Sparkling feather reflections of a bird-of-paradise explained by finite-difference time-domain modeling Bodo D. Wiltsa,1,2, Kristel Michielsenb, Hans De Raedta, and Doekele G. Stavengaa,2 aComputational Physics, Zernike Institute for Advanced Materials, University of Groningen, NL-9747AG, Groningen, The Netherlands; and bInstitute for Advanced Simulation, Jülich Supercomputing Centre, Research Centre Jülich, D-52425 Jülich, Germany Edited by David A. Weitz, Harvard University, Cambridge, MA, and approved January 29, 2014 (received for review December 18, 2013) Birds-of-paradise are nature’s prime examples of the evolution of Parotia lawesii, Ramsey, 1885; Aves: Passeriformes: Paradisaeidae), color by sexual selection. Their brilliant, structurally colored feathers which seduce females with a stunning display of strongly colored play a principal role in mating displays. The structural coloration of feathers during an extravagant dancing ritual, the so-called “bal- both the occipital and breast feathers of the bird-of-paradise Lawes’ lerina dance” (2,3,12,13).TheplumageofmaleLawes’ parotia parotia is produced by melanin rodlets arranged in layers, together consists of mostly jet-black feathers (Fig. 1A). These feathers acting as interference reflectors. Light reflection by the silvery col- contrast strongly with silver-colored, occipital (nape) feathers, ored occipital feathers is unidirectional as in a classical multilayer, which reflect light specularly, due to a precisely spaced, layered but the reflection by the richly colored breast feathers is three- arrangement of melanosomes (11) in a keratin matrix (Fig. 1 B and directional and extraordinarily complex. Here we show that the re- D). The multicolored breast feathers also contain a multilayer flection properties of both feather types can be quantitatively of melanosomes, but these are much smaller and more densely explained by finite-difference time-domain modeling using realistic packed (Fig. 1 C and E). The breast feathers’ unique, boomerang- feather anatomies and experimentally determined refractive index shaped cross-section, enveloped by a thin film, gives rise to three- dispersion values of keratin and melanin. The results elucidate directional reflections that allow rapid switching between an the interplay between avian coloration and vision and indicate orange, green, or blue color when the bird makes its moves (3, 12). tuning of the mating displays to the spectral properties of the Whereas the essential features of the occipital feather reflec- avian visual system. tions are well described by classical multilayer theory (13), the SCIENCES optical properties of the breast feathers have not yet been APPLIED PHYSICAL biophotonics | body colors | courtship | signaling | reflectance quantitatively treated, because the morphology of the barbules is too complex to apply analytical models (12). To unravel the re- irds-of-paradise are best known for their magnificent color- flection properties of the morphologically complex breast feathers Bation. Living isolated on Papua New Guinea and its satellite as determined by spectrometry and imaging scatterometry, we islands (1), the absence of predators has allowed these birds to applied an advanced computational approach, finite-difference become extremely specialized for female sexual selection (2). time-domain (FDTD) modeling. FDTD allows fully explicit com- Male birds-of-paradise have evolved extravagant ornamental putation of the interaction of light with matter by directly solving ECOLOGY ’ – traits, with intricate sounds and ritualized sets of dance steps and Maxwell s equations in the time domain (14 16). By using the movements accompanied by simultaneous elaborate feather known barbule anatomy and detailed measurements of the re- movements, all combined in beautiful displays to win the favor of fractive index values of melanized feather components (13), FDTD females (1–4). Among the 39 species of birds-of-paradise almost all modeling has provided detailed understanding of the silvery re- colors of the rainbow can be found, and often the males advertise flectance of the occipital feathers as well as allowed substantial, themselves with brilliant, vivid colors framed within a jet-black quantitative insight into the optical mechanisms underlying the background. The females on the other hand have dull brownish plumage which has remained in its ancestral color state (1, 2). Significance Whereas the biological purpose of the colorful displays is relatively well understood (1, 2), the coloration mechanisms of Birds-of-paradise are brilliant examples of colorful displays in the birds’ displays and the connection to the visual system of the nature. The dazzling colors of the display, used in ritualized animals are poorly explored. Feather coloration can be generally dances to attract the attention of mates, arise from the in- categorized in two forms: pigmentary and structural. Randomly terference and diffraction of light within photonic nanostructures arranged, inhomogeneous media containing pigments are col- on their feathers. This study reports a quantitative investigation ored, because the pigments absorb the diffusely scattered light in of the complex photonic structures by connecting experimental a restricted wavelength range. For instance, carotenoids cause photonics with a state of the art computational model. The the colorful yellow or red feathers of many songbirds (5), and the methods used in this study may be applied to numerous appli- ubiquitous, broad-band absorbing pigment melanin causes feathers cations, e.g., for optimized photonic crystal designs. Here it has to be black (6). Structural colors occur in feather barbs due to allowed us to unveil the coloration mechanisms in the feathers of quasiordered spongy structures, and in feather barbules due to a bird-of-paradise and investigate the connection of feather col- melanosomes––nanosized, melanin-containing granules––regularly orstotheavianvisualsystem. arranged in layers within a keratin matrix, resulting in directional reflections because of constructive interference (7–11). Differ- Author contributions: B.D.W. and D.G.S. designed research; B.D.W., K.M., H.D.R., and D.G.S. performed research; K.M. and H.D.R. contributed new analytic tools; B.D.W. ences in the morphology of the structural colored feathers, i.e., in and D.G.S. analyzed data; and B.D.W. and D.G.S. wrote the paper. the dimensions of the spongy structured barbs or the melanosome The authors declare no conflict of interest. multilayers in the barbules, can modify the color of the reflected This article is a PNAS Direct Submission. light and can thus tune the optical properties of the feathers. In- 1Present address: Cavendish Laboratory, Department of Physics, University of Cambridge, deed, the various bird-of-paradise feathers impressively demon- Cambridge CB3 0HE, United Kingdom. strate how modifications of morphological traits can lead to 2To whom correspondence may be addressed. E-mail: [email protected] or D.G. dramatic changes of visual effects. [email protected]. We here investigate the occipital (nape) and breast feathers of This article contains supporting information online at www.pnas.org/lookup/suppl/doi:10. the males of the bird-of-paradise species Lawes’ parotia (Fig. 1A, 1073/pnas.1323611111/-/DCSupplemental. www.pnas.org/cgi/doi/10.1073/pnas.1323611111 PNAS | March 25, 2014 | vol. 111 | no. 12 | 4363–4368 Downloaded by guest on September 26, 2021 Fig. 1. Bird of paradise Lawes’ parotia, P. lawesii.(A) Habitat view (photo courtesy of Tim Laman). (B) Photograph of the nape of the bird, showing the silver- colored, mirror-like occipital feathers. (C) Slightly oblique view of the breast feathers showing the drastic variation in color along the differently inclined feathers. (D) TEM of a barbule of an occipital feather. (E) TEM of a barbule of a breast feather. Scale bars: (A)5cm,(B)1cm,(C)1cm,(D)2μm, (E)5μm. three-directional reflections of the breast feathers. The calcu- including multilayer structures. Upon adding a vertically polar- lated reflectance spectra suggest that the reflection character- izing filter into the incident light beam (Fig. 2D; see also Movie istics of the male breast feathers are tuned to the female’s S1), reflectance minima emerge in the vertical plane, that is, for color vision properties. transverse magnetic (TM)-polarized light, showing a Brewster’s angle of ∼60° (20). Results To be able to perform a quantitative analysis of the optical Barbule Morphology. The feather barbules of both the breast and properties of the occipital feathers, we measured the feathers’ nape area contain well-ordered layers of melanosomes sur- reflectance as a function of illumination angle for transverse electric rounded by a keratin cortex (Fig. 1 D and E). Whereas the oc- (TE)- as well as for TM-polarized light with a goniometric fiber cipital feather barbules are more or less flat and contain layers of setup (Fig. 2 E and G). The occipital feathers have for normal light melanosomes having a diameter of ∼250 ± 20 nm with an in- incidence a reflectance maximum in the near-IR, at ∼1,300 nm, terlayer spacing of ∼400 ± 20 nm, the melanosomes of the breast whereas the reflectance in the visible wavelength range slightly feather barbules have a much smaller diameter, ∼120 ± 15 nm, varies, yielding a silvery-bluish color (Figs. 1B and 2 E and G). The and the interlayer spacing here is ∼230 ± 20 nm. Furthermore, reflectance spectra measured for a number of angles of light the layers in