MORLEYO. STONE
RAJESHR. NAIK
Wright-Patterson Air Force Base Dayton, Ohio
INTRODUCTION
Literally, the termbiomimeticsmeans to imitate life. Prac- tically, biomimetics is an interdisciplinary effort aimed at understanding biological principles and then applying those principles to improve existing technology. This ap- proach can mean changing a design to match a biologi- cal pattern, or it can mean actually using biological ma- terials, for example, proteins, to improve performance (1).
Biomimetics had its earliest and strongest footholds in ma- terials science, and it is rapidly spreading to areas such as electromagnetic sensors and computer science.
The area of biomimetics covered in this article applies to sensing electromagnetic (EM) radiation. Volumes have been written regarding how higher organisms perceive visible light, and thus, this will be largely ignored here.
Mostly, coverage is limited to biological sensing of EM ra- diation on either side of the visible, the ultraviolet, and the infrared. From a biological sensing perspective, spectral re- gions are defined as follows: near-ultraviolet wavelengths (λ) from 200–400 nm and infrared wavelengths from 0.75–
15µm (Fig. 1). Operationally, both the ultraviolet and infrared extend over larger wavelength intervals. This article outlines some of the electromagnetic detection/
sensitive systems in biology.
BIOLOGICAL ULTRAVIOLET AND VISIBLE SYSTEMS The electromagnetic spectrum extends from gamma and X rays of wavelengths less than 0.1 nm through ultravio- let, visible, infrared, radio, and electric waves. The solar spectrum of radiation that reaches the earth’s surface ranges from 300–900 nm; radiation in the ultraviolet (200–
300 nm) is mostly absorbed by the ozone layer in the upper atmosphere. Light that passes through the atmosphere reaches the earth’s surface and also enters large water bod- ies. As penetration increases, the extremes of the visible spectrum are absorbed, allowing a narrow radiation of
Visible 0.4 - 0.7µm Near-ultraviolet
0.2 - 0.4µm
Near-infrared 0.75 - 3 µm
Mid-infrared 3 - 6 µm
Far-infrared 6 -15 µm
Figure 1. Chart of EM radiation definitions used in this article.
blue-green light (500 nm) to penetrate at depths greater than 100 meters. Radiation in the near ultraviolet, from 300–500 nm, is important in photobiological responses that include phototropism, phototaxis, and vision. For example, the spectral sensitivity of many insects and some birds is from 360–380 nm, and for invertebrates, it is from 500–
600 nm. Radiation from 600–700 nm is important in photosynthesis, and radiation from 660 nm into the near-infrared is important for plant and animal growth, flowering of plants, and sexual cycles in animals. Nucleic acids and proteins absorb ultraviolet radiation at 260 nm and 280 nm, respectively. Absorption at these wavelengths produces damaging effects including mutations and cell death. Fortunately, organisms can repair the damaging ef- fects of ultraviolet light on their genetic material by acti- vating UV repair mechanisms.
Insect Vision
The discovery of visual sensitivity in insects dates back to the 1800s, but substantial proof of the visual sensitivity of insects was provided in the last 20 years or so. The spec- tral range visible to insects extends from the ultraviolet through the red. Studies of the behavioral response of in- sects suggest that insects have wavelength-dependent be- haviors. The ability of an organism to discriminate diffe- rences in wavelength distribution and use this information to direct its behavioral response within a given environ- mental setting enables it to select its food source, avoid detection by prey, and identify potential mates (2).
The compound eyes of insects are made of eye facets, or ommatidia. The number of ommatidia varies from one species to an other: about 10,000 in the eyes of dragonflies, 5500 in worker honeybees, 800 inDrosophila, and one in ants. Each ommatidium is a complete eye that consists of an optical system and the photoreceptor, which converts light energy to electric energy. The optical system consists of the corneal lens and the crystalline cone that transmits the image to the photoreceptors. The compound eye of the common fruit flyDrosophila melanogasteris composed of about 800 ommatidia (Fig. 2); each ommatidium is approx- imately 10µm in diameter and 100µm long. The ommatid- ium consists of a corneal lens, a crystalline cone, retinula cells, and a sheath of pigment cells that extend across the entire length of the rhabdom (2). The rhabdom consists of eight individual rhabdomeres (R1 to R8), but as seen in Fig. 2D, only R1–R7 are visible; R8 is not visible because it lies underneath R7 (1). The ommatidia of honeybees consist of nine rhabdomeres (3). The rhabdomeres con- tain unique photopigments (opsins) that have character- istic spectral properties.
Image formation depends on the optical properties of the corneal lens and crystalline cone that aids in maximi- zing the amount and quality of light and focuses that light onto the rhabdomeres. The chromoproteins (rhodopsins) within the rhabdomeres interact with visible photons and in turn convert light energy to electrical energy (4). The rhabdom acts as a light guide or waveguide, mainly be- cause of its long narrow cylindrical geometry. The length of the rhabdom increases the probability that an entering photon of visible light will interact with the visual pigment.
BIOMIMETIC ELECTROMAGNETIC DEVICES 113
(a) (b)
(c) (d)
1 2
4
7 5
6 3
Figure 2. (A) Scanning electron micrograph of the adult eye; (B) longitudinal section through the eye showing the corneal lens, crystalline cone, rhabdom and the pigment sheath; (C) cross section through the ommatidium; and (D) cross section through the rhabdom to show the orientation of the photoreceptors (courtesy of John Archie Pollock).
Light that enters the rhabdom at a certain angle to its long axis is totally reflected and contained within the rhabdom, whereas light that enters at oblique angles is lost.
Rhabdomeres whose diameters (0.5µm) are similar to the wavelength of light in the visible spectrum function as waveguides. The rhabdomere can transmit or guide this electromagnetic energy within its small cross-sectional area. The small cross-sectional area of rhabdomeres prevents light from being uniformly distributed which causes interference. This, in turn, causes the light to
propagate in patterns known as modes (dielectric wave- guide). The effect of confining the photopigment within a rhabdomere of small cross section, it is believed, causes a shift from its visible absorptive peak to lower wavelengths and increases the UV peak absorption (5). In other words, the physical properties (size and shape) of rhabdomeres affect their spectral, polarization, angular, and absolute sensitivity. For example, inDrosophila, photoreceptor R7 that has a smaller diameter filters out a high proportion of the ultraviolet and blue light, whereas R8 (beneath R7)
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Figure 3. A scanning electron micrograph of a transparent insect wing (courtesy H. Ghiradella).
receives longer wavelengths. In bees, the rhabdomeres that are short and have a larger cross-sectional area mediate po- larized vision (3). The sky appears bright blue because sun- light is scattered by molecules in the atmosphere (Rayleigh scattering), and as a result the light becomes polarized. The polarization pattern of skylight offers insects a reference for orientation. The ommatidia in the dorsal rim of com- pound eyes in insects are used as a polarized light detector (3). Rhabdomeres generally fall into three classes that are maximally sensitive to light: 350 nm (ultraviolet), 440 nm (blue), and 540 nm (green) (6).
Optical engineers have attempted to develop imaging systems that function like the eyes of animals. Although replicating the visual system of an eye is probably a very arduous task, imaging systems have been developed that combine light sensors, photocells, microchips, and cameras.
Nature has developed optical systems in animals through millions of years of evolution, so much can be learned by studying animal or insect eye architecture. The compound eyes of insects have been quite informative in designing imaging devices. A multiaperture lens that has an array of glass rods arranged in a hemisphere was developed by Zinter in 1987. The multiaperture lens consists of hun- dreds of rod elements that have a graded index of refrac- tion, and each rod or optic element acts as a single lens.
Each lens transmits a small portion of the image, and at the focal point, each rod produces an overlapping image.
The images are then transmitted via optic-fiber bundles, and the superimposition of the image creates an intensified image. This type of device has advantages such as detect- ing objects in low light and a wide field of view.
Antireflective Coatings
The surfaces of compound eyes of numerous insects ap- pear smooth, but in certain insects, the front surface of the corneas are completely covered by protuberances known
as “corneal nipples” (7). These corneal nipples are an an- tireflective device in the broadband wavelengths from the near-UV to red (8). It is believed that these structures func- tion to match the impedance of air to that of the lens cu- ticle; thereby they increase the transmission of light and decrease the reflection from the corneal surface across a broad wavelength range. The nipple array gives the in- sect two important advantages: greater camouflage and increased visibility.
Apart from insect eyes, insect wings also, it is known, function as antireflective devices. The transparent wing of a hawkmothCephonodes hylasfunctions as an antireflec- tive device (9). It was shown that the wing reduces light reflectance by about 29–48% across a broad wavelength range (200–800 nm). An examination of the wing surface reveals the presence of nanosized protuberances similar to the corneal nipples in insect eyes (Fig. 3). The wing pro- tuberances, like the corneal nipple, also function to match the impedance between the cuticle and air. The individual protuberances are not detectable under visible light be- cause their small size limits visible light diffraction. Each single protuberance functions as an antireflective device.
By packing the protuberances closely in two-dimensional space, nature has optimized the most efficient way for the wing to function as an antireflective device. The transpar- ent wing is difficult to distinguish from the background and provides good camouflage to the insect. Interestingly, wings coated by a thin layer of nanosized gold particles (8 nm) reduced the metallic reflection of the gold particles presumably by changing the surface metal from a reflec- tive to a dark absorptive one (9). The optical properties of the nanostructures on insect wings can be used as a model for designing new optical devices that consist of nanosized structures (Fig. 4).
Butterfly Wings
The wings of butterflies are adorned by beautiful patterns and colors. Some wings are uniformly colored, whereas oth- ers reflect yellow, orange, red, green, blue, violet, or black.
The colors of butterfly wings as well as insect eyes are gen- erated by interference, diffraction, and scattering. The na- ture of the wing surface structure leads to the absorption of certain wavelengths and the reflection of other wave- lengths of light; in addition, some wavelengths may even be transmitted. The rainbow-like display of colors on but- terfly wings is caused by iridescence, due to the reflection from multiple thin-film interference filters on the wing scales (10). For example, the metallic iridescence ofMorpho butterflies is an interference color attributable to the struc- tural features of its wings. Interference colors result from the reflection of light from a series of superimposed struc- tures separated by distances equal to the wavelengths of light. The wing scale of the butterflies consists of a flat basal plate that carries a large number of vanes (or ridges) that run parallel to the length of the scale (Fig. 5). Each vane consists of a series of obliquely horizontal and ver- tical lamellae oriented lengthwise on the scale and their spacing is comparable to the bands of reflection. InMor- phowing scales, the horizontal lamellae are approximately 185 nm apart and are stacked in an alternate fashion to each other.Morphobutterfly wings produce a metallic blue
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(a) (b)
10 µm 1800 X
Figure 4. The fine nipples function as an antireflective coating. (a) Microlens array that functions to focus light onto the active area of a sensor; (b) subwavelength structure that functions as an antireflective surface (courtesy SY Technology, Inc.).
Ridges
Ridges stacked opposite to each other
Figure 5. Butterfly wing scale structure.
interference color.Morphobutterflies can be seen from low- flying aircraft due to the iridescent colors of their wings and are visible from a quarter of a mile (11).
The maleEuremawing scales reflects light whose peak wavelength is 350 nm. The lamellae in theEuremawing scales are stacked opposite each other and separated by an equal spacing of 83 nm. Ghiradella et al. (1972) demon- strated ultraviolet reflection from wing surfaces when the wing was tilted by 20◦ with respect to the incident light. The flapping of butterfly wings caused a change in hue proportional to the angle of the wing. A change in reflectance, abrupt intensity change, and a strong ul- traviolet component that contrasts with the background may serve as long-range communication signals between insects. As mentioned earlier, insect compound eyes are maximally sensitive to UV, and hence, UV patterns caused by this reflection may serve as a potential source of com- municative signals. Furthermore, vegetation generally ab- sorbs UV wavelengths in this region, and this may serve to maximize color contrast with respect to insect vision. Most vertebrates do not see UV, so this spectral region may serve as a private channel of communication among insects.
BIOLOGICAL INFRARED DETECTION
The ability of biological organisms to sense infrared radi- ation has been studied in snakes, beetles, moths, bacteria, numerous other organisms, and even subcellular orga- nelles. In much of this study, there is overlap and confusion between differentiating a process as infrared photon de- tection versus thermal detection. This is evidenced by the fact that literature comprising the infrared sensing area is quite limited; however, literature in the thermoreception area is voluminous. This section treats infrared and ther- mal reception as indistinguishable processes from a biolog- ical standpoint, and the terms are used interchangeably.
Additionally, this treatment extends to three experimen- tal infrared/thermal systems: snake, beetle, and bacteria.
Before delving into the specifics of biological infrared de- tection, a brief tutorial on blackbody radiation and thermal sources of IR is needed. Warm objects, such as mammals, emit energy in the infrared part of the electromagnetic spectrum. Table 1 lists three different temperatures: 300 K is listed as a background temperature, 310 K is listed to represent 37◦C prey, and the 1000 K listing is representa- tive of a forest fire. The 310 K listing and the 1000 K listing pertain to the snake model and beetle model of infrared
Table 1. List of Blackbody Infrared Emission Values For Objects at Various Temperatures
Bandpass Flux Bandpass Flux Temperature λmax Total Flux 3–5 Microns 8–12 Microns
(K) (µm) (W/cm2) (W/cm2) (W/cm2)
300 9.66 4.59e-02 5.84e-04 1.21e-02
310 9.35 5.23e-02 8.31e-04 1.42e-02
1000 2.90 5.67 2.04 5.04e-01
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reception, respectively, because each system tries to detect objects at these temperatures.
At first glance, the main difference between snake- based and beetle-based infrared detection is the wave- length region of peak intensity (λmax). Cooler objects, for example, mammals at 37◦C, emit maximally in the far-IR, in the 8–12µm atmospheric transmission window. As an object becomes hotter, for example, a forest fire at∼750◦C, theλmaxshifts to shorter wavelengths that place it in the 3–5 µm atmospheric transmission window. Roughly two orders of magnitude more total flux come from a 1000 K object compared to that from a 310 K object. An object at 310 K emits 27% of its total flux in the 8–12µm bandpass and 1.6% in the 3–5µm bandpass. Alternatively, an object at 1000 K emits 8.9% of its total flux in the 8–12µm band- pass and 36% in the 3–5µm bandpass. This discussion of infrared emitting objects and which is the better emitter is important to keep in mind as we discuss biological infrared detectors.
Bacterial Thermoreception
Cellular processes are influenced by temperature, and therefore, cells must possess temperature-sensing devices that allow for the cell’s survival in response to ther- mal changes. Virtually all organisms show some kind of response to an increase or decrease in temperature, but sensing mechanisms are not well understood. When bacte- rial cells are shifted to higher temperatures, a set of pro- teins known as “heat-shock” proteins are induced. These proteins include molecular chaperones that assist in re- folding proteins that aggregate at higher temperatures as well as proteases that degrade grossly misfolded proteins (12,13). Changes in temperatures can also be sensed by a set of coiled-coil proteins called methyl-accepting pro- teins (MCPs), that regulate the swimming behavior of the bacterium Escherichia coli (14). Coiled-coil proteins are formed when a bundle of two or more alpha-helices are wound into a superhelix (Fig. 6) (15). The MCPs can be reversibly methylated at four or five glutamate residues (16). Methylation and demethylation, it is presumed, is the trigger that dictates the response during temperature
Figure 6. A cartoon showing the coiled-coil structure of MCP-II fromEscherichia coli.
changes. The mechanism through which MCPs sense tem- perature is still not fully understood. In Salmonella, a coiled-coil protein known as TlpA has been identified as a thermosensing protein (17). TlpA regulates the transcrip- tion of genes by binding to sequence-specific regions on the DNA molecule. At low temperatures (<37◦C), TlpA in- teracts with another molecule of TlpA to form a functional (dimeric) molecule. As the temperature increases, TlpA dis- sociates from itself and becomes nonfunctional. However, the unwinding of TlpA helices is highly reversible, and a downshift in temperature leads once again to the formation of functional dimers. Because TlpA is not irreversibly dena- tured, it serves as an active thermosensing device. The fact that the denaturation and renaturation process is rapid al- lows cells to adapt quickly to changes in temperature. As shown in Fig. 7, the change in the structure of TlpA was measured by circular dichroic spectroscopy as a function of temperature. We observed that the thermal unfolding–
folding is reversible and the protein displayed 100% recov- ery. To date, of all the proteins tested by us, TlpA exhibits the highest degree of reversibility with respect to this ther- mal unfolding transition. It is likely that TlpA, as well as MCPs, represent an adaptation of the coiled-coil motif as a temperature sensor by coupling its folding and unfolding to temperature cues. In addition, the ability of short synthetic coiled-coil peptides to undergo rapid thermal denaturation and renaturation (Naik and Stone, unpublished observa- tions), suggests that the coiled-coil motif would be a model for designing new peptide-based thermosensing devices.
Snake Infrared Reception
The longest and best studied system of biological infrared sensing is the snake system. Snakes from two families, Crotalidae (pit vipers) and Boidae (boas and pythons), can sense infrared radiation by using specialized organs. In the crotalines, two infrared pit organs are positioned on either side of the head between the eyes and upper jaw. In boids, an array of infrared pit organs line the upper and lower jaw, and the number of pit organs is species specific. The ability of these organs to detect thermal energy was first
5 10−5
−5 10−5
−1 10−4
−1.5 10−4
−2 10−4 0 100
Molar ellipticity at 222 nm (change in protein structure)
0 1 2 3 4 5 6 7
25°C
10°C 10°C 55°C
75°C
10°C
Time (min)
Figure 7. Reversibility of the thermal unfolding of TlpA.
BIOMIMETIC ELECTROMAGNETIC DEVICES 117
2 µm
Figure 8. SEM micrograph of IR pit organ surface.
described by Noble and Schmidt in the 1930s (18). Bullock and co-workers at UCLA further defined this area by their electrophysiological studies in the 1950s. His publications from this period continue as the referenced sources for the stated sensitivity of 0.003◦C for crotaline infrared pit or- gans (19,20). Hartline continued to further the study of thermoreception in snakes throughout the 1970s, and he wrote a wonderful review article for the layperson in 1982 (21). For more than three decades, the center of snake in- frared research has been in Japan based on the work of Terashima and Goris. Recently, this group published a book that compiles their research papers from this past decade (22).
Much of this previous body of work has been electro- physiological and descriptive using electron microscopy techniques. We recently published a detailed examina- tion of the morphology of Boidae infrared pits using both atomic force microscopy (AFM) and scanning electron mi- croscopy (SEM) (23). Our results were consistent with the earlier results of Amemiya et al. (24). In both publications, the function of the unique surface morphology that covers the infrared pit organs was speculated about (see Fig. 8).
This speculation centered on the hypothesis that unwanted wavelengths of light, that is, visible, were being scattered and desired wavelengths of light, that is, infrared, were being preferentially transmitted.
To prove the speculation about visible light, we con- ducted a series of spectroscopy experiments to test the spectral properties of infrared pit scales compared to other parts of the snake (Fig. 9). This data suggested that the IR pit organ surface microstructure indirectly aids infrared detection by scattering unwanted visible wavelengths of light. Using various samples and repeated measurements, there was consistently more than a fourfold reduction in the amount of transmitted visible light. This loss of
Shed eye scale
Shed pit scale 50
40
30
20
10
0400 450 500 550 600 650 700
Wavelength (nm)
Percent transmisson
Figure 9. Fiber-optic spectrophotometry, visible wavelengths.
transmission was attributed to scatter due to measure- ments using a helium–neon laser at 632 nm and a silicon detector. Shed IR pit skin transmission dropped faster as a function of detector distance compared to eye scale trans- mission; this indicated an increased scattering angle and limited sample absorption. The increased visible light scat- ter can be accounted for by using a simple Rayleigh model of scatter and incorporating the micropit dimensions of dif- ferent snakes (23).
This difference in skin surface morphology as a func- tion of location on the snake is a wonderful example of evolved tissue engineering. These unique dimensions are confined to a few square millimeters within the IR pit or- gan. From the standpoint of chemical composition, there is no difference, as indicated by FT-IR analysis (Fig. 10).
The FT-IR spectra from shed IR pit skin and shed spectacle (eye) skin are identical to the amide bands of keratin that dominate the absorbance profile. Interestingly, note that regions of high skin transmission correspond to regions of high atmospheric transmission (3–5 and 8–12 microns).
As mentioned previously, the sensitivity of crotaline (pit viper) infrared detection, widely stated as 0.003◦C, refers to the seminal work by Bullock and co-workers (20). How- ever, this value was never measured directly but rather ex- trapolated from calculated assumptions. Furthermore, the measured values were determined as water was running over the pits—a conductive mode rather than a radiant mechanism of heat transfer. The function of prey detection has been studied extensively for these sensors (25). Bear- ing this function in mind, we attempted to examine the phenomenon of snake infrared reception in the context of the thermal radiative transfer among the sensor, prey, and background.
The actual molecular mechanism for infrared pit organ function is an active area of research in our group and others. Several models were proposed by de Cock Buning, and based on his work, we sought to construct a radia- tive transfer model that would measure the radiant flux of a biological object as a function of distance (26–28). De Cock Buning (27) presented thresholds and corresponding