Six species of birds of paradise and one close relative…More

Six species of birds of paradise and one close relative. a,b Species with normal black plumage patches. c–g Species with super black plumagepatches. a Paradise-crow (Lycocorax pyrrhopterus). b Lesser Melampitta (Melampitta lugubris), a Papuan corvoid closely related to birds of paradise. c Princess Stephanie’s Astrapia (Astrapia stephaniae). d Twelve-wired Birds-of-Paradise (Seleucidis melanoleucus). e Paradise Riflebird (Ptiloris paradiseus during courtship display). f Wahnes’ Parotia (Parotia wahnesi). g Superb Bird-of-Paradise (Lophorina superba) during courtship display with female (brown plumage). Photocredits: a @Hanom Bashari/Burung Indonesia; b Daniel López-Velasco; c Trans Niugini Tours; d–f Tim Laman; g Ed Scholes.

Examples of normal and super black feather microstructure…More

Examples of normal and super black feather microstructure. a SEM micrograph of Lycocorax pyrrhopterus normal black feather with typical barbule morphology; scale bar, 200 µm. b SEM micrograph of Parotia wahnesi super black feather with modified barbule arrays; scale bar, 50 µm. c Gold sputter-coated normal black breast feather of Melampitta lugubris appears gold. d Gold sputter-coated super black breast feather of Ptiloris paradiseus retains a black appearance indicating structural absorption. SEM stubs are 12.8 mm in diameter.

Ray-tracing simulations. a Simulation from FRED…More

Ray-tracing simulations. a Simulation from FRED showing the trace of a ray that scatters multiple times between barbules of a super black feather. b Substantial variation in frequency of multiple scattering events among species predicts variation in structural absorption. c Measured reflectance is significantly negatively correlated with the proportion of reflected rays that scattered at least twice (linear regression: R2 = 0.68, slope = −0.063, SE = 0.021, and P < 0.05)

Abstract

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 we show that feathers from five species of birds of paradise (Aves: Paradisaeidae) structurally 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.

Acknowledgements

Xianghui Xiao and the 2-BM beamline group provided assistance with CT scanning and analysis at the APS facility, Argonne National Lab. Jeremiah Trimble and Kate Eldridge assisted with collections usage…More. The research has been improved by discussions with David Brainard, David Shoehalter, Kristof Zyskowski, David Haig, James Harvey, Ryan Irvin, and members of the Prum Lab. Ed Scholes, Tim Laman, Trans Niugini Tours, Hanom Bashari, and Daniel López kindly gave permission to reproduce photos of birds of paradise (Fig. 1). Andrew Farris assisted with kermal regressions for the directional reflectance plots. This research was funded by the W. R. Coe Fund of Yale University, by a Sigma XI student research fellowship to D.E.M., and by a Mind, Brain, and Behavior Graduate Student Award to D.E.M. D.E.M. was supported by the Department of Defense (DoD) through the National Defense Science and Engineering Graduate Fellowship (NDSEG) Program. D.E.M. was also supported by a Theodore H. Ashford Graduate Fellowship in the Sciences. Tomography data collections at the Advanced Photon Source beamline 2-BM, Argonne National Laboratory were supported by the U.S. Department of Energy Office of Science (Proposal ID 41887). T.J.F. was supported by a NSF Postdoctoral Fellowship in Biology (#1523857). Richard Pfisterer of Photon Engineering graciously licensed FRED to T.A.H. for this research. This work was performed in part at the Harvard University Center for Nanoscale Systems (CNS), a member of the National Nanotechnology Coordinated Infrastructure Network (NNCI), which is supported by the National Science Foundation under NSF ECCS award no. 1541959.
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Press Coverage:

• New York Times: Ultra-Black is the New Black
  

• Scientific American: Back to Black: How Birds-of-Paradise Get Their Midnight Feathers
  

• Audubon: Birds-of-Paradise Have Feathers That Act Like Black Holes
  

• The Atlantic: Super-Black is the New Black
  

• Science: ‘Superblack’ bird of paradise feathers absorb 99.95% of light
  

• Wired: The World’s Most Metal Bird Makes Darkness Out of Chaos
  

• Gizmodo: These Birds Evolved Feathers So Dark, They’re Like a ‘Black Hole’
  

• Inside Science: BRIEF: For Birds of Paradise, Super-Black Feathers Make Bright Spots Shine
  

• Smithsonian: Scientists Shine New Light on the Blackest  Black Feathers
  

Six species of birds of paradise and one close relative. a,b Species with normal black plumage patches. c–g Species with super black plumagepatches. a Paradise-crow (Lycocorax pyrrhopterus). b Lesser Melampitta (Melampitta lugubris), a Papuan corvoid closely related to birds of paradise. c Princess Stephanie’s Astrapia (Astrapia stephaniae). d Twelve-wired Birds-of-Paradise (Seleucidis melanoleucus). e Paradise Riflebird (Ptiloris paradiseus during courtship display). f Wahnes’ Parotia (Parotia wahnesi). g Superb Bird-of-Paradise (Lophorina superba) during courtship display with female (brown plumage). Photocredits: a @Hanom Bashari/Burung Indonesia; b Daniel López-Velasco; c Trans Niugini Tours; d–f Tim Laman; g Ed Scholes.

Ray-tracing simulations. a Simulation from FRED showing the trace of a ray that scatters multiple times between barbules of a super black feather. b Substantial variation in frequency of multiple scattering events among species predicts variation in structural absorption. c Measured reflectance is significantly negatively correlated with the proportion of reflected rays that scattered at least twice (linear regression: R2 = 0.68, slope = −0.063, SE = 0.021, and P < 0.05)

Examples of normal and super black feather microstructure. a SEM micrograph of Lycocorax pyrrhopterus normal black feather with typical barbule morphology; scale bar, 200 µm. b SEM micrograph of Parotia wahnesi super black feather with modified barbule arrays; scale bar, 50 µm. c Gold sputter-coated normal black breast feather of Melampitta lugubris appears gold. d Gold sputter-coated super black breast feather of Ptiloris paradiseus retains a black appearance indicating structural absorption. SEM stubs are 12.8 mm in diameter.

Abstract

Our objective is to provide ornithologists with a tool for looking at 3D models of birds through the eyes of other birds. This tool overcomes the limits of the human visual system to allow scientists to quantify and analyze avian color in a completely novel way.

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Acknowledgements

National Science foundation grant 0852844. The specimens used in creating 3D models are housed at the Yale Peabody Museum (YPM). We thank Kristof Zyskowski of the Yale Peabody Museum for assisting with bird selections and…More Rômulo Carleial of the Universidade Federal de Minas Gerais for assisting with measurements. Our pipeline uses Patrick Min’s MESHCONV 3D model converter.
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Abstract

Light interacts with an organism's integument on a variety of spatial scales. For example in an iridescent bird: nano-scale structures produce color; the milli-scale structure of barbs and barbules largely determines the directional pattern of reflected light; and through the macro-scale spatial structure of overlapping, curved feathers, these directional effects create the visual texture. Milli-scale and macro-scale effects determine where on the organism's body, and from what viewpoints and under what illumination, the iridescent colors are seen. Thus, the highly directional flash of brilliant color from the iridescent throat of a hummingbird is inadequately explained by its nano-scale structure alone and questions remain. From a given observation point, which milli-scale elements of the feather are oriented to reflect strongly? Do some species produce broader "windows" for observation of iridescence than others? These and similar questions may be asked about any organisms that have evolved a particular surface appearance for signaling, camouflage, or other reasons.

In order to study the directional patterns of light scattering from feathers, and their relationship to the bird's milli-scale morphology, we developed a protocol for measuring light scattered from biological materials using many high-resolution photographs taken with varying illumination and viewing directions. Since we measure scattered light as a function of direction, we can observe the characteristic features in the directional distribution of light scattered from that particular feather, and because barbs and barbules are resolved in our images, we can clearly attribute the directional features to these different milli-scale structures. Keeping the specimen intact preserves the gross-scale scattering behavior seen in nature. The method described here presents a generalized protocol for analyzing spatially- and directionally-varying light scattering from complex biological materials at multiple structural scales.

Acknowledgements

The authors would like to thank Jaroslav Křivánek, Jon Moon, Edgar Velázquez-Armendáriz, Wenzel Jakob, James Harvey, Susan Suarez, Ellis Loew, and John Hermanson for their intellectual contributions…More. The Cornell Spherical Gantry was built from a design due to Duane Fulk, Marc Levoy, and Szymon Rusinkiewicz. This research was funded by the National Science Foundation (NSF CAREER award CCF-0347303 and NSF grant CCF-0541105).
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Average directional reflectance of rectangular regions of Chrysococcyx cupreus…More

Average directional reflectance of rectangular regions of Chrysococcyx cupreus: (A–C) 3 regions of the medial vane, (a–c) 3 regions of the lateral vane, and (Aa & Bb) 2 regions spanning both vanes. Luminance plotted in direction cosine space.

Special Committee

Dr. Susan Suarez, Dr. Steve Marschner, Dr. Kim Bostwick, Dr. Ellis Loew, and Dr. John Hermanson

Abstract

Birds have evolved diverse plumage through sophisticated morphological modifications. The interaction of light with these modifications alters the reflectance from feathers, producing complex and directionally-variable visual signals. I hypothesize that structural modifications of the feather produce anisotropic reflectance, the direction of which is determined by the orientation of the structure of the vane.

Variation in reflectance originates from the interplay of light with two classes of feather structure: its surface and subsurface volume. Different structural scales within the two structural classes influence light scattering within the UV-visible spectrum. The overall shape and surface of the feather vane (the macro-scale) and of its component members (the milli-scale) scatter light according to principles of geometric optics. Subsurface nano-scale structure in many feathers generate so-called “structural coloration,” which is a purely physical optics phenomenon and can differ drastically from ordinary coloration mechanisms such as pigmentation. Iridescence, from which many feathers derive their vivid, eye-catching changeable color, is one type of structural color that varies as a function of viewing angle.

This thesis presents investigations into a previously understudied aspect of avian visual signaling: directional reflectance and its relationship to milli-scale structure. Having observed that the stratified nano-scale morphology of structurally-colored plumage contours the milli-scale cortex of the vane, I determined that measurements of the milli-scale could be substituted for a more complex study of directional reflectance from the nano-scale. I thereby hypothesize that the direction of the reflectance from a vaned feather can be predicted from the orientation of its milli-scale morphology—its barbs and barbules. In collaboration with my colleagues at Cornell University, I developed non-destructive tools and methods to investigate the signaling potential of the feather. I correlate measurements of directional light scattering to the milli-scale morphology of select samples of structurally-colored bird plumage. The results of these analyses lead to a more thorough understanding of the relationships between directional reflectance and the structure of the feather itself. Having found the reflectance to be anisotropic, I demonstrate that the change in the direction of the reflectance over the surface of the vane can in fact be predicted from the orientation of the different branches of the barb. The improved understanding of the variation in directional reflectance over the surface of the feather, a phenotypic component, should allow for better comprehension of avian behavior, evolution of morphological adaptations, and the synthesis of more accurate predictive models.

RGB directional reflectance of a region between 2 barbs of the medial vane was subdivided…More

RGB directional reflectance of a region between 2 barbs of the medial vane was subdivided into 44 linear divisions. The Average reflectance of 22 subsampled divisions is shown: (1) of line 1 along a length of ramus; (2–21) along sequential lines following step-wise movements; (22) of line 22 along a length of the adjacent ramus.