Structural colors in nature

1.5.1 Origin, proximate causes, and characterization of structural colors

Life on earth is colorful. Both animals and plants show an enormous variability of colors to attract mates or pollinators, deter enemies, or to hide from predators. The whole spectrum of

light from the ultraviolet to the infrared is used and some of the phenomena like polarized light (Sweeney et al. 2003) are not visible for the human eye. Colors in general have either a pigmentary origin or originate from the interaction of light with regular structures with the size of these structures being in the order of magnitude of the wavelength of visible light.

While colors derived from pigments are more widespread in nature, so called structural colors are usually more attractive due to their intensity, the iridescence, and their color variation depending on the angle of vision.

Though the diversity of structures provoking colors is very high, it can be stated generally that structural colors originate from the interaction of periodic nanostructures with photons.

These structures are able to affect the movement of photons. Depending on the lattice constant (i.e. the distance between the periods of the nanostructure) and the refractive indices (RI) 0f the two materials involved (see below) light of a certain wavelength is “not allowed” to propagate in the periodic nanostructure and will be totally reflected. Such a periodic nanostructure has been proposed to be a “photonic crystal” (John 1987;

Yablonovitch 1987) and the periodicity of the structures can occur in one to three dimensions. The simplest case of such a photonic crystal is a multilayer (i.e. a 1D photonic crystal). Light of a certain wavelength will be reflected in one direction, the right angle to the surface of the multilayer. The reflected color will change from longer to shorter wavelengths as the angle of vision increases. A 2D photonic crystal has a periodicity in two dimensions and light will be reflected in two dimensions. The most complicated photonic crystal shows a periodicity in three dimensions and will reflect light of a certain wavelength in three dimensions (3D photonic crystal). Such a structure might be built for example by three-dimensional stacking of beams or spheres (Parker et al. 2003).

It is important to mention that within the periodic structure, the alternating layers have to have different RIs. Noticeable, the RI of biological substances is rather low as compared to materials like glass or metal. In insects, the prevailing material involved in the occurrence of structural colors is chitin. Chitin is the main substance of the cuticle of insects and all structural colors of insects originate in the cuticle or in derivatives of the cuticle. The average refractive index of chitin is 1.52 (Welch & Vigneron 2007). The RI of chitin can be higher if other substances like uric acid are embedded into the chitinous matrix (RI = 1.68, Vigneron, pers. comm.). Noticeable, the material with the highest RI involved in biological color-producing structures, is guanine with RI = 1.83 (Welch & Vigneron 2007; for comparison:

glas RI = 1.45 – 2.14, titanium dioxide, an important white pigment RI = 2.71). In most cases, the second material of the periodic nanostructure is air. Air has a RI of 1.00 and therefore, the RI contrast in biological photonic structures is rather low (Welch & Vigneron 2007).

Photonic structures in biological materials can be investigated with different methods. First of all, reflectance spectra can be obtained to measure the wavelength of maximum reflectance. These reflectance spectra can be measured in the visible spectrum of light, the UV and the IR spectrum, and with different angles of incidence (Vigneron et al. 2006). After obtaining reflectance spectra of the structures of interest, one can predict the lattice constant of the periodic nanostructure responsible for the color origin. Afterwards, Scanning Electron Micrographs (SEM) should be taken from the structure. In the case of insect cuticle, the cuticle might be broken by freeze-fracture technique, thereby exposing the structure. Using SEM, the periodic nanostructures can be identified, and its properties (e.g. the dimensionality, the lattice constant, and the number of layers) can be measured and characterized. To complement the reflectance spectral analysis and the SEM characterization, one can model the optical properties (i.e. the reflectance spectrum) of the observed material taking the lattice constant, the proposed RIs, and the number of periodicities into account. If the results of the reflectance spectra, the characteristics obtained from the SEM, and the modeled reflectance spectra are consistent, one can be sure that the observed structure is responsible for the coloration (see Vigneron et al. 2006 for details).

1.5.2 Occurrence, function, and ultimate causes of structural colors

Most natural structural colors occur in animals (Vukusic & Sambles 2003) whereas structural colors can only very rarely be seen in plants (Lee 1991; Lee 1997; Lee & Lowry 1975; Vigneron et al. 2007) and in non-living matter like opal (Parker et al. 2003). Most reports on structural colors in nature deal with insects and among insects, butterflies are the classic example.

Butterfly wings have drawn a lot of attention, especially during the last few years (Prum et al.

2006; Vukusic 2006; Vukusic et al. 1999; Wickham et al. 2006; Yoshioka & Kinoshita 2006;

Yoshioka & Kinoshita 2006), but lately also other insect taxa like beetles (Parker et al. 1998;

Parker et al. 2003; Vigneron et al. 2005; Vigneron et al. 2005; Vigneron et al. 2007; Welch et al. 2007) and damselflies (Vukusic et al. 2004) have been the subject of intensive studies.

Structural colors can also be found in marine invertebrates (McPhedran et al. 2001; Parker et al. 2001; Welch et al. 2006) and vertebrates like fish (Bagnara et al. 2007), amphibians (Bagnara et al. 2007; Schmuek & Linsenmair 1988), birds (Doucet et al. 2006; Dresp &

Langley 2006; Vigneron et al. 2006; Zi et al. 2003), and mammals (Prum & Torres 2004).

Photonic structures can even be found in the fossil record with an age of up to 515 million years (Parker 2000; Parker 2004; Parker 2005; Parker & McKenzie 2003).

Though the before mentioned structural colors are very striking to the observer, the function of the coloration is not always clear. However, in classical examples of structural colors, males exhibit the colorful structures whereas females usually have a dull coloration and it is very likely that these structures have evolved for intraspecific signaling and more specifically for mate attraction. Therefore, these structures are probably a sexually selected trait and the result of female choice (Vukusic & Sambles 2003; Welch et al. 2007; Welch & Vigneron 2007;

Zi et al. 2003). Recently, evidence has accumulated that these structural colors have also the potential to signal male quality (Kemp & Rutowski 2007; Kemp et al. 2006; Loyau et al.

2007).

In other cases, the function of the structural colors is not so clear. Sometimes, interspecific signaling (e.g. warning coloration/aposematism, mimicry, startling, crypsis) can be assumed as the ultimate cause for the coloration. Still, in other cases neither intra- nor interspecific communication seems to be the reason for coloration. The coloration might serve for thermoregulation (Biro et al. 2003; Kobelt & Linsenmair 1992; Koon & Crawford 2000;

Schmuek & Linsenmair 1988) or the structures giving rise to the coloration have special mechanical properties and the colors are just a side-effect of the mechanical properties.

However, if the optical appearance would be detrimental for the animal, it would probably be counterselected and the structures could either be covered with a pigment or the periodic structures could be tuned in a way that the reflection maximum turns into the ultraviolet or infrared spectrum. Recently, it has been recognized that the evolution of a color producing structure might be driven by several factors simultaneously, which would result in a multifunctional structure (Welch & Vigneron 2007). Due to the optical properties, natural photonic structures are subject to imitation by man, but so far, the success of this biomimetism is rather limited (Biro 2007; Chen 2001; Deparis 2006; Large et al. 2007;

Vigneron et al. 2005).