Effect of nanostructural irregularities on structural color in the tail feathers of the Oriental magpie Pica serica

Abstract

The tail feathers of magpies are iridescent, with hues ranging from navy to violet and green. It has been previously shown that the hexagonal arrangement of melanosomes in the distal barbules is responsible for these colors, but previous simulation models have relied on average values for the parameters associated with this arrangement (e.g., periodicity), and it remains to be studied whether the actual (rather than averaged) structural arrangement and its inherent irregularities reliably predict structural color. Previous studies using unmodified images for the analysis have not focused on the effect of such irregularities on the color production. In this study, we conducted finite-difference time-domain (FDTD) simulations using actual transmission electron microscopy (TEM) images obtained from the distal barbules of a magpie tail feather, compared the reflectance spectra predicted using the FDTD simulation with those measured with a spectrometer, and found a substantial discrepancy between the two. Fourier analysis suggests that the non-uniform arrangement of the melanosomes within the barbule is responsible for this discrepancy by creating variation in the periodicity. Our results suggest that a simple model in which the parameters for internal structures are averaged cannot fully explain the variation in the structural colors observed in biological samples such as the feathers of birds.

Fig 1. Photographs and microscopic details of the uppermost tail feather of the Oriental magpie (P. serica).

The tail feather of the magpie was observed using an optical camera. The barbs extend from the rachis, and the barbules reach out from the barbs in succession. The surface of the flattened and elongated parts (pennulum) of the distal barbules is iridescent green, transforming into iridescent violet and navy around the tip of the feather. The scale bars in left and right represent 50 μm, 200 μm, respectively.

Fig 2. Optical and electron microscopic images and the structural model of the barbule.

A Surface of the barbule under an optical microscope (x1000) showing multi-colored domains. The red arrows indicate yellow, violet, and blue from top to bottom. The dashed red line indicates the horizontal band. The yellow point represents the direction of light propagation. B Scanning electron microscopy image of the barbule surface. C Transmission electron microscopy image of the barbule cross-section showing the hexagonal structure of the melanin stack. The yellow arrow indicates the direction of light propagation. D Structural model of the barbule and the type of the structure classified as type 5 from Durrel’s classification. The scale bars in A, B, and C represent 10 μm, 20 μm, and 1 μm, respectively.

Fig 3. Reflectance spectra measured using the experimental setup and calculated using FDTD simulations.

A Reflectance spectra of the barbule in the green area indicated by the red circle measured using the experimental setup. The wide spectrum has a dominant peak at about 520 nm. B−E Spectra calculated using FDTD simulations. The keratin, melanin, and air are represented by black, gray, and white in the simulated images, respectively. The refractive indices for keratin and air are 1.55 and 1.00 [25]. The refractive index of melanin was taken from Stavenga et al. [25] and fit with a Lorentzian function. The B and C spectra agree well with the experimental spectra, while the D and E spectra differ. The solid blue and orange lines represent TE and TM mode, respectively.

Fig 4. Reflectance spectra obtained from FDTD simulations.

A Four simulated sections of the barbule, each with a height of around 1 μm, corresponding to the size of the color domain. Enlarged images are presented in S3 Fig. B Spectra for the sections of the barbule calculated from the FDTD simulations. Each section has different peaks. Bar (A): 1 μm.

Fig 5. Fourier transforms for the sections from a single-barbule TEM image.

The Fourier transforms for the refractive index distribution in the barbule are expressed in spatial frequency. The peak wavelengths predicted from Fourier analysis are listed under each image.