Coloration (Insects)

Coloration is, as the word implies, the tapestry of hues with which an organism arrays the surfaces that it presents to the world. The signals thus produced may aid in species identification and mate choice, camouflage, warning, and temperature regulation; all in all, they serve as a mute “language” with which an individual organism may communicate its place in the community within which it lives.
Insects are master chemists whose virtuosity is particularly evident in the design of the cuticle, the nonliving material that makes up the exoskeleton and serves as the boundary between the living animal and the outside world (see Neville, 1975, for review). Cuticle, a composite of chitin fibrils and various proteins and lipids, can be tailored for strength, rigidity, flexibility, permeability, or elasticity, as needs dictate. It is also a technical and artistic medium with which insects, who are also master physicists and optical engineers, manipulate light to attire themselves with brilliant color on their bodies and wings. This article briefly reviews the bases of this ability. It begins, however, with an overview of the physics of color production, particularly with respect to structural colors, because only with this background can the reader really appreciate what a biological system, in its handling of light and color, can do.
General treatment of many of the following subjects may be found in Parker (2005), who also considers how visual systems interpret the physical light signal to produce the subjective sensation of “color,” and in Simon (1971).


TYPES OF COLOR

“Light” by definition involves wavelengths within the visible part of the electromagnetic spectrum. For humans it consists of wavelengths ranging from approximately 400 nm (violet) to approximately 725 nm (red). Many organisms, including insects, extend this range into the near ultraviolet (300^100nm). “White” light for a particular organism consists of all wavelengths visible to that organism. Colored light has an incomplete spectrum in which only some wavelengths are represented.
Matter interacts with white light in various ways to produce color. One way is by selective absorption of particular wavelengths by a chemical, or pigment. The absorbed wavelengths (which are determined by the pigment’s molecular structure) are essentially subtracted from the total spectrum, whereas the rest are reflected or transmitted to produce the visible color. Because pigments subtract colors, as additional pigments are added to a mix, additional wavelengths are absorbed and lost to view, changing the perceived color. When all wavelengths of the visible spectrum are absorbed, we call the sensation “black.” (This is a somewhat simplified view: visual physiologists and psychophysicists would point out that additional processing by the visual system tempers what humans actually “see.”) Pigmentary colors may be found in the cuticle or, if that is transparent, in the underlying tissues and even in the gut contents.
A second basis for color is structural, caused by the interaction of white light with minute and precise arrays on or in the material. The effects depend on the architecture, rather than the chemical makeup of the material. Light may be reflected, refracted, diffracted or scattered, but it is not absorbed, and so structural colors are “additive”: if two are combined, both sets of wavelengths are represented in the final effect. If all wavelengths of the visible spectrum are reflected, we call the sensation “white.” (Technically, white, even if caused by a pigment, is always a structural color, because it is the absence of any absorption of light.) Because the underlying architecture must generally be precise and stable, most structural colors are typically produced by stiff, nonliving materials, and of these insect cuticle is literally a brilliant example.
In biological systems, pigmentary colors are more common in the “warm” range—red, orange, and yellow—although green and blue pigments do exist. Biological structural colors, in contrast, are more likely to be “cool”—green, blue, violet, and ultraviolet. Figure 1 shows part of a butterfly wing: the dark colors are pigmentary, whereas the iridescent colors and the whites are structural. Many insects display both types, which are sometimes used together to produce yet additional effects. For example, a structural blue may be added to a pigmentary red to make a luminous violet, or a structural color may be “deepened” or intensified by a “backing” pigment that absorbs stray light leaking in from the “wrong” direction.
This article considers both pigmentary and structural colors. The following consideration of insect pigments is abstracted from the reviews of Chapman (1998), Fox (1976), and Nijhout (1991).
Urania riphaeus, portion of hind wing, showing the typical lepidopteran investiture of shingle-like scales (on the surface) and bristles (at the edges). The scales in the black areas are colored by a pigment, probably melanin, whereas the iridescent scales and the white bristles are structurally colored.
FIGURE 1 Urania riphaeus, portion of hind wing, showing the typical lepidopteran investiture of shingle-like scales (on the surface) and bristles (at the edges). The scales in the black areas are colored by a pigment, probably melanin, whereas the iridescent scales and the white bristles are structurally colored.

INSECT PIGMENTS

Insects can make most of their pigments (some apparently from waste products that were historically simply stored or excreted), whereas others must come from their diets. Several general classes of pigments are recognized. These differ in the color ranges they generate and in the precursors used to produce them. As they share the same underlying mechanism of color production (selective absorption of some wavelengths of light), they can be reviewed with a simple list.
Melanins are black, brown, tan, or reddish brown pigments whose production and deployment involve a complex system of gene products and biochemical pathways. They are often present as granules in the exocuticle, although in lepidopteran scales they may be diffusely distributed, and they are responsible for most of the dark patterning in the body and wings. Eumelanin, the black form, commonly requires dopamine and tyrosine as precursors, whereas the chemistry of phaeomelanin, the brown, tan, or reddish brown form, is less well understood and may require the incorporation of additional kinds of molecules into the compound.
Pterins are white, yellow, or red pigments derived from a purine, guanosine triphosphate. Some function as cofactors of enzymes important in growth and differentiation; they may help control these processes. They are also cofactors in ommochrome (see later) production and often occur with these latter pigments, for example in the screening-pigment cells in the ommatidia of the eyes.
Ommochromes are red, yellow, or brown pigments derived from tryptophan, which they may serve to use up if it is in excess supply during times of high protein turnover (e.g., in metamorphosis). They usually occur in granules coupled with proteins and, as mentioned
above, are present as screening pigments in the eyes as well as in the colors on the body. In insects displaying Tyndall blue (see later), they may serve as background pigments to absorb extraneous light.
Tetrapyrroles are pigments commonly classified into two groups. The first, the ring-shaped porphyrins, may add and incorporate iron to become hemes, which in turn may link to proteins to become (1) cytochromes, proteins important in cellular respiration in all higher organisms, or (2) hemoglobin, the protein that vertebrates and other organisms use to facilitate oxygen transport to their cells. Of necessity, all insects make cytochromes. Some that live in habitats of very low oxygen tension may make hemoglobin as well.
The other class of tetrapyrroles, the bilins, may in themselves be green or may link with proteins to make blue chromoproteins. These may in turn link with carotenoid pigments (see later) to make many insect greens.
Papiliochromes are yellow and red/brown pigments found only in butterflies in the family Papilionidae.
Quinone pigments are pigments of uncertain origin found in the Homoptera. Anthraquinones are found in members of the family Coccidae, in which they give red and sometimes yellow coloration; these include cochineal dye of historical importance. Aphins are characteristic of aphids, to whom they impart a purple or black coloration.
Carotenoids are yellow, orange, red, and, if bound to the appropriate protein, blue pigments that are made from dietary carotenes and their oxidized derivatives, xanthophylls. In combination with blue pigments (often bilins) they may produce an insect green, insectoverdin. They are also sources of retinal, a component of the photopigment of the eye.
Flavonoids are plant-derived pigments that produce cream or yellow colors, particularly in the Lepidoptera. Like the carotenoids, they cannot be synthesized but must come from the diet.
Some insect pigments are fluorescent; they absorb short-wave light and re-emit light of longer wavelengths (readers familiar with “black light” [e.g., ultraviolet light] displays will know the effect).
Finally, there are visual and accessory eye pigments. Although not directly in the purview of this topic, they are obviously both interesting and important. Stavenga (2002) presents a useful review of this subject.

STRUCTURAL COLORS

There are many mechanisms by which structural colors can be produced. All depend directly or indirectly on the fact that a particular piece of material scatters or refracts different wavelengths of light to different degrees. This property of the material can be expressed in terms of its index of refraction, n, a measure of the degree to which a given wavelength of light entering the material is “retarded” or slowed down. For insect cuticle, n typically ranges from 1.5 for long-wave (red) light to 1.6 for short-wave (UV) light, although in special cases n < 1.4 has been reported (for comparison, n for air is by definition 1). Structural colors described so far in biological systems fall into two general classes, scattering and interference.

Scattering

Scattering of light occurs when white light encounters a distributed cloud or array of molecules, particles, or other structures (Fig. 2). At least some of the component wavelengths of the beam will be reflected in random directions, including toward the observer. If the scattering agents are relatively large (700 nm or more), all visible wavelengths are scattered, and the resulting color is a matte white (the color of whole milk is an example of such scattering). If the particles are smaller (in the 400 nm range), the short wavelengths are scattered to a much greater degree than the long ones, which tend to pass on through the system and not reach the eye of the observer. The resulting color, Tyndall blue, is commonly seen in blue eyes and bluejay feathers; in insects it occurs in blue dragonflies and in some blue butterflies. Often, the blue structure is underlaid by a layer of ommochrome pigments, which, as mentioned above, deepen and intensify the color by absorbing stray light. Lacking such pigment backing, the blue is a dilute “powder” blue.

Interference

The general category of interference includes those situations in which the rays of a beam of white light are temporarily separated and then brought back together in such a manner that some have traveled a longer path than others. Depending on the geometry,
Scattering of light to produce Tyndall blue (as originally described for this type of scale structure). When full-spectrum (white) light encounters structures or particles of the right dimensions, the shorter wavelengths are preferentially scattered in all directions, including toward the eye of the observer, who sees a blue color. The longer wave light passes through unscattered (and therefore bypasses the observer). We now know that at least some scales of this type are optically much more complex (see text).
FIGURE 2 Scattering of light to produce Tyndall blue (as originally described for this type of scale structure). When full-spectrum (white) light encounters structures or particles of the right dimensions, the shorter wavelengths are preferentially scattered in all directions, including toward the eye of the observer, who sees a blue color. The longer wave light passes through unscattered (and therefore bypasses the observer). We now know that at least some scales of this type are optically much more complex (see text).
when the rays recombine, certain wavelengths are in phase and reinforced (“constructive interference”); these will shine with particular brilliance. Others are out of phase and cancel each other (“destructive interference”) . The results are the shimmering colors we call “iridescent.” There are many ways of producing iridescence; this article considers only those of known importance in insects.

DIFFRACTION

Diffraction occurs when light strikes the edge of a slit, groove, or ridge. Different wavelengths bend around the edge to different degrees and the spectrum fans out into its components. If many such grooves or ridges occur in a regularly spaced array (e.g., a “diffraction grating” such as that in Fig. 3) light of different wavelengths is reinforced at different angles so that the colors change with the position of the viewer (e.g., consider iridescent bumper stickers and other shimmering plastic labels). Many insect cuticles have fine gratings etched into them; these and the ridge and crossrib structures (see later) of some lepidopteran scales and bristles produce diffraction colors.

THIN-FILM INTERFERENCE

Thin-film interference involves, as the name implies, the interaction of light with ultrathin films of a material (e.g., iridescence from soap bubbles and oil slicks). Light reflecting from the top surface of such a film interacts with that reflecting from the bottom surface (Fig. 4A) and depending on the optical thickness of the film (its index of refraction, n, times its actual thickness, d),
Diffraction (in this example, from a grating). Light hitting an edge or discontinuity gets bent or refracted to different degrees, depending on its wavelength. When it is then reflected, which of the component wavelengths are reinforced varies with the position of the observer, so that from one angle shorter wave light (SW) predominates, whereas from another, longer wave (LW) light predominates
FIGURE 3 Diffraction (in this example, from a grating). Light hitting an edge or discontinuity gets bent or refracted to different degrees, depending on its wavelength. When it is then reflected, which of the component wavelengths are reinforced varies with the position of the observer, so that from one angle shorter wave light (SW) predominates, whereas from another, longer wave (LW) light predominates.
some wavelengths are reinforced and others not. Because the wavelengths of the reinforced light are four times the optical thickness of the film (i.e., a film of 100 nm optical thickness results in reflected light of wavelength 400 nm), such films are commonly called “quarter-wave interference reflectors” or “quarter-wave films.” Because a slanted beam of light has to penetrate a greater thickness of film, thereby changing the effective optical geometry, thin-film colors shift toward the shorter wavelengths when the films are tilted with respect to the light source (e.g., the familiar blue of the morpho butterflies becomes more violet).
Of course, any film thin enough to act as a quarter-wave reflector can catch and reflect only a portion of the incident light; the rest passes through. The presence of other films below the first increases the likelihood that light will be reflected, and in fact the most efficient of these reflector systems are stacks of thin films (“stacked multilayers”) of the material in question, separated by other films with a different refractive index or by air (n = 1), so that the light is reflected from layers of alternating high and low n. If all the films are equivalent in nd, their optical thickness, the emerging colors are relatively pure, whereas varied spacing produces a less intense but broader range of reflected wavelengths. As in all these systems, there may be behind the “mirror” a layer of pigment that intensifies the color by eliminating stray light that would otherwise interfere with the efficiency of the interference and thereby dilute the color.
Many iridescent colors are produced by other ordered systems that will pass some wavelengths of light while restricting others. These are now called photonic crystals and are generally designated as two dimensional (2D – imagine a group of soda straws packed together into a 2D array), or three dimensional (3D, such as the lattices to be discussed next). See Yablonovitch (2001) for an overview.
 Two forms of interference from layers. (A) Thin film. A thin film can be described in terms of its optical thickness, its index of refraction, n, times its actual thickness, d. When white light encounters such a film, part of the light reflects from the top surface and part from the bottom. When these two beams recombine, those wavelengths four times the optical thickness of the film are constructively reinforced and the others not. If many films are stacked into a multilayer, light not reflected by the first film may be so by the others; if the films are alternated with others of equal optical thickness but of a different refractive index (so that = nd2), the stack reflects essentially all light of the reinforced wavelength. (B) 3D photonic crystal. A lattice of points, spheres, or other structures reflects light in a manner analogous to that of some forms of crystal. Each plane reflects part of a beam and transmits the rest (transmitted light not diagramed here). If the planes are evenly spaced, they reflect light the wavelength of which is twice the spacing, that is, they will form a half-wave reflector. As in the case of thin films, with enough reflective planes, essentially all the light of the reinforced wavelength will be reflected.
FIGURE 4 Two forms of interference from layers. (A) Thin film. A thin film can be described in terms of its optical thickness, its index of refraction, n, times its actual thickness, d. When white light encounters such a film, part of the light reflects from the top surface and part from the bottom. When these two beams recombine, those wavelengths four times the optical thickness of the film are constructively reinforced and the others not. If many films are stacked into a multilayer, light not reflected by the first film may be so by the others; if the films are alternated with others of equal optical thickness but of a different refractive index (so that = nd2), the stack reflects essentially all light of the reinforced wavelength. (B) 3D photonic crystal. A lattice of points, spheres, or other structures reflects light in a manner analogous to that of some forms of crystal. Each plane reflects part of a beam and transmits the rest (transmitted light not diagramed here). If the planes are evenly spaced, they reflect light the wavelength of which is twice the spacing, that is, they will form a half-wave reflector. As in the case of thin films, with enough reflective planes, essentially all the light of the reinforced wavelength will be reflected.

LATTICES

A “Bragg” or space lattice (Fig. 4B) is a highly regular array of spheres or other units. Light entering such a lattice is reflected from the various layers, and the beams interfere in a manner analogous to that in thin film stacks. In this case, the wavelength reinforced is twice that of the spacing between the layers of the lattice, which therefore acts as a half-wave reflector. The familiar brilliance of the mineral opal is an example of this type of interference, caused in this instance by a lattice of tiny silica spheres. These lattices are very common in the biological world; those described so far in insects are mostly “reverse” lattices, consisting of spheres of air in a matrix of cuticle.

HELICOIDS

The metallically colored cuticles of many beetles and flies (Fig. 5) either are thin film (Fig. 6D) or owe their iridescence to yet another mechanism, one analogous to that shown by the familiar and brightly colored liquid crystal displays in our electronic world. Cuticle is of course a composite of chitin fibrils in a complex matrix that is laid down sequentially in what can be considered a series of layers. If the fibrils in a particular layer are lined up in the same direction, the layer exhibits form birefringence, that is, different indices of refraction parallel to and normal to the fibrils. In many cuticles, the layers precess, that is, each is laid down slightly rotated relative to the previous one (Fig. 6E). In essence, the structure can be considered a helicoid, and like all helical structures, it repeats itself with a certain spacing (called a “pitch”). As the layers precess, so does the difference in refractive index, so that viewed from a given direction a helicoidal array displays what are essentially layers of alternate high and low n, reminiscent of those in thin films. (Unlike thin films, helicoids also circularly polarize light, which insects may be able to see and which may therefore carry additional information to them.) If the spacing is regular and the pitch is appropriate, the helicoid behaves like a half-wave
This beetle shows the metallic coloration typical of many beetles and flies. Such colors may have at least two possible origins: they may be caused by a thin film stack in the exocuticle (or sometimes the endocuticle) (Fig. 6D) or they may be the result of a helicoidal arrangement of chitin fibrils in the exocuticle (Fig. 6E). The latter effect is analogous to that produced by certain types of liquid crystal in common technological use. The red and black coloration in the eyes, on the other hand, is almost certainly pigmentary.
FIGURE 5 This beetle shows the metallic coloration typical of many beetles and flies. Such colors may have at least two possible origins: they may be caused by a thin film stack in the exocuticle (or sometimes the endocuticle) (Fig. 6D) or they may be the result of a helicoidal arrangement of chitin fibrils in the exocuticle (Fig. 6E). The latter effect is analogous to that produced by certain types of liquid crystal in common technological use. The red and black coloration in the eyes, on the other hand, is almost certainly pigmentary.
interference reflector, that is, it reflects light of wavelengths twice the pitch. In the typical metallic cuticles, the helicoids of the exocu-ticle are so tuned, and because the helicoidal arrangements of their fibrils resemble those of the molecules in one iridescent class of liquid crystals, they are often referred to as “liquid crystal analogs.” Some insects intensify the effect by doping the cuticle with uric acid, which increases its birefringence.

BASES OF STRUCTURAL COLORS IN INSECTS

Several research groups have recently produced stunning evidence of the optical sophistication and complexity with which insects make and fine tune structural colors. Space limitations here preclude more than a few examples; Kinoshita and Yoshioka (2005) present a fine and comprehensive review.
As mentioned above, because scattering colors (whites and Tyndall blues) can be produced by granules or droplets as well as hard structures, these may come from the epidermis and internal tissues, as well as from the integument. Interference colors, which require stable structures to produce them, are limited to the cuticle and its investiture. Figure 6 shows diagrammatically a patch of cuticle with its two basic layers, the thin outer epicuticle and the inner procuticle. The procuticle commonly shows the helicoidal arrangement described above, which results in a banded or layered appearance in section. In hard or stiffened cuticle, the procuticle is commonly further subdivided into a cross-linked, more tightly woven distal exocuticle and a basal, more loosely structured endocuticle.
The cuticular surface and the exocuticle are most likely to be modified to produce structural colors, although in some insects the endocuticle may be as well. Several possibilities exist (Fig. 6). For example, the surface may be invested with layers of scales and/or bristles (Fig. 6A), which carry the color, especially in the Lepidoptera (see later). Alternatively, it can be sculpted into a series of nipplelike protuberances (Fig. 6B—more about this later) or into the fine grooves that characterize diffraction gratings (Fig. 6C). In the
How to make an interference color. A block of hard insect cuticle (bottom center) typically consists of a relatively thin epicuticle (here represented as a featureless covering layer) and an inner procuticle, which in turn consists of a distal exocuticle and an inner endocuticle (this diagram also shows the attendant epithelial cells). The layering of the procuticle is common in most (but not all) cuticles and is the visible manifestation of the helicoidal architecture of the chitin fibrils. Such a block of cuticle may be modified in any of several ways to manipulate light. (A) The surface investiture (the scales and/or bristles) may be modified to produce scattering or iridescent colors (see Fig. 7). (B, C) The cuticle surface may be sculpted into fine protuberances that serve as an antiglare coating (see Figs. 8 and 9) or into fine parallel grooves that act as diffraction gratings. (D) Part of the procuticle may be elaborated into a quarter-wave thin-film reflector stack. (E) The chitin fibrils of the exocuticle may be arranged in a "helicoidal" array, analogous to that in a liquid crystal and producing color by a similar mechanism. (The apparent parabolic bending of the fibers is an optical illusion.)
FIGURE 6 How to make an interference color. A block of hard insect cuticle (bottom center) typically consists of a relatively thin epicuticle (here represented as a featureless covering layer) and an inner procuticle, which in turn consists of a distal exocuticle and an inner endocuticle (this diagram also shows the attendant epithelial cells). The layering of the procuticle is common in most (but not all) cuticles and is the visible manifestation of the helicoidal architecture of the chitin fibrils. Such a block of cuticle may be modified in any of several ways to manipulate light. (A) The surface investiture (the scales and/or bristles) may be modified to produce scattering or iridescent colors (see Fig. 7). (B, C) The cuticle surface may be sculpted into fine protuberances that serve as an antiglare coating (see Figs. 8 and 9) or into fine parallel grooves that act as diffraction gratings. (D) Part of the procuticle may be elaborated into a quarter-wave thin-film reflector stack. (E) The chitin fibrils of the exocuticle may be arranged in a “helicoidal” array, analogous to that in a liquid crystal and producing color by a similar mechanism. (The apparent parabolic bending of the fibers is an optical illusion.)
exocuticle (and sometimes the endocuticle) metallic colors can be produced by stacks of thin films of alternating refractive indices (n = 1.58 alternating with n = 1.38 has been measured in one of these systems) (Fig. 6D) or by appropriately tuned helical rotation of the chitin fibrils (Fig. 6E). (As yet another example of insect command of light, in many corneas, the helicoidal architecture of the cuticle is tailored not to produce structural colors but to control refractive index, so that incoming light is appropriately focused as it enters the ommatidia.)
Scales and bristles are particularly impressive in the variety and complexity of their architecture (Fig. 7). They commonly exist in two and sometimes three layers on the body or wing surface (Fig. 7A), and each layer may be modified in shape and color. A typical scale consists of a flattened sleeve of cuticle whose lower surface (that toward the wing) is relatively featureless, whereas the upper surface is elaborated into a reticular network of longitudinal ridges joined at intervals by transverse crossribs (Fig. 7B). Fine flutings or microribs line the sides of the ridges and sometimes run out across the crossribs. Slender pillars join top and bottom surfaces. Pigments in some groups (typically the Pieridae) may exist in discrete granules, or “beads,” whereas in other insects they are laid into the general scale cuticle.
Virtually any part of this basic scale can be elaborated to produce a structural color. The spacing of the ridges and/or crossribs may be appropriate to produce diffraction colors. The crossribs and microribs may extend to fill in the windows with what in the older literature was described as a network of “alveolae” that reflects Tyndall blue (Fig. 7C), but which are now designated examples of 2D photonic crystals; in at
 Closer look at the investiture (scales and bristles), which in the Lepidoptera typically carries the color. Scales and bristles are complex cuticular structures each elaborated by a single cell, and they are often both pigmentarily and structurally colored. (A) As in Fig. 6A, a patch of cuticle surface showing several overlapping scales and one empty socket. (B) Diagrammatic view of a small fragment of a more or less typical unspecialized scale. The scale may be thought of as a flattened sac, the two surfaces of which are joined by fine pillars. (A bristle would be cylindrical, rather than flattened, but it is essentially the same type of structure.) The upper surface is a rectangular grid made up of longitudinal ridges (r) joined at regular intervals by transverse crossribs from which, in some species, hang pigment beads (arrows); in other insects, pigment is incorporated into the general cuticle. Ridges and crossribs together frame a series of windows opening into the interior of the scale. Virtually any part of this basic scale may be elaborated into a reflective structure. In the following examples, scales have been fractured to show their interior structures; lines indicate which basic scale structures have been elaborated to produce each structural color. [Modified from Ghiradella, H. (1998). Hairs, bristles and scales. In "Insecta." (M. Locke, ed.), Vol. 11A of "Microscopic Anatomy of Invertebrates" (F. W. Harrison, ed.), pp. 257-287. Wiley, New York. © 1998 John Wiley & Sons. Reprinted by permission of John Wiley & Sons.] (C) Papilio zalmoxis, fragment of upper scale surface. The ridges are low and unornamented, but the crossribs have "filled in" the windows with a network of "alveolae" that may scatter light to produce a Tyndall blue color (compare Fig. 2) or contribute to a more complex optical effect (see text). Bar, 1 urn. (D) Morpho menelaus, fragment of deep blue iridescent scale, fractured longitudinally to show a side view of a ridge (r), together with the pillars that join it to the bottom layer of the scale. The ridge (and those behind it) has been elaborated into a slanting multilayer, stacks of slanting thin films that reflect the characteristic blue of this butterfly. Bar, 1um. (E) Urania riphaeus, fractured green iridescent scale (see Fig. 1). The ridges and crossribs are not particularly elaborate, but the interior of the scale is filled with a stack of thin films that produces the color. Bar, 1 urn. (F) Teinopalpus sp., fractured green iridescent scale. The scale interior is filled with a 3D photonic crystal that produces the color. Bar, 1 urn.
FIGURE 7 Closer look at the investiture (scales and bristles), which in the Lepidoptera typically carries the color. Scales and bristles are complex cuticular structures each elaborated by a single cell, and they are often both pigmentarily and structurally colored. (A) As in Fig. 6A, a patch of cuticle surface showing several overlapping scales and one empty socket. (B) Diagrammatic view of a small fragment of a more or less typical unspecialized scale. The scale may be thought of as a flattened sac, the two surfaces of which are joined by fine pillars. (A bristle would be cylindrical, rather than flattened, but it is essentially the same type of structure.) The upper surface is a rectangular grid made up of longitudinal ridges (r) joined at regular intervals by transverse crossribs from which, in some species, hang pigment beads (arrows); in other insects, pigment is incorporated into the general cuticle. Ridges and crossribs together frame a series of windows opening into the interior of the scale. Virtually any part of this basic scale may be elaborated into a reflective structure. In the following examples, scales have been fractured to show their interior structures; lines indicate which basic scale structures have been elaborated to produce each structural color. [Modified from Ghiradella, H. (1998). Hairs, bristles and scales. In "Insecta." (M. Locke, ed.), Vol. 11A of "Microscopic Anatomy of Invertebrates" (F. W. Harrison, ed.), pp. 257-287. Wiley, New York. © 1998 John Wiley & Sons. Reprinted by permission of John Wiley & Sons.] (C) Papilio zalmoxis, fragment of upper scale surface. The ridges are low and unornamented, but the crossribs have “filled in” the windows with a network of “alveolae” that may scatter light to produce a Tyndall blue color (compare Fig. 2) or contribute to a more complex optical effect (see text). Bar, 1 urn. (D) Morpho menelaus, fragment of deep blue iridescent scale, fractured longitudinally to show a side view of a ridge (r), together with the pillars that join it to the bottom layer of the scale. The ridge (and those behind it) has been elaborated into a slanting multilayer, stacks of slanting thin films that reflect the characteristic blue of this butterfly. Bar, 1um. (E) Urania riphaeus, fractured green iridescent scale (see Fig. 1). The ridges and crossribs are not particularly elaborate, but the interior of the scale is filled with a stack of thin films that produces the color. Bar, 1 urn. (F) Teinopalpus sp., fractured green iridescent scale. The scale interior is filled with a 3D photonic crystal that produces the color. Bar, 1 urn.
least one species these are part of a highly sophisticated optical system (see Vukusic and Hooper, 2005) that involves a fluorescent pigment that absorbs short wave light and re-emits it at wavelengths close to those optimal for the animal’s visual system while at the same time guiding the light to the bottom interior of the scale, where a multilayer reflects it back up and out to the world. The ridges of the scale may bear stacks of thin films (examples known so far reflect green, blue, or ultraviolet) (Fig. 7D). The interior of the scale may be filled with stacks of thin films tuned to produce green or blue (Fig. 7E), or it may contain 3D photonic crystals that reflect iridescent green (Fig. 7F ) . And, as mentioned earlier, these structural colors may be combined with pigments to give yet additional colors and effects.
More detailed study of some of these systems is revealing yet more complicated and sophisticated optical effects. For example, in blue Morpho butterflies, the deep blue iridescent scales (whose color comes from thin-film iridescence on the ridges—Fig. 7D ) are overlaid by a layer of “glass scales,” which, though otherwise transparent, do have iridescent ridges. The apparent function of the glass scales is to broaden the effective angle of reflection (see Vukusic et al. , 1999). The iridescent scales of Papilio palinurus have stacks of internal thin films, but rather than being flat, the stacks are puckered into shallow cup-shaped depressions whose bottoms reflect yellow light, whereas the sides reflect blue, giving the human observer the sensation of green (see Vukusic et al., 2000)—st is not known why these animals have developed this mechanism to produce green scales when other iridescent greens are produced by more conventional thin films or by lattices. Kinosohita et al. (2002) reported that in many Morpho, the final color effect depends both on thin film and diffraction effects from ridge multilayers.
There are other intriguing scale and bristle types whose optics are now being studied, and from these insect systems new and sophisticated insights into the effective control of light can be expected.

ANTIGLARE COATINGS

Insect handling of light does not stop with the production of colors. Figure 8 shows the clarity with which light may be transmitted through the wing of a clearwing moth. Although the cuticle is somewhat rippled and one would expect some of its surfaces to show glare, they do not. Figure 9 shows why: the wing surface is covered by fine arrays of protuberances that are commonly found on cuticles that are engineered not to maximize the reflection of light but to minimize it (besides the wings of these clearwing moths, such arrays have been reported on the eye corneas of nocturnal moths, where they may help to “harvest” scarce nocturnal light and/or reduce tell-tale glare that would reveal the eye— and its bearer—to a potential predator). The arrays provide a gradual transition in refractive index from that of air (n = 1) to that of cuticle
Effects of an antiglare coating. Even though the wing of this clearwing moth is somewhat wrinkled and parts of it would therefore be expected to reflect light, its matte surface (Fig. 9) allows the text to be read through it with minimal loss.
FIGURE 8 Effects of an antiglare coating. Even though the wing of this clearwing moth is somewhat wrinkled and parts of it would therefore be expected to reflect light, its matte surface (Fig. 9) allows the text to be read through it with minimal loss.
 (Top) Podosesia syringae, patch of wing fractured to show its internal structure as well as the fine protuberances or nipples that form the antiglare coating. A few of those on the wing reverse show through the break at bottom center. Bar, 1 |im. (Bottom) Basis of the antiglare effect. The tapered shape of the protuberances produces a gradual change in refractive index from that of air (n = 1) to that of cuticle (n = 1.5 in this example), so that at the interface there is neither refraction nor reflection to disturb the passage of light.(typically n = 1.5-1.6) so that there is no sharp interface to refract or reflect light as it passes from one phase to the other.
FIGURE 9 (Top) Podosesia syringae, patch of wing fractured to show its internal structure as well as the fine protuberances or nipples that form the antiglare coating. A few of those on the wing reverse show through the break at bottom center. Bar, 1 |im. (Bottom) Basis of the antiglare effect. The tapered shape of the protuberances produces a gradual change in refractive index from that of air (n = 1) to that of cuticle (n = 1.5 in this example), so that at the interface there is neither refraction nor reflection to disturb the passage of light.(typically n = 1.5-1.6) so that there is no sharp interface to refract or reflect light as it passes from one phase to the other.
In summary, the complexity associated with insect colors extends, for pigments, to the sophisticated biochemistry with which insects make (and often recycle) the compounds that characterize their chemical colors and, for structural colors, to the production and control, often by single cells, of the precise cuticular architecture reviewed here. Other effects abound; for example, many insects are capable of physiological color change, by reversibly hydrating or dehydrating their cuticles to change the optical thickness of the layers or by moving pigment or fluid about. To all this, we must add more global effects, those of cover and ground scales working together (for example) and at least one in which even the wing membrane carries the same color (white in this case) as displayed by its associated scales (see Yoshioka and Kinoshita, 2006).

PERSPECTIVE

An easy question is why such arrays of color? Insects share the same challenges as humans and so they use color and patterning for species and mate recognition, camouflage, startling potential predators, and mimicry. Energy is also almost certainly a factor: dark colors absorb more heat, and butterflies, for example, may use pigments and possibly interference mechanisms to increase the absorption of infrared. It can only be speculated as to why structural colors predominate at the short end of the visible spectrum. As a biological material, cuticle is assumed to have a limited range of refractive indices and if so, only shorter wavelengths may be refracted and scattered effectively enough to produce the needed effects. It could also be that short-wave structural colors are metabolically “cheaper” (i.e., require less energy to produce) or easier to make than short-wave pigments, which do seem relatively rare in biological systems. Further study may enlighten both biologists and engineers.
How are these structures and color patterns made? On one timescale the question is developmental: how can an animal transform its genetic information into the complicated structures observed? This is the general question of pattern formation, the nested series of instructions that must be carried out by a developing organism on many levels at once. A developing butterfly must specify, for example, the general shape of its wing, the precise venation pattern, the distribution of scale and/or bristle types on both sides and on all edges of the wing, the distribution of pigment(s), and finally whether scales are to be structurally colored and if so, what type of structure they are to have. Nijhout, (1991) has provided an authoritative review of pattern formation in butterfly wing systems; many other researchers are currently studying the molecular and genetic mechanisms underlying pigment formation and deployment. Common themes are emerging, but much still remains to be done, especially on the role of physical forces that almost certainly work along with the biochemical ones to bring forth the final form.
The formation of the microarchitecture underlying structural color systems is less well understood. Ghiradella in 1998 reviewed development of structural colors in scale systems, and Neville in 1993 reviewed of the formation of helicoidal and other fibrous composite systems. However, despite their value as potential models for human research and development, particularly of optical systems, little is known about these systems. There surely are lessons to be learned here. For example, photonic crystals are of interest to engineers seeking more efficient transmission of information along optical fibers, and scale optics is becoming of interest to the photonics research community, which is seeking to develop structures and materials that can control light for purposes of communication, paints, surface coatings, electronic displays, etc. Again, the insect systems have a lot to teach us, especially since their structures are made at room temperature and without toxic solvents.
On the longer timescale, how did these systems evolve? In some cases there are grounds for speculation. As mentioned above, many pigments may have originally been metabolic by-products that, because of actual or potential ability to absorb some wavelengths of light, were somehow co-opted for purposes of display. The helicoidal arrangement of chitin fibrils in cuticle is part of a larger structural adaptation of cuticle as a building material. As in all skeletons, fibril orientation in cuticle is tailored to local challenges. Helicoidal arrangements, with their multidirectional fibril orientation, are well equipped to provide toughness and strength in the face of multidirectional stresses and are common in areas exposed to such stresses. Having evolved such a helicoidal arrangement to confer a particular type of strength, the animals needed only to make the pitches of the helices regular and to tune them to have fine iridescent reflectors at the same time.
The evolution of the thin film, diffraction, and other systems is at present a very open question. They appear to be of great antiquity. Parker (1999a, b) reported diffraction and antiglare structures in Burgess shale fossils and suggested that the emergence at the beginning of the Cambrian period of image-forming eyes (to quote Parker, “… the lights were effectively turned on …”) may have produced extreme selection pressure for potential prey animals to develop rigid armor (with its inherent potential for forming structural colors) and at the same time a need for, and an opportunity to develop, camouflage, recognition patterns, and all the other common uses and expressions of biological color.
To this point coloration has been considered in terms of passive and static displays on the surfaces of insects. But in living insects, the color-producing structures are situated on a moving body with moving appendages, and so the displays are modulated over time. The resulting signals are four dimensional, which adds to them a richness of information that we cannot begin to appreciate, especially because the true capabilities of the insect eye (which is much “faster” than that of the human) in its processing of either color or movement are not known.
The subject of insect mastery of light must also include biolumi-nescence. Lantern types and flash patterns come in a variety of forms; superficially, the mechanisms by which they are produced seem to differ radically from those already discussed. But here too, the insect displays mastery of architecture, in the design of the lantern cells themselves and of the chemistry, to create light signals that can be controlled in space and time, but at those times of day when sunlight is not available to power the display. In doing so, the insects have truly made “the lights come on,” replacing in their signaling the warmth of sunlight with their own colder light. As researchers continue to learn about these systems, they are exploring worlds within worlds of complexity and can only gain in appreciation of the enormous capabilities of biological systems in their communication with their environments … and with each other.

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