Electron tomography, three-dimensional Fourier analysis and colour prediction of a three-dimensional amorphous biophotonic nanostructure

Abstract

Organismal colour can be created by selective absorption of light by pigments or light scattering by photonic nanostructures. Photonic nanostructures may vary in refractive index over one, two or three dimensions and may be periodic over large spatial scales or amorphous with short-range order. Theoretical optical analysis of three-dimensional amorphous nanostructures has been challenging because these structures are difficult to describe accurately from conventional two-dimensional electron microscopy alone. Intermediate voltage electron microscopy (IVEM) with tomographic reconstruction adds three-dimensional data by using a high-power electron beam to penetrate and image sections of material sufficiently thick to contain a significant portion of the structure. Here, we use IVEM tomography to characterize a non-iridescent, three-dimensional biophotonic nanostructure: the spongy medullary layer from eastern bluebird Sialia sialis feather barbs. Tomography and three-dimensional Fourier analysis reveal that it is an amorphous, interconnected bicontinuous matrix that is appropriately ordered at local spatial scales in all three dimensions to coherently scatter light. The predicted reflectance spectra from the three-dimensional Fourier analysis are more precise than those predicted by previous twodimensional Fourier analysis of transmission electron microscopy sections. These results highlight the usefulness, and obstacles, of tomography in the description and analysis of three-dimensional photonic structures.

Structure and optical function of amorphous photonic nanostructures from avian feather barbs: a comparative small angle X-ray scattering (SAXS) analysis of 230 bird species

“…However, fundamental uncertainty remains about the exact organization of these three-dimensional amorphous feather barb nanostructures. Shawkey et al [26] recently performed three-dimensional electron tomographic reconstruction of the channel-type barb nanostructure in blue rump feathers of Eastern Bluebird (Sialia sialis), and made a reasonable prediction of the optical reflectance from the azimuthal average of the threedimensional Fourier transform of the tomogram. However, sample shrinkage and tomographic distortion limited the accuracy of structural and optical analyses [26,27].…”

Brilliant camouflage : photonic crystals in the diamond weevil, Entimus imperialis

“…Three-dimensional photonic crystals have been found in the scales of many weevils and beetles [1,21 -24], but also in butterflies [25 -28]. Quasi-ordered three-dimensional photonic crystal structures, which are periodic in all three dimensions, although imperfect, have been identified in bird feathers [29] and in the scales of some coleopterans [30].…”

Iridescent structural colour production in male blue-black grassquit feather barbules: the role of keratin and melanin

“…thin film) and bidimensional structures have been described (e.g. Greenwalt et al 1960;Prum et al 1998;Andersson 1999;Zi et al 2003), and recent techniques have provided new insights indicating that three-dimensional photonic structures may also be found in the medullar cortex of feather barbs (Shawkey et al 2009). Structures organized in one and two dimensions have the additional feature of being iridescent, i.e.…”