PHOTONICS APPLIED: BIOMIMETICS: Optical biomimetics emerge from a deep, dark past

ANDREW PARKER

"In the country of the blind, the one-eyed man is king." This famous dictum from H. G. Wells tells us something that may seem self-evident: sight matters. But imagine for a moment that the country of the blind is in fact the whole world, 521 million years ago. It's a world in which life is primitive and aimless, and evolution slow and painstaking.

Then something remarkable happens. Over the next million years, the process of evolution kicks into overdrive. For the first time, animals evolve hard external parts. Both hunters and prey develop armaments and defenses. So in this short space of time—the blink of an eye in geological terms—all animals on Earth, no matter how unrelated, leave their soft skins behind. When I traced back the origin of vision, I found that the first image-forming eye evolved in a predatory animal (one that could have an impact on others) around 521 million years ago, precisely at the beginning of this Big Bang of evolution. Hence vision appears to have lit the fuse for life's explosion.¹

But why is this important to the photonics community? Because with those first hard parts in animals came the first photonic nanostructures on Earth. With the evolution of the eye, the size, shape, color, and behavior of animals were suddenly revealed for the first time. The animal kingdom exploded into life. Color was among their main weapons. And from that moment until today, color on Earth has functioned to provide camouflage and crypsis, as well as warning colors and mating colors to attract the eye (see Fig. 1).

Natural photonic structures

Narrowband multilayer reflectors in the corneas of some eyes are tuned to perfectly transmit (at the normal) those rays of optimal detection by the retinal cells below. Similar filters can also be found in plants, such as in plant leaves to transmit wavelengths used in photosynthesis. On the other hand, broadband multilayer reflectors are found in eyes to back-reflect and sometimes focus all wavelengths of light, while hatchet fish possess a network of tubes lined with mirrors to guide light from a single, bioluminescent source out of many exit points and into specific directions.

A similar system of light guides is evident in dark caves of Australia and New Zealand. As one's eyes adjust to the darkness, tiny spots of blue light become visible on the cave's ceiling, appearing like stars. Turn on a torch light, however, and all is revealed. The ceiling is coated in a meshwork of transparent fibers—tubes secreted by the larvae of the fungus gnat. The tubes mimic optical fibers, transmitting the blue light produced by the bioluminescent organ of a larva (living within one of the tubes) by total internal reflection. That is, until it meets a junction from where another tube branches and hangs vertically from the ceiling. But the larva has one final trick. Over these dangling, transparent threads, it secretes a viscous, transparent fluid of the same refractive index, so that a series of droplets coat the tubes at regular intervals. These become exit points from the tube system for the bioluminescent light. Suddenly the angles become right for light to no longer reflect internally, and so it escapes the system and the droplets light up like tiny light-emitting diodes (LEDs).³

Does any of this sound familiar? Like something encountered in industry, perhaps? So far the comparisons are rather unfortunate for biomimetics, the art of extracting good design from nature.⁴ Optical engineers have gotten there before the biologists. But why not see what else nature has to offer?

From nature to industry

The nanoscale fibers within the corneas and lenses of eyes, including our own, are arranged in a network that reduces scattering and so provide enhanced transparency in the material. On the surface of some corneas, antireflective surfaces exist in one of two forms of zero-order gratings. One of these—the 2-D "fly-eye structure" found in a 45-million-year-old fly specimen from amber—has been replicated for use on solar panels, providing a 10% increase in energy capture through reducing sunlight reflection.

The 3-D "moth-eye" grating is found also on the transparent wings of some insects to prevent surface reflections and thus enhance camouflage (see www.laserfocusworld.com/articles/311580). And indeed, we are already making artificial analogues using various techniques from lithographic and ion-beam etching to chemical self-assembly (from the top down to the bottom up).⁵

But there are some extra, less-expected lessons we are learning along the way, which relate to the first point I was making about the lack of a design goal in nature. I have alluded to the idea that nature's "products"—the structures animals have evolved on their bodies—stand the test of time only if they help the animal to survive in its environment (to reach reproduction age and hence pass on the new genes for the structure). This must be done with the minimal of energy. Such energy conservatism has led to a tradeoff in design perfection over efficiency. And this is where nature really does have "one over" on us.

From studying a range of antireflective gratings on butterfly wings, I have found structures that at first sight appear rather rough around the edges—less than periodic in organization and with only semiregular parameters—but actually compare favorably to their perfect counterparts on the animals' eyes (see www.laserfocusworld.com/articles/355177). They reduce reflectivity by a factor of 9, rather than 10. The reason the more random antireflectors have evolved in butterflies is that much less energy was required to develop or make the structures (the precision in control has been greatly reduced). Conveyed to industry, many more techniques become available if the more random structure will suffice—and at nine-tenths of the optimal performance, in many cases it will. The additional techniques are likely to be cheaper, and the biomimetic structure may suddenly find itself commercially viable; a valuable lesson indeed.

Returning to light transmitting through natural fibers, there is a scenario with direct implications for the laser industry: the case of the comb jelly (a gelatinous "relative" of the jellyfish). Here, rows of paddles called "combs" beat rhythmically to propel the animal through the water, where the combs are made of flexible, hexagonally closely packed, submicron fibers. Interestingly, in some species a bioluminescent organ exists at the base of each comb, and the blue light it produces is transmitted through the fibrous comb in a direct analogy with a photonic crystal fiber, complete with partial band-gap in the blue region. The blue light enters the sea only from the ends of the combs, and its direction varies as the combs beat. So, in an analogy with forensic lasers and their attached light guides (used for revealing fluorescent evidence at a crime scene), here are photonic-crystal fibers directing blue light produced into a collimated beam.

Also on this subject, the majority of species on Earth—insects with compound eyes—achieve sight with the aid of light- transmitting fibers. Some insects can adapt to different levels of light through the migration of absorbing (melanin) pigment granules in the walls of the light guides in their eyes. More spectacular for their pigment migration, however, are chromatophores. These are cells that can alter the distribution of their pigment so that the cell appears either visible (as a pixel) or invisible to the eye. Chameleons and cuttlefish achieve their color change through closely packed chromatophores of various hues.

Chromatophores are dynamic. Iridophores are types of chromatophores that are packed with multilayer reflectors. In some cases these thin layers are tilted like in a Venetian blind, and may actually open and close through a similar, chord-operated mechanism. Effectively, the reflectors can be made to turn on and off or to shift their reflectance wavelengths in less than a second. Just as effective but not so fast, some beetles can alter their reflectors by interchanging one of the materials in a multilayered system (between water and air).⁶ In this way they can alternate between camouflage and conspicuousness, through activating a multilayer mirror to reflect their background, or to reveal only the red pigment beneath. Biomimetic duplication of these color-changing and camouflage-capable natural structures could have significant implications to industrial and defense-related applications.

From nature to the laboratory

My colleagues and I have begun making analogs of various animal reflectors in our engineering labs, including beetle cholesteric stacks made as titanium films, the electric blue of Morpho butterflies using combined chemical vapor deposition and ion-beam etching, and diatom shells using deep photochemical etching. We have constructed a new Massachusetts Institute of Technology (MIT)–Natural History Museum/Oxford collaboration, and hope to report new successes soon, but we would welcome any interest from industry.

Recently I have begun to question how animals make their often precise nanostructures. For example, the moth-eye-type antireflector is made when the outer wall of each cell involved forms hexagonally arranged microvilli with hemispherical tips, onto which chitin is secreted. As an extension of this work, we may eventually farm off and manipulate natural photonic products, with the ultimate aim to provide an alternative to current engineering techniques. For example, already we can attach antibodies to, and incorporate dyes into, the photonic crystal-shells of diatoms, which we can produce by the ton. We hope to report an application soon, and see no shortage of natural structures that will inspire novel photonic devices for industry.

REFERENCES

1. A. R. Parker, In the Blink of an Eye, Simon & Schuster (London), and Perseus Press (Cambridge, MA) (2003).
2. A. R. Parker, J. Optics A: Pure and Applied Optics 2, p. R15-28 (2000).
3. A. R. Parker, Seven Deadly Colours, Simon & Schuster (London; 2005).
4. T. Mueller, National Geographic, p. 68 (April 2008).
5. A. R. Parker and H. E. Townley, Nature Nanotechnology 2, p. 347 (2007).
6. J. P. Vigneron et al., Phys. Rev. E 76, p. 031907 (2007).
7. A. Ingram and A. R. Parker, Phil. Trans. Royal Soc. Lond. B 363, p. 2465 (2008).

Andrew Parker is a research leader for the Natural History Museum (London, England) and Green Templeton College, Oxford University; Natural History Museum, Cromwell Road, London SW7 5BD, England; e-mail: [email protected]; www.gtc.ox.ac.uk/andrew-parker.