 μm in diameter.30 This 12708


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high mass fraction of melanin acts by absorbing light and providing an effective and dense “smoke screen” during inking behavior. After inking, the formation of dark and diffuse clouds of black melanin-rich ink renders cephalopods invisible to predators and enables their quick escape upon an attack and/or, to a lesser extent, provides a visual alarm cue for nearby cephlapods.31 Pigments Containing Metals. In nature, a variety of metalcontaining pigments create distinct coloration by preferentially absorbing certain wavelengths of light. Metal ions are an integral part of biology and in controlling the functionality and absorbance of many different pigments (i.e., chlorophyll and heme groups). In total, they are used to regulate redox processes, oxygen binding, protein stabilization, enzymatic activity, and respiration.32 Transition metals are optically active by absorbing visible light equal to its d-orbital energy levels. This visible light absorption leads to d → d electronic transitions, excited states, and production of highly colored metals. The light energy needed to promote these transitions is dependent on the oxidation state and ligand coordination. Most notably, magnesium and/or iron coordinated using substituted porphyrin ligands exhibit strong optical transitions with visible light and are critical to the functionality of many biological systems. They represent the basic heme subunit group that imparts oxygenation activity to hemoglobin and myoglobin, forms the active sites in peroxidase and catalase enzymes, and is the principal structural reactive element of hemozoin crystals produced by the malaria parasite discussed below.33,34 Heme groups are optically active by containing an intense Soret absorption band at ∼414 nm due to an S0 to S2 transition and are sensitive to ligand binding.35 For example, the heme group of hemoglobin changes color in response to oxygen binding and changes in electron distribution. For this reason, absorbance is used to interrogate the level of oxygenated vs deoxygenated hemoglobin. Unlike carotenoids, melanin pigments exhibit a high binding affinity for metals and strongly participate in metal coordination due to their highly cross-linked structure and abundance of metal-chelating groups.29 In total, melanin contains an assortment of hydroxyl, carboxyl, amine, quinone, and semiquinone groups for metal chelation.36 This coordination behavior enables the accumulation and binding of different metals, giving it a broad binding affinity and accounting for its biological significance in the storage of metals. As a result, natural melanins are always associated with metals (Fe3+, Cu2+, Ca 2+ , Zn 2+ , Mg 2+ , K + , and Na + ) and occur at high concentrations. For example, melanin contains large reservoirs of Ca2+ and Zn2+ with concentrations as high as 1.6 mmol/g of melanin.29 Microbial Pigments. Microorganisms are a natural and rich source of diverse pigments that strongly absorb light and offer different levels of coloration (Figure 3).37 By comparison to plant and animal pigments, microbial-generated pigments exhibit higher water solubility and are more stable to light, heat, and pH.38 Pigment coloration varies significantly across microorganisms and, in many cases, is a nonessential product of a biochemical pathway and a passive material property used to filter, protect, and/or manipulate light that is tangential to its genetically programmed function. The natural functions of microbial pigments include protection against UV light, oxidants, extreme temperatures, and antimicrobial compounds and acquisition of nutrients and energy. Spectrally, the coloration of naturally produced microbial pigments ranges

Figure 3. Petri plate showing diverse colonies of microorganisms producing a variety of colored pigments. Reprinted with permission from ref 44. Copyright 2016 Springer.

from the yellow pigments of riboflavin (vitamin B2) to a newly discovered deep blue water-soluble pigment from Pantoea agglomerans.39 In terms of production yields, microorganisms are capable of producing large amounts of pigments. For example, the fungus Paecilomyces sinclairii biosynthesizes red pigments in amounts up to 4.73 g/L.40 Biochemical production of these pigments in high yields is achieved by the bioconversion of many different feedstock sources, i.e., agricultural waste, domestic compost, and environmental and industrial pollutants.37 Recently, the biochemistry and genetic basis of pigment production by microorganisms has provided new insights and clues to unfold the biological consequence/significance of pigment color beyond random coincidence. The use of coloration/pigmentation by microorganisms is believed to serve as an active warning signal, an indicator of virulence factor, and/or a signal of the pathogenic potential of microorganisms. 26 This concept and basis of pigment coloration in the microbial world is analogous to the use of color by animals to warn of danger, i.e., the brightly colored poisonous dart frogs of the Amazon. For example, hemecontaining crystalline malaria pigments of hemozoin function in the detoxification of free heme but, as a fortuitous consequence, also display strong optical absorption at 450 and 655 nm. The absorptive nature of hemozoin generates black-brown-pigmented coloration visible in patients infected with malaria.41 In other examples, the golden-colored Staphylococcus aureus contains carotenoid pigments (absorption maximum 400−500 nm) that contribute to its virulence and resistance to antibacterial agents,42 while black melanin pigments coat the surface of the fungal pathogen Cryptococcus neoformans and impede phagocytosis.43 In this case, melanin serves in an active role to increase virulence. At the same time, certain microbialproduced pigments also possess unique functionality beyond simple light absorption by offering antioxidant, antimicrobial, anticancer, and antiviral properties and functions to organisms.44 Antibacterial activity was best exemplified by the redcolored pigment of prodigiosin produced by Serratia marcescens. 12709


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Prodigiosin was shown to effectively work against both Gramnegative and Gram-positive bacteria.45 2.1.2. Biological Transparency. Optical transparency is the opposite and inverse process of light absorption, whereby light is fully transmitted through a biological object or surface with little to no optical loss due to absorption or scattering. The significance of biological transparency is for the purpose of providing camouflage and invisibility against visual predation and/or reducing energy consumption required to biochemically synthesize colored pigments.3 Eloquent examples of biological transparency are demonstrated by jellyfish, shrimp, and phytoplankton and attractively displayed in the complex structures of insect wings (Figure 4). Unlike traditional animal

Marine animals exhibit highly transparent body structures and can occur in the context of gelatinous forms of jellyfish and/or by the cuticle exoskeleton structures of crustaceans. Biochemically, the gelatinous form of jellyfish is composed of ∼90% water, 5.3% protein rich in glycine, glutamic acid, aspartic acid, lysine, and arginine amino acids, ∼ 2% fatty acids, 3.4% carbohydrates, and trace amounts of inorganic salts.46,47 For marine animals, the level of optical transparency is significantly affected by changes in environmental conditions. Consequently, in response to different environmental factors and pressures, transparent animals can lose their ability to maintain natural transparency. This of course has severe consequences to their survival because of increased visibility to predators. The grass shrimp, Palaemonetes pugio, provides such an example of a highly transparent coastal species that is hypersensitive to changes in water salinity and temperature.48 Not surprisingly then, the transparency of grass shrimp is constantly threatened by changes and fluctuations in salinity levels and water temperatures in a typical coastal habitat due to changing tides and/or differing amounts of rain. These environmental pressures are ultimately reflected by the amount of transparency displayed by the grass shrimp under different conditions. For example, changes by as little as 5 ppt salt or by a few degrees in temperature can decrease the total observed transparency from ∼40% to 0%. Alternatively, in an effort to avoid transparency losses endured by exposure to increases in salinity and temperature, P. pugio has adapted different behavioral responses to counter the effects of these pressures on transparency, such as migrating to deeper water. Insect wings are another extraordinary example of transparency in nature, for example, the wings of dragonflies, desert locusts, cicadas, household flies, butterflies and moths, and bees and wasps. For flying, insect wings are mechanically tough and lightweight structures formed by the integration of narrow structural veins with 1−2 μm ultrathin membranes of chitin.49 Optically, they are highly transparent due to the thinness of the chitin membrane (100× smaller than human hair) and maximized for flight. In the case of dragonfly wings, these membranes are coated both ventrally and dorsally with a nanostructured wax coating that is associated with a wavelength-dependent and complex refractive index of 1.38−1.40.50 These nanostructured wax protrusions give rise to antiwetting behavior, self-cleaning properties, low reflectance, and an overall reduction in aerodynamic surface drag during flight.

Figure 4. Transparency of marine animals: (A) Amphitretus pelagicus (octopus); (B) Leptodora kindtii (freshwater cladoceran); (C) Phylliroe bucephala (nudibranch); (D) Pterosagitta draco (chaetognath). Reprinted with permission from ref 3. Copyright 2001 University of Chicago Press.

2.2. Photonic Structures

During the course of evolution, vision and light−matter interactions have played a crucial role in the development of structural color in various organisms. The unique light manipulation strategies employed by various organisms have led to the codevelopment of predator and prey coloration and visual communications that determine mating preferences. Unlike pigmental color (described in section 2.1.1.1), structural color is formed by highly sophisticated multiscale hierarchical architectures. The astonishing structural color observed in natural and biological materials is the consequence of interference, diffraction, or the selective reflection of light from photonic structures. Photonic crystals (PCs) are periodic (on the order of the wavelength of light) dielectric structures that exhibit a photonic band gap, forbidding the propagation of light of certain frequencies. The band gap of the photonic crystals depends on the orientation of light propagation in the crystal, often quantified by the lattice reciprocal space and

camouflage involving only interactions between light and surfaces, transparency must be consistent throughout the entire volume of an animal’s body to be effective as a protective mechanism in an actual ecological habitat with the exception of the eyes and gut.3 The eyes and the gut are special exceptions to animal transparency and by necessity must be highly light absorbing to function as is the case with eyes. Transparency by nature is difficult to achieve and highly dependent on the tissue/biochemical composition, refractive indices of components within the tissue and surroundings, ultrastructural and anatomical modifications to eliminate scattering, and homogeneous density distribution within the tissue and most importantly requires a complete system of nonabsorbing components.3 12710


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Figure 5. (A) Sea mouse (Aphroditidae). Images of a sea mouse spine illuminated with light from an incandescent lamp (B) perpendicularly and (C) obliquely. (D) Transmission electron micrograph of the sea mouse spine. The dark areas are chitin, while the white areas are voids with a spacing of 0.5 μm. Reprinted with permission from ref 61. Copyright 2001 CSIRO Publishing.

Figure 6. (A) Black-billed magpie, Pica pica, commonly found in Europe and North America. (B) Scanning electron and optical (inset) microscopy images of an isolated barb (scale bar 200 μm). (C) Cross-section of a barbule of a yellow-green tail feather showing the cortex surrounding the central core (scale bar 1 μm). (D) Cross-section of a barbule in a blue feather showing the holes in the hexagonal lattice larger than those of the yellow-green feather (scale bar 1 μm). Reprinted with permission from ref 62. Copyright 2006 American Physical Society.

corresponding to the iridescence reflection peaks.51 Depending on the orientation of the periodic arrangement of the dielectric materials with respect to the direction of light propagation, photonic crystals can be classified into one-dimensional (1D), two-dimensional (2D), or three-dimensional (3D) photonic crystals. Natural 2D photonic crystals provide coloration to various marine animals and birds,52−54 while archetypical 3D photonic crystals are more commonly found in insects.51,55−58 2.2.1. Photonic Structures in Nature. The earliest example of photonic crystal structure was found in the sea mouse, Aphroditidae, whose spine exhibits a spectacular iridescence (Figure 5).59 The spine has a brilliant red color under normally incident light, but shifts to green and blue stripes running parallel to the axis of the spine under obliquely incident light. The electron micrograph of the sea mouse spine displays an internal structure with holes arranged in a regular, hexagonal close-packed structure with a submicrometer period, which resembles nanoscale structures that are found in photonic-crystal fibers.60 The striking color is due to the presence of longitudinally arranged chitin fibrils that cause structural coloration and is a remarkable example of photonic engineering in living organisms.61 A similar structure is found in the black-billed magpie, Pica pica (Corvidae), which demonstrates weak iridescence due to ribbon-shaped barbules (Figure 6). The peripheral layer of the barbules contains cylindrical holes arranged in a hexagonal lattice within the cross-section.62 Another example of bright structural color is found in male peacock feathers that demonstrate a brilliant iridescence, diversified coloration, and intricate patterns due to the presence of nanoscale periodic

structures of melanin rods. The coloration arises from the peacock’s ability to control the lattice spacing of melanin and the number of melanin layers in the photonic crystal structure. Varying the lattice constant of the photonic crystal structure shifts the midgap frequency of the partial photonic band gap, while the number of periods controls the production of additional colors, which eventually leads to the formation of striking and diversified colors by additive and mixed coloration.52 2.2.2. Phenomena Responsible for the Formation of Photonic Crystals. 2.2.2.1. Interference. The reflection of light from the upper and lower boundaries (interfaces) of a thin film results in constructive or destructive interference of light at certain wavelengths. The formation of structural colors in most biological systems arises from the alternating spatial arrangement of low and high refractive index dielectric materials. For example, in Morpho butterflies, photonic structures form discrete multilayers of cuticle and voids, resulting in an ultralong-range visibility of their structural color.63 The structural color occurs due to the presence of lamellar structures in the ridges that offer a strong reflection in a given wavelength range. Additionally, the irregularity in the ridge height eliminates the interference among the ridges, resulting in a diffuse and broad reflection of a uniform color.64 The origin of bright green coloration in the wing scales of Papilio palinurus is due to the dual color mixing modulation imposed on the multilayers by the juxtaposition of the flat and inclined regions between the concavities.65 This type of spatial color averaging has been observed in beetles as well.66 12711


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Figure 7. (A) Configuration of thin-film interference of thickness d and refractive index ηB. (B, C) Reflectivity from a thin chitin film (n = 1.5) of thickness 100 nm at (B) n = 1.0 and (C) n = 2.0. (D) Configuration of the interference of a multilayer consisting of layers A and B with thicknesses dA and dB and refractive indices ηA and ηB. (E, F) Reflectivity of multilayers of (E) chitin (n = 1.5) and air (n = 1.0) and (F) chitin (n = 1.5) and water (n = 1.33) of 0.25 μm thickness each.

Figure 8. (A) Photo image of a typical Morpho butterfly (Morpho didius). (B) SEM image of the scales of M. didius at low magnification (scale bar 100 μm). (C) Schematic image of a scale. (D) Cross-sectional SEM image along the red line shown in (C), which shows the nanostructure in the Morpho butterfly’s scale (scale bar 1 μm). Reprinted with permission from ref 72. Copyright 2006 SPIE.

transmittance of a multilayer with arbitrary refractive indices and thicknesses and without a periodicity can be calculated by the transfer matrix method (Figure 7D−F).68,69 Multilayered interference is responsible for the brilliant iridescent colors produced in natural structures. This phenomenon is caused by thin layers of high and low refractive indices piled together in a periodic fashion with a physical thickness on the order of the wavelength of light. More commonly, multilayer interference is responsible for the striking colors found in neon tetra fish, Morpho butterfly, male Sapphirinid copepods, Plateumaris sericea beetles, greencolored Calloodes grayanus, jewel beetles, and birds-of-paradise Lawes’s parotis, Parotia lawesii.4,9,54,64,68,70,71 Neon tetra fish exhibits remarkable color due to the periodically arranged stacks of guanine crystals within iridiphore cells.54 A similar arrangement of multilayered platelets is found in the epidermal cells of the dorsal integuments in S. copepods.9 The brilliant blue of Morpho butterfly is attributed to the lamellar structure on the ridges that is responsible for multilayer reflection (Figure 8). The iridescent blue with high reflectivity is a result of coherent scattering in the periodic arrays of scales.64 However, in the case of Morpho butterfly, the multilayers exhibit a distribution of tilts with respect to the scales, resulting in a low angle dependence of the reflected blue

The simplest case of structural color arises from thin-film interference. When a plane wave is incident on a thin film of thickness d and refractive index ηb at an angle of refraction θr, then the reflected beams from the two interfaces interfere. The condition for constructive interference of incident wavelength λ is given by67 2ηbd cos θr = mλ

where m is an integer or half an integer depending on whether the thin film is attached to a material of high refractive index. This suggests that, as the incident angle increases, the wavelength corresponding to the maximum reflection changes to a shorter wavelength, which is a characteristic of structural color and color change associated with the viewing angle. Multilayer interference is a phenomenon that occurs due to the periodic arrangement of thin layers. Consider two layers, A and B, with thicknesses dA and dB and refractive indices ηA and ηB. When ηA > ηB, the condition for constructive interference is given by67 2(ηbdA cos θr + ηbdB cos θr) = mλ

with the angle of refraction in layers A and B given by θA and θB (Figure 7). Although this is a simplified version of understanding multilayered reflection, the reflectivity and the 12712


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Figure 9. (A) Plumage of a male Lawes’s parotia consisting of mostly jet black feathers (scale bar 5 cm). (B) Photograph of the nape of the bird, showing the silver-colored, mirror-like occipital feathers (scale bar 1 cm). (C) Slightly oblique view of the breast feathers showing the drastic variation in color along the differently aligned feathers (scale bar 1 cm). (D) TEM image of an occipital feather (scale bar 2 μm). (E) TEM image of a barbule feather (scale bar 5 μm). Reprinted with permission from ref 4. Copyright 2014 National Academy of Sciences.

Figure 10. (A) Polished shell of a mollusk, Haliotis glabra, with striking iridescent colors. (B) Cross-section of the abalone shell showing layered aragonite platelets (scale bar 10 μm). (C) Typical diffraction patterns produced by the shell showing a set of fine fringes at the zeroth-order position. (D) Hibiscus trionum flower. (E) Base of the H. trionum petal, showing iridescence overlaying red pigment (scale bar 50 μm). (F) SEM image showing striations on the petal surface of Tulipa kolpakowskiana, resembling a line grating with a periodicity of 1.2 ± 0.3 μm (scale bar 1 μm). The inset shows the optical appearance of the two gratings in transmission. Reprinted with permission from ref 5 (copyright 2004 Optical Society) and ref 77 (copyright 2009 American Association for the Advancement of Science).

color.72 Most often, the structural color is the consequence of multiple physical phenomena; in the case of Morpho butterfly, the brilliant blue is due to multilayer interference, diffraction, scattering, and pigment-induced absorption, causing angleindependent reflection of blue on the scales.73 Another striking example of multilayered interference is found in birds-of-paradise Lawes’s parotia, P. lawesii (Figure 9). The structural color of the feather barbules is due to quasiordered spongy structures of melanosomes (nanosized, melanin-containing granules) (described in section 2.1.1.1)

within a keratin matrix, resulting in a directional reflection due to constructive interference.4 The presence of melanosomes also provides a pigment coloration component to colored feathers by utilizing strongly absorbing melanin granules. In combination with the feather’s microstructure, melanin helps to enhance, filter, and generate a diverse palette of colors. Additionally, the precise arrangement of melanin as a basal layer enables absorption of incoherently scattered light from the feather barb and offers increased color purity. In total, the selfassembled structures of melanin represent a simple route for 12713


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Figure 11. Male and female Pierella luna butterflies viewed at different angles. The male butterfly behind the female butterfly exhibits iridescence when the illumination is 45° from the normal and originates from a point opposite the viewer. As the viewing angle is decreased with a fixed light source, the delineated area on the forewing of the butterfly exhibits a rainbow iridescence with (A) red, (B) yellow, (C) green, (D) cyan, and (E) blue perceived colors. (F) Spectral distribution of the light measured from the iridescent forewing at various viewing angles ϕ (emergence angle measured from the vertical). Reprinted with permission from ref 79. Copyright 2010 American Physical Society.

layers of nacreous layers of aragonite contribute to the multilayered interference. The closely spaced grooves result in a diffraction pattern due to the reflection grating structure of the shell surface. The bright spots are diffused and are not sharp due to the uneven microstructure of the grooves.5 The groove spacing d1 can be calculated using the relation

displaying many different colors in bird feathers. The plumage of male Lawes’s parotia consists of mostly black feathers with strongly silver-colored patterns. Interestingly, the feathers’ unique boomerang-shaped construction, enveloped in a thin film, gives rise to three-directional reflections that allow rapid switching between orange, green, and blue color when the bird moves.74 These colors are generated from a multilayered structure of dense pigment and structural coloration layers. 2.2.2.2. Diffraction. Diffraction is a phenomenon that occurs due to the bending of light around an obstacle or aperture (on the order of the wavelength of light), resulting in the formation of a geometric shadow of the obstacle. A periodic arrangement of apertures results in the formation of a diffraction pattern of the geometric shadow. Iridescent colors in seashells and pearls are attributed to the diffraction effect caused by evenly grooved surface microstructures like that of a diffraction grating.75 The iridescence of the mollusk shell is attributed to the combination of diffraction and interference (Figure 10A−C).76 The uniform

d1 =

λD y

where y is the spacing between the bright spots and D is the distance between the point of reflection on the shell surface and the screen. The iridescence in the flowers of Hibiscus trionum and Tulipa species is generated due to the diffraction gratings widespread among flowering plants (Figure 10D−F).77 H. trionum petals are white with a patch of red pigment at the base, which is iridescent, appearing blue, green, or yellow depending on the viewing angle. The structure of the petal has cuticular striations 12714


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Figure 12. Optical properties of the curled scales of Pierella luna. (A) Optical images under diffuse lighting (left) and directional lighting at grazing angle (right) (scale bar 10 nm). (B) Optical micrograph of P. luna scales under oblique illumination (scale bar 50 μm). (C) Diffraction microscopy image of the colored spot of the P. luna wing showing multiple orders of diffraction in similar angular locations due to the variation in the position and angle of the diffracting scales. (D) SEM image of scales in the colored wing region (scale bar 50 μm). (E) Magnified SEM image of the white dashed boxes in (D) showing the curled regions of the scales. (F) Gray-scale encoded reflection intensity as a function of the wavelength and propagation direction showing the inverse color-order diffraction pattern for 65° light incidence. The red dashed line indicates the predicted location of the diffraction due to the cross-rib structures for an orientation of the curled regions of the scales from which the color originates. Reprinted with permission from ref 6. Copyright 2014 National Academy of Sciences.

P. luna iridescence, the blue exits at a higher emergent angle than the higher wavelength red. This color change from red to blue with increasing observation angle cannot be explained by conventional diffraction gratings.80 The reverse color diffraction effect of the P. luna results from the local morphology of individual scales within the colored spot on the forewings. The top parts of the scales are curled upward with periodically arranged cross-ribs perpendicular to the wings. In this case, the difference in the path lengths of the two rays scattered by two successive cross-ribs is given by the sum

that resemble a diffraction grating. The surface structure overlays the pigment and the rest of the petal. However, in many species of Tulipa, the iridescence is only evident to the naked eye when the pigment color and the petal surface structure are separated. The spectrally resolved reflectivity was determined using the diffraction grating equation, given by78 mλ = d(sin θD − sin θI)

where λ is the wavelength of the light, d is the periodicity of the grating, and m is the diffraction order. The wing scales of the butterfly Pierella luna show an intriguing rainbow iridescence effect. When illuminated along the axis of the body to the tip of the wings, the wings of the male butterfly decompose white light like a diffraction grating. However, the color sequence is reversed when compared to the usual mechanism of diffraction due to the grating periodicity parallel to the surface of the wing (Figure 11). The reverse color sequence is produced due to the macroscopic deformation of the entire scale to form a vertical grating perpendicular to the wing surface that functions in transmission instead of reflection.79 In the case of a flat grating or flat multilayer, when light of wavelength λ is incident at an angle θ, a grating of period b generates diffracted beams of various spectral orders exiting at different emergent angles ϕ, given by sin ϕ = sin θ + m

Δθ + Δϕ = b cos θ + b cos ϕ

When the path difference is an integer multiple of the wavelength of light cos ϕ = − (cos θ ) + m

λ b

Per this equation, the emergence angle is larger for shorter wavelengths corresponding to the reverse color sequence observed in P. luna. The dorsal and side of the forewings and hind wings of P. luna males are dull brown in the ambient illumination (Figure 12). When exposed to directional illumination incident at the grazing angle, a coin-sized spot on each forewing displays an angle-dependent color variation across the visible spectrum. By increasing the observation angle, the color changes from red to blue, resulting in reverse color diffraction due to the local morphology of the individual scales of the colored spot of the forewings.6 The alignment of the gratings perpendicular to the wing surface results in the reverse color sequence that can be

λ b

where m is an integer labeling the diffraction order. According to the equation, the specular deviation in higher order diffraction gratings (m > 0) is higher. However, in the case of 12715


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Figure 13. (A) Calculated reflectance vs number of layers in the stack for protein/air, guanine/water, and protein/water systems. (B) Spectral reflectance with varying layer numbers for the guanine/water system. Reprinted with permission from ref 83. Copyright 1972 Elsevier.

nonpolarizing reflections could have a tremendous impact on the future development of such devices.87−90 2.3.1.1. Ideal Reflective Multilayers. Multilayer reflectors are alternating layers of high and low refractive index. The reflection at a single interface can be calculated using the Fresnel equation. For a single chitin/air interface, the reflection at normal incidence is 4.8%.83 This reflection can be dramatically increased due to constructive thin-film interference in a multilayer stack (described in section 2.2.2.1). The simplest example is an “ideal” stack in which each high and low refractive index layer is a quarter-wavelength thick. As there is a halfwavelength phase change at each low to high refractive index interface, the light that is reflected from these interfaces emerges in phase and interferes constructively. Many multilayer reflectors can be broadly categorized into three different material systems. Guanine/water (n1 = 1.83, n2 = 1.33) stacks are commonly found in the scales of fish and the tapetum of scallops. Protein (or chitin)/water (n1 = 1.56, n2 = 1.33) stacks are commonly found in the reflective tissues of cephalopods and mollusks. Protein (or chitin)/air (n1 = 1.56, n2 = 1) stacks are commonly found in insects. Figure 13A shows that the reflectance increases for each of these three systems with increasing number of stacks (plates). The reflectance also increases among the material systems as the difference in refractive index between the two materials increases. For the protein/air and guanine/water systems, 100% reflectance can be achieved in under 10 layers.83 Figure 13B shows the spectral reflectance curves for an “ideal” multilayer system with different numbers of layers for the guanine/water system. These curves show that the reflectance increases with the number of layers (as expected from Figure 13A), and also that the bandwidth of the reflection decreases with increasing numbers of layers. The reflection bandwidth also increases with increasing difference in refractive index. For example, in the protein/air system with 10 layers, the width of the reflection at half-maximum is about 33% of the λmax compared to 15.5% for the protein/water system. Though the ideal multilayer stack can achieve 100% reflectance, the reflected light exhibits strong coloration with a dependence on the angle of incidence.83 While the ideal quarter-wave stack can adequately describe many biological reflectors, two particular features of many highly reflective tissues, broad-band and

observed in angularly resolved reflection spectra and in the diffraction pattern.6 2.3. Reflective and Antireflective Structures

Optical reflections arise due to a transition in the medium in which light is traveling. The medium (glass, water, air, etc.) is characterized by the refractive index (n), which quantifies the speed of light in the medium with respect to a vacuum. Thus, as light travels through a sharp change in refractive index, a reflection can occur. The Fresnel equation provides a preliminary mathematical model of reflection and refraction. The fraction of incident light reflected at an interface is measured as reflectance, R, and on the basis of conservation of energy, the remainder is transmitted (refracted) and measured as transmittance, T. According to the Fresnel equation, the reflectance behavior depends on the s (electric field perpendicular to the plane of incidence) and p (electric field parallel to the plane of incidence) polarization of light. For the case of normal incidence, there is no difference between the s and p polarization, and the reflectance is given by ⎡ n − n 2 ⎤2 R=⎢ 1 ⎥ ⎣ n1 + n2 ⎦

For light traveling from air (n1 = 1) into glass (n2 = 1.5), at normal incidence the reflectance is about 4% and increases to 100% at grazing angles. 2.3.1. Reflective Structures. Highly reflective tissues are found commonly in almost every phylum and play a major role in critical functions, including camouflage, vision, communication, and light generation.81−86 The most common examples of such reflective tissues include the silvery scales of fish and the tapetum of many species. The optical reflections from the vast majority of highly reflective tissues arise due to constructive thin-film interference from alternating layers of high and low refractive index materials (described in section 2.2.2.1). As mentioned in the above section, constructive interference can give rise to spectacular structural coloration. In this section, we will focus on the use of such multilayer stacks as reflectors and discuss variant structures that display broad-band and nonpolarizing reflections. Dielectric mirrors are optical devices with tremendous technological importance, and an understanding of biological strategies to achieve tunable, broad-band, and 12716


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Figure 14. (A) Reflected light optical image of the cuticle of the Anoplognathus parvulus beetle. (B) Cross-sectional TEM image of the cuticle from the gold beetle (Aspidomorpha tecta) showing alternating high and low refractive index layers with gradually varying spacing through the thickness of the stack. (C) Visible to infrared reflectance spectra of light reflected from the dorsal surfaces of beetles with chirped reflectors. (D, E) Spectral reflectance and optical images of koi fish scales showing broad-band reflectance. (F) Cryological SEM images showing a broad distribution of guanine crystal spacing in the iridophores of koi fish. Reprrinted with permission from ref 70 (copyright 1998 Company of Biologists) and ref 94 (copyright 2014 American Chemical Society).

Specifically, at least three strategies have been identified in which organisms can create multilayer stacks with broad-band reflectance. .87 This strategy has been observed in the tropical beetles (Figure 14A).70 Parts B and C of Figure 14 show a cross-sectional transmission electron microscopy (TEM) image of such a chirped stack and the measured reflectance spectra.70 Finally, the stack can exist as a disordered arrangement of layer thicknesses about a mean value. This type of disordered structure is commonly found in the silver reflective scales of marine fish.92 Parts D and E of Figure 14 show the reflectance spectra and optical images silver reflectance from Koi fish scales.94 In this case, the multilayer stack is comprised of thin guanine crystals separated by cytosol with a distributed spacing that allows for broad-band silver reflection (Figure 14F).94 Nonpolarizing Reflection. The biological coevolution of predators and prey in the open marine environment has led to selection pressures for the evolution of increasingly effective vision and crypsis. A particularly interesting example of this coevolution may be the development of polarized vision and nonpolarizing reflectors. It is well-known that polarized vision is well distributed among marine organisms (discussed in section 2.5.1.2), and it has been hypothesized that a role of such vision may be to break the crypsis provided by broad-band reflectors.88,95−97 From the Fresnel equation, reflections at a high to low refractive index interface at non-normal incidence are polarized due to the differential reflectance of s- and ppolarized light. Thus, predators with polarized vision should

nonpolarizing reflection, require deviations from the ideal multilayer and will be described in the next section. 2.3.1.2. Deviations from the Ideal Multilayer. Broad-Band Reflection. Reflectors that uniformly reflect light across the visible spectrum appear silver to the human eye, whereas goldcolored reflections are missing the violet and blue portions of the spectrum.91 Broad-band reflectors that generate such characteristic silver and gold reflections are an important variant of the ideal multilayer reflector. In marine fish that inhabit the top 100 m of the open ocean, significant illumination makes bulk transparency a challenging strategy for crypsis.92 Thus, broad-band silver reflecting scales allow such fish to reflect light with color and intensity that matches the rear illumination, providing for effective camouflage when viewed from the side.81 Similarly, tropical beetles have developed broad-band silver and gold reflections that allow them to mimic the reflections from wet leaves.70,87,93 As described above, ideal multilayer stacks result in a narrow reflection band due to the nature of constructive interference used to achieve high reflectivity and the fundamental limit in the difference in refractive index that can be achieved using biomaterials. As such, the generalized strategy to achieve broadband reflection in a multilayer stack is to create varied spacing so that the conditions for constructive interference are met for multiple wavelengths of light in the visible spectrum. The cost of such a strategy is that, to achieve a high degree of reflectance over the broad band, the multilayer must become very thick. 12717


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the low refractive index axis is in the direction of the stacking. Recent measurements show that a second type of guanine crystal (type 2) has the low refractive index axis in the plane of the crystal normal to the direction of stacking. Optical modeling of multilayers of mixed type 1 and 2 crystals indicate that the mixed multilayers may result in reflections with a significantly lower degree of polarization compared to those of stacks comprised of only type 1 crystals or optically isotropic crystals. Thus, the ability for certain fish to regulate crystallization of guanine crystals may represent a strategy for polarization-independent crypsis.88,98 2.3.2. Antireflective Structures. While most biological photonic structures are associated with bright coloration or broad-angle reflectivity, the surface nanostructure commonly known as a “moth eye” structure plays an important role in minimizing surface reflections at broad angles and frequency ranges.99−101 A large mismatch in the refractive index of an object and the surrounding medium can cause an object that does not otherwise absorb or scatter light to become highly reflective and limit light transmission (consider a diamond ring).3 The moth eye structure is an ordered array of subwavelength cones or cylinders that serve to gradually match the optical impedance of the object with the surroundings.102 As the name suggests, the structures were first discovered on the compound eye structures of moths, where it is hypothesized they may serve to improve vision in low light and provide camouflage by minimizing surface reflections.103,104 Subsequently, similar structures have been discovered on the compound eyes and transparent wings of a diverse range of arthropods.50,105−107 The technological importance of antireflective coatings in a broad range of lightgenerating (such as light-emitting diodes (LEDs) and displays) and light-collecting (such as optical lenses, photodetectors, and photovoltaic cells) applications has led to significant research efforts in studying and mimicking the moth eye structure.108−110 2.3.2.1. Physics of Moth Eye Antireflection. Antireflective coatings were initially discovered by Lord Rayleigh in the 19th century when he observed that the tarnishing of a glass surface increased optical transmission instead of reducing it.101 This led to the strategy of achieving antireflectivity by gradually matching the refractive index of the substrate and surrounding ambient. A thin film on the surface of glass can reduce reflection. This effect can be explained by envisioning a thin coating with refractive index nc between the air (n1) and the glass (n2). The incoming light now reflects twice, once at the air/coating interface (R1c) and once at the coating/glass interface (Rc2). From the Fresnel equation (shown above), both R1c and Rc2 can be calculated, and it can be shown that if the refractive index of the coating is the geometric mean of the air and glass [√(n1n2)], both R1c and Rc2 become equal and the overall reflectance is lowered. This concept can be extended to further improve performance by creating multilayer coatings where the refractive index of each layer is between that of the layers immediately adjacent. The ultimate extension of this is a coating similar to that observed by Lord Rayleigh in which the refractive index is graded continuously through the thickness of the coating from that of the air to the glass. The distribution of material in the moth eye nanostructure creates the effect of grading the refractive index. This graded transition results from the size, spacing, and shape of the nanoscale features. In contrast to macroscale features, the fact that the size and spacing of moth eye structures are well below

observe contrast between the reflected light from the organism and the backside illumination. Recently, a potential strategy to overcome this detection by generating nonpolarized reflections has been discovered in several fish species. These species contain two distinct types of guanine crystals with different refractive indices (Figure 15A).88 Guanine crystals are highly birefringent with refractive indices of 1.85, 1.81, and 1.46 measured in crystals from Clupea harengus. Previous models of fish reflectors have been based on the assumption that the guanine crystals are arranged such that

Figure 15. (A) Refractive indices of type 1 and 2 guanine crystals found in several fish species. (B) Schematic for the arrangement of type 1 and 2 guanine crystals in a broad-band nonpolarizing reflector. (C) Degree of polarization as a function of the angle of incidence for reflectors comprised of mixed type 1 and 2 guanine crystals (red line) and only type 1 or optically isotropic guanine crystals (blue and black lines, respectively). Reprinted with permission from ref 88. Copyright 2012 Nature Publishing Group. 12718


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2.3.2.2. Antireflective Moth Eye Structure. As mentioned above, the antireflective moth eye structure was first observed in electron microscopy studies on photoreceptor structures in a night moth, Prodenia eridiana (Sphingidae).103,104 The moth has a compound eye comprised of a hexagonal array of ommatidia (individual optical elements) (Figure 17A). Bernhard and Miller discovered that the corneal surface of the ommatidium was further covered with a hexagonal array of cone-shaped nanoprotuberances, about 200 nm in height, which were termed “nipples” (Figure 17B). The antireflective function of the moth eye structure was first demonstrated in scaled-up microwave experiments on dielectric lens models scaled to the frequency of the microwaves and confirmed in comparative spectrophotometric measurements on corneal fragments from insects with nippled and non-nippled facets.103 Subsequently, comprehensive electron microscopy surveys found similar ordered nipple arrays among a wide range of Lepidoptera species, including both moths and butterflies.104 Surprisingly, more than 30 years after the original discovery of the moth eye structure, a nearly identical nanostructure in the transparent wing regions of the hawkmoth was discovered (Figure 17C,D).105,112 Spectroscopic studies of these transparent wings have shown that the moth eye nanostructures are antireflective across broad ranges of both visible wavelengths and angles of incidence. The antireflective property of the wing nanostructures was surprising considering that the vast majority of nanostructures in Lepidoptera wings provide structural coloration.113−115 Similar moth eye nanostructures have also been found on the transparent wings of cicadas, butterflies, and dragonflies.50,107,116 Recently, two insect examples have emerged that directly point to the antireflective function of the moth eye structure. The first example is the whirligig beetle (Figure 18A), which lives at the water surface. This beetle has eyes that are divided into overwater and underwater parts that are responsible for vision in the respective medium (air or water). Interestingly, atomic force microscopy (AFM) analysis of the different eye parts shows dramatically different nanoscale topographies. While the underwater part is smooth, the overwater part contains a mazelike topography (discussed later) that provides antireflection in the air, where the refractive index mismatch is much greater (1−1.54 vs 1.3−1.54).117 The phenotypic role of the moth eye structure has also been observed in the model organism Drosophila melanogaster (Figure 18B). AFM studies of the insect eyes show that the ommatidia are covered with an ordered array of conical nanostructures (Figure 18B, top), which result in a wild-type lusterless eye phenotype (Figure 18B, top inset). Several Drosophila mutants display a glossy eye phenotype (Figure 18B, bottom inset). AFM analysis of the eye surfaces shows a loss of the moth eye nanostructure (Figure 18B, bottom).118 2.3.2.3. Variants of Moth Eye Structure. Previously, we have discussed “ideal” moth eye structures (highly ordered hexagonal arrays) and their prevalence on corneal surfaces and transparent wings. Recently, however, broad atomic force microscopy surveys of corneal surfaces of diverse insect orders have found variant structures that are broadly distributed (Figure 19).119 These variant structures (Figure 19B) have the similar effect of creating a gradient refractive index. It is proposed that these variant structures may be precursors to the highly ordered moth eye structure. Interestingly, the resemblance of these variant nanostructures to Turing patterns may suggest a role for a reaction−diffusion mechanism in the formation of these

the wavelength of visible light causes the light to interact with the surface wholly as if it had a graded refractive index (Figure 16A,B).101 The refractive index varies through the thickness

Figure 16. (A, B) Schematics illustrating the interaction of light with a macrostructure and subwavelength nanostructures. (C) Graph showing how the refractive index varies with the thickness for different nanostructure profiles. (D−F) Graphs showing antireflective properties of various nanostructure profiles with varying feature height. Reprinted with permission from ref 101 (copyright 2011 Royal Society of Chemistry) and ref 111 (copyright 2006 The Royal Society).

along with the proportion of corneal material gradually changing from 0% at the tip to 100% at the base of the nanostructures. Mathematical calculations of various moth eye feature profiles, heights, and spacing have been performed to investigate an ideal moth eye structure (Figure 16C−F).111 Features with a parabolic profile and height of 250 nm show excellent antireflective properties across the visible spectrum. Additionally, it has been demonstrated that the antireflective properties of moth eye structures persist over broad angles of incidence and are independent of the polarization of incoming light. 12719


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Figure 17. Highly ordered moth eye nanostructures found on the corneal surface (A, B) and wing surface (C, D) of the insects. Reprinted with permission from ref 111 (copyright 2006 The Royal Society) and ref 112 (copyright 2015 American Chemical Society).

Figure 18. (A) Optical and AFM images of the overwater and underwater eyes of the whirligig beetle. Antireflective nanostructures are only found on the overwater eyes where refractive index mismatch is higher and reflections are more prevalent. (B) Optical and AFM images of wild-type and mutant fruit flies. Mutant fireflies exhibit a glossy eye phenotype which corresponds with a loss of the ordered nipple array. Reprinted with permission from refs 117 and 118. Copyright 2014 and 2011, respectively, Nature Publishing Group.

structures.120−122 In 1952, Alan Turing proposed a mathematical description of a reaction−diffusion mechanism, where two morphogens, one a slow-diffusing activator and the other a fastdiffusing inhibitor, react to form a diverse range of biological patterns. If a biochemical pathway for reaction−diffusion-based

formation of moth eye nanostructures can be found, it could provide insights for biomimetic strategies to synthesize similar structures in a scalable bottom-up manner. Examples of the variant moth eye structures have also recently been discovered in noncorneal structures. Parts A−D 12720


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Figure 19. (A) Phylogenetic tree and (B) AFM images showing variant antireflective nanostructures and their prevalence on insect corneas. Reprinted with permission from ref 119. Copyright 2015 National Academy of Sciences.

Figure 20. Optical (A, E) and SEM (B−D, G−I) images showing variant antireflective nanostructures found on the wing and light organ surfaces of the glasswing butterfly and firefly, respectively. Reprinted with permission from ref 109 (copyright 2012 National Academy of Sciences) and ref 123 (copyright 2015 Nature Publishing Group).

of Figure 20 show a highly irregular nipple pattern found in the transparent wings of the glasswing butterfly.123 These irregular

nipple patterns show optical properties similar to those of the highly ordered arrays with excellent antireflection over broad 12721


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Figure 21. (A) A large white, Pieris brassicae, on a butterfly bush (scale bar 1 cm). (B) The scales of a small white, Pieris rapae, are generally scalloped, and are locally interspersed with plume scales (scale bar 40 μm). (C) SEM image of a white scale of P. rapae. The ridges have only slightly overlapping lamella, and the cross-ribs are densely adorned with beads. (D) A black scale, lacking beads (scale bar 1 μm). (E) Image of heliconine Heliconius melpomene (scale bar 1 cm). (F) SEM image showing the wing scales without beads with variably sized windows (scale bar 2 μm). Reprinted with permission from ref 7. Copyright 2004 The Royal Society.

reflection needs much thicker films owing to the requirements of optical processes for multiple light scattering. Despite the striking coloration, coherent optical effects result in wavelengthdependent coloration and iridescence, which will not result in uniform white coloration independent of the incident angle or wavelength. To realize a uniform white coloration, nature utilizes optical scattering effects from a disordered arrangement of randomly positioned scattering centers. A class of butterflies of the family Pieridae exhibit bright white coloration attributed to the inherent scattering of incident light and the absorption of pterin pigments in the scale structures (Figure 21A--C).124 Pterins are a class of pigments with different absorption properties (leucopterin absorbs in the UV wavelengths, while erythopterin absorbs up to a wavelength of 500 nm) found in pierid butterfly scales.125 Furthermore, on the scales of Pieris rapae, the presence of pterin ellipsoidal beads enhances the wing reflection by increasing the brightness of the beads at wavelengths where the pigment absorption is negligible.7 The white scales are densely covered with ellipsoidal beads, while black scales are devoid of them (Figure 21C). The structural difference between the white and black scales suggests an optical function for the ellipsoidal beads (hollow beads made of pterin) (Figure 21D). A comparison of the reflectance of the wing scales of two species of butterflies, Heliconius melpomene and P. rapae, suggest that the presence of the ovoid beads is responsible for the enhanced reflection (Figure 21E,F). In P. rapae, the white scales have low reflection in the UV wavelengths due to the presence of UV-absorbing pigments, while the black scales have low reflection in the entire visible range. In H. melpomene, the reflection spectra of all scales except black converge beyond 650

wavelengths and angles of incidence and indiscriminate polarization. Another striking example is the presence of a parallel strand nanostructure on the cuticle surface of the firefly light organ (Figure 20E−I).109 This is the first example where the antireflective nanostructure enhances transmission of light generated by the organism and where light travels from the high refractive index medium (chitin) to a low refractive index medium.101 The parallel strand nanostructure is only found on the chitin covering the light organ (Figure 20I). Chitin covering adjacent regions (Figure 20H) shows a much shallower mazelike morphology. The enhancement of light output would aid fireflies in communication and mating, making it a positive selection factor. 2.4. Scattering

Scattering is often defined as the interaction and consequent deviation of light from a straight path with small particles/ structures distributed randomly in a continuous medium. Many familiar effects in nature and biology such as blue sky, red sunsets, and blue eyes and feathers of male butterflies of the species Papilio zalmosis are due, at least partially, to scattering of light. Scattering is also responsible for the whiteness of foam, milk, snow, paints, and certain biological structures described below. As mentioned earlier, teasing apart the numerous optical effects responsible for nonpigmentary biological colors is often difficult and runs into the problem of oversimplification. In contrast to structural color attributed to the selective absorption or reflection of light at certain wavelengths, certain species of butterflies and beetles exhibit a bright white diffuse reflection. A broad-band white reflection is harder to obtain because all wavelengths of light need to reflect with the same efficiency. While submicrometer thick films are enough to generate colors using interference effects, a broad-band light 12722


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Figure 22. (A) Image of a Cyphochilus beetle. (B) Scales on the surface of the Cyphochilus beetle (scale bar 400 μm). (C) SEM image of an entire scale (scale bar 25 μm). (D) SEM image of an entire scale (scale bar 2 μm). Reprinted with permission from ref 130. Copyright 2015 John Wiley and Sons.

2.5. Polarized Light in Nature and Helicoidal Structures

nm, suggesting the scales scatter light in the same way as P. rapae except for the specific pigments. However, in comparison, P. rapae shows higher reflectance than H. melpomene attributed to the presence of ellipsoidal beads on the cross-ribs in the scales.7 Furthermore, the removal of the pterin beads in the pierid butterfly scales results in reduced reflectance of the scales.111,126 Certain classes of beetles (Cyphochilus and Lepidiota stigma) are known to exhibit an exceptional bright whiteness due to the pronounced multiple scattering, unlike the Pieridae butterfly scales that exhibit single scattering (Figure 22).127 The scales of the beetle are known to be the most strongly scattering low refractive index materials.127 In an ordered structural assembly, the lower the refractive index n of the scattering elements, the thicker the system has to be to achieve a pronounced brightness, which reduces the overall scattering strength.128 Instead, due to the anisotropic shape and orientation of the scattering elements forming the disordered network, beetles exhibit an exceptionally high scattering strength even for a small thickness. The scales appear white at any angle of observation due to the scattering of light in the internal random network of interconnecting rodlike filaments of chitin.129 The disorder in Cyphochilus scales has evolved to avoid spatial correlations, and yet maintain a high filling fraction due to the anisotropic shape of the scatterers.130 The anisotropic arrangement and the shape of the scatterers are responsible for the anisotropic light transport that increases the scattering strength along the out-of-plane direction, leading to a pronounced total reflection, i.e., brightness.131 The degree of anisotropy is a key microscopic structural feature in determining a bright white reflectance in thin, low refractive index optical coatings. In contrast to the broad-band reflection obtained from the random arrangement of scattering centers, certain species of fish and spiders use an ordered arrangement to realize a white coloration.132 To realize these structures, they employ biogenic crystals of guanine that are known to have one of the highest refractive indices (n = 1.83) for a biological material.133 However, instead of alternate layers of guanine and cytoplasm, usually found in photonic crystals that reflect a single wavelength of light (described in section 2.2.2.1), the iridophores with white coloration use alternate layers of guanine crystals and amorphous guanine. The presence of amorphous guanine instead of cytoplasm between the guanine crystals is responsible for the higher reflectivities found in koi fish and the spiders Tetragnatha extensa and Tetragnatha montana.132

2.5.1. Polarized Light. In nature, light is emitted by the sun in a fully depolarized form, although after entering the earth’s atmosphere, it quickly becomes strongly polarized in the sky. This polarization effect is due to scattering and reflection of light by the abundance of particulate matter and geometrically shaped surfaces.134 Also, the degree of polarization varies dramatically depending on the time of day and angle of the sun. For example, polarization is the strongest during twilight hours at sunrise or sunset when the sun is near the horizon. Due to the ubiquitous occurrence of polarized light, all organisms are indiscriminately sensitive to some amount of polarized light in nature on a broad molecular basis, but on the macroscale and larger, the utilization and detection of polarized light highly depends on the organization, structure, arrangement, and anatomy of photoreceptors. As a result, the arrangement and type of photoreceptor decide who and what are capable of detecting and visualizing polarized light. Additionally, the physical size, number, and location of photoreceptors are equally important in determining whether polarization vision is diurnal or nocturnal in nature and its physiological function (imaging, navigation, communication, or signaling). In total, these components mutually form the basis for polarized vision and will be briefly discussed according to their basic anatomies and physiological purpose. At the molecular level, polarization sensitivity originates from the presence of a strong linear absorption dipole associated with molecular dichroic chromaphores (11-cis-retinaldehyde) in all photoreceptors.135 However, on the macroscale and beyond, polarization sensitivity of membrane-bound protein photoreceptors can be strongly enhanced or destroyed by the orientation and arrangement on the membrane surface. 2.5.1.1. Polarized Vision of Invertebrates and Terrestrial Organisms. Generally, for vertebrates, the chromaphore dipole of photoreceptors lies parallel to the membrane surface and results in a random array of dipoles.135 Thus, for perpendicularly aligned incoming light, macroscale polarization effects are canceled out. Alternatively, invertebrates respond strongly to incoming polarized light due to their unique anatomy and presence of microvilli. In this case, both the chromaphore dipole and microvillus structures are aligned parallel to the incident polarized light field, thereby maximizing absorption. Positionally, these polarization-sensitive microvillus structures are confined and limited to the dorsal rim area of the eye. In total, the ability to visually process, filter, and precisely differentiate polarized light is a process that is unique to terrestrial invertebrates on the basis of the classifications and anatomy of photoreceptors described above. These include insects and spiders, butterflies, beetles, locusts, and birds.136 These organisms share a major advantage by being able to send 12723


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2.5.1.2. Polarized Vision of Aquatic Organisms. Polarized Light in Water. Polarization of light in water is much weaker by comparison to that in air and is generated entirely by scattering dominated processes. This is due to the lack of reflection underwater by objects and the presence of multiple scattering paths from water molecules to suspended particles of minerals or sand, which quickly degrades light polarization.134 Nevertheless, light polarization in water is visible from any direction, is used as an important substitute for color vision, and provides a series of visual cues used by fish, cephalopods, arthropods, and crustaceans. Linearly Polarized Light Vision. Aquatic organisms possess a highly specialized ability to distinguish polarization differences and features within a single object which would otherwise appear as featureless or transparent to humans. This function is similar to the way we visualize colored objects from other colors and, by analogy, enables octopuses and squid to rapidly identify invisible prey/food targets (transparent jellyfish) with distinct polarization signatures from the background and hunt more effectively. Cuttlefish are a close cousin to squid and octopuses and, not surprisingly, exhibit equally strong polarization vision in place of the ability to view colors. The physiological basis for this polarization vision is due to the limited amount of spectral color and light intensity present in their habitat at deep water depths; in addition, it improves the visibility of objects of prey or predator in highly turbid water.148 Moreover, fiddler crabs are even more sensitive to polarized light. For example, they are able to detect small differences in the angle of polarization by as little as 3.2° because of containing a high density of polarization-sensitive receptors spread across the entire surface of the eye.149 As a result, this visual acuity enables fiddler crabs to see in high definition and to view/parse whole polarized images or objects.150 In contrast, many open ocean fish have adapted the ability to camouflage themselves from polarization-sensitive predators by displaying highly reflective fish scales rich in guanine crystals.151 Consequently, the specific arrangements of reflective scales produce angle-dependent polarized light that matches polarization signals coming from the background, thereby allowing them to blend in with the environment. In addition to polarization vision, all cephalopods are capable of producing highly controlled polarization signals or patterns on their body surface during certain social situations (aggressive or sexual encounters) by using dynamically controlled polarization reflectors (i.e., iridophores).152 Iridophores are flat platelet cells located beneath the skin composed of reflectin proteins.153 Reflectin proteins are comprised of several repeating amino acid sequence regions rich in aromatic residues that self-assemble to form insoluble protein structures with Bragg-type diffraction properties. The presence of iridophores is unique to aquatic organisms and allows dynamic control over reflected polarized light such that it can be actively turned on or off depending on the activity, behavioral response, and/or situation. This ability to turn reflection on or off is under strong neural command and occurs by morphological changes to the iridophore cell structure. Mantis Shrimp. Mantis shrimp are one of the most advanced biological organisms at viewing different forms of light (Figure 23). In total, they are capable of viewing and filtering ultraviolet, visible, and polarized light (both linearly and circularly polarized light) via a set of compound eyes composed of highly specialized and spectrally tuned photoreceptors and optical structures (∼16 functional types). Structurally, their

and receive highly specific and cryptic polarized light signals or patterns that are invisible to every other species, to quickly identify and distinguish specific objects or complex patterns in a visually chaotic and noisy background encountered in natural biological settings (i.e., rainforests with dense canopies), and to use and interpret polarization patterns for orientation and navigation. For example, honey bees, insects, and more recently mouse-eared bats were discovered to use direct polarization patterns in the celestial sky for navigation purposes.137 Similarly, dung beetles, spiders, and migratory birds also use polarization patterns in the sky as a celestial compass and are preferentially more active at twilight when the polarization is the strongest. By being active during periods of strong polarization, these animals possess normal- to small-sized photoreceptors that are arranged spatially in such a manner to maximize the viewing angle of the nearly horizontally polarized light. Dung beetles use celestial polarization patterns to precisely roll balls of freshly scavenged dung along a straight path away from the larger dung pile, thereby enabling them to travel over short distances in a faster amount of time.138 Similarly, desert locusts detect polarized light reflected from the water surface to avoid crossing the ocean during long migrations along the coast.139 Besides navigational purposes, bumblebees were found to actively use polarization vision to identify pollen-producing flowers from complex landscapes and use this detail to learn and segregate specific polarization patterns on certain flowers.140 In a similar example, Papilio butterflies view polarized reflected light in combination with color to produce false coloration of leaves for egg laying.141 By comparison, most animals use color and polarization vision independently to avoid false coloration, and under certain instances, polarization vision is used to compensate when limited color information is available and vice versa. This dual vision sensory ability enables animals to function under different lighting conditions and extract the most amount of light information available. Also, water beetles rely on horizontal polarization generated by light reflection from natural water surfaces for orientation. However, artificial sources of polarized light endanger many water-tactic insects (mayflies) by producing high levels of polarized light pollution that include the horizontally polarizing reflective surfaces of black-painted car surfaces and/or the thousands of miles of dry asphalt roads.142,143 Alternatively, after much debate and a lack of direct evidence, it is unlikely that scarab beetles visually respond to polarized light, but however possess a unique exoskeleton cuticle, which is universally known to strongly reflect left-handed circularly polarized light, giving it a green- and/or gold-metallic-colored appearance.144,145 Structurally, the cuticle reflects polarized light reminiscent of cholesteric crystals by containing evenly rotated and ordered layers of parallel chitin fibers at a constant pitch which appear as star-shaped cavities.146 Optically, this represents a nonvisual mode of polarization signaling that is highly specialized and not yet directly connected to behavior or any known biological significance. Butterflies provide another important example of polarization-sensitive color signals. As described in section 2.2, butterfly wings possess extraordinary photonic structures that reflect intense iridescent light. At the same time, the microstructures created from periodic ridges within butterfly wings create direction-dependent-polarizationsensitive color signals.147 These polarized color reflections occur during the flight of female butterflies and result in a flashing signal used to attract males. 12724


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than linearly polarized light and is almost exclusively produced by a few animal surfaces. Notably, the ability to view circularly polarized light originates from the unique and precise arrangement of birefringent UV photoreceptors into a multitiered structure with angular dependence. Structurally, a top pair of UV receptors sensitive to 360 nm light are rotated at 90° to each other. The twisted rotation of UV receptors in this case functions as a quarter-wave retarder plate and converts incoming circularly polarized light into linearly polarized light.156 The converted linearly polarized light would then be at +45° or −45° to the UV receptor axis depending on the original handedness of circularly polarized light (right-handed or left-handed light). Orthogonal to each UV receptor, there are two large visible photoreceptors tuned to 500 nm that form underlying perpendicularly aligned stacked microvillus structures and are strongly responsive to linear polarization. The presence of two distinct sets of photoreceptors within the mantis shrimp enables the detection of both linearly and circularly polarized light and increases the amount of visual information they can collect from their environment. However, this architecture represents a simple and static structural mechanism for the detection and analysis of polarized light. More recently, a dynamic component of polarization vision for the mantis shrimp that is linked to behavior and physiology has been discovered. Mantis shrimp are able to enhance and maximize polarization information through a complex series of eye movements.157 By comparison, mantis shrimp are like many other animals (blowflies, pigeons, crabs, and cats) in that they employ gaze stabilization to avoid blurred vision during movement, while also maximizing visual cues. Generally, gaze stabilization by animals is accomplished by using a combination of eye, head, and body movements to geospatially fix onto an object or target. In contrast, mantis shrimp perform gaze stabilization by precisely controlling only eye movements through a series of pitch, yaw, and torsional rotations to align the angle and orientation of specific photoreceptors relative to the angle of polarization from a visual stimulus (Figure 23b). Consequently, response to a polarized light stimulus resulted in an average torsional rotation of 15° at a rotational speed of 45 ± 8 deg s−1. In total, this complex set of orchestrated eye movements helps to maximize the polarization contrast between an object and the background, unless the background is polarized as well. Mantis Shrimp Body Patterning/Signaling. Mantis shrimp are capable of generating intense patterns of circularly polarized light from their body structures as a means of signaling. These designated patterns/signals are of course only visible to other mantis shrimp with circularly polarized vision, and are remarkably similar to the circularly polarized light patterns produced from the scarab beetle exoskeleton. However, unlike scarab beetles where circularly polarized light signals are entirely based on reflection from the optical structuring of the beetle cuticle, the circularly polarized body signals of mantis shrimp are generated by a molecularly dominated mechanism involving dichroic carotenoid pigments.158 These dichroic pigments contain red-colored astaxanthin and are located in the antenna scales. To date, these are the only two known examples of biological structures capable of creating circularly polarized light in nature. It is interesting to note that each animal is bound and biologically isolated from one another by their respective terrestrial and marine-based environments, thereby ensuring their highly specialized light signals cannot be intercepted or diluted by similar polarization signals.

Figure 23. (a) Full-body view of a mantis shrimp (Gonodactylus smithii). (b) Eye movement of a mantis shrimp showing rotational degrees of freedom. Reprinted with permission from ref 151. Copyright 2016 Nature Publishing Group.

compound eye is formed by six parallel rows (ommatidia) of photoreceptors, each being sensitive to a specific wavelength and/or polarization. These rows are further arranged spatially and angularly by the wavelength sensitivity and function of each photoreceptor. Each row is constructed with UV receptors on top followed by an underlying tier of color-sensitive receptors. Notably, the UV photoreceptors are composed of crystalline mycosporine-like amino acid pigments.154 This arrangement of photoreceptors enables the mantis shrimp to visually process more detail by using polarization to augment or replace color patterns especially when light becomes spectrally restricted at low ocean depths. Circularly Polarized Vision of Mantis Shrimp. More impressively, mantis shrimp have adapted the ability to visually distinguish circularly polarized light. To date, this is the only example of visual function utilizing circularly polarized light and is unlike linear polarization vision used by all other organisms. In water, circularly polarized light is generated by the total reflection of linearly polarized light at the water−air interface outside of Snell’s window (compressed 97° viewing angle underwater) and reflection of light from the birefringent cuticle of mantis shrimp discussed below and/or from light traveling through the transparent body of single-cell dinoflagellates.136 The biological significance of circularly polarized light vision has likely evolved as a sophisticated means for covert communication to overcome the widespread use of linearly polarized light used by all invertebrates and/or to visually sense and detect burrows occupied by other mantis shrimp.155 Also, circularly polarized light in nature by comparison is much rarer 12725


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Figure 24. Photographs of the beetle Chrysina gloriosa: (A) in unpolarized or right circularly polarized light showing a bright green color with silver stripes, (B) in right circularly polarized light showing the loss of green color. (C) Optical micrograph showing the exoskeleton of the beetle C. gloriosa showing a bright yellow reflection from the core of each cell (∼10 μm) and green reflections from the edges. (D) SEM image of the beetle exoskeleton showing nested arcs and a waxy layer on the top. (E) Angled 3D image of the upward cones of each cell showing the concentric bright/ dark spiraled regions. (F) Typical x−y section showing a relief feature with concentric rings that are resolved at a high magnification and present only near the free surface. (G) AFM image of the cholesteric focal conic domains at the free surface, showing double spirals that form a shallow cone. (H) AFM image of the microtome cut perpendicular to the free surface. (I) Schematic representation of the relative arrangement of chiral mesogens in a cholesteric liquid crystal, stacked in a single twist structure. (J−L) Optical micrographs of the exoskeleton of C. gloriosa (J) in bright field with a wide aperture, (K) near normal incidence with a lower aperture, and (L) in dark field, where near-normal incidence is not present. Reprinted with permission from ref 66 (copyright 2009 American Association for the Advancement of Science) and ref 166 (copyright 1996 American Physical Society).

2.5.2. Helicoidal Structures. As described above, many species such as fish, cephalopods, crustaceans, and insects, among others, have evolved to perceive polarized vision as a means of navigation, communication, and mate selection.139,159−161 During this course of evolution, various species have developed structural color using helical architectures.8,66,162,163 A distinct feature of the structural color formed from helical structures is the angle-dependent reflection, resulting in a striking iridescence and the selective reflection of single-handed polarized light.67 Beetles exhibit a brilliant iridescence and an angle-dependent “flash light” appearance due to the presence of helical architectures on the exocuticle.164 An investigation of the first known anomalous reflection from beetles’ elytra revealed that the reflected light is circularly polarized even at normal incidence.165 The degree of circular polarization is maximum at blue wavelengths, decreases to completely unpolarized light at orange-yellow wavelengths, and is polarized at red wavelengths. Furthermore, the beetles’ elytra exhibits an angle-dependent reflection and turns completely black in the presence of right circularly polarized light.165 Jewel beetles also exhibit a brilliant iridescence due to the unique interaction of the nanoscale features on the exoskeleton with light.66 The exocuticle of the beetle Chrysina gloriosa (or

Plusiotis gloriosa) selectively reflects left circularly polarized light and has a brilliant metallic appearance (Figure 24A). If left circularly polarized light is blocked from the incident light using a quarter-wave plate and a polarizer, the beetle loses its bright green reflection (Figure 24B). The selective reflection of circularly polarized light in certain species of beetles is attributed to the nanoscale helicoidal features on the exoskeleton with the periodicity of the wavelength of light. The exoskeleton of the beetles consists of a richly decorated mosaic, consisting of a regularly spaced lattice that distinguishes one species of beetle from the other. The structure of C. gloriosa consists of hexagonal cells (∼10 μm), and under a bright field, each cell appears green with a bright yellow core or nucleus (Figure 24C). The scanning electron microscopy (SEM) image of the exoskeleton of beetles reveals nanoscale concentric regions (Figure 24D). Furthermore, the fluorescence map (autofluorescence under the excitation of a 488 nm laser) of the exoskeleton reveals concentric regions of bright and dark regions that show the existence of nested arcs, with a conical protrusion at the center (Figure 24E,F). The microstructure of the beetle surface is similar to that of the focal conic domains on the free surface of a siloxane oligomer-based cholesteric liquid crystal (Figure 24G,H).166 12726


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Figure 25. Photographs of Pollia condensata fruits: (A) single fruit from dried herbarium specimen, (B) infructescence (cluster of fruits) from alcohol-preserved specimens. (C) TEM image of the single thick-walled cell from the outer epicarp of the fruit. (D) TEM image of the cellulose microfibrils that constitute the thick cell walls. The red lines highlight the twisting direction of the microfibrils. (E) Scheme showing a wedge of an LH helicoid with the arched pattern exposed on the oblique face (shown on the left). Circularly polarized beams of light, with k⃗ the wave vector of the light (shown on the right). (F) The handedness of the transmitted and reflected light depends on the handedness of the helicoid. Here, the light transmitted through the structure (k⃗ pointing down) is LH circularly polarized, while the reflected light (k⃗ pointing up) is RH circularly polarized. 3D representation of the orientation of the cellulose microfibril assembly and a transmitted circularly polarized beam. (G−I) Polarized reflection of P. condensata fruit. (G) LH and (H) RH optical micrographs of the same area of the fruit under epi-illumination. The inset shows a zoom of the central area, with white lines delimiting the cells. (I) Same area imaged under cross-polarizers. (J) Spectra from two different cells (continuous and dotted lines) for two polarization channels (red and blue color). Auxiliary minor spectral features leading to the double-peak structure arise from the stacked nature of the cells in the epicarp, leading to spectral contributions from underlying cells with different p values. Reprinted with permission from ref 8. Copyright 2012 National Academy of Science.

wavelength λo = nP, where n is the average refractive index.167 The largest reflectivity for a given color is obtained when the optical thickness of the half-pitch is equal to the wavelength of the color.168 The spectral width of the reflection peak is related to the birefringence (Δn = ne − no) and is given by λo = PΔn, where ne and no are the refractive indices for polarizations perpendicular and parallel to the axis of anisotropy, respectively.66 Under white light illumination, the beetle structure appears as green hexagons with yellow at the center (Figure 24C). For an oblique incidence at an angle ϕ, the reflection for a helical axis oriented at some angle θ with respect to the surface normal resulting in Bragg reflection is given by λ = nP cos(ϕ − θ).

A cholesteric liquid has long-range orientational order described by a unit vector n, known as the director, whose equilibrium director structure is a helicoid. The director advances uniformly, tracing a helix of pitch P (Figure 24I). The selective reflection of circularly polarized light by a chiral structure is given by167 λmax = nav P sin θ

where nav is the average refractive index of the liquid crystal, P is the pitch of the helix, and θ is the angle of incidence. Due to its chiral and periodic helicoidal structure, the cholesteric phase with a pitch comparable to the wavelength of visible light shows Bragg-like reflection at normal incidence and a peak at 12727


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Figure 26. (A, B) Cryo-SEM images of Sapphirina metallina. Transverse view showing the guanine crystals aligned perpendicular to the dorsal surface of the animal. The iridophores are located just beneath the chitin procuticle (Pc). Dorsal view showing the tightly packed perfectly hexagonal crystals and the alternating layers of guanine crystals and cytoplasm beneath the procuticle. Reflectance and structural properties of individual copepods: light microscopy images (C−F) (violet-magenta, red, yellow, blue-green) and (G−J) measured reflectance of S. metallina. Images of copepod color change at different tilt angles (K−N) and their measured reflectance spectra (O−R) of S. metallina. Reprinted from ref 9. Copyright 2015 American Chemical Society.

When the angle of incidence increases, ϕ − θ becomes smaller; hence, cos(ϕ − θ) increases, resulting in a higher wavelength of the reflected light (yellow). This is evident by an increase in the locus of yellow reflection at the center upon increasing the

angle of incidence (Figure 24J,K) and the extinction of the yellow reflection at the center in dark field (no normal incidence) (Figure 24L) in the optical images of the beetle structure. In addition to the angle of incidence, the selective 12728


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Figure 27. (A) Reversible color change of two males (m1 and m2): during excitation (white arrows), the background skin shifts from the baseline state to yellow/orange and both the vertical bars and horizontal midbody stripe shift from blue to white (m1). (B) Haematoxylin and eosin staining of a cross-section of white skin showing the epidermins176 and the two thick layers of iridophores (scale bar 20 μm). (C) TEM images of guanine nanocrystals in S-iridophores in the excited state and three-dimensional model of an fcc lattice (shown in two orientations) (scale bar 200 nm). (D) TEM image of guanine nanocrystals in D-iridophores (scale bar 200 nm). (E) TEM image of the lattice of guanine nanocrystals in S-iridophores from the same individual in relaxed and excited states (two biopsies at a distance of 80%) found in 12736


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marine environments.229 It is thought that the sparse visual environment of the open ocean led many organisms to move to greater depths to avoid predation. At these depths, the limited ambient light created evolutionary pressure for enhanced visual signaling through light production. Bioluminescent organisms in the ocean vary vastly, including bacteria, dinoflagellates, squid, and fish to name a few (Figure 33A).12 On land, bioluminescence is much less common and is primarily found in insects, with fireflies being the most well-known example, but can also be found in other species, including fungi (Figure 33B).230 As a biophotonics strategy, bioluminescence is used by organisms for camouflage, communication, illumination, defense, and attraction and has been developed independently many times, with more than 30 distinct incidences currently known.231 Common features that link the majority of bioluminescent organisms include a light-generating reaction between a substrate (known generally as a luciferin) and molecular oxygen, the presence of an enzyme (known generally as a luciferase) to catalyze the reaction, and a source of energy for excitation obtained from the breakdown of a luciferase-bound peroxide intermediate. In spite of these similarities, the luciferases found in the bioluminescent reactions of fireflies, coelenterates, and bacteria, for example, show no homology to each other. Moreover, the luciferins used in these reactions are also chemically unrelated.228 2.8.2.1. Chemistry of Bioluminescence. The emission of a photon in a bioluminescence reaction requires the radiative decay of an excited electronic state. In contrast to fluorescence and phosphorescence, where the excited state is generated by the absorption of a higher energy photon, the energy for the excited state in bioluminescence arises from a highly exergonic reaction. This reaction can be stated generally by the following equation: luciferase

luciferin + O2 ⎯⎯⎯⎯⎯⎯⎯⎯→ intermediates → P* → P + light

Here, as mentioned above, the intermediates are commonly luciferase-bound peroxides. The peroxide typically decomposes to an excited carbonyl compound and CO2. The lifetime of the excited state is generally only a few nanoseconds, and its radiative decay results in light emission. Interestingly, while luciferases are typically unique to each species, there is a significant overlap in the luciferins. Several of the most common luciferins are shown in Figure 34.232 In general, the color of a bioluminescence reaction matches the fluorescence emission of the excited luciferase-bound product. However, there are several factors that can change the bioluminescence color. In fireflies, for example, single amino acid substitutions can alter the luciferase structure and shift the emitted light color. In coelenterates and bacteria, on the other hand, accessory proteins such as green fluorescent protein (GFP) and yellow fluorescent protein (YFP) are used to shift the color of light emission through nonradiative coupling with the excited-state luciferase-bound reaction product.232 2.8.2.2. Coelenterate Bioluminescence. Two of the most widely studied bioluminescent organisms are coelenterates, the sea pansy Renilla and the jellyfish Aequorea, which utilize coelenterazine as a luciferin and contain GFP accessory proteins. Their luciferases and the chemical mechanism for light production, however, seem to be unique, though both are triggered by calcium. Renilla utilizes four proteins in its

Figure 34. Common luciferins. Reprinted with permission from ref 233. Copyright 2014 IEEE.

bioluminescent reaction. The first is a sulfokinase that converts the storage form of coelenterazine into the active form by removing a sulfate. The coelenterazine then binds to a luciferinbinding protein and is released only in the presence of calcium. The released coelenterazine is then oxidized by the Renilla luciferase through the formation of a dioxetanone intermediate. The result of this reaction is the oxidized luciferin in the excited state, whose radiative decay results in light emission. The final protein involved is green fluorescent protein, Renilla GFP, which red shifts the emitted light. Initially, Aequorea did not seem to have a luciferase/luciferin system or to require oxygen for bioluminescence. Using a chelator, it was possible to isolate aequorin, a photoprotein that only required calcium for light emission. However, it was discovered that aequorin is a stable reaction intermediate in the luciferase/luciferin bioluminescence reaction. In this case, calcium triggers the reaction to go to completion rather than controlling the availability of luciferin.232 Renilla and Aequorea both utilize GFP to shift the color of emitted light. GFP accepts energy through a nonradiative bioluminescence resonance energy transfer (BRET) directly from the excited state of coelenterazine. This results in a shift in 12737


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beetle exocuticle, fruits insect compound eyes cephalopods, chameleons, beetles, damselfish

photonic crystals (opal/inverse opal structures) helicoidal structures antireflective surfaces responsive materials

butterflies, birds

reflection of circularly polarized light antireflection dynamic tunable color, mechanochromism

template-assisted replication, atomic layer deposition, electron beam lithography, focused ion beam CVD, PDMS molds, double imprint templating chiral molecule templating, liquid-crystal assembly replica templating self-assembly of diblock copolymers, polymerization of liquid crystals

264−268 247, 248 149, 249−252 279−291, 316−321 293−315 237, 319, 320 292, 324−329 extraction from plants/cyanobacteria recrystallization on a chitosan substrate recombinant protein expression in Escherichia coli, self-assembly/flow coating photosystem guanine reflectin films

salmon trees, bacteria cephalopod skin and ink, bird feathers, retinas plants, cyanobacteria fish cephalopods

absorption/light harvesting reflection thin-film interference, infrared camouflage structural coloration, reflection

269−271 272−278 236−246 sonication, spin coating liquid-crystal assembly, delignification/polymer infiltration enzyme oxidation, spontaneous oxidation, Ce(IV) oxidation, dopamine polymerization

dissolution in LiBr/ionic liquid/HFIP, drop casting

waveguiding, transparency, photonics, structural coloration electron-blocking layer, transparency transparency, optical brightening agent broad-band absorption silkworms, spiders

biological inspiration biomimetic material

Table 2. Bioinspired Optical Materials

optical properties

3. BIOINSPIRED OPTICAL MATERIALS AND DEVICES As exhaustively described in the previous section, nature has designed materials and structures with remarkable optical functionalities that have been refined and perfected through the course of evolution. Biological systems in nature offer new approaches, templates, and inspiration for the biomimetic design, synthesis, and fabrication of light-absorbing molecular pigments and crystals, structural and functional recombinant proteins, optically active biomaterials, and light-manipulating micro- and nanostructures. This is best exemplified by the exquisite structural coloration displayed in bird feathers and created from precise nanostructured assemblies of melanin pigments. In another example, cephalopods utilize protein-rich pigments and self-assembled structures for dynamic adaptive coloration and camouflage. In total, biological materials display amazing optical properties and an extraordinary ability to manipulate light that range from specialized light absorption (molecular pigments) to reflection from highly reflective surfaces (cephalopod proteins) to photonic crystals (guanine crystals). Alternatively, nature also provides an abundance of exquisite structural biomaterials that lack true optical functionality, but through simple processing can be converted into high-quality optical biomaterials as highlighted below by silk, DNA, and cellulose-based biomaterials (Table 2). These biologically tuned optical properties rival those of conventional man-made optical materials obtained by traditional synthetic approaches in terms of spectral response. As a result, biologically inspired materials are highly appealing for optical applications that include optoelectronics, optogenetics, multifunctional photonic devices, biomedical imaging, light detection/sensing, light-responsive/adaptive coatings, photocatalysts, and as a means of photoprotection. In the following subsection, we will describe the biomimetic synthesis of melanin and guanine pigments exhibiting strong light absorption, the use of recombinantly expressed marine proteins to produce films with nanostructured optical gratings, and the processing of optically nonfunctional biomolecules (silk, DNA,

silk biomaterials (films, fibers, foams, hydrogels) DNA films cellulose artificial melanin pigments

fabrication method

refs

emission from blue (480 nm) to green (509 nm). Owing to its remarkable stability, the ability to fluoresce without any substrate or cofactor, and the fact that it is encoded by a single gene and can be added as a tag to other proteins, GFP has become one of the most widely used markers for monitoring gene expression and imaging.232 2.8.2.3. Bacterial Bioluminescence. Bactera utilize two substrates, a reduced flavin mononucleotide (FMNH2) and a long-chain aliphatic aldehyde (RCHO), which are oxidized by molecular oxygen and luciferase. The aldehyde is continuously produced by the bacteria, allowing for a persistent glow. Genomics analysis has shown that bioluminescent bacteria utilized the lux operon gene sequence to encode for the production of luciferase and its substrates. Although the gene sequences for luciferases from different species have variations, all are comprised of five core lux genes, luxCDABE, which encode for the basic requirements of light production. Some species also have regulatory genes, for example, the quorumsensing system that was first identified in Vibrio fischeri. Here, the bacteria continually synthesize a small molecule called an autoinducer. Once the autoinducer reaches a threshold concentration, the light-producing genes are switched on. This allows the bacteria to delay the high energy cost of bioluminescence until there are enough bacterial cells for the emitted light to be visible.232

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Figure 35. Biosynthesis of artificial biomelanin using chicken egg white. (A) Melanin precursors, including chicken egg white and dopamine. (B) Image of artificial biomelanin pigments. (C) Absorption spectrum of biomelanin showing an increase in absorbance. (D) Flexible film of plasticized biomelanin. (E) Electron paramagnetic resonance spectrum of melanin and artificial biomelanin from 0.01% and 0.1% (w/w) 5,6-dihydroxyindole. Reprinted from ref 238. Copyright 2014 American Chemical Society.

produced in chicken egg white exhibited an order of magnitude larger broad-band light absorption when compared to natural and synthetic eumelanin suspensions (Figure 35). These enhanced optical properties are expected to produce more saturated colors in materials. In an alternative synthetic approach, variants of natural melanin were synthesized by a chemoenzymatic method whereby di- and tripeptides containing tyrosine were oxidized by a tyrosinase enzyme to yield nanosized peptide-derived melanin.239 Peptide−melanin variants revealed a broad range of physiochemical properties that included distinctly different shades of brown pigments depending on the peptide sequence and extent of self-assembly, albeit with similar absorption maxima. The use of peptides during oxidative polymerization adds a functional element to melanin synthesis by introducing different peptide functional groups. Thin films of melanin were also prepared via a layer-bylayer solution-based method. In this approach, multilayers of cerium(IV) and polyphosphate were used to control surface oxidization of melanin precursors of 5,6-dihydroxyindole present in solution to produce a uniform, conductive, and high-quality film of melanin with 10 nm thickness.240 Similarly, thin films of dopamine-derived melanin were effectively deposited on a variety of substrate surfaces to achieve functional coatings. In this case, silica substrates were modified with well-defined surface chemistries (C18, phenethyl, and aminopropyl) and used to control the nucleation and growth of melanin films.241 Of all the strategies for the synthesis of melanin, the most common approach involves the autoxidative polymerization of dopamine monomers in the presence of ammonia.234,241,242 This simple and effective method generated single-component dopamine-derived melanin nanoparticles with excellent broadband absorption, a high refractive index of 1.741, and average sizes of 146 nm.234 In total, these properties are consistent with natural melanin and possess sizes similar to those of melanosomes found in ducks (120−170 nm) and peacocks (140−180 nm).243,244 Subsequently, synthetic melanin nanoparticles were assembled into structurally colored films using an

and cellulose) into optically active biomaterials. The subsequent subsections focus on bioinspired design and fabrication of higher order structures (nano- and microscale structures, periodic structures, and material structures with dynamic optical properties) that emulate the structure and optical functions of bio-optical materials. 3.1. Molecular Biomimetics

3.1.1. Pigment-Based Materials. 3.1.1.1. Synthetic Melanin Pigments. Naturally derived melanin pigments are highly admired for their strong optical absorption of UV and visible light as well as for the production of structural coloration displayed in bird feathers. In particular, the broad-band absorption of melanin produces saturated colors unlike polymeric particles which lack significant absorption of visible light.234 As discussed above in earlier sections, the structure and composition of natural melanin are complex and largely unknown. This is because of the complexity of melanin in its natural state, structural heterogeneity from chemical disorder, insolubility, a tendency to aggregate, and a general lack of biosynthetic detail at the molecular and cellular levels. Consequently, the goal of achieving a comparable biomimetic and synthetic analogue of melanin of similar biological quality is extremely challenging by current synthetic methodologies. As a result, there have been many different strategies aimed at controlling the biomimetic synthesis of an artificial melanin pigment. The mussel-inspired adhesive proteins of polydopamine can be used to produce highly cross-linked and polymerized melanin-like films that are strongly adherent to ceramic, metal, metal oxide, and semiconductor surfaces using a simple dip-coating procedure.235 Additionally, polydopamine films were modified and functionalized with antifouling agents, metal nanoparticles grown in situ, and enzymes to create multifunctional coatings.236,237 In these examples, the optical properties were uncharacterized. In another synthetic approach, the addition of ∼1% (w/w) 5,6-dihydroxyindole to chicken egg white resulted in the spontaneous oxidative polymerization of a black water-soluble biomelanin.238 Optically, the biomelanin 12739


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Figure 36. (A) Optical image of camouflage fatigues with uncoated tape and reflectin-coated tape and a plant leaf under visible light illumination. (B) Corresponding infrared image of the same camouflage under infrared light illumination. Reprinted with permission from ref 250. Copyright 2015 Royal Society of Chemistry.

evaporation-assisted self-assembly approach. This approach produced films of different colors and film thicknesses, including blue and red structurally colored films with thicknesses of ∼274 nm and 602 nm, respectively. In addition, synthetic melanin assembled thin films responded to changes in humidity with fast and reversible changes in structural coloration.242 Mechanistically, the humidity-induced dynamic color changes are due to the hygroscopic nature of synthetic melanin, an increase in film thickness due to swelling of melanin nanoparticles, and a change in thin-film interference. Color saturation of films was further enhanced by the addition of carbon black nanoparticles and reduction of incoherent scattering. 3.1.1.2. Synthetic Guanine Crystals. The superior reflective properties of biogenic guanine molecular crystals in nature are created from the formation of multilayer stacks of crystallized guanine nucleic acid bases as discussed in the previous section. Appropriately, the ability to harness the optical properties of a biomimetic form of guanine crystals is highly desired for their use as controllable organic micromirrors, in reflective coatings, and for solar reflectors. Unlike the complex nature and biosynthesis of melanin, the structure and biomimetic synthesis of guanine crystals are representative in morphology and reflective properties of the biogenic form that occurs in aquatic organisms. For example, to mimic the mesocrystal structure and orientation of thin plates of guanine molecular crystals in the skin of a banded blue sprat, guanine was recrystallized on a chitosan-modified substrate in the presence of organic molecule additives. Using this biomimetic approach, the recrystallization of guanine formed thin plates of guanine crystals that were

oriented parallel to the chitosan substrate and exhibited morphologies similar to those of biogenic guanine.245 Recently, it was shown that the reflective properties of guanine microcrystal platelets in terms of light reflection anisotropy could be attenuated using precise magnetic control.246 In this example, biogenic guanine crystals from goldfish scales with dimensions of 5 μm × 20 μm × 70 μm were magnetically controlled by applying a magnetic field (500 mT). The introduction of a magnetic field caused a change in crystal orientation and reflectivity, thus enabling reflectivity to be switched on or off. 3.1.2. Protein-Based Materials. 3.1.2.1. Reflectin Proteins from Cephalopods. Cephalopods display a remarkable ability to control dynamic camouflage and, at the same time, represent one of the best known examples of biological adaptive coloration in nature (refer to section 2.6). For these reasons, cephalopods have generated tremendous interest by the military for the design of biomimetic camouflage materials/ systems that are capable of modulating reflectance across the visible to near-IR spectrum. Also, the discovery of reflectin proteins from cephalopods has inspired the development of tunable optical materials, protein coatings that provide active infrared camouflage applications, and improvement of numerous optical devices such as electronic paper (e-paper).247 Reflectin proteins are compositionally and functionally different from reflective guanine biomaterials in marine and aquatic organisms. By comparison, they can elicit large volume changes upon condensation and possess a dynamic ability to modulate reflection. The unique optical properties of reflectin are generated upon the self-assembly of reflectin proteins into 12740


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Figure 37. Image of a free-standing silk film with patterned inverse opals with SEM images showing the green and blue silk opals. Reprinted with permission from ref 259. Copyright 2012 Nature Publishing Group.

flage coatings to arbitrary surfaces and shapes.250 In this example, infrared tunable camouflage in the form of a flexible tape adhesive sticker was applied to fabric surfaces and viewed by an infrared camera (Figure 36). The optical properties of reflectin-coated tape featured blue coloration with a maximum relectance occurring at 400 nm for a 64 nm thick film, and for a 163 nm thick film, the peak reflectance was shifted to ∼1063 nm.250 Similarly, the reflectance of the protein-coated tape could be reversibly shifted between visible and near-IR wavelengths by applying uniaxial strain to both ends of the tape as well as gentle heating. In this case, the strained tape exhibited enhanced reflectance at 705 nm, while the unstrained tape reflected light at ∼980 nm.250 In total, infrared camouflage protein coatings feature the ability to switch between visible and near-IR reflection, are vieweable by an infrared camera independent of the viewing angle, and are capable of responding to multiple stimuli (acidic vapor, mechanical strain). 3.1.2.2. Optically Active Silk Materials. Naturally abundant silk is a highly resilient and mechanically tough proteinaceous material exhibiting tensile strengths exceeding those of steel and Kevlar (tensile strength of 740 MPa).251 Consequently, silk is well-known and is widely utilized in composites, structural materials requiring high strength, and textiles because of its mechanical superiority. The mechanical strength of natural silk is due in part to its hydrophobic nature, β-sheet secondary structure forming units, presence of repeating glycine−X segments, where X = alanine, serine, threonine, or valine, inter- and intramolecular interactions involving hydrogenbonding and van der Waals forces, and high molecular weights (>400000). However, like most proteins in nature that serve a

precise nanostructures and Bragg-type diffraction gratings.153 Reflectin films were prepared by flowcoating a 15% (w/w) solution of reflectin/hexafluoroisopropyl alcohol (HFIP) to generate a gradient of different film thicknesses and spectral responses. In total, these films were shown to produce structural color on the basis of a thin-film interference mechanism and to respond to water vapor by shifting their reflectance. Similarly, a truncated version of the full-length reflectin protein from Euprymna scolopes was shown to selfassemble and form single-layer and multilayer thin films that displayed tunable color.248 To create protein coatings possessing infrared camouflage, thin films of reflectin proteins from the cephalopod Loligo pealeii were deposited on graphene oxide-coated substrates at various film thicknesses.249 Optically, this biological thin-film architecture exhibited a large tunable reflectance window of over 600 nm that could be reversibly modulated by exposure to acidic vapor. In response to acidic vapor, the protein films swelled and generated a new reflectance peak at 1200 nm. The acid-induced swelling mechanism of the reflectin films and near-IR reflectance were attributed to an increase in the positive charge on the protein.249 Qualitatively, the infrared camouflage properties of the cephalopod-inspired coatings were demonstrated as a proof or concept using an infrared camera. Using an infrared adapted camera, illumination of the protein-coated substrate by infrared light showed a relative brightness of 100% with exposure to acetic acid vapor and a loss of brightness and color without acid treatment. More recently, similar reflectinbased protein coatings were applied to transparent and flexible substrates of fluorinated ethylene propylene tape, thereby extending the utility and functionality of biomimetic camou12741


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I (PSI) were immobilized on a gold electrode surface in the dried state or onto a reduced graphene oxide electrode.262,263 In both cases, high current densities were achieved upon light illumination of photosystem I using planar electrode configurations. Alternatively, chlorophyll and photosystem II were embedded in an aqueous hydrogel matrix of conductively active agarose (used for gel electrophoresis) to form a new type of low-cost and flexible photovoltaic system utilizing an aqueous soft matter biocompatible material (Figure 38).264 In this

single highly specialized physiological function, naturally derived silk from spiders and Bombyx mori silkworms does not exhibit intrinsic optical functions or properties except for perhaps simple UV protection of developing silkworm larvae provided by silk cocoons and/or the innate transparency of finely spun spider webs used to capture unaware and unsuspecting prey. These last examples highlight the potential of silk as an optical biomaterial candidate. As a biomaterial for optical applications, silk possesses amazing mechanical properties as described above, but, at the same time, can also function as a high-quality optical biomaterial after simple processing. Silk fibers collected directly from Nephila edulis spiders were used as a superlens with a conventional white light microscope for imaging 100 nm features with a resolution of λ/6, while, in another example, unprocessed silk fibers were used as effective waveguides for delivering light over short distances.252,253 As highlighted by these examples, natural silk possesses the ability to act as a lens and waveguide in its unaltered state; however, the processability and ability to obtain a pure fraction of watersoluble silk fibroin have expanded the functionality of silk and enabled the fabrication of various exquisite optical materials based on a highly processable form of silk. The processing of naturally derived silk involves the use of lithium bromide or ionic liquid (1-butyl-3-methylimidazolium chloride) to produce soluble and pure silk fibroin fractions in water or HFIP at a high weight percentage that is devoid of sericin adhesive proteins.251 For example, processed silk films were shown to exhibit extremely large third-order nonlinear optical properties.252,254 In other examples of waveguiding, degummed and processed silk films (index of refraction 1.54) were encapsulated in a silk hydrogel (index of refraction 1.34) to create a step index optical waveguiding material,255 while a fiber with dimensions of 10 cm length × 5 mm diameter consisting of a silk foam core with 94% porosity and air as the cladding showed terahertz spectral responses.256 One of the best features of silk is its ability to be easily processed and patterned by photolithography, direct-write photolithography, conventional printing techniques, and/or nanoimprinting. For example, silk biophotonic materials in the form of a self-sensing optofluidic film were created by nanoimprinting degummed silk fibroin to contain grating structures with sub 50 nm spacings.257 Also, silk was micropatterned into 2D arrays with high fidelity and periodic structures using photolithography. The patterned silk structures displayed angle-dependent iridescence over large areas, while offering a mechanically stable and transparent film.258 Additional examples of patterned silk structures include an inverse opal 3-D photonic structure that displayed a pseudophotonic band gap and structural coloration (Figure 37) and the direct writing of silk-printed optical waveguides crystallized in a methanol coagulation reservoir.259,260 As an alternative to natural silk, silk-elastin-like polymers (SELPs) with molecular weights of 47000 were genetically engineered to possess both the mechanical toughness of silk and the elastic qualities of elastin proteins and processed into polymeric films. SELP films were processed via noncovalent cross-linking using methanol to yield high optical transparency (95%).261 3.1.2.3. Molecular Photosystems. The use of molecular photosystem complexes from plants and bacteria to harvest light with near perfect quantum efficiencies and provide fast charge separation has been an appealing biomimetic approach for photovoltaic applications. To obtain efficient energy conversion in a biomimetic device, multilayers of photosystem

Figure 38. (a) Photovoltaic architecture of photosystem II embedded in an aqueous hydrogel matrix of agarose. (b) Flexible photovoltaic device. (c) Photovoltage of chlorophyll or PSII devices with light illumination. Reprinted with permission from ref 264. Copyright 2011 Royal Society of Chemistry.

device configuration, PSII and chlorophyll operated under aqueous conditions to generate photocurrents of 0.2 μA/cm2 and photovoltages of 0.07 and 0.16 V, respectively. Moreover, the coupling of molecular photosystems to different active enzyme components provided a means of using light to drive an enzymatic reaction and address new pathways not present in nature. For example, photosystem II (PSII) was directly wired to a hydrogenase enzyme in an electrochemical cell for the quantitative production of H2 and O2 at a light to hydrogen conversion efficiency of 5.4%.265 This provided a semiartificial pathway for hydrogen and oxygen formation not accessible by nature. PSII was also coassembled with ATPase to create an artificial chloroplast for ATP synthesis using light and generation of a proton gradient from PSII-driven water splitting.266 3.1.3. Optically Active Nonprotein Biological Materials. 3.1.3.1. Genomic DNA as an Active/Passive Optical 12742


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Figure 39. Optically transparent nanofiber paper (shown on the left) and corresponding SEM image (upper left) of 15 nm cellulose nanofibers. Conventional cellulose paper (shown on the right) and corresponding SEM image of 30 μm pulp fibers (upper right). Reprinted with permission from ref 270. Copyright 2009 Wiley-VCH.

absorption in the final processed biomaterial. For example, wood in its natural form was delignified to remove all lightabsorbing lignin components and backfilled with an indexmatching prepolymerized methyl methacrylate (PMMA) to create optically transparent wood with an 85% transmittance.266 In this case, delignified and PPMA-impregnated wood maintained its original structural integrity, insulating properties, and mechanical strength, but with the added benefit of optical transparency. Similarly, nanofibrillated cellulose components obtained from plants and wood fibers were processed into single sheets of transparent nanofiber paper (Figure 39) and inverted organic photovoltaic devices.270,271 Both examples of nanofibrillated cellulose displayed excellent optical performance as a transparent biomaterial and photovoltaic. Additional forms of cellulose with promising optical characteristics and structures include nanocrystalline cellulose and bacterial nanocellulose. Notably, both forms of nanocellulose can be processed as films, biofoams, and/or aerogels.272 For example, nanocrystalline cellulose was mixed with guar guam to produce a highly transparent, water-soluble, barrier layer against oxygen.273 Additionally, the rodlike anisotropic structures and liquidcrystalline nanocrystalline cellulose whiskers were shown in composite materials to display iridescence, polarization, and birefringence when elongated.274 As an example of an application, the unique liquid-crystal behavior of nanocrystalline cellulose to form a chiral nematic phase was exploited in nanostructured films for optical encryption and anticounterfeiting measures and to impart covert functionality.275,276 In these optically encrypted materials, nanocrystalline cellulose strongly reflected left-handed circularly polarized light and was effectively tuned by increasing the chiral nematic pitch of nanocrystalline cellulose by addition of an optical brightening agent.276

Component. DNA represents the molecule of life and is critical to the construction and storage of the genetic code in all living organisms. The sequence of DNA is used to program cellular functions, for transcription and translation of proteins, and ultimately to transfer hereditary traits to offspring. These genetically encoded features as well as the general material properties of DNA (thermal stability limit 200−250 °C) have been successfully used to mediate nanoparticle assembly, create nanoparticle superstructures, assemble unique origami structures of DNA, and to a much lesser extent form optically active films. Consequently, we will briefly highlight the recent and limited work utilizing DNA as a passive and active optical material for integration with photonic devices. As an optical biomaterial, DNA features a high optical transparency with low optical loss (100% transmission), a dielectric constant of 7.8 at low frequencies for a 200 nm thick film, and an index of refraction that varies from 1.535 to 1.48.267 Additionally, abundant sources of genomic DNA are readily available as waste material from salmon that can be simply processed into a pure DNA−surfactant complex. For these reasons, DNA complexed with cetyltrimethylammonium surfactants have been utilized to boost light emission in BioLEDs by serving as a combined electron-hole-transporting and electron-blocking layer.268,269 In this optical configuration, DNA increased the quantum efficiency to 4% and overall brightness (∼6580 cd/ m2), in addition to significantly enhancing the color purity. 3.1.3.2. Cellulose-Based Optical Materials. The polysaccharide of cellulose comprises the cell walls of all plants and algae and, as a result, is the most abundant biomolecule on earth. Consequently, the biological significance of cellulose is to provide structural properties to biological systems (2−3 GPa), but in its native state, it does not possess any defined optical functions in nature.270 However, like silk biomaterials discussed above, cellulose can be biomimetically processed and converted into an optically active material by reducing light scattering and 12743


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Figure 40. (A) Optical microscopy images of the alumina replicas of butterfly wing scales. The color change from original blue to pink is indicative of the increase in thickness of the alumina layer. (B) SEM image of the alumina replicas of the butterfly wing scales on a silicon substrate after the butterfly template was completely removed. (C) Higher magnification of the SEM image showing fine structures of the wing on the alumina replica. The inset shows two broken rib tips on the replica. (D−F) TEM images of the replicated alumina scales. The higher magnification images show (E) the hollow periodic lamella structure and (F) a broken edge of the lamella showing the hollow channel under the ribs. (G) Reflectance spectra of the original butterfly wings, alumina-coated wings, and alumina replicas in the UV−visible light range. (H) SEM image of the replica structure with a bifurcated lamellar structure. (I) Corresponding dark field optical microscopy image showing the potential application as a beam splitter. Reprinted from ref 13. Copyright 2006 American Chemical Society.

3.2. Bioinspired Periodic/Aperiodic Structures

the annealing process, the amorphous inorganic layer is gradually crystallized into a more robust polycrystalline shell. As mentioned earlier, the ALD technique provides the feasibility to precisely control the thickness during deposition on micro- and nanoscale features of the biotemplates.282 Due to the atomic scale deposition of the inorganic layer, the intricate nanoscale features of the wing scales are preserved (Figure 40B−D). Furthermore, the hollow ribs, subribs, and even the thin film in the inter-rib spaces can be easily distinguishable (Figure 40E,F). The structure formed by template-assisted fabrication can be viewed as an inverse two-dimensional (2D) photonic crystal, where the periodic air spaces are confined and surrounded by a dielectric outer shell. Furthermore, due to precise replication of the structure of the photonic material, the optical properties of the wing scales are retained in the inorganic replica. The alumina replica, which has the inverse structure of the butterfly wing scales, has the same reflection spectrum as that of the butterfly wing scale (Figure 40G) with a reflection peak at ∼420 nm. The biomimetic two-dimensional photonic crystals (PCs) can be used as waveguides due to their ability to guide and focus light with high efficiency, which is essential in optical communications and computing. The light-propagating traces indicate the arrangement of the lamellar rows perpendicular to the observing plane (Figure 40H,I). Interestingly, the split of the lamella, observed when the scale becomes wider, indicates the configuration of a beam-splitting device at the nanometer scale. The arrangement of waveguides and beam splitters can potentially result in a complex photonic integrated circuit with improved efficiency.13 The design of alternate approaches for the fabrication of biomimetic photonic structures calls for the careful understanding of the features and their function. As described in the preceding section, in the Morpho class of butterflies, the high reflectivity and the lack of coloration are attributed to both

3.2.1. Photonic Crystals. Due to the remarkable biomaterial structures employed by biology to create interesting optical effects, a multitude of research in biomimetic photonic engineering has escalated.19,20 As described in the preceding section, a remarkable collection of micro- and nanoscale structures are found in nature that can be used as templates for the fabrication of a wide range of photonic materials.277,278 Template-assisted replication using well-developed and finely engineered structures in nature as templates is an attractive method for the fabrication of inorganic biomimetic photonic materials.13,279−281 The use of natural structures as templates to achieve synthetic replicas can be simple, highly reproducible, and inexpensive. These synthetic structures can be designed to mimic the micro- and nanoscale structure and function of the biological templates while preserving their inherent material properties (e.g., mechanical, thermal, and chemical) absent in the biological counterparts. One of the examples for biotemplating is utilizing the atomic layer deposition (ALD) technique to replicate the intricate structural features of butterfly (Morpho peleides) wing scales.13 ALD is a particularly attractive technique for the replication of complex three-dimensional structures owing to self-limiting deposition, high conformality, non-line-of-sight deposition, and precise control of the thickness of the film with the number of deposition cycles. In the case of wing scale replication, the thickness of the deposited inorganic layer (alumina) determines the reflected color of the wing scales (Figure 40A). The wavelength of the reflected light from the film is red-shifted after the atomic layer deposition due to the increase in the refractive index associated with a thick alumina film. Following the deposition of an inorganic layer, the template is removed by annealing the samples to burn the organic templates. During 12744


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Figure 41. Schematic view of the principles of the Morpho butterfly: (A) side and (B) top views. (C) SEM image of a quasi-one-dimensional pattern on a quartz substrate, fabricated by electron beam lithography and dry etching. (D) Morpho structure emulated by deposition of a TiO2/SiO2 multilayer on the nanopattern. (E) Photograph of Morpho didius and replicated Morpho blue (left, protoype; right, plate fabricated by the nanoimprinting method). (F) Cross-sectional SEM image of the reproduced Morpho structure (TiO2/SiO2 multilayer on a quartz plate). Comparison of the measured angular dependence of the reflectivity from normal incidence white light in (G) M. didius and (H) a reproduced Morpho film. (I, J) Scanning ion microscopy image of the Morpho butterfly scale quasi-structure fabricated by FIB-CVD. (K) Optical microscopy images of the Morpho butterfly scale quasi-structure observed with a 5−45° incidence angle of white light. Reflection spectra of (L) Morpho butterfly scales and (M) the Morpho butterfly scale quasi-structure. Reprinted with permission from ref 14 (copyright 2009 SPIE) and ref 15 (copyright 2005 Japanese Society of Applied Physics).

interference and diffraction due to the proficient arrangement of ordered (regular) and disordered (irregular) optical nanostructures.64 The arrangement of the nanoscale features in a single scale is responsible for (i) interference from a single shelf to determine the wavelength of the reflection, (ii) diffraction limited to a small width on the order of one wavelength, (iii) randomness in height to preclude the interference of light scattered from neighboring discrete pieces, and (iv) a narrow gap to provide high reflectivity and prevent transmission (Figure 41A,B).14 These structures can be fabricated by using electron beam lithography and dry etching by fabricating a multilayered structure composed of alternating layers of high and low refractive index on a nanopatterned surface (Figure 41C,D). In the multilayer deposition process, metal oxides are most commonly employed due to the ability to precisely control their thickness and the variability in their refractive indices.283 The fundamental characteristics of the Morpho blue wing scales feature the brilliant blue with high reflectivity, a wide angular range of a single color, onedimensional isotropy of the brilliance, and a smooth hue, which can be reproduced in the synthetic film (Figure 41E). Furthermore, the optical characteristics (angular dependence of reflection) of the reproduced film are comparable to those of the Morpho blue wing scales (Figure 41G,H).

Another nanofabrication technique to fabricate three-dimensional nanostructures is focused-ion-beam chemical vapor deposition (FIB-CVD), which can be used to fabricate the Morpho butterfly scale quasi-structure.15 The fabrication procedure involves the design of a three-dimensional mold using computer-aided design as an FIB scanning apparatus. The Morpho butterfly scale quasi-structure can be made using diamond-like carbon with a reflection peak close to 440 nm to replicate the optical characteristics of a Morpho butterfly scale (Figure 41I,J). The optical microscopy images of the quasistructure with the light incident angle ranging from 5° to 45° suggests that the brilliant blue reflection from the quasistructure occurs for a wide range of incident light angles (Figure 41K). The comparison of the reflection spectra of the Morpho butterfly scale and the quasi-structure suggests that their optical characteristics are comparable (Figure 41L,M). Due to the unique optical response of biomimetic photonic structures based on Morpho butterfly, they have been utilized for vapor-sensing applications.284 Bioinspired photonic materials that mimic the reverse colororder diffraction can be designed by understanding the optical principles underlying the natural structural color in Pierella luna. The presence of periodic arrays of vertically oriented microdiffraction gratings is essential for the reverse color-order 12745


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Figure 42. Geometry and optical properties of the artificial photonic structures mimicking Pierella luna with vertically oriented (top) and tilted (bottom) diffraction gratings. (A) SEM image of the array of scalloped microplates (scale bar 5 μm). (B) SEM image of an individual plate with regular scallops (scale bar 2 μm). (C) Variable-angle spectroscopic data for 45° light incidence showing the arc-shaped diffraction pattern caused by the diffraction from the scallops coupled with the diffraction due to the plates. Inset: measurement geometry. (D) Top: diffraction pattern caused by the periodic ensemble of microplates for 45° light incidence. Bottom: diffraction patterns resulting from scallops on individual plates. The diffraction order within blue and yellow frames corresponds to the diffraction observed in the angular range marked in blue and yellow, respectively. (E−H) Same as (A)−(D) for titled angles. Reprinted with permission from ref 6. Copyright 2014 National Academy of Sciences.

Figure 43. (A, B) The bright green wings of the Papilio blumei butterfly result from the mixing of the different colors of light that are reflected from different regions of the scales found on the wings of these butterflies (scale bars (A) 1 cm and (B) 100 μm). (C) Optical micrographs (scale bar 5 μm) and (D) scanning electron micrograph (scale bar 2 μm) showing that the surface of a wing scale is covered with concavities (diameter ∼5−10 μm) that are arranged in ordered lines along the scale. (E) Sample fabrication procedure. (F, G) SEM images of concavities covered by a conformal multilayer stack of alternating layers of titania and alumina: (F) top view (scale bar 2 μm) and (G) cross-section (scale bar 1 μm). (H) Under a light microscope, the concavity edges appear turquoise, and the centers and interstitial regions are yellow (shown on the left) and between cross-polarizers (shown on the right). (I) Spectral maps for λ = 450 nm showing the anisotropic reflectivity of the concavities for unpolarized light (shown on the left) and between crossed polarizers (shown on the right). Reprinted with permission from ref 285. Copyright 2010 Nature Publishing Group.

possibilities of tailoring the interaction of light beyond the diffraction induced by scallops of plates (Figure 42A,E). The light incidence angle θI is fixed and the observation angle θD is varied in the plane of light incidence to capture light reflected in an angular range of ±75° around the sample surface normal:

diffraction (as discussed in section 2.2.2). The microdiffraction gratings are formed using multiple etching and passivation steps in conjugation with photolithography to give rise to periodic undulations on the microplate surface.6 The pitch and height of the gratings can be controlled by controlling the etching parameters. Positive replicas of the silicon master are cast using soft-lithographic techniques from a negative poly(dimethylsiloxane) (PDMS) mold using a UV-curable epoxy. The individual microdiffraction gratings in the artificial system are intentionally arranged in a highly periodic manner to result in a higher diffraction signature and provide additional

λ=

d (cos θI + cos θD) m

where d is the grating periodicity, m is the diffraction order, θI is the light incidence angle, and θD is the diffraction angle. The equation describes the arc-shaped pattern observed in the 12746


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Figure 44. (A) Tubes containing gibbsite platelets (σD = 17%) at various concentrations under cross-polarizers. From left to right, the concentration (ϕ) ranges from 0.19 (I + N) to 0.28 (N), 0.41 (N + C), and 0.47. (B, C) Transmission electron microscopy images of gibbsite platelets: (B) σD = 25% and (C) σD = 17%. (D) Phase diagram of the suspensions with the relative volume of the nematic and columnar phases depicted after phase separation as a function of the platelet volume fraction ϕ. (E) SEM image of large arrays of well-aligned helical ZnO on the top of base ZnO rods. (F) High-magnification SEM image of two long helical ZnO nanorods. (G) Surface of the helical columns of the well-defined hexagonal platelike structures. (H) Layered structure in the helical columns. Reprinted with permission from ref 294 (copyright 2000 Nature Publishing Group) and ref 16 (copyright 2002 American Chemical Society).

alternating layers of cuticle and air to create an intense structural color (Figure 43A,B).285 The bright coloration is due to the juxtaposition of blue and yellow-green light reflected from different microscopic regions on the wing scales. The wing scales have concavities with centers (yellow) and edges (blue) that are 5−10 μm wide clad with a perforated cuticular multilayer (Figure 43C).65 Light from the center of the cavity is directly reflected, while the light incident on the concave edges undergoes retroreflection, resulting in double reflection off the cavity multilayer that results in geometrical polarization rotation.286 Understanding the structural features of the P. blumei wing scales enables the replication of the biomimetic photonic system. The biomimetic replication to form a periodically shaped multilayer has been demonstrated using soft lithography.285 The replication process involves (i) the deposition of polystyrene colloids on a gold-coated silicon substrate, (ii) growth of platinum or gold in the interstices of the colloidal array by electroplating, (iii) removal of the polystyrene spheres from the substrate by ultrasonication in acetone, and (iv) sputtering of a thin carbon film and ALD of a stack of

variable-angle spectroscopy measurements on vertical plates (Figure 42C). For a given angle of incidence θI, the diffraction caused by the periodic ensemble of plates is most clearly observed when the specular reflection θD = −θI. The tilt angle β relative to the surface normal results in the diffraction grating equation being reformulated as λ=

d (cos(θI − β) + cos(θD − β)) m

From the arc-shaped intensity distribution across the different diffraction orders in variable-angle spectroscopic data (Figure 42G), the tilt angle of the plates relative to the surface normal can be computed as β ≈ 23°, which is in agreement with the angle measured from the SEM images. The agreement in experimentally observed tilt angles suggests that a mechanistic understanding of the diffraction patterns can be made feasible in the replicated biomimetic structures, which is not possible in microdiffraction gratings of the butterfly wings. Certain classes of butterflies such as Papilio blumei and Papilio palinurus have intricate structural features that consist of regularly deformed multilayer stacks that are made of 12747


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Figure 45. (A) TEM image of negatively stained cellulose nanocrystals (CNCs) (scale bar 200 nm). (B) Schematic of the synthesis of chiral nematic silica from CNCs and tetramethyl orthosilicate (TMOS). (C) Polarization optical microscopy image of the CNC−silica composite showing the characteristic fingerprint-like structure showing the formation of a chiral nematic phase. (D) Optical images of mesoporous organosilica films (scale bar 18 mm). (E) UV−vis transmission spectra (solid line) and CD spectra (dashed line) of chiral mesopourous organosilica films. (F) SEM image of the cross-sectional view of chiral nematic mesoporous silica revealing a left-handed chiral nematic structure. (G) Photograph of chiral nematic ethylene-bridged organosilica films showing the uniformity. (H) SEM images of chiral nematic titania films. (I) Cyclic voltammogram of a symmetric capacitor setup with cellulose nematic mesoporous carbon (CNMC). Reprinted with permission from ref 299 (copyright 2012 American Chemical Society), ref 303 (copyright 2010 Nature Publishing Group), ref 309 (copyright 2015 John Wiley and Sons), ref 304 (copyright 2011 John Wiley and Sons), and ref 305 (copyright 2012 John Wiley and Sons).

3.2.2. Helicoidal Structures. Over the course of evolution, nature has evolved to perceive circularly polarized light by developing sophisticated helicoidal architectures made up of chitin, cellulose, and collagen (refer to section 2.5). Inspired by the periodic helicoidal structures found in nature, various synthetic helicoidal structures have been explored.288−290 Chiral molecules undergo self-templating assembly because of multiple kinetic factors that influence the assembly of incoming building blocks to produce nonequilibrium structures. The fabrication of helicoidal structures has been inspired by the selfassembly of supramolecular structures found in natural materials. A liquid-crystalline phase in a material has the physical attributes of a liquid, but its molecular units have ordering at the domain scale, giving rise to anisotropy. Due to their tendency to order, liquid crystals assemble to form supramolecular structures. Liquid crystals can be classified into three main classes, nematic (N), columnar (C), and smectic (S). While each of these phases exhibits a long-range orientational order, the smectic phase is characterized by a one-dimensional periodic array of layers of particles and the columnar phase has

alternating titania (TiO2) and alumina (Al2O3) layers (the arrow indicates the precursor gas flow). Alternatively, (v) the polystyrene colloids are molten to cover the cavities with a homogeneous film (vi) followed by covering by a TiO2−Al2O3 multilayer (Figure 43E). The artificial mimic contains multilayer concavities with alternating layers of titania and alumina (Figure 43F,G). The choice of materials and the layer thickness determines the optical characteristics of the multilayers (the quarter-wave stack with a stopband center wavelength in the green-yellow spectral range to match the reflectance spectra of the natural Papilio structure closely). The artificial multilayered patterns also exhibit a color variation from the concavity centers to their edges similar to that of the natural structures (Figure 43H). Furthermore, between cross-polarizers, the local surface normal of ∼45° gives rise to a double reflection at the opposing cavity walls, causing the polarization rotation (Figure 43I).287 The light at the edges is blue-shifted relative to the light reflected from the center of the concavities. Thus, the artificial multilayered pattern displays the same optical characteristics as that of the natural P. blumei wing scale structure. 12748


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Figure 46. (A) Hetero-PBG structure with an anisotropic layer sandwiched between two L-helical CLC layers with the same pitch and showing total reflection. (B) Two dispersion curves of left circularly polarized (LCP) light for CLC1 and CLC2. (C) Dispersion curves for a hetero-PBG structure with an anisotropic layer. (D, E) Transmission spectra of OHAS: (D) forward and (E) backward curves with circularly polarized handedness the same as and opposite that of the CLC helix indicated by solid and broken curves, respectively. The insets show the dispersion of the OHAS through circularly polarized light with the handedness the same as (shown on the left) and opposite (shown on the right) that of the CLC helix. Reprinted with permission from ref 310. Copyright 2005 Nature Publishing Group.

44G,H). A similar phenomenon is reported in the chiral crystal growth of calcium carbonate (calcite) when chiral molecules such as aspartic acid and polyaspartate are used to mediate mineral growth.296 Liquid-crystalline phases have also been observed in many natural sources (lipids, cellulose, and DNA) that are sustainable alternatives due to the high abundance and biocompatibility.297 The organization of cellulose microfibrils plays a key role in plant morphogenesis due to their arrangement in a helicoidal pattern around the cell that directs anisotropic cell expansion.298 Cellulose nanocrystals (CNCs) derived from sulfuric acid-catalyzed hydrolysis of bulk cellulose are used for biomimetic self-assembly to fabricate helicoidal structures (Figure 45A). A chiral nematic organization of CNCs is realized by evaporation-induced self-assembly (EISA) under thermodynamic (equilibrium) control in solution.299 The chirality of CNCs arises from the asymmetric carbon atom on D-glucose at the molecular level, the screw-shaped morphology of individual crystals at the nanoscale, and the left-handed chiral nematic long-range order of the lyotropic liquid-crystalline phase.300 Due to the inherent chirality, CNCs have the ability to form photonic crystals with a periodically changing refractive index in one, two, or three dimensions that can selectively diffract light.301 The reflected light depends on the pitch (P) of the chiral nematic structure and the refractive index (ηav) of the material. The selective reflectance is given by302

a two-dimensional lattice of periodic arrangement. The formation of liquid crystals in concentrated suspensions of particles is driven by a gain in excluded volume entropy.291 Polydispersity (σD) in the particles will affect the positional ordering due to the variability in the lateral dimensions. Theoretical models of a dense system of rods suggest that polydispersity in the rod length of 18% will yield a stable smectic phase while a higher polydispersity will result in a columnar phase.292 On the other hand, hard-plate-like particles exhibit an isotropic (I) phase, an N phase, and a C phase upon increasing the concentration of the platelets.293 One such example is the assembly of a suspension of monodisperse colloidal particles with nonspherical shapes (such as rods and plates) due to the ability to form liquid crystals.294 The platelets are gibbsite (Al(OH)3) colloids whose surface is grafted with modified polyisobutylene (Figure 44A). Owing to a stabilization layer, the particles interact through a short-range repulsive interaction potential when dispersed in apolar solvents.295 The monodisperse platelets of gibbsite can self-assemble to form an I, an N, or a C phase by increasing the concentration of the platelets during self-assembly (Figure 44B).294 Isotropic−nematic phase coexistence is observed at ϕ = 0.2, yielding an isotropic upper phase and a birefringent nematic bottom phase. Upon increasing the plate volume fraction to roughly twice the I−N coexistence density, ϕ ≈ 0.4, the suspension enters a biphasic region where a nematic upper phase coexists with a columnar phase (Figure 44C). On the basis of the reflections for wavelengths of visible light, the crystalline order pertains to the periodicity on a length scale of the plate diameter (characteristic of columnar ordering) rather than the much smaller plate thickness (as in smectic ordering). Another example of inorganic materials that exhibit unusual extended and oriented helical ordering is ZnO nanorods.16 The morphology of ZnO nanostructures shows remarkable resemblance to the growth morphology of nacreous calcium carbonate in red abalone (gastropod Haliotis rufescens). The hexagonal surface (002) of the ZnO crystals is used to grow precisely aligned ZnO nanorods (Figure 44E,F). Furthermore, the structure of the aligned ZnO nanorods is composed of vertically layered structures in the helical ZnO columns (Figure

λmax = ηav P sin θ Due to the chiral long-range order, light reflected from the chiral nematic liquid crystal is circularly polarized with a handedness that is determined by the helicoidal orientation of the liquid crystal. To fabricate functional materials based on cellulose nanocrystals, template-assisted synthesis of silica using cellulose liquid-crystal templates has been used.303 The silica− CNC composite yields a reflected wavelength λmax varying between visible to near-infrared by varying the relative concentrations of the silica and CNC (Figure 45B). The similar refractive indices of the silica and CNC (ηSiO2 = 1.46 and 12749


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Figure 47. (A) Photograph of the weevil Lamprocyphus augustus and an optical image of its green-colored photonic scales (inset) (scale bar 200 μm). (B) SEM image of cross-sectional views of the beetle intrascale biopolymeric photonic structure (scale bar 1 μm). (C) SEM image of the inverse structure of the beetle photonic lattice made of hybrid silica (scale bar 1 μm). (D) SEM image of a titania replica of the original beetle photonic structure templated from an intermediary hybrid silica structure (scale bar 1 μm). SEM (E) cross-sectional view and (F) titled view of the biotemplated diamond-based tiania photonic crystal lattice along the Γ−L (111) direction (scale bar 1 μm). (G) Calculated band structure diagram of a high-dielectric (RI of 2.3) PC with a diamond-based lattice derived from the beetle L. augustus. (H) Angle-dependent reflectance of a titaniareplicated structure at normal incidence (black), −15° off-normal (blue), and +15° off-normal (red). Reprinted with permission from ref 312. Copyright 2010 John Wiley and Sons.

ηCNC = 1.54) suggest that the observed increase in the λmax for samples with higher silica content is due to the increase in the pitch P caused by a greater silica wall thickness and the repulsive interactions between the negatively charged silica species and cellulose nanocrystals during the condensation process (Figure 45D,E). The removal of cellulose templates by calcination of the composite film at 540 °C under air results in a free-standing mesoporous silica film (Figure 45B). The calcined films result in a blue shift in the reflection spectrum of about 300 nm attributed to the removal of cellulose during pyrolysis, which results in iridescent silica films that reflect light at different wavelengths across the entire visible spectrum (Figure 45D,E). The structure of the chiral nematic mesoporous silica reveals a left-handed chiral nematic structure (Figure 45F). The silica-based approach can be extended to other sol−gel precursors, (RO)3Si−R′−Si(OR)3 to produce periodic mesoporous organosilicas that are flexible due to the ethylene-bridged organosilica (Figure 45G).299 The mesoporous silica templates can be used to synthesize functional materials using titania, zirconia, silver nanoparticles, and quantum dots.304−308 The hard-templating approach can also be used in the fabrication of mesoporous carbon, which is a promising material for chemical capacitors, catalyst supports, and field-effect transistors. An interesting example of using biomimetic helical assemblies is the development of an optical heterojunction anisotropic structure (OHAS) consisting of an anisotropic layer sandwiched between two polymer layers with different periodicities of the helix (heterophotonic band gap (PBG)) to obtain an optical diode effect (Figure 46A).310 A half-wave phase retarder layer made of a planar nematic liquid crystal (NLC) is sandwiched between two PBG cholesteric liquid crystal (CLC) layers with the same sense of helix handedness but different pitches (P1 < P2). The dispersion relations for forward and backward propagation of light are readily obtained by introducing an anisotropic dielectric tensor that depends on

the propagation direction as well as on the position. For CLCs, the band gaps are the same for forward and backward propogations; there is no optical diode effect (Figure 46B). For a hetero-PBG structure with anisotropic layers, the spectral position of PBGs depends on the direction of light propogation, showing optical diode performance for nonreciprocal transmission (Figure 46C). For the transmission at 500 nm, the film is opaque for forward propagation, while it is transparent for backward propagation, demonstrating the optical diode characteristics. The optical diodes thus created are electrotunable due to the variability of Δη of the NLC anisotropic layer. The transmission spectra were measured for the fabricated OHAS cell in both forward and backward propagation directions and for a circularly polarized light with handedness the same as (solid curve) and opposite (broken curve) that of the CLC (Figure 46D,E). Furthermore, the dispersions of the OHAS for forward and backward propagating circularly polarized light are the same in opposite circular polarizations. 3.2.3. Opal/Inverse Opal Structures. The striking colors produced by various insects are a result of grating-like morphologies, multilayered structures, and elaborate threedimensional structures.57 The lattice structure of a brilliantly green beetle weevil, Lamprocyphus augustus, is a result of exoskeletal scales with a complex diamond-based PC structure arranged in a pixel-type array of selectively oriented singlecrystalline domains (Figure 47A,B).311 The biopolymeric photonic crystals have refractive indices (RIs) of 1.5−1.6, which are too low to open a complete photonic band gap, and can potentially be manipulated into high-dielectric materials by utilizing the biopolymeric photonic crystals as unique structural templates to fabricate inorganic photonic crystals. The replication of a three-dimensional photonic lattice of L. augustus has been achieved by a double-imprint biotemplating route.312 The choice of the material to create an inverse original biopolymeric beetle photonic structure is critical to ensure that 12750


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Figure 48. (A) Photograph of antifogging mosquito eyes. (B) SEM image of a single mosquito eye. (C) SEM image of the biomimetic hexagonal close-packed (hcp) PDMS microhemispheres and silica nanospheres mimicking the mosquito compound eyes. (D) Spherical water droplet on the artificial compound-eye surface showing the antifogging properties of the compound eye. (E, F) SEM images of biomimetic antireflective surfaces showing the tilted top view (H) and cross-sectional view (I) of antireflective silicon nanotips. Reprinted with permission from ref 315 (copyright 2007 John Wiley and Sons) and ref 235 (copyright 2007 Nature Publishing Group).

“ommatidia” that have light-diffracting facet lens (Figure 48A,B).314 The ommatidia are almost hemispherical and are spherically arranged along a curvilinear surface in a hexagonal pattern (Figure 48B). The surface of the ommatidia is not smooth but is covered by highly packed nanosized protuberant hemispheres that act as gratings to enhance the light absorption of the eyes. The surface of the compound eye can be replicated by utilizing the compound eyes as biological templates for the fabrication of light diffraction facet lens. The deposition of alumina (Al2O3) by ALD on the surface of the compound eye, followed by the removal of the original eye template by annealing, results in the formation of a biomimetic alumina replica. The annealing also results in the gradual crystallization of the amorphous alumina layer into a robust polycrystalline structure. The replicated structure retains the optical properties of the compound eye structure, which is evident from the reflectance spectra measured on the alumina replica and the surface of the compound eye. Furthermore, the design principles employed by biology in designing the structure of compound eyes can be utilized to design advanced material structures. The antifogging properties of the mosquito eye arise from the microscopic structure and morphology of the compound eye.315 The heterogeneous curved surfaces composed of air and solids in hierarchical micro- and nanostructures are responsible for the surface wettability with superhydrophobic characteristics. The intricate design is rather difficult to mimic using conventional fabrication techniques. The air trapped between spaces between the nanonipples and microhemispheres to form a stable air cushion acts as an effective water barrier, reducing the contact of tiny fog drops with the eye surface. The surface of a mosquito compound eye can be mimicked by the fabrication of a nanonipple structure on the surface of arrayed microhemispheres by soft lithography.315 The pattern is fabricated by

the overall shrinkage of the lattice constant is less than 5%. The inverse of the original biopolymeric beetle photonic structure is created by a silica-based sol−gel chemistry route.312 The inverse of a single scale of L. augustus is created by infiltrating an organic/inorganic precursor solution of SBA-type hybrid silica due to its superior structural properties (minimized crack propagation and framework collapse) upon drying followed by acid etching of the template (Figure 47C). The inverse structures have an accessible framework to create a subsequent titania replica of the original diamond-band structure. The silica framework is infiltrated with an acid-stabilized titania sol−gel precursor to induce dense titania nanocrystallization.312,313 The acid etching of the silica template results in the formation of a high-dielectric framework of a titania (measured refractive index of 2.3) based photonic crystal with lattice periodicities corresponding to the visible wavelength (Figure 47D). The structure of the titania replica with the diamond lattice was preserved with ABC stacked layers of hexagonally ordered air cylinders in a surrounding titania matrix (Figure 47E,F). The calculated band structure diagram revealed a 5% wide complete photonic band gap (Figure 47G). The reflectance spectra of a natural biopolymeric PC exhibited three distinct features from the individual Γ−X, Γ−K, and Γ−W directional stop gaps, which overlap in the high-dielectric titania replica into a single, nearly featureless angle-independent reflection peak (Figure 47H). The approach of using a high-dielectric material to fabricate biomimetic photonic crystals enables the development of new optical phenomena based on photonic band gaps at visible frequencies, which is not feasible with low refractive index biopolymeric photonic crystals. 3.2.4. Antireflecting Surfaces. Compound eyes in the insect world present attractive physiological optics in high sensitivity and antireflection (refer to section 2.3.2). The compound eye consists of thousands of small eyes called 12751


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Figure 49. (A) Schematic diagram of a photonic gel film and the mechanism of color tuning. (B) SEM image of a dry PS-b-QP2VP lamellar photonic film deposited on a silicon wafer. The inset shows a TEM image of the stained lamellar film (shown on the left) and a reflection mode laser scanning confocal microscopy (xz scan) image of the film defect channels (shown on the right). (C) Environmental SEM micrographs of the film at different humidity levels. (D) Ultraviolet−visible−near-infrared absorbance spectra of PS-b-QP2VP photonic gels with different concentrations of NH4Cl aqueous solution. The gray region represents the visible wavelength region. Reprinted with permission from ref 17. Copyright 2007 Nature Publishing Group.

transfer lithography by a two-step soft lithography and stamp transfer using SiO2 nanospheres to mimic the structure of a mosquito compound eye (Figure 48C). Due to the intricate structure and morphology, the surface of the artificial biomimetic compound eye is water-resistant. As a result, the surface of the artificial counterpart is very hydrophobic (Figure 48D). Antireflecting surfaces can also be made using aperiodic, randomly arranged features that reduce the reflected light from the surface. A large-area biomimetic silicon nanotip can be fabricated using high-density electron cyclotron resonance (ECR) plasma etching (Figure 48E,F).235 The reflectance of these randomly positioned silicon nanotips is lower than that of the conventional multimaterial films over a broad range of wavelengths.316

The color change triggered in these organisms has a low response time (a few seconds to a minute) and is reversible (for multiple cycles), which are critical parameters in designing a synthetic analogue. Understanding the biological mechanisms of tunable structural color can provide effective solutions toward the bioinspired design in the development of responsive optical materials. Bioinspired optically responsive materials induce a change in the structural color in response to an external trigger (pH, ionic concentration, mechanical strain, and temperature).320−324 The choice of the functionally responsive materials in a photonic material is determined on the basis of the external trigger required to induce a change in the structural color. An example of biomimetic color tuning is a photonic gel prepared by the self-assembly of a diblock copolymer, polystyrene-b-quaternized poly(vinylpyridine) (PS-b-QP2VP).17 The block copolymer lamellar stack consists of alternating nonswellable glassy block layers and polyelectrolyte block gel layers (Figure 49A). The swelling and deswelling of QP2VP gel layers by aqueous solvents modulates both the domain spacing and the refractive index contrast to shift the wavelengths of light (hν) reflected by the stopband. The diblock copolymer has a well-ordered structure with periodic layers parallel to the substrate and a microdomain periodicity with equal thicknesses of each layer (Figure 49B). The QP2VP domains in the diblock copolymer are swollen in high-humidity environments, resulting in an increase in the thickness of up to 550% (Figure 49C). Due to the low domain spacing and refractive index contrast (ηPS ≈ ηP2VP), the dry photonic gel film does not have a stopband in the visible range of wavelengths (the film is transparent). Upon immersion in water, the film exhibits a color dependent on the degree of cross-linking. The swollen polyelectrolyte gel can be collapsed by osmotic deswelling in salt solution.325 As the salt concentration decreases, the primary stopband is shifted to

3.3. Responsive Materials

The design of materials that can dynamically change their properties (optical, mechanical, or electrical properties) upon demand and in response to changes in the environment (e.g., temperature, light, chemical ambient, electrical field, and magnetic field) not only is an exciting fundamental challenge but also is highly attractive for a wide range of applications. Especially, the development of materials that are capable of dynamically controlling the transmission and reflection of visible and near-infrared light is important for a number of applications, including energy-saving smart windows, transparent displays, telecommunications, lasers, etc.317,318 The principles of camouflage and optical tunability in various biological organisms such as cephalopods, chameleons, paradise whiptail, hercules beetles, blue damselfish, etc. have inspired various biomimetic designs of responsive tunable color.319 As discussed in section 2.6, the tunable color in these organisms is achieved by actively controlling the lattice spacing of guanine or reflectin-based photonic crystals in the dermal iridophores.10,11 12752


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Figure 50. (A) Mechanochromism of a PS-b-P2VP block copolymer photonic gel deformation with an indenter. (B) Color changes of the gel as a function of deformation. (C) Stopband at the center of contact (λpc) versus strain (ε) as a function of the displacement rate (v). (D) Stress (σ) versus λpc. (E) Schematic of the microdomain deformation by the microspherical probe, leading to changes in the optical path length through the swollen P2VP layers equivalent to deforming arrays of springs connected in series. Reprinted with permission from ref 328. Copyright 2011 John Wiley and Sons.

sensitive photonic stopband in the visible wavelength regime with highly tunable mechanochromic properties. An increase in the compressive strain of the photonic block copolymer results in a shift in to lower stopband wavelengths (Figure 50C). As the compression direction is parallel to the orientation of the microdomains, the compressed photonic gel will have a stopband wavelength at λpc = 2(ηPSdPS + ηP2VPdP2VP), where the dimensions of the P2VP microdomains, dP2VP, decrease, corresponding to the amount of compressive strain. Additionally, the unique feature of the mechanochromic response of these photonic gels is the corresponding change in the refractive index of the microdomains.328 Due to the changes in both the thickness and the refractive index of the microdomains, the stopband wavelength is sensitive to the swelling and deswelling of the photonic gel. Another kind of mechanochromic sensing is found in a class of liquid-crystalline polymers that exhibit rubber-like elasticity combining the optical properties of liquid crystals along with the mechanical properties of rubber.329 A stretchable liquidcrystalline polymer gel that is electro-optically switchable under moderate applied voltages can be fabricated using in situ polymerization of a mixture of mono- and diacrylate reactive mesogens.287 A mechanical stimulus (applied strain) can be used to manipulate the optical properties of the blue-phase liquid-crystalline elastomeric gel. The liquid-crystalline order is formed before the polymerization and cross-linking in a low molar mass system to enable a high degree of alignment. The unstretched gel has a characteristic blue-phase texture, while the stretching of the gel results in an apparent color change (Figure 51A−C). The observed mechanochromic behavior is attributed to the imposed lateral stretch, which induces a reduction in the effective photonic crystal lattice periodicity along the viewing direction (Figure 51D−F). The transmission spectra of the chiral nematic elastomers are blue-shifted, concomitant with the color change observed with increasing strain (Figure 51G). The biomimetic liquid-crystal polymer gel exhibits a strain-induced reversible color change in the entire range of visible

longer wavelengths (Figure 49D). The ion concentration can be used as an external trigger to manipulate the color change in this bioinspired photonic gel. Alternatively, a tunable structural color in a photonic material can be induced by a mechanical strain (mechanochromism). The mechanical strain causes a change in the optical path length of one or more of the domains of the photonic crystal, resulting in a shift in the stopband. As discussed in section 2.2, a one-dimensional photonic crystal (Bragg stack) with alternating refractive indices η1 and η2 and thicknesses d1 and d2 will have a stopband wavelength at λpc = 2(η1d1 + η2d2). However, when subjected to an external deformation, the stopband wavelength is shifted depending on the extent and type of deformation. Under a uniaxial compression or tension applied along the normal to the layer thickness, the stopband wavelength of the strained photonic crystal changes linearly with the uniaxial and is given by326 λpc = 2(η1d1 + η2d 2)(1 + εz)

where εz is the uniaxial strain normal to the layers of the photonic crystal. Under a shear stress, which involves an effective change in the optical path length along the viewing direction, the stopband wavelength increases nonlinearly with the shear strain and is given by326 λpc =

2(η1d1 + η2d 2) cos(tan−1 εxz)

where εxz is the shear strain on the photonic crystal. In a photonic gel of polystyrene-b-poly(vinylpyridine) (PS-bP2VP) diblock copolymer lamellar stacks, the P2VP microdomains are swollen in acetic acid and water, resulting in a color change due to the changes in the thickness and refractive index (Figure 50A).327 When the photonic gel is compressed by a spherical indenter, a reversible shift in the photonic stopbands along with a noticeable color change is observed (Figure 50B).328 This phenomenon is used to generate a strain12753


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Figure 51. (A−C) Polarizing optical images of a 20 μm thick layer placed across a variable-width aperture. (A) The unstretched state exhibits a characteristic blue-phase texture. Arrows indicate the direction of the cross-polarizers. The scale bar represents 1 mm. (B, C) As the aperture is widened, the sample is stretched and a color change is induced. (D−F) Schematic diagrams of a typical deformation of the blue-phase-I unit cell, viewed along the [011] direction and stretched along an axis perpendicular to it. (G) Spectral analysis of a sample with uniformly aligned [011] platelets showing the relative transmitted intensity, I, as a function of the vacuum wavelength of transmitted light, λ. Curves with reflection bands from right to left correspond to aperture widths in this experiment of 0.6 (unstrained), 0.65, 0.7, 0.75, 0.8, 0.85, and 0.9 mm, respectively. (H) The maximum selective wavelength, λc, defined as the minimum of I(λ), is plotted as a function of the aperture and width, d, normalized by the values in the initial, unstrained state, λo and do. Inset: schematic diagram showing the geometry of the experimental setup. Reprinted with permission from ref 287. Copyright 2014 Nature Publishing Group.

photonic systems. Most impressively, much of the optical performance in these diverse systems comes in spite of a limited selection of material building blocks. As a result, the performance is derived from the ability to engineer these systems at hierarchical length scales from the molecular scale to the macroscale. Along with a fundamental understanding of biophotonics, tremendous progress has been made in the development of biomimetic and bioinspired photonic devices. These device demonstrations are not limited by the inherent materials selection and processing limitations of living organisms and as a result often exhibit unparalleled performance characteristics. Despite this progress, several critical hurdles remain. To date, a majority of the biomimetic and bioinspired optical materials demonstrated rely on materials manufacturing processes that have limitations in scalability. The ability to mimic hierarchical assemblies in a scalable manner is a critical challenge that will require an improved understanding of the bottom-up materials synthesis strategies utilized by organisms along with insights into how to tailor such strategies for engineered optical materials and on how to integrate them with conventional manufacturing processes. Moving forward, a major emphasis

wavelengths over reversible cycles similar to that of a panther chameleon.10,287

4. CONCLUSIONS AND OUTLOOK Light−matter interactions have a central role in the origin and evolution of life. Sunlight delivers 89300 TW of power to the surface of the earth, which is the energetic basis for nearly all life. Over the past 3 billion years, living organisms have developed the molecular machinery to efficiently capture this energy and convert it into the form of biopolymers with an overall efficiency that is unrivaled by any man-made effort. Next, the development of the ability to detect light and subsequently vision provided an incredibly effective sensory perception for organisms to navigate the environment and interact with others. With the ability to see came a need to manipulate light both to serve as a way to communicate and to avoid detection from predators. Ultimately, this evolutionary arms race has led to highly engineered optical materials and systems whose design and function were refined through millennia of selective pressures. The study of these biological optical materials and systems has provided key insights into fundamental structure−function relationships in optical and 12754


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has to be placed on improving our understanding of “nature’s micro- and nanofabrication methods” and possibly learning or adapting these approaches to create synthetic optical analogues. In addition, one of the major hallmarks of many biophotonic camouflage and vision systems is their ability to dynamically respond and reconfigure. One of the strategies used by organisms is the combination of multiple responsive photonic elements to achieve a multiparametric response, a greater dynamic range of response, and a finer degree of control. Finally, many optical biomaterials are inherently multifunctional, and their materials properties are tailored accordingly. The ability to mimic such multifunctional material strategies would provide tremendous benefit in terms of cost, size, and deployability of next-generation devices.

worked as a Howard Hughes Research Fellow at the Center for Advanced Biotechnology and Medicine at Rutgers University. He joined the Materials and Manufacturing Directorate at the Air Force Research Laboratory, Dayton, OH, in 1999 as a research scientist, where he was assigned the position of Biotechnology Group Leader. In 2007, he was appointed the technology advisor for biotechnology in the Nanostructure and Biological Materials Branch. He also served as the Chair for AFRL’s Bio-X Strategic Technology Team from 2008 to 2011. Currently, he is the Chief Scientist of the 711th Human Performance Wing of the Air Force Research Laboratory, Air Force Materiel Command. His research interests include biologically enabled routes to advanced inorganic and composite materials, protein engineering, bioelectronics, biomimetic sensors for chemo−biodetection, and the interface between biological materials and nanomaterials. Srikanth Singamaneni obtained his bachelor’s degree in electronics and communication engineering from Nagarjuna University in 2002 and his master’s degree in electrical engineering from Western Michigan University in 2004. He received his Ph.D. in polymer materials science and engineering from the Georgia Institute of Technology in 2009. He was an assistant professor in the Department of Mechanical Engineering and Materials Science at Washington University in St. Louis from 2010 to 2015. Currently, he is an associate professor in the Department of Mechanical Engineering and Materials Science. His research interests include the design, synthesis, and self-assembly of plasmonic nanostructures for various biomedical applications, multifunctional materials based on nanocellulose, metal−organic frameworks for biopreservation, bioinspired structural and functional materials, polymer surfaces and interfaces, responsive and adaptive materials, and scanning probe microscopy and surface force spectroscopy of soft and biological materials.

AUTHOR INFORMATION Corresponding Authors

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

Rajesh R. Naik: 0000-0002-7677-928X Srikanth Singamaneni: 0000-0002-7203-2613 Notes

The authors declare no competing financial interest. Biographies Sirimuvva Tadepalli received her bachelor’s degree in metallurgical and materials engineering from the National Institute of Technology, Warangal, India, in 2012. She received a master’s degree in materials science in 2014 and is a Ph.D. candidate in the same department at Washington University in St. Louis. Her research interests include functional bio-nano hybrids, biomimetic nanocomposites, and bioinspired materials.

ACKNOWLEDGMENTS We acknowledge support from the Air Force Office of Scientific Research (Grants FA9550-15-1-0228 and 12RX11COR), National Science Foundation (Grants CBET1254399 and CBET 1512043), Office of Naval Research (Grants N000141612426 and N000141210089), and Air Force Research Laboratory/711th Human Performance Wing (AFRL/711 HPW).

Joseph Slocik was born in Natrona Heights, PA. He received a bachelor’s degree in chemistry from Ohio University in 1997. In 2001, he received an M.S. degree in chemistry from the University of Pittsburgh, and in 2004, he received a Ph.D. in chemistry from Vanderbilt University under Prof. David Wright. From 2004 to 2007, he was a National Research Council Postdoctoral Fellow at the Air Force Research Laboratory with R. R. Naik and is currently a research scientist in the group of R. R. Naik at the Materials and Manufacturing Directorate at Wright-Patterson Air Force Base in Dayton, OH. His research interests include biomimetic synthesis of nanomaterials, bioenergetic materials, and protein-based materials.

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Maneesh K. Gupta graduated with a B.S. degree in chemical engineering from the University of Illinois at Urbana-Champaign in 2004, an M.S. degree from Wright State University in 2007, and a Ph.D. in materials science and engineering from the Georgia Institute of Technology in 2012. His doctoral thesis was on the spatial and temporal control of stimulus-responsive hybrid nanomaterials. Subsequently, he was an Intelligence Community Postdoctoral Fellow at Princeton University, where he developed additive manufacturing techniques for programmable control of biochemical gradients. Currently, Maneesh is working at the Materials and Manufacturing Directorate at the Air Force Research Laboratories in Dayton, OH, where he is working on developing bioinspired materials processing strategies for multifunctional and reconfigurable biomaterials. Rajesh R. Naik obtained his B.S. in microbiology from the University of Bombay, India, in 1990 and a Ph.D. in the field of molecular biology from Carnegie-Mellon University, Pittsburgh, PA, in 1998. He later 12755


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