Varying and Unchanging Whiteness on the Wings of Dusk-Active and Shade-Inhabiting Carystoides Escalantei Butterflies

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Varying and Unchanging Whiteness on the Wings of Dusk-Active and Shade-Inhabiting Carystoides Escalantei Butterflies Varying and unchanging whiteness on the wings of dusk-active and shade-inhabiting Carystoides escalantei butterflies Dengteng Gea,b, Gaoxiang Wua, Lili Yangc, Hye-Na Kima, Winnie Hallwachsd, John M. Burnse, Daniel H. Janzend,1, and Shu Yanga,1 aDepartment of Materials Science and Engineering, University of Pennsylvania, Philadelphia, PA 19104; bState Key Laboratory for Modification of Chemical Fibers and Polymer Materials, Institute of Functional Materials, Donghua University, Shanghai 201620, People’s Republic of China; cState Key Laboratory for Modification of Chemical Fibers and Polymer Materials, College of Materials Science and Engineering, Donghua University, Shanghai 201620, People’s Republic of China; dDepartment of Biology, University of Pennsylvania, Philadelphia, PA 19104-6018; and eDepartment of Entomology, National Museum of Natural History, Smithsonian Institution, Washington, DC 20013-7012 Contributed by Daniel H. Janzen, May 23, 2017 (sent for review January 19, 2017; reviewed by May R. Berenbaum, Jun Hyuk Moon, and John Shuey) Whiteness, although frequently apparent on the wings, legs, Natural whiteness is often attributed to the scattering or dif- antennae, or bodies of many species of moths and butterflies, along fusion of light from (sub)micrometer-sized textures including with other colors and shades, has often escaped our attention. Here, ribs, ridges, pores, and others (25, 26) as seen as white spots and we investigate the nanostructure and microstructure of white spots stripes on the wings of Morpho cypris and Morpho rhetenor helena on the wings of Carystoides escalantei, a dusk-active and shade- (18, 27) in the Nymphalidae. Other species, such as Pieris inhabiting Costa Rican rain forest butterfly (Hesperiidae). On both brassicae and Delias nigrina in the Pieridae, have 100- to 500-nm males and females, two types of whiteness occur: angle depen- beads randomly packed in-between ribs and cross-ribs, enhanc- dent (dull or bright) and angle independent, which differ in the ing the whiteness (19). Metallic to silvery whiteness occurs on microstructure, orientation, and associated properties of their some butterfly wings as the result of mixing structure colors scales. Some spots on the male wings are absent from the female reflected from the membrane scale. For example, the thickness EVOLUTION wings. Whether the angle-dependent whiteness is bright or dull between ribs and scale membrane on Argyrophorus argenteus depends on the observation directions. The angle-dependent (Nymphalidae) wings changes across the wing; although multiple scales also show enhanced retro-reflection. We speculate that reflective colors can be seen at the microscopic scale, bright Carystoides the biological functions and evolution of spot pat- metallic white appears at the macroscopic scale (28). The ease terns, scale structures, and their varying whiteness are adapta- with which shining metallic whiteness could be distinguished ’ tions to butterfly s low light habitat and to airflow experienced from dull whiteness and other colors could be important for on the wing base vs. wing tip. communication between butterflies and for the butterfly’s evolution–devolution. butterfly wings | whiteness | angle dependent | retro-reflection | Here, we investigate a dusk-active and shade-inhabiting Costa Area de Conservación Guanacaste Rican hesperiid butterfly, also known as a “skipper butterfly,” Carystoides escalantei (janzen.sas.upenn.edu/) (29), which has utterflies and moths display on their wings a dazzling array of different types of whiteness, including angle dependent (dull vs. Bcolors (1, 2)—from jet black, looking like a hole in the wing, — to bright white like a bicycle reflector in automobile headlights Significance and with every imaginable color chart hue in-between. Not only are the colors there, but they occur in hundreds of thousands of Whiteness, although frequently apparent on the wings, legs, patterns. Wings are flying billboards and exceedingly complex antennae, or bodies of many species of moths and butterflies, answers to the optimization that past and present natural se- has often escaped our attention. Here, we investigate the lection imposes, whether to some aspect of courtship or escape nanostructure and microstructure of white spots on the wings from predators (3, 4), and even at times in regulating body of Carystoides escalantei, a dusk-active and shade-inhabiting temperature or as serendipitous outcomes of selection for Costa Rican rain forest butterfly (Hesperiidae). We identify two texture, toughness, waterproofing, light weight, and air friction types of whiteness: angle dependent and angle independent. – (5 7). To date, most attention has been on the mechanics and We speculate that the biological functions and evolution of chemistry of a particular color of some easily accessible species Carystoides spot patterns, scale structures, and their varying that are particularly attractive to humans. For example, the whiteness are adaptations to the butterfly’s low light habitat bright blue morpho butterflies (8–12) have inspired many phys- and to airflow experienced on the wing base vs. wing tip icists, materials scientists, and engineers to investigate how the during flight. Sex and species differences in the location of color is produced (9, 13–15), and then to mimic the color and its angle-dependent white spots on the wings may function in mechanisms, or the combination of color and water repellency both intraspecific and interspecific communication. (11, 16, 17). Whiteness, although frequently apparent on the wings, legs, or Author contributions: D.G., W.H., D.H.J., and S.Y. designed research; D.G., G.W., L.Y., and bodies of many species of moths and butterflies, along with other H.-N.K. performed research; J.M.B. and D.H.J. identified the butterflies; D.G., G.W., L.Y., – H.-N.K., W.H., D.H.J., and S.Y. analyzed data; and D.G., W.H., J.M.B., D.H.J., and S.Y. wrote colors and shades (18 21), has received relatively little attention the paper. and is easily ignored. Although “white” may often be simply one Reviewers: M.R.B., University of Illinois at Urbana–Champaign; J.H.M., Sogang University; more color among many within a larger complex pattern, there and J.S., The Nature Conservancy. are times when the whiteness itself appears to be a key signal. “ ” The authors declare no conflict of interest. Note that there is no pigment for whiteness. Indeed, structural 1To whom correspondence may be addressed. Email: [email protected] or whiteness is technologically important in systems ranging from [email protected]. power-efficient computer displays, to sensors, to energy-efficient This article contains supporting information online at www.pnas.org/lookup/suppl/doi:10. buildings, windows, and vehicles (22–24). 1073/pnas.1701017114/-/DCSupplemental. www.pnas.org/cgi/doi/10.1073/pnas.1701017114 PNAS Early Edition | 1of6 Downloaded by guest on September 27, 2021 bright) and angle independent, on its wings and antennae. We (janzen.sas.upenn.edu/) (30). It likely serves three broad func- tested the white spots on all of the species of Carystoides ex- tions: part of courtship under low or limiting light conditions amined here, and none of them is UV reflective. Some of the (poor visibility at dusk or dawn), part of aposematic warning white spots on the male Carystoides wing are not present on the coloration, and when the skipper is perched, some mimetic re- female forewing, suggesting an intersexually different biological semblance to rotting and fungus-attacked inedible foliage. function. We characterize the micromorphology of each white Carystoides escalantei (Fig. 1) (Hesperiidae), a medium-small spot and infer the relationship between the optical properties denizen of Neotropical rain forest, is common in ACG mid- and structures. The wing scales from angle-independent white elevation rain forests. Its caterpillars, feeding on the leaves of spots are laid down and stacked on top of each other on the wing understory palms (janzen.sas.upenn.edu/caterpillars/database. membrane. These scales have high aspect ratio (AR = length/ lasso), have often been found and reared by the ACG Lepi- width) of ∼3–5. The scales on angle-dependent white spots, doptera inventory (31, 32). The adult butterflies, however, are however, stand vertically on the membrane at different scale rarely seen because they fly at dusk and in the deep shade, and angles. It appears that the hierarchically structured contours their colors are dull, drab, and inconspicuous compared with the consisting of ridges, nanoribs, and scale membranes, all con- brilliant colors of many other more sun-loving butterflies. When tribute to the appearance of the whiteness on Carystoides escalantei. a pinned, dried specimen of Carystoides escalantei with its wings The scales in angle-independent white spots have micrometer-sized spread open in a horizontal plane is placed on a flat surface for periodically occurring ridges with micropores in-between, whereas routine perpendicular examination, the large spots on the wing the scales in angle-dependent white spots have vertically tilted look plain white; but when viewed at a low angle, the white spots scales with undulated, periodic ridges, and the ribs are perpen- look brilliant. This in turn prompted reexamination of living dicular to the ridges on both sides of the scale. Whether the butterflies when they perched on plants (Fig. 1 A–C). In the angle-dependent whiteness is bright or dull depends on whether image of a male Carystoides, ventral hindwing spots are bright the scales are observed from the wing base or the wing tip. white in an oblique frontal view (Fig. 1B) but inconspicuous in a Furthermore, the angle-dependent scales show enhanced retro- perpendicular side view (Fig. 1A). The female Carystoides, on the reflection. We postulate that the different kinds of whiteness other hand, has nearly lost the white spots on the underside of its resulting from microstructure and orientation of Carystoides are hindwing (Fig. 1C). adaptations to their low light habitat and interspecific and in- On the midsection of the upper side of the male Carystoides traspecific communication.
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