Biomimetics: Lessons on optics from nature’s school Free

Biological systems achieve color effects via two mechanisms. The first employs chemistry: Pigments absorb at some wavelengths and reflect at others. Pigment coloration is effective and widespread, but it has its disadvantages. When pigments degrade over time, the organism must expend energy to replace them. And suitable pigments may not even be available to deliver the desired color effect.

The second mechanism, structural coloration, employs physics. Structures patterned on the scale of hundreds of nanometers—the wavelength of visible light—deliver color by effects such as interference, diffraction, and scattering. The color effects are essentially permanent, lasting as long as the structural form is preserved. Looking at a preserved collection of butterflies in a museum, one can immediately distinguish the still-vivid structural colors from the faded pigment colors.

One material present in many natural photonic structures is chitin, a component of insect exoskeletons, crustacean shells, fungal cell walls, and more. Its refractive index at visible wavelengths, n_c = 1.53–1.56, offers only a weak contrast with air (refractive index near 1), or with water (refractive index of 1.33). Even so, chitin structures can produce strong color effects that frequently exhibit iridescence, or variation of color with angle.

For a simple example, consider a stack of thin chitin films separated by layers of air. A single thin film of chitin in air has high transmittance and low reflectance across the visible spectrum, as shown in figure 1a. But with a regular structure of 10 layers of chitin and 9 intervening layers of air, one sees an oscillating reflectance with a strong peak at red wavelengths, as shown in figure 1b.

The 10-layer system may be regarded as a thin-film stack—or from a more modern perspective, as a one-dimensional photonic crystal. In the latter view, the number of chitin layers determines the number of photonic bandgaps, which show up in the spectrum as transmittance troughs or reflectance peaks. For normally incident light, the reflectance and transmittance are independent of polarization. For light incident at other angles, the reflectance becomes strongly polarization dependent; at the Brewster angle, $tan−1nc$⁠, the reflected light is totally polarized, as shown in figure 1c.

More complicated effects can be achieved by inserting structure within layers. For example, a chitin layer containing an array of long, parallel cylindrical air pores may behave as if it had an anisotropic refractive index, with one value applying along the length of the pores and another across them. The reflectance may then be polarization dependent even for normally incident light. Stronger polarization effects can be achieved with air pores that are tilted with respect to the layer surfaces. All those possibilities, and others as well, occur in biological systems.

For example, layered structures are found in some fishes that swim near the surface of a sea or lake. They often have shiny underbellies and dull backs: two different optical strategies to minimize detection by predators below and above them. From below, the water’s surface looks like a shiny mirror, thanks to total internal reflection. From above, deep water looks dark and dull. By mimicking both those effects, a fish can blend in with its environment—an interesting anticipation of the stealth-technology technique called carpet cloaking devised by John Pendry and colleagues (see the article by Martin Wegener and Stefan Linden, Physics Today, October 2010, page 32). Electron-microscopic analysis of the mirror-like underbelly scales of one such fish show that they are composed of layers of guanine crystals with random spacing. In contrast to the spectrum of regularly spaced layers in figure 1b, random spacing lowers the peak reflectance but makes the reflectance more broadband.

The hatchetfish, which lives at depths between 200 m and 1000 m, where sunlight is blue, has mirror-like structures not only on its silvery sides but also lining a system of tubes within its body. A light-producing organ shines blue light down the tubes, which reflect the light and guide it to one of many exit points on the fish’s underside. The fish adjusts the intensity of the light it produces to match the sunlight falling on its back. Any predatory fish swimming below the hatchetfish can no longer see a silhouette above them—the hatchetfish simply vanishes from sight! That camouflage strategy was copied by UK and US military planes during World War II. Lights were fitted on the leading edges of the planes to disguise them against the horizon, where they were too far away to be heard. Just as it began to work, however, radar was invented.

Multilayers are periodic in the direction of propagation of normally incident light. Another way to achieve structural coloration is through periodicity in the direction perpendicular to the propagation of normally incident light. If periodicity exists only in one direction, we speak of gratings, whereas if periodicity occurs along two different directions, we may use the terminology of 2D photonic crystals (see the Quick Study by Peter Vukusic, Physics Today, October 2006, page 82).

In a diffraction grating, if the spacing of the periodic structures is d and light of wavelength λ strikes at an angle of θ_i, then the grating gives rise to diffracted orders m whose angles of diffraction θ_m are given by the grating equation sin θ_m = sin θ_i + mλ/d. Rigorous methods exist to calculate how much energy is diffracted into each of those orders.¹ The distribution of energy is strongly polarization dependent and may vary rapidly with wavelength or angle of incidence, especially when the angle of diffraction of an order is close to 90°.

A stack of diffraction gratings can be regarded as a 2D photonic crystal, and the propagation of light in the structure can be described by a band diagram akin to those for electrons in semiconductors. If the refractive index of the grating elements is high enough, then a stack of gratings can stop all propagation of light in a wavelength range, irrespective of its direction of propagation. That range is called a total bandgap. Although living systems do not have access to such high refractive indices, they can still exploit partial bandgaps to achieve spectacular structural color effects.

Manmade gratings date back to the work of US astronomer David Rittenhouse² in the 1780s, and photonic crystals were introduced in a pair of seminal 1987 papers by Eli Yablonovitch and Sajeev John.³ Nature, however, has been using such structures in living creatures for more than 500 million years. Exceptionally well-preserved specimens, such as those found in the 508-million-year-old Burgess shale in British Columbia, Canada, provide examples of structural colors in long-extinct animals and in some whose cousins exist today. If we are lucky, we can follow the evolution of an optical design toward increasing complexity and better functionality in a sequence of animals on a branch of the evolutionary tree.

We turn now to a humble sea creature with a splendid name, the sea mouse or Aphrodita aculeata, a type of bristle worm that lives on the seabed, at depths from a few meters to a few thousand meters. As seen in figure 2a, it is generally dull in color to blend in with sandy or muddy seafloors. But the lower edge of its body carries long hairs with beautiful iridescence, and stout but equally colorful spines decorate the animal’s upper edges. Presumably, the iridescence highlighting the protective spines serves to warn predators that the creature is not particularly good eating.

The iridescence was known to fishermen centuries ago, and Carl Linnaeus, who classified the species in 1758, also commented on it. It is intriguing that the animal can achieve such brilliant coloration with the index contrast of materials available to it: Its bristles are chitin, and it lives in water. Figure 2b shows an electron micrograph of a spine that reflects nearly 100% of incident red light. The spine is a hollow tube, with its wall punctuated by an amazingly regular array of close-packed microtubes.

One can view the spine structure as a set of interference layers, each of which contributes a weak reflectance to the total optical effect. To achieve strong coloration, the spine must have a large number of layers that add their reflectances coherently. That can happen only when the spacing of the layers is almost perfectly regular.

Viewed as a photonic crystal, the spine has to rely on a partial bandgap rather than a total gap to achieve structural color effects. The result is adequate for the sea mouse’s purposes: The spine exhibits strong reflectance in a narrow band, which shifts with angle of incidence and gives the creature its characteristic iridescence.

The same mechanism is employed in microstructured optical fibers, developed in the 1990s by Philip Russell and colleagues at the University of Bath. The fibers confine light through repeated back-reflection by a regularly arranged set of (generally low-index) inclusions. One notable advance made possible by microstructured fibers was the octave-spanning supercontinuum recognized by the 2005 Nobel Prize in Physics (see Physics Today, December 2005, page 19, and the article by John Dudley and Goëry Genty, Physics Today, July 2013, page 29).

Optical systems found in living creatures frequently contain a mixture of single and double periodicity in a single element. For example, the structure sketched in figure 3 shows a combination of elements that, with variations, is present in the scales of many butterflies. The doubly periodic array of holes in the bottom layer can act as a reflector, or it can be combined with chemical pigments to absorb almost all incident light. The grating structure just above it acts as a wavelength-selective reflector, possibly with polarization dependence. The Christmas-tree fins on the grating ribs are akin to thin-film stacks. Those three elements, arranged in different ways, produce various structural iridescent effects in butterflies.

Other diverse optical elements are also found in butterfly scales: microribs with nanoridges, concave multilayered pits, randomly punctuated nanolayers, and diffraction gratings that are “blazed”—that is, they concentrate most of the reflected light into a single diffraction order. Most of those were discovered during the 1970s and 1980s by John Huxley at the Natural History Museum in London, where he left a treasure trove of electron micrographs for others to study and publish.⁴ The micrographs revealed structural black-and-white scales, double-reflecting micropits, fluorescence-aiding structures, and all manner of other configurations that today are under test for use in commercial products. The exciting results of the current prototyping work should be revealed in the next year or two.

A simple but important triply periodic structure occurs in the gemstone opal, whose color results from close-packed spheres of hydrated silica, around 500 nm in diameter, arranged in hexagonal or face-centered-cubic lattices. The structure is frequently used in photonic-crystal designs, often in the inverse form, where low-index spherical inclusions are arranged in a connected background of high-index material.

The opal structure has been discovered in the scales of a weevil of genus Metapocyrtus. The 3D periodicity and isotropy of the microstructure, shown in figure 4a, result in the hue of the color scales (figure 4b) appearing equal from all viewing directions, in part due to global averaging in our eye. Curiously, a similar-looking weevil, shown in figure 4c, employs the inverse opal structure.

Many bird species have structurally colored feathers. Hummingbird feather barbs contain ultrathin layers of alternating porosity that cause iridescent effects. Those structures have been mimicked using aqueous-based layering techniques. Structural blue feathers, such as the cotinga feather in figure 5, contain closely spaced air pockets from which reflected light rays interact constructively. Paints that form similar morphologies after drying are currently under development.

The cuticles of many beetles contain structurally chiral films that produce iridescent effects with circular or elliptical polarization properties. Their structures have been replicated in titania for specialized coatings. Mimetic samples are tested against the model beetle until an accurate reproduction of the variation in reflectance with angle is achieved. The titania mimics can then be nanoengineered to tune their resonant wavelengths over a wide range.

So far, our focus has been on structural color produced by the reflection of light. But some insects also benefit from antireflective surfaces, either on their eyes to help them see under low-light conditions or on their wings to reduce surface glare that might catch a predator’s eye. Antireflective surfaces occur on the corneas of all moth and butterfly eyes and on the transparent wings of hawk moths. They consist of rounded-tip nodules arranged in a hexagonal array with a periodicity of about 240 nm. The nodule profile introduces a shallow effective gradient from the refractive index of air to that of chitin. With no sharp interfaces off which light can reflect, the surfaces reduce reflectivity by a factor of 10.

That so-called moth-eye structure, shown in figure 6a, was first reproduced at its correct scale by crossing three lithographically produced gratings at 120°. Commercially, it was first employed as an antireflective coating for glass windows in Scandinavia. Today the moth-eye structure can be made with extreme accuracy using electron-beam etching, and it is used commercially on solid plastic and other lenses.

A different antireflective structure, a sinusoidal grating with 250-nm periodicity, was discovered on the cornea of a 45-million-year-old fly preserved in amber. That structure is particularly useful when light is incident at a range of angles within a single plane, all perpendicular to the grating grooves. Consequently, it has been applied on the surfaces of solar panels to increase energy capture by 10%. A demonstration of its glare-reducing capability is shown in figure 6b.

Sometimes nature’s optical nanostructures have such an elaborate architecture at such a small scale that we simply cannot copy them using current engineering techniques. And sometimes it’s possible to make one copy, but the effort is so great that commercial-scale manufacture would never be cost effective.

An alternative approach is to make the structures the same way the animals or plants do: with living cells. The success of cell culture depends on both the species and the type of cell. Insect cells, for instance, can be cultured at room temperature, whereas an incubator is required for mammalian cells. Cell culture is not a straightforward method: A culture medium must be found to which the cells adhere before they can be induced to develop to the stage where they make their photonic devices.

Current work in that area centers on butterfly scales. The cells that make the scales are identified and harvested from chrysalises. Then the individual cells are separated, kept alive in culture, and prompted through the addition of growth hormones to manufacture scales. One of us (Parker) and Helen Townley have recently cultured blue Morpho butterfly scales that have identical optical and structural characteristics to natural scales.⁵ Unfortunately, butterfly cells use up their internal structures during the making of a single scale. Weevil cells, on the other hand, do not, so potentially one could induce cultured weevil cells to make the opal structure for as long as they are fed nutrients and kept alive.

A far simpler task emerges when the iridescent organism is a single cell itself, such as a diatom. Diatoms are unicellular photosynthetic microorganisms. Of their more than 100 000 species, most are 20–200 µm in size, but some can be up to 2 mm long. Their cell walls, called frustules, are made of pectin impregnated with silica. The frustules contain pores and slits, often extremely intricate in structure, that give the cell interior access to the external environment. Whether frustules’ optical properties have any biological function is unknown, but they may affect light collection for photosynthesis. Diatom- inspired photonic devices can be made in silicon using a deep photochemical etching technique. However, exploiting diatoms themselves could be useful to build devices directly in 3D. Diatoms carry the advantage of exponential growth in numbers: Each individual can give rise to 100 million descendants in a month. And unlike most manufacturing processes, diatoms achieve a high degree of complexity and hierarchical structure under mild physiological conditions.

Using cell-culture techniques, with or without genetic engineering, researchers may be able to harvest some of nature’s techniques for molding the flow of light and make them available on a large scale. We could then have access to a range of smart materials for applications such as permanent color displays that are not subject to photobleaching, low-reflectance coatings for more efficient solar cells, new stealth technologies that use visual deception rather than broadband invisibility, wavelength- dependent polarizers, and many others—all inspired by the lessons from nature’s school.⁶ 

This article is dedicated to the memory of our colleagues and friends Nicolae Nicorovici and Jean-Pol Vigneron.

Ross McPhedran is a professor of physics at the University of Sydney in Sydney, Australia, and a chief investigator at the Centre for Ultrahigh Bandwidth Devices for Optical Systems. Andrew Parker is a research leader in the life sciences department at the Natural History Museum in London.