Black Bird 4

[Melissa Russian]

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Bird coloration is a model system for understanding evolution, speciation, and sexual selection1. Color-producing mechanisms are generally assigned to two categories1: (i) pigmentary colors produced by molecules and (ii) structural colors produced by light scattering from nanoscale variation in refractive index (e.g., channels of air within a keratin matrix). In addition to color, the directional distribution of scattered light can also affect plumage appearance. The shape, orientation, and smoothness of the feather barbs and barbules create directionally dependent appearance, such as with glossy or iridescent plumage2, 3.

Here we use spectrophotometry, scanning electron microscopy (SEM), high-resolution synchrotron tomography (nano-CT), and optical ray-tracing simulations to investigate the role of structural absorption in black feathers from seven species of birds of paradise. Unlike normal black feathers with typical barbules, we find that super black feathers have highly modified barbules arranged in vertically tilted arrays, which increase multiple scattering of light and thus structural absorption. Super black feathers reduce specular reflection by one to two orders of magnitude compared to that of normal black feathers and have extreme directional bias corresponding to the viewing direction of a female observing a displaying male. Therefore, we hypothesize that these feathers evolved to enhance the perceived brilliance of adjacent color patches by generating an optical/sensory illusion during mating displays.

Reflectance spectra of black and super black plumages. a Total integrated (diffuse and specular) reflectance. b Normal, directional reflectance. Dotted lines are super black plumages. See Supplementary Figs. 1 and 2 for detailed spectra for each species

Often, color-producing feather pigments or nanostructures are restricted to the exposed tips of overlapping feathers in the plumage1. We found a similar pattern with super black barbule modifications. Barbules toward the tip of super black feathers were highly modified, whereas barbules toward the base of the same feathers had a typical normal morphology (Supplementary Fig. 7). Also, black feathers from the back of Lophorina superba, which are not used during display, had a typical normal morphology and were more reflective than super black feathers from the display cape with modified barbules (Supplementary Figs. 1c, h and 2c, h and Supplementary Table 1). These observations support the conclusion that the modified barbule morphology of super black feathers serves an optical, signaling function.

To directly quantify the effects of barbule surface microstructure on light absorption in feathers, we used virtual ray-tracing simulations to model the interaction of light with 3D nanoscale tomographic models of normal black and super black feathers (Supplementary Fig. 8). Ray-tracing simulations calculate the path and radiant power of light rays as they interact with a 3D model. Each time a simulated light ray intersects the feather surface (a scattering event), a portion of its radiant power is reflected from the surface, and the remaining portion is transmitted into the material where it can be absorbed. Our simulations assumed no surface roughness and 100% absorption of transmitted light. These assumptions restricted light scattering to the specular direction and allowed us to control for any variation in pigmentation, internal structure, or surface roughness that might be present in the real feathers. Thus, the ray-tracing experiments isolated the effects of external feather microstructure on light scattering to characterize structural absorption among feathers with different barbule morphologies.

Our findings demonstrate that super black bird of paradise feathers structurally absorbs up to 99.95% of directly incident light, and that variation in external surface microstructure can contribute to observed differences in visual appearance of bird plumage. The vertically tilted barbule arrays of super black bird of paradise feathers create deep, curved cavities. This morphology is distinct from the longitudinal ridges of butterfly scales11 and the vertical cones of snake scales13, substantially expanding the diversity of structurally absorbing biological materials in nature.

The extreme directional reflectance bias in super black feathers is congruent with field observations of bird of paradise courtship behavior22. Males of many species perform displays that maintain a specific directional orientation between their ornaments and the viewing females17 (Fig. 1g). We hypothesize that the tilted barbule arrays function in coordination with the behavioral repertoire to ensure that females view super black plumage patches at their darkest orientation.

Further research is required to understand the role of multiple scattering among barbs and barbules of multiple feathers in structural absorption by the entire plumage, and on the color correction mechanisms of birds. However, it is clear that structural absorption should be considered along with pigments, structural coloration, and specular reflection, as an important component in determining the visual appearance of organisms. Biological examples of structural absorption have in at least one case inspired the fabrication of new biomimetic materials15, and the feather structures described herein may have similar direct applications.

Five bird species with profoundly black plumage and two species with normal black plumage were identified by visual observation of museum study skins from the Yale Peabody Museum (YPM), Harvard Museum of Comparative Zoology (MCZ), American Museum of Natural History (AMNH), and the University of Kansas Biodiversity Institute (KU). Details of the specimens and plumage patches studied are summarized in Supplementary Table 1. To the human observer, super black plumage had a strongly matte appearance with so little specular reflectance that it was difficult to focus on the surface of the plumage and distinguish individual feathers. The species with normal black plumage lacked any conspicuous glossy specular highlights. Individual contour feathers were sampled from museum skins for scanning electron microscopy (SEM) and synchrotron-radiation X-ray microtomograhy (nano-CT). We could not obtain SEM of Lophorina superba back feathers or CT scans for Lophorina superba back and display cape feathers due to availability of material. Visual inspection of the Lophorina back plumage using a light microscope confirmed that the barbules have normal morphology, without the modified barbule arrays present in super black feathers.

Light reflectance and absorbance by the plumage can be influenced by the specific orientation of the feathers in the plumage and also by the interaction of light scattered by multiple feathers. The optical properties of the intact plumage cannot be reconstructed reliably by plucking feathers and then laying them (singly or together) on a different surface. Therefore, reflectance spectra of super black and normal black plumage patches were recorded directly from the plumage of prepared museum skins.

The directional reflectance, transmittance, and absorbance of super black and normal black plumage patches were analyzed by numerical ray trace simulations using the software package FRED31 (Photon Engineering LLC). Simulations employing two types of illumination were conducted for each feather: (1) omni-directional and (2) directional.

The ray-tracing simulation proceeded as follows: first, rays with equal amounts of radiant power were emitted from the light source and propagated in the direction of the feather. Then, rays repeatedly intersected the surfaces of the feather vane and reflected from those surfaces in the specular direction until they exited the volume of space occupied by the feather vane and terminated on a hemisphere. For each ray, the simulation recorded the number of light ray-surface intersections, the hemisphere of and spherical coordinates of the termination point, and the ending radiant power. For each ray, absorbance was calculated from the difference between the starting and ending radiant power. For comparison with the directional reflectance spectrophotometry measurements, total absorbance under 0 normal directional illumination was calculated as the sum of reflected light rays that terminated within an angular range of 27. Percent multiple scattering was calculated as the percentage of this set of rays that scattered two or more times off of the surface of the feather.

To determine how reflectance varies based on the angle incident light and viewing directions, we calculated the locally averaged reflectance at different viewing directions with a nonparametric kernel regression fit using the kreg function with default settings from the R package gplm. The kernel density estimate and regression fits were evaluated at 400 points, representing different viewing directions that were uniformly distributed over the reflectance hemisphere, and the results were plotted as a log-scale color gradient on orthogonal projections of the hemisphere using the persp3d function from the R package rgl.

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