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Light Manipulation Principles in Biological Photonic Systems

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Light Manipulation Principles in Biological Photonic Systems © 2013 Science Wise Publishing & DOI 10.1515/nanoph-2013-0015 Nanophotonics 2013; 2(4): 289–307 Review article Tim Starkey* and Pete Vukusic Light manipulation principles in biological photonic systems Abstract: The science of light and colour manipulation wavelength-selective absorption of light by chromo- continues to generate interest across a range of disci- phores, the name given to colour-producing molecules plines, from mainstream biology, across multiple phys- [1]. If white light is incident upon a pigment, the resulting ics-based fields, to optical engineering. Furthermore, the scattered light will have some proportion of the light sub- study of light production and manipulation is of signifi- tracted from the incident spectrum. The molecular struc- cant value to a variety of industrial processes and com- ture of a pigment determines the wavelength band over mercial products. Among the several key methods by which it absorbs strongly. Pigmentary colour of a biologi- which colour is produced in the biological world, this cal species is usually synthesised by their physiological review sets out to describe, in some detail, the specifics processes, although some animals obtain these absorbing of the method involving photonics in animal and plant molecules through their diet [2]. Pigments that are synthe- systems; namely, the mechanism commonly referred to sised by many insects include melanins, pterins, ommo- as structural colour generation. Not only has this theme chromes, tetrapyrroles, papiliochromes and quinomes, been a very rapidly growing area of physics-based inter- while carotenoid and flavonoid pigments are generally est, but also it is increasingly clear that the biological obtained from their diet [2]. Colours produced using pig- world is filled with highly evolved structural designs by ments are often relatively broadband and cause relatively which light and colour strongly influence behaviours and low-intensity diffuse angle-independent hues. ecological functions. Modified chromophore chemistry leads to the inelas- tic scattering processes that give rise to fluorescent colour Keywords: structural colour; photonics; multilayer inter- emission. The common fluorophore-based emissions ference; diffraction; biology; butterfly. observed in biological systems usually comprise near-UV absorption with many examples of emission in the blue and green colour wavelengths. Use of fluorescence emission for *Corresponding author: Tim Starkey, Natural Photonics Group, signalling has been observed in many animals including School of Physics, University of Exeter, Exeter, EX4 4QL, UK, e-mail: [email protected] parrots, spiders and stomatopods [3–5], whilst the direc- Pete Vukusic: Natural Photonics Group, School of Physics, tional control of fluorescence emission by photonic crystals University of Exeter, Exeter, EX4 4QL, UK has been studied in Swallowtail butterflies [6]. Chemiluminescence is a less common process for Edited by Romain Quidant colour production, in which light emission arises from a chemical reaction. In biological systems this process is called bioluminescence [1, 2], a well known example of which is the firefly, a species of the Lampyridae beetle 1 Introduction family [7]. These light emitting chemical processes are seen in a broad range of organisms, including fungi, bac- Colour production in biological systems may be divided teria, fly larve, millipedes and earthworms [8], and many into two principle categories: the first is usually associated deep sea marine animals [9]. with chemical processes such as absorption and lumines- The non-pigment-based pathway to colour production cence; the second relates entirely to coherent scattering is described in terms of structural colour. This phrase is processes that underpin the interaction of light with mate- used to describe the wavelength-selective scattering that rials that have periodic variations in refractive index. arises from the interaction of light with structures that Pigmentation is the most common biological means have physical dimensions on the order of the wavelength of colour production and is the consequence of the of light. Coherent scattering produces the vivid optical Brought to you by | University of Exeter Authenticated Download Date | 6/21/16 1:21 PM 290 T. Starkey and P. Vukusic: Biological light manipulation principles © 2013 Science Wise Publishing & effects attributed to these structures. The characteristics The invention, and development, of the electron of this in biological systems can be: intense reflected nar- microscope (EM) in the 1930s and 1940s enabled the inves- row-band or broad-band colour [10, 11], metallic appear- tigation of biological and synthetic features having micro- ances [12], angle-dependent (iridescent) appearances scale dimensions. The first EM studies reported on the [13, 14], directional colour variation [15], low-reflective colour-producing structures found within bird feathers, absorbing [16] or transparent systems [17], and strong and within the scales of butterflies and beetles [29, 30]. polarisation signatures [18]. Although limited in the image quality and resolution they In this review, we discuss aspects of the fundamen- offered, elaborate multilayer structures with features tal optical processes used in biological systems that have smaller than the wavelength of light were identified [31]. evolved for structural colour production. In addition to One of the first mathematical treatments of the describing the existence of structural colour systems optical properties of films was undertaken by Rayleigh in across a range of different animal and plant phyla, we will 1887 [32]. Later, Abelès, in 1949, published a rigorous and particularly describe coherent optical scattering associ- useful method to obtain the reflection and transmission of ated with the scales of the insect order of Lepidoptera. thin films [33]. In 1968, intended for an audience of those As a vehicle for this we present a brief overview of interested in biological reflectors, Huxley published a photonic crystals and demonstrate the associated coher- recursive method for calculating the reflection and trans- ent scattering principles using the example of a one- mission of regularly spaced non-absorbing multilayer dimensional layered structure. We describe the existence films [34]. His discussion emphasised the optical effects of more complex photonic structures in a range of bio- relating to layer thicknesses, wave phase and amplitude. logical phyla, and go on to describe the photonic features In 1972, Land elucidated Huxley’s results in the context associated with the general design of lepidopteran scales. of the coloured appearance of many biological systems, We then present a summary of a range of investigations describing the structure, function and constituent mate- that have focused specifically on Morpho butterfly species. rials of the optical systems present in a wide variety of Finally we briefly review the growing field of bioinspired animals [35]. research to which Morpho photonics has contributed. Ghiradella et al., in 1972, described the bright ultra- violet reflection from a male Eurema lisa butterfly, dem- onstrating that its structural (UV) colour was derived from a very unusual microstructure that appears tree-like in 2 Historical perspective cross-section. Optical measurements combined with elec- tron micrographs revealed the branches of these tree-like Some of the earliest scientific investigations into the 3D ridges formed multilayer reflecting lamellae that were science of structural colour phenomena were made responsible for its UV-iridescent colour appearance [36]. by Hooke and Newton. In his 1665 microscope study This was one of the key early examples of a structurally Micrographia, Hooke remarked on “All the colours of the coloured insect system featuring a photonic structure that Rainbow” produced by cleaving seemingly colourless was rather distinct from the more regular 1D semi-infinite muscoy glass [19]. Hooke suggested that the iridescent multilayered structures theoretically described by Huxley. colour of a Peacock feather may be due to an “indefinite Two later studies examining Callophrys butterflies in the number of plain and smooth Plates, heaped up, or incum- 1970s, described the diffraction of light from 3D simple- bent on each other” [19]. Newton also studied the irides- cubic networks of ordered porous elements. These were cence of Peacock feathers and remarked that a “great among the earliest studies of highly ordered biological variety of colours” are produced when blowing upon a three-dimensional photonic crystals [37, 38]. soapy liquid [20]. Modern research into the optics of biological systems The early 20th century saw more thorough investi- has undergone a great deal of change. Plants and animals gations by Mason, Onslow, Rayleigh and others. Their are not only being investigated to elicit better understand- studies of the colours of bird feathers, butterfly wing- ing of their evolutionary, developmental and biological scales and beetle elytra elucidated some of the role played functions; multidisciplinary research into all aspects of in colour production by structures comprising multiple such natural systems is extremely active. Greater empha- reflecting layers [21–27]. The different visual appearances sis is now placed not only on understanding how these of many biological systems were attributed to different structures manipulate light, but also how technology specific physical phenomena,
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