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Structural Color and Its Interaction with Other Color-Producing Elements

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Structural Color and Its Interaction with Other Color-Producing Elements Structural color and its interaction with other color-producing elements: perspectives from spiders Bor-Kai Hsiung*, Todd A Blackledge, and Matthew D Shawkey Department of Biology and Integrated Bioscience Program, The University of Akron, Akron, Ohio 44325, USA ABSTRACT Structural color is produced when nanostructures alter light in contrast with pigment-based colors that are produced by selective absorption of certain wavelengths of light. Research on biogenic photonic nanostructures has primarily focused on bird feathers, butterfly wings and beetle elytra, and not diverse groups such as spiders. We argue that spiders are a good model system to study the functions and evolution of colors in nature for the following reasons. First, these colors clearly function in some spiders outside of sexual selection, which is likely the dominant driver of the evolution of structural colors in birds and butterflies. Second, within more than 44,000 currently known spider species, a hugely diverse set of colors is produced using the same materials. Using spiders, we can study how colors evolve to serve different functions under a variety of selective pressures, and how those colors are produced within a relatively simple system. Here, we first review the different color-producing materials and mechanisms (i.e., light absorbing, reflecting and emitting) in birds, butterflies and beetles, the interactions between these different elements, and the functions of colors in different organisms. We then summarize the current state of knowledge of spider colors and compare it with that of birds and insects. We then raise questions including: 1. Could spiders use fluorescence as a mechanism to protect themselves from UV radiation, if they do not have the biosynthetic pathways to produce melanins? 2. What functions could color serve for nearly blind tarantulas? 3. Why are only multilayer nanostructures (thus far) found in spiders, while birds and butterflies use many diverse nanostructures? And, does this limit the diversity of structural colors found in spiders? Addressing any of these questions in the future will bring spiders to the forefront of the study of structural colors in nature. Keyword list: structural color; pigment; bird; insect; spider; interference; scattering; diffraction; interaction; biomimicry 1. INTRODUCTION Structural colors are produced by coherent or incoherent interaction between light and materials with different refractive indices that are structured at nano-scales. This contrasts with most colors that are produced by selective absorption of light by pigments. Biological structural colors were first described, independently, by Hooke and Newton when they investigated the tail feathers of peacocks1,2. Since then, many more examples of structural colors in animals have been described3, particularly in birds (Class: Aves), butterflies and beetles (Class: Insecta)4. These are familiar, colorful organisms and hence it is not surprising that they are well studied. In contrast, our knowledge of structural colors in spiders (Class: Arachnida) is limited5. While the vast majority of spiders are relatively dull and brown, some have bright and conspicuous iridescent colorations. In particular, tarantulas (Family: Theraphosidae) and jumping spiders (Family: Salticidae) display the most color varieties6. Here, we review our current understanding of color-producing materials and mechanisms in birds, butterflies, beetles and spiders. Mainly, we focus on birds and anthropods, because in those taxa, structural colors are produced outside of living cells by hard biomaterials, such as keratins or chitins respectively, and we have a detailed understanding about them due to previous research5,7. On the other hand, structural colors in other taxa, such as cephalopods and plants, often occur in soft living tissues and/or have not been extensively researched5. * Email: [email protected] The Nature of Light: Light in Nature V, edited by Rongguang Liang, Joseph A. Shaw, Proc. of SPIE Vol. 9187, 91870B · © 2014 SPIE · CCC code: 0277-786X/14/$18 · doi: 10.1117/12.2060831 Proc. of SPIE Vol. 9187 91870B-1 Downloaded From: http://proceedings.spiedigitallibrary.org/ on 09/10/2014 Terms of Use: http://spiedl.org/terms By comparing and contrasting the materials and mechanisms that produce colors in spiders with those of butterflies and beetles, and those of more distantly related birds, we raise some interesting and important questions that can only be answered by investigating spiders in more detail, such as: 1. Why do spiders not produce melanins? 2. Do schemochromes, other than multilayers, exist in spiders? 3. How and why do diverse colors evolve when they do not seem to serve any obvious function to the host organisms (e.g., nearly blind tarantulas)? Furthermore, we provide thoughts on how answering those questions could increase our understanding of color evolution and color-producing mechanisms in nature. Finally, we discuss future directions for investigating structural colors in spiders and how this could inspire future biomimetic applications. There are many reviews providing general backgrounds about colors, color theory, different ways to produce colors in nature and also the optical principles involved in structural color production3,5,8-11. Here, we focus on the three different color-producing strategies found in spiders: pigment-based colors, structural colors and fluorescent colors. Basic definitions for terminology in this article are in Box 1. Box 1. Glossary 1. Interference: Waves of light superposed to form a resultant wave is defined as interference. Interference usually occurs between waves of light that are from the same source or have the same frequency. Interference can alter the composition of light, enhancing or decreasing the intensity of certain wavelengths of light, and hence produce colors. 2. Diffraction: Diffraction is the change in the directions and intensities of a group of waves after passing by an obstacle or through an aperture whose size is approximately the same as the wavelength of the waves. Diffraction per se does not alter the wavelength of the diffracted waves. 3. Scattering: While interference and diffraction consider light as a form of wave, scattering emphasizes its particulate nature. Scattering is the changing of directions of propagation of photons after colliding with scatterers. After light is scattered, its wavelength may change due to inelastic scattering, or elastic scattering with moving scatterers (e.g., Doppler effect). 4. Coherence: When the phase differences among interacting waves of light are constant, it is called coherence. The phase relationships do not need to be exactly in-phase or out-of-phase to be coherent. When the distances between scatterers are smaller than the wavelengths of light, waves scattered from nearby scatterers are nonrandom in phase, making the waves coherent. 5. Incoherence: When the phase relationships among interacting waves of light are random, it is called incoherence. When the distances between scatterers are larger than the wavelengths of light, those scatterers are spatially independent. A spatially independent scatterer array is an incoherent array. 6. Pigments: Molecules, often insoluble, that produce colors as results of selectively absorbing specific wavelengths of light due to their chemical structures. 7. Biochromes: Biological pigments. 8. Chromatophores: Cells or tissue that contain biochrome granules inside. 9. Iridophores: Cells or tissue containing granules which producing iridescent appearances. 10. Structural colors: Colors produced by light interacting with nanostructures through optical principles. 11. Schemochromes: Biogenic nanostructures that producing colors when interacting with light. 12. Fluorophores: Things that absorb light of certain wavelengths and then re-emit light at longer wavelengths later. In the following sections, we will first review the materials that act as building blocks for color-producing mechanisms in nature independently. Proc. of SPIE Vol. 9187 91870B-2 Downloaded From: http://proceedings.spiedigitallibrary.org/ on 09/10/2014 Terms of Use: http://spiedl.org/terms 2. COLOR-PRODUCING MATERIALS 2.1 Pigments 2.1.1 Biochromes that are common but missing in spiders Biochromes can be grouped into different classes based on their core chemical structures that result from varying biosynthetic pathways. Common biochromes are summarized in Table 1. Table 1. Summary for common biochromes and their colors Type Subtype Chemistry Color Organism Cross-linked 5,6-dihydroxyindole (DHI) and Eumelanin black, brown Common, but not found Melanin 5,6-dihydroxyindole-2-carboxylic acid in arachnids. (DHICA) copolymers. Pheomelanin Benzothiazine and benzothiazole oligomer. red, brown Depending on the position Xanthophyll C40HxOy and length of their conjugated yellow Common. Carotenoid double bound system, they Only found in some mites absorb light ranging from among arachnids. Carotene C40Hx orange, red 400-550 nm. Low molecular weight, yellow, Ommatin Invertebrates Tryptophan soluble in alkalis. orange, red Ommochrome (first found as visual metabolites High molecular weight, red, brown, Ommin pigments) insoluble in alkalis. black Bilin - Tetrapyrroles green, blue Common Highly conjugated double bond system, strongly absorb visible light. Common, but not found Porphyrin - red Usually bond with metals (porphyrins that in arachnids. bond with irons are hemes). Common yellow, Pterin - Derivatives of 2-keto, 4-amino pteridine. (used as visual
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