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Structural Absorption by Barbule Microstructures of Super Black Bird of Paradise Feathers

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Structural Absorption by Barbule Microstructures of Super Black Bird of Paradise Feathers Structural absorption by barbule microstructures of super black bird of paradise feathers The Harvard community has made this article openly available. Please share how this access benefits you. Your story matters Citation McCoy, Dakota E., Teresa Feo, Todd Alan Harvey, and Richard O. Prum. 2018. “Structural absorption by barbule microstructures of super black bird of paradise feathers.” Nature Communications 9 (1): 1. doi:10.1038/s41467-017-02088-w. http://dx.doi.org/10.1038/ s41467-017-02088-w. Published Version doi:10.1038/s41467-017-02088-w Citable link http://nrs.harvard.edu/urn-3:HUL.InstRepos:34869052 Terms of Use This article was downloaded from Harvard University’s DASH repository, and is made available under the terms and conditions applicable to Other Posted Material, as set forth at http:// nrs.harvard.edu/urn-3:HUL.InstRepos:dash.current.terms-of- use#LAA ARTICLE DOI: 10.1038/s41467-017-02088-w OPEN Structural absorption by barbule microstructures of super black bird of paradise feathers Dakota E. McCoy 1, Teresa Feo2, Todd Alan Harvey3 & Richard O. Prum3 Many studies have shown how pigments and internal nanostructures generate color in nature. External surface structures can also influence appearance, such as by causing multiple scattering of light (structural absorption) to produce a velvety, super black appearance. Here fi 1234567890 we show that feathers from ve species of birds of paradise (Aves: Paradisaeidae) structu- rally absorb incident light to produce extremely low-reflectance, super black plumages. Directional reflectance of these feathers (0.05–0.31%) approaches that of man-made ultra- absorbent materials. SEM, nano-CT, and ray-tracing simulations show that super black feathers have titled arrays of highly modified barbules, which cause more multiple scattering, resulting in more structural absorption, than normal black feathers. Super black feathers have an extreme directional reflectance bias and appear darkest when viewed from the distal direction. We hypothesize that structurally absorbing, super black plumage evolved through sensory bias to enhance the perceived brilliance of adjacent color patches during courtship display. 1 Department of Organismic and Evolutionary Biology, Harvard University, Cambridge, MA 02138, USA. 2 Department of Vertebrate Zoology, MRC-116, National Museum of Natural History, Smithsonian Institution, Washington, DC 20013, USA. 3 Department of Ecology and Evolutionary Biology, and Peabody Museum of Natural History, Yale University, New Haven, CT 06520, USA. Dakota E. McCoy and Teresa Feo contributed equally to this work. Correspondence and requests for materials should be addressed to D.E.M. (email: [email protected]) NATURE COMMUNICATIONS | (2018) 9:1 | DOI: 10.1038/s41467-017-02088-w | www.nature.com/naturecommunications 1 ARTICLE NATURE COMMUNICATIONS | DOI: 10.1038/s41467-017-02088-w ird coloration is a model system for understanding evolu- (Supplementary Table 1). For Lophorina, we examined both the tion, speciation, and sexual selection1. Color-producing profoundly black plumage of the display cape and the normal B 1 mechanisms are generally assigned to two categories : (i) black plumage of the back, which is not used in display. pigmentary colors produced by molecules and (ii) structural We measured the spectral reflectance of each plumage patch colors produced by light scattering from nanoscale variation in using two methods: (1) total integrated (specular and diffuse) refractive index (e.g., channels of air within a keratin matrix). In reflectance was measured using an integrating sphere with a addition to color, the directional distribution of scattered light diffuse light source, and (2) normal directional reflectance was can also affect plumage appearance. The shape, orientation, and measured with a directional light source and a detector oriented smoothness of the feather barbs and barbules create directionally normal to the feather vane (see “Methods” for details). Both the dependent appearance, such as with glossy or iridescent plu- total integrated and normal directional reflectance measurements mage2, 3. confirmed that the profoundly black plumage patches were – However, the mechanism of “structural absorption4 8,” which darker than normal black plumage (Fig. 2, Supplementary Figs. 1 occurs when superficial features cause multiple scattering of and 2, and Supplementary Table 1). The directional reflectance of light5, 9, can also influence visual appearance. Each time light the profoundly black plumage patches was extremely low scatters at a surface interface, a proportion of that light is (0.05–0.31%), and was one to two orders of magnitude less than transmitted into the material, where it can be absorbed9.By the normal black plumages (3.2–4.7%) (Fig. 2b, Supplementary increasing the number of times light scatters, structurally Fig. 2, and Supplementary Table 1). The extremely low directional absorbing materials can increase total light absorption to produce reflectance of these five plumages is comparable to that of other – – a profoundly black appearance. For example, a shiny metal with a natural and man-made super black materials4 8, 10 15. smooth surface that reflects 30–70% of visible light can be con- Reflectance spectra differed between normal and super black verted to a matte black material that reflects less than 5% of light plumage: spectra of normal black plumages sloped upward above by adding microstructural surface complexity that increases ~600 nm (Fig. 2 and Supplementary Figs. 1a–c and 2a–c), which structural absorption5. Natural examples of structural absorption is typical of melanin pigments19. In contrast, reflectance spectra – have been described in the wing scales of butterflies10 12 and the of all five super black plumages were nearly flat (Fig. 2 and body scales of a snake13. Structurally absorbing, “super black”14, 15 Supplementary Figs. 1d–h and 2d–h), which is reminiscent of materials (which have extremely low, broadband reflectance) have super black carbon nanotube materials with exceptionally low important applications for a wide range of optical, thermal, reflectance over the entire visible range14. Super black plumage mechanical, and solar technologies, including thin solar cells4 and reflectance curves were also flatter than many man-made velvet the lining of space telescopes8. fabrics (Supplementary Fig. 3), profoundly black snake scales13, Decades of previous research have focused on the physics, and butterfly scales12. Super black plumages of birds of paradise chemistry, social function, and evolutionary history of bird plu- appear to have a more efficient, broadband absorption than other mage coloration1, 16. The polygynous birds of paradise (Aves: biological examples of structural absorption. Paradisaeidae) have evolved some of the most elaborate mating displays and plumage ornaments in all animals17 (Fig. 1). In multiple species from multiple genera in the family, males have Feather microstructure. SEM and nano-CT revealed striking deep, black, and velvety plumage patches immediately adjacent to differences in microscopic barbule morphology between normal brightly colored, highly saturated, and structurally colored plu- black and super black feathers (Fig. 3a, b and Supplementary mage patches (Fig. 1c–g). These black plumage patches have a Figs. 4–6). Barbules of normal black feathers had a typical, open strikingly matte appearance (i.e., lacking specular highlights) and pennaceous morphology with smooth margins and a horizontal appear profoundly darker than normal black plumage of closely orientation restricted to the plane of the barb rami (Fig. 3a and related species18 (Fig. 1a, b). Supplementary Figs. 4a, b, 5a, b, and 6a, b). In contrast, barbules Here we use spectrophotometry, scanning electron microscopy of all super black feathers had a highly modified morphology, (SEM), high-resolution synchrotron tomography (nano-CT), and with microscale spikes along the margins, reminiscent of dried optical ray-tracing simulations to investigate the role of structural oak leaves. Super black barbules curved up from the plane of the absorption in black feathers from seven species of birds of barb rami to form a densely packed array tilted ~30° toward the paradise. Unlike normal black feathers with typical barbules, we distal tip of the feather (Fig. 3b and Supplementary Figs. 4c–g, find that super black feathers have highly modified barbules 5c–f, and 6c–f). The resulting morphology––an array of deep, arranged in vertically tilted arrays, which increase multiple scat- curved cavities between the smallest branches of the feather vane tering of light and thus structural absorption. Super black feathers —is distinct from the microstructure of super black snake and – reduce specular reflection by one to two orders of magnitude butterfly scales13 and from man-made super black materials4 8. compared to that of normal black feathers and have extreme Often, color-producing feather pigments or nanostructures are directional bias corresponding to the viewing direction of a restricted to the exposed tips of overlapping feathers in the female observing a displaying male. Therefore, we hypothesize plumage1. We found a similar pattern with super black barbule that these feathers evolved to enhance the perceived brilliance of modifications. Barbules toward the tip of super black feathers adjacent color patches by generating an optical/sensory illusion were highly modified, whereas barbules toward the base of the during mating displays. same feathers had a typical
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