in

Air temperature drives the evolution of mid-infrared optical properties of butterfly wings

  • 1.

    Kinoshita, S., Structural Colors in the Realm of Nature (World Scientific, 2008).

  • 2.

    Sun, J., Bhushan, B. & Tong, J. Structural coloration in nature. RSC Adv. 3, 14862–14889 (2013).

    CAS 
    ADS 

    Google Scholar 

  • 3.

    Whitney, H. M. et al. Floral iridescence, produced by diffractive optics, acts as a cue for animal pollinators. Science 323, 130–133 (2009).

    CAS 
    PubMed 
    ADS 

    Google Scholar 

  • 4.

    Whitney, H. M., Kolle, M., Alvarez-Fernandez, R., Steiner, U. & Glover, B. J. Contributions of iridescence to floral patterning. Commun. Integr. Biol. 2, 230–232 (2009).

    PubMed 
    PubMed Central 

    Google Scholar 

  • 5.

    Moyroud, E. et al. Disorder in convergent floral nanostructures enhances signalling to bees. Nature 550, 469–474 (2017).

    CAS 
    PubMed 
    ADS 

    Google Scholar 

  • 6.

    Mason, C. W. Structural colors in feathers. II. J. Phys. Chem. 27, 401–448 (2005).

    Google Scholar 

  • 7.

    Mason, C. W. Structural colors in insects. III. J. Phys. Chem. 31, 1856–1872 (2005).

    Google Scholar 

  • 8.

    Roberts, N. W., Marshall, N. J. & Cronin, T. W. High levels of reflectivity and pointillist structural color in fish, cephalopods, and beetles. Proc. Natl. Acad. Sci. 109, E3387–E3387 (2012).

    CAS 
    PubMed 
    PubMed Central 
    ADS 

    Google Scholar 

  • 9.

    Zi, J. et al. Coloration strategies in peacock feathers. Proc. Natl. Acad. Sci. 100, 12576–12578 (2003).

    CAS 
    PubMed 
    PubMed Central 
    ADS 

    Google Scholar 

  • 10.

    McCoy, D. E., Feo, T., Harvey, T. A. & Prum, R. O. Structural absorption by barbule microstructures of super black bird of paradise feathers. Nat. Commun. 9, 1–8 (2018).

    CAS 
    PubMed 
    PubMed Central 
    ADS 

    Google Scholar 

  • 11.

    Teyssier, J., Saenko, S. V., Van Der Marel, D. & Milinkovitch, M. C. Photonic crystals cause active colour change in chameleons. Nat. Commun. 6, 1–7 (2015).

    Google Scholar 

  • 12.

    Cooper, K. M., Hanlon, R. T. & Budelmann, B. U. Physiological color change in squid iridophores. Cell Tissue Res. 259, 15–24 (1990).

    CAS 
    PubMed 

    Google Scholar 

  • 13.

    Glover, B. J. & Whitney, H. M. Structural colour and iridescence in plants: The poorly studied relations of pigment colour. Ann. Bot. 105, 505–511 (2010).

    PubMed 
    PubMed Central 

    Google Scholar 

  • 14.

    Shi, N. N. et al. Keeping cool: Enhanced optical reflection and radiative heat dissipation in Saharan silver ants. Science 349, 298–301 (2015).

    CAS 
    PubMed 
    ADS 

    Google Scholar 

  • 15.

    Preciado, J. A. et al. Radiative properties of polar bear hair. Am. Soc. Mech. Eng. Bioeng. Div. 54, 57–58 (2002).

    Google Scholar 

  • 16.

    Bosi, S. G., Hayes, J., Large, M. C. J. & Poladian, L. Color, iridescence, and thermoregulation in Lepidoptera. Appl. Opt. 47, 5235–5241 (2008).

    PubMed 
    ADS 

    Google Scholar 

  • 17.

    Kinoshita, S., Yoshioka, S., Fujii, Y. & Okamoto, N. Photophysics of structural color in the Morpho butterflies. Forma-Tokyo 17, 103–121 (2002).

    Google Scholar 

  • 18.

    Tabata, H., Kumazawa, K., Funakawa, M., Takimoto, J. I. & Akimoto, M. Microstructures and optical properties of scales of butterfly wings. Opt. Rev. 3, 139–145 (1996).

    Google Scholar 

  • 19.

    Krishna, A. et al. Infrared optical and thermal properties of microstructures in butterfly wings. Proc. Natl. Acad. Sci. USA 117, 1566–1572 (2020).

    CAS 
    PubMed 
    PubMed Central 
    ADS 

    Google Scholar 

  • 20.

    Tsai, C. C. et al. Physical and behavioral adaptations to prevent overheating of the living wings of butterflies. Nat. Commun. 11, 1–14 (2020).

    ADS 

    Google Scholar 

  • 21.

    Wilts, B. D., Vey, A. J. M., Briscoe, A. D. & Stavenga, D. G. Longwing (Heliconius) butterflies combine a restricted set of pigmentary and structural coloration mechanisms. BMC Evol. Biol. 17, 1–12 (2017).

    Google Scholar 

  • 22.

    Berthier, S. Thermoregulation and spectral selectivity of the tropical butterfly Prepona meander: A remarkable example of temperature auto-regulation. Appl. Phys. A Mater. Sci. Process. 80, 1397–1400 (2005).

    CAS 
    ADS 

    Google Scholar 

  • 23.

    Vukusic, P. & Sambles, J. R. Photonic structures in biology. Nature 424, 852–855 (2003).

    CAS 
    PubMed 
    ADS 

    Google Scholar 

  • 24.

    Siddique, R. H., Diewald, S., Leuthold, J. & Hölscher, H. Theoretical and experimental analysis of the structural pattern responsible for the iridescence of Morpho butterflies. Opt. Express 21, 14351–14361 (2013).

    PubMed 
    ADS 

    Google Scholar 

  • 25.

    Steindorfer, M. A., Schmidt, V., Belegratis, M., Stadlober, B. & Krenn, J. R. Detailed simulation of structural color generation inspired by the Morpho butterfly. Opt. Express 20, 21485–21494 (2012).

    PubMed 
    ADS 

    Google Scholar 

  • 26.

    Munro, J. T. et al. Climate is a strong predictor of near-infrared reflectance but a poor predictor of colour in butterflies. Proc. R. Soc. B Biol. Sci. 286, 20190234 (2019).

    Google Scholar 

  • 27.

    Incropera, F. P., DeWitt, D. P., Bergman, T. L. & Lavine, A. S. Fundamentals of Heat and Mass Transfer (Wiley, 2006).

  • 28.

    DeWitt, D. P., Incropera, F. P. “Physics of thermal radiation” in Theory and Practice of Radiation Thermometry, (1988), pp. 19–89.

  • 29.

    Howell, J. R., Menguc, M. P., Siegel, R. Thermal Radiation Heat Transfer (CRC Press, 2016).

  • 30.

    Lord, S. D. A new software tool for computing earth’s atmospheric transmission of near- and far-infrared radiation. NASA Tech. Memo. 103957 (1992).

  • 31.

    Raman, A. P., Anoma, M. A., Zhu, L., Rephaeli, E. & Fan, S. Passive radiative cooling below ambient air temperature under direct sunlight. Nature 515, 540–544 (2014).

    CAS 
    PubMed 
    ADS 

    Google Scholar 

  • 32.

    Krishna, A. & Lee, J. Morphology-driven emissivity of microscale tree-like structures for radiative thermal management. Nanoscale Microscale Thermophys. Eng. 22, 124–136 (2018).

    CAS 
    ADS 

    Google Scholar 

  • 33.

    Zhai, Y. et al. Scalable-manufactured randomized glass-polymer hybrid metamaterial for daytime radiative cooling. Science 355, 1062–1066 (2017).

    CAS 
    PubMed 
    ADS 

    Google Scholar 

  • 34.

    Zhang, X. A. et al. Dynamic gating of infrared radiation in a textile. Science 623, 1–15 (2019).

    Google Scholar 

  • 35.

    Xu, C., Stiubianu, G. T. & Gorodetsky, A. A. Adaptive infrared-reflecting systems inspired by cephalopods. Science 359, 1495–1500 (2018).

    CAS 
    PubMed 
    ADS 

    Google Scholar 

  • 36.

    Xie, D. et al. Broadband omnidirectional light reflection and radiative heat dissipation in white beetles: Goliathus goliatus. Soft Matter 15, 4294–4300 (2019).

    CAS 
    PubMed 
    ADS 

    Google Scholar 

  • 37.

    Heinrich, B. Thermoregulation in endothermic insects. Science 185, 747–756 (1974).

    CAS 
    PubMed 
    ADS 

    Google Scholar 

  • 38.

    Kingsolver, J. G. Thermoregulation and flight in Colias butterflies: elevational patterns and mechanistic limitations. Ecology 64, 534–545 (1983).

    Google Scholar 

  • 39.

    Rawlins, J. E. Thermoregulation by the black swallowtail butterfly, Papilio polyxenes (Lepidoptera: Papilionidae). Ecology 61, 345–357 (1980).

    Google Scholar 

  • 40.

    Clench, H. K. Behavioral thermoregulation in butterflies. Ecology 47, 1021–1034 (1966).

    Google Scholar 

  • 41.

    Bonebrake, T. C., Boggs, C. L., Stamberger, J. A., Deutsch, C. A. & Ehrlich, P. R. From global change to a butterfly flapping: Biophysics and behaviour affect tropical climate change impacts. Proc. R. Soc. B Biol. Sci. 281, 20141264 (2014).

    Google Scholar 

  • 42.

    Nève, G. & Hall, C. Variation of thorax flight temperature among twenty Australian butterflies (Lepidoptera: Papilionidae, Nymphalidae, Pieridae, Hesperiidae, Lycaenidae). Eur. J. Entomol. 113, 571–578 (2016).

    Google Scholar 

  • 43.

    MacLean, H. J., Higgins, J. K., Buckley, L. B. & Kingsolver, J. G. Morphological and physiological determinants of local adaptation to climate in Rocky Mountain butterflies. Conserv. Physiol. 4, 1 (2016).

    Google Scholar 

  • 44.

    Tsai, C. C., et al., Butterflies regulate wing temperatures using radiative cooling in 2017 Conference on Lasers and Electro-Optics (CLEO), (IEEE, 2017), p. 9.

  • 45.

    Watanabe, K., Hoshino, T., Kanda, K., Haruyama, Y. & Matsui, S. Brilliant blue observation from a Morpho-butterfly-scale quasi-structure. Jpn. J. Appl. Phys. 44, L48–L50 (2005).

    CAS 
    ADS 

    Google Scholar 

  • 46.

    Wilts, B. D., Giraldo, M. A. & Stavenga, D. G. Unique wing scale photonics of male Rajah Brooke’s birdwing butterflies. Front. Zool. 13, 1–12 (2016).

    Google Scholar 

  • 47.

    De Keyser, R., Breuker, C. J., Hails, R. S., Dennis, R. L. H. & Shreeve, T. G. Why small is beautiful: Wing colour is free from thermoregulatory constraint in the small lycaenid butterfly, Polyommatus icarus. PLoS One 10, e0122663 (2015).

    Google Scholar 

  • 48.

    Biró, L. P. et al., Role of photonic-crystal-type structures in the thermal regulation of a lycaenid butterfly sister species pair. Phys. Rev. E Stat. Physics, Plasmas, Fluids, Relat. Interdiscip. Top. 67, 7 (2003).

  • 49.

    Sala-Casanovas, M., Krishna, A., Yu, Z. & Lee, J. Bio-inspired stretchable selective emitters based on corrugated nickel for personal thermal management. Nanoscale Microscale Thermophys. Eng. 23, 173–187 (2019).

    CAS 
    ADS 

    Google Scholar 

  • 50.

    Phan, L. et al. Reconfigurable infrared camouflage coatings from a cephalopod protein. Adv. Mater. 25, 5621–5625 (2013).

    CAS 
    PubMed 

    Google Scholar 

  • 51.

    Pris, A. D. et al. Towards high-speed imaging of infrared photons with bio-inspired nanoarchitectures. Nat. Photonics 6, 564–564 (2012).

    CAS 
    ADS 

    Google Scholar 

  • 52.

    Krishna, A. et al. Ultraviolet to mid-infrared emissivity control by mechanically reconfigurable graphene. Nano Lett. 19, 5086–5092 (2019).

    CAS 
    PubMed 
    ADS 

    Google Scholar 

  • 53.

    Moharam, M. G. & Gaylord, T. K. Rigorous coupled-wave analysis of planar-grating diffraction. J. Opt. Soc. Am. 71, 811 (1981).

    ADS 

    Google Scholar 

  • 54.

    Moharam, M. G. Coupled-wave analysis of two-dimensional dielectric gratings in Holographic Optics: Design and Applications, (1988), p. 8.

  • 55.

    Peng, S. & Morris, G. M. Efficient implementation of rigorous coupled-wave analysis for surface-relief gratings. J. Opt. Soc. Am. A 12, 1087 (1995).

    ADS 

    Google Scholar 

  • 56.

    Moharam, M. G., Gaylord, T. K., Grann, E. B. & Pommet, D. A. Formulation for stable and efficient implementation of the rigorous coupled-wave analysis of binary gratings. J. Opt. Soc. Am. A 12, 1068 (1995).

    ADS 

    Google Scholar 

  • 57.

    Taflove, A., Hagness, S. C. Computational Electrodynamics: The Finite-Difference Time-Domain Method (Artech House, 2005).

  • 58.

    Fang, J. et al. Enhanced photocatalytic hydrogen production on three-dimensional gold butterfly wing scales/CdS nanoparticles. Appl. Surf. Sci. 427, 807–812 (2018).

    CAS 
    ADS 

    Google Scholar 

  • 59.

    Wilts, B. D., Leertouwer, H. L. & Stavenga, D. G. Imaging scatterometry and microspectrophotometry of lycaenid butterfly wing scales with perforated multilayers. J. R. Soc. Interface 6, S185–S192 (2009).

    PubMed 

    Google Scholar 

  • 60.

    Aideo, S. N., Mohanta, D. Investigation of manifestation of optical properties of butterfly wings with nanoscale zinc oxide incorporation. J. Phys: Confer. Ser. 765, 012019 (2016).

  • 61.

    Guan, Y. et al. Ordering of hollow Ag-Au nanospheres with butterfly wings as a biotemplate. Sci. Rep. 8, 1–7 (2018).

    Google Scholar 

  • 62.

    Simonsen, T. J. et al. Phylogenetics and divergence times of Papilioninae (Lepidoptera) with special reference to the enigmatic genera Teinopalpus and Meandrusa. Cladistics 27, 113–137 (2011).

    PubMed 

    Google Scholar 

  • 63.

    Wilts, B. D., Pirih, P., Arikawa, K. & Stavenga, D. G. Shiny wing scales cause spec(tac)ular camouflage of the angled sunbeam butterfly, Curetis acuta. Biol. J. Linn. Soc. 109, 279–289 (2013).

    Google Scholar 

  • 64.

    Wu, L., Han, Z., Qiu, Z., Guan, H. & Ren, L. The microstructures of butterfly wing scales in northeast of China. J. Bionic Eng. 4, 47–52 (2007).

    CAS 

    Google Scholar 

  • 65.

    Azofeifa, D. E., Arguedas, H. J. & Vargas, W. E. Optical properties of chitin and chitosan biopolymers with application to structural color analysis. Opt. Mater. (Amst) 35, 175–183 (2012).

    CAS 
    ADS 

    Google Scholar 

  • 66.

    Vargas, W. E., Azofeifa, D. E. & Arguedas, H. J. Índices de refracción de la quitina, el quitosano y el ácido úrico con aplicación en análisis de color estructural. Opt. Pura y Apl. 46, 55–72 (2013).

    Google Scholar 

  • 67.

    Herman, A., Vandenbem, C., Deparis, O., Simonis, P. & Vigneron, J. P. Nanoarchitecture in the black wings of Troides magellanus : A natural case of absorption enhancement in photonic materials. Nanophotonic Mater. VIII 8094, 80940H (2011).

    Google Scholar 

  • 68.

    Yoshioka, S. & Kinoshita, S. Wavelength-selective and anisotropic light-diffusing scale on the wing of the Morpho butterfly. Proc. Biol. Sci. 271, 581–587 (2004).

    PubMed 
    PubMed Central 

    Google Scholar 

  • 69.

    Catalanotti, S. et al. The radiative cooling of selective surfaces. Sol. Energy 17, 83–89 (1975).

    ADS 

    Google Scholar 

  • 70.

    Long Kou, J., Jurado, Z., Chen, Z., Fan, S. & Minnich, A. J. Daytime radiative cooling using near-black infrared emitters. ACS Photonics 4, 626–630 (2017).

    Google Scholar 

  • 71.

    Wasserthal, L. T. The role of butterfly wings in regulation of body temperature. J. Insect Physiol. 21, 1921–1930 (1975).

    Google Scholar 

  • 72.

    Peel, M. C., Finlayson, B. L. & McMahon, T. A. Updated world map of the Köppen-Geiger climate classification. Hydrol. Earth Syst. Sci. 11, 1633–1644 (2007).

    ADS 

    Google Scholar 

  • 73.

    New, M., Lister, D., Hulme, M. & Makin, I. A high-resolution data set of surface climate over global land areas. Clim. Res. 21, 1–25 (2002).

    Google Scholar 

  • 74.

    Weather Spark Weather Data. https://weatherspark.com (July 10, 2019).

  • 75.

    Weather Underground Historical Weather. https://www.wunderground.com/history/ (August 2, 2018).

  • 76.

    Liu, F. et al. Replication of homologous optical and hydrophobic features by templating wings of butterflies Morpho menelaus. Opt. Commun. 284, 2376–2381 (2011).

    CAS 
    ADS 

    Google Scholar 

  • 77.

    Chen, T., Cong, Q., Qi, Y., Jin, J. & Choy, K. L. Hydrophobic durability characteristics of butterfly wing surface after freezing cycles towards the design of nature inspired anti-icing surfaces. PLoS ONE 13, e0188775 (2018).

    PubMed 
    PubMed Central 

    Google Scholar 

  • 78.

    Fang, Y., Sun, G., Wang, T. Q., Cong, Q. & Ren, L. Q. Hydrophobicity mechanism of non-smooth pattern on surface of butterfly wing. Chin. Sci. Bull. 52, 711–716 (2007).

    Google Scholar 

  • 79.

    Garland, T., Harvey, P. H. & Ives, A. R. Procedures for the analysis of comparative data using phylogenetically independent contrasts. Syst. Biol. 41, 18–32 (1992).

    Google Scholar 

  • 80.

    Felsenstein, J. Phylogenies and the comparative method. Am. Nat. 125, 1–15 (1985).

    Google Scholar 

  • 81.

    Felsenstein, J. Phylogenies and quantitative characters. Annu. Rev. Ecol. Syst. 19, 445–471 (1988).

    Google Scholar 

  • 82.

    Espeland, M. et al. A comprehensive and dated phylogenomic analysis of butterflies. Curr. Biol. 28, 770–778.e5 (2018).

    CAS 
    PubMed 

    Google Scholar 

  • 83.

    Maddison, W. P. & Maddison, D. R. Mesquite: a modular system for evolutionary analysis. 2010. Version 2, 73 (2008).

    Google Scholar 

  • 84.

    Cai, W., Shalaev, V. M. Optical Metamaterials, 10th Ed. (Springer, 2010).

  • 85.

    Zheludev, N. I. & Kivshar, Y. S. From metamaterials to metadevices. Nat. Mater. 11, 917–924 (2012).

    CAS 
    PubMed 
    ADS 

    Google Scholar 

  • 86.

    Chen, Z., Zhu, L., Raman, A. & Fan, S. Radiative cooling to deep sub-freezing temperatures through a 24-h day-night cycle. Nat. Commun. 7, 1–5 (2016).

    Google Scholar 

  • 87.

    Mandal, J. et al. Hierarchically porous polymer coatings for highly efficient passive daytime radiative cooling. Science 362, 315–319 (2018).

    CAS 
    PubMed 
    ADS 

    Google Scholar 

  • 88.

    Lenert, A. et al. A nanophotonic solar thermophotovoltaic device. Nat. Nanotechnol. 9, 126–130 (2014).

    CAS 
    PubMed 
    ADS 

    Google Scholar 

  • 89.

    Quintiere, J. Radiative characteristics of fire fighters’ coat fabrics. Fire Technol. 10, 153–161 (1974).

    CAS 

    Google Scholar 

  • 90.

    Energy Sector Management Assistance Program (ESMAP). Global Solar Atlas 2.1: Technical Report. https://globalsolaratlas.info (World Bank, December 2019).

  • 91.

    Yoshioka, S. & Kinoshita, S. Direct determination of the refractive index of natural multilayer systems. Phys. Rev. E 83, 051917 (2011).

    ADS 

    Google Scholar 

  • 92.

    Leertouwer, H. L., Wilts, B. D. & Stavenga, D. G. Refractive index and dispersion of butterfly chitin and bird keratin measured by polarizing interference microscopy. Opt. Express 19, 24061–24066 (2011).

    CAS 
    PubMed 
    ADS 

    Google Scholar 

  • Great tits feed their nestlings with more but smaller prey items and fewer caterpillars in cities than in forests

    Longitudinal monitoring in Cambodia suggests higher circulation of alpha and betacoronaviruses in juvenile and immature bats of three species