Cicada; Fluorescence; Insect; Nonlinear optics; Resilin; SHG; Two-photon fluorescence; Chemical aspects; Fluorescence emission; Insect wings; Linear optical techniques; Nonlinear optical technique; Physical aspects; Two photon fluorescence; Biophysics; Biochemistry; Atomic and Molecular Physics, and Optics; Chemistry (all); Condensed Matter Physics; General Chemistry
Abstract :
[en] For most natural organisms, the physical, chemical and biological aspects of fluorescence emission are poorly understood. For example, to the best of our knowledge, fluorescence from the transparent wings of any of the 3000 known species of cicadas has never been reported in the literature. These wings are known to exhibit anti-reflective properties arising from quasi-periodic arrays of nipples. Our study, using linear and nonlinear optical techniques, including spectrofluorimetry, two-photon fluorescence spectroscopy and Second Harmonic Generation (SHG), reveals the fluorescence properties in the wings the grey and the common cicadas (Cicada orni and Lyristes (Tibicen) plebejus, respectively), as well as the broad-bordered bee hawk-moth (Hemaris fuciformis). The study suggests that fluorescence would be more widespread in transparent insect wings than what was previously believed. Comparing this result to the fluorescence emission from the wings of the Bornean damselfly (Vestalis amabilis), we inferred that this emission probably arises from resilin, a protein reported to enhance wing flexibility. Moreover, the nonlinear optical investigation of the insects’ wings provided further insight into wing structure, indicating that multiphoton techniques add valuable information for the analysis of insect integuments. The strong SHG signal detected from the wing veins implies that these veins are materially organised in a non-centrosymmetric and hence non-random fashion.
Disciplines :
Physics
Author, co-author :
Mouchet, Sébastien R. ; School of Physics, University of Exeter, Exeter, United Kingdom ; Department of Physics & Namur Institute of Structured Matter (NISM), University of Namur, Namur, Belgium
Verstraete, Charlotte; Molecular Imaging and Photonics, Department of Chemistry, KU Leuven, Heverlee, Belgium
Bokic, Bojana; Center for Photonics, Institute of Physics, University of Belgrade, Belgrade, Serbia
Mara, Dimitrije; Molecular Imaging and Photonics, Department of Chemistry, KU Leuven, Heverlee, Belgium ; L3 – Luminescent Lanthanide Lab, Department of Chemistry, Ghent University, Ghent, Belgium ; Institute of General and Physical Chemistry, Belgrade, Serbia
Dellieu, Louis; Department of Physics & Namur Institute of Structured Matter (NISM), University of Namur, Namur, Belgium
Orr, Albert G.; Environmental Futures Centre, Griffith University, Nathan, Australia
Deparis, Olivier; Department of Physics & Namur Institute of Structured Matter (NISM), University of Namur, Namur, Belgium
Van Deun, Rik; L3 – Luminescent Lanthanide Lab, Department of Chemistry, Ghent University, Ghent, Belgium
Verbiest, Thierry; Molecular Imaging and Photonics, Department of Chemistry, KU Leuven, Heverlee, Belgium
Vukusic, Pete; School of Physics, University of Exeter, Exeter, United Kingdom
Kolaric, Branko ; Université de Mons - UMONS ; Center for Photonics, Institute of Physics, University of Belgrade, Belgrade, Serbia
Language :
English
Title :
Revealing natural fluorescence in transparent insect wings by linear and nonlinear optical techniques
R400 - Institut de Recherche en Science et Ingénierie des Matériaux
Funding text :
SRM was supported by the Belgian National Fund for Scientific Research (FRS-FNRS) ( 91400/1.B.309.18F ), the Maturation Fund of the Walloon Region , and a BEWARE Fellowship (Convention n° 2110034 ) of the Walloon Region ( Marie Skłodowska-Curie Actions of the European Union - COFUND - contract 847587 ), as a Postdoctoral Researcher. DM acknowledges KU Leuven Postdoctoral Mandate Internal Funds (PDM) for a Postdoctoral fellowship ( PDM/20/092 ). TV acknowledges financial support from the Hercules Foundation . BK and BB acknowledge financial support of the Ministry of Education, Science and Technological Development of the Republic of Serbia (grant III 45016 ). BK, BB and DM acknowledge the support of the Office of Naval Research Global through the Research Grant N62902-22-1-2024 . In addition, BK acknowledges support from FRS-FNRS . This research used resources of the Lasers, Optics & Spectroscopies (LOS) Technology Platform ( https://platforms.unamur.be/los ) of UNamur.
Pavan, M., Vachon, M., Sur l'existence d'une substance fluorescente dans les téguments des scorpions (Arachnides). C. R. Acad. Sci. 239 (1954), 1700–1702.
Tani, K., Watari, F., Uo, M., Morita, M., Fluorescent properties of porcelain-restored teeth and their discrimination. Mater. Trans. 45 (2004), 1010–1014.
Vukusic, P., Hooper, I., Directionally controlled fluorescence emission in butterflies. Science, 310, 2005, 1151.
Iriel, A., Lagorio, M.G., Is the flower fluorescence relevant in biocommunication?. Naturwissenschaften 97:10 (2010), 915–924.
Iriel, A., Lagorio, M.G., Implications of reflectance and fluorescence of Rhododendron indicum flowers in biosignaling. Photochem. Photobiol. Sci. 9 (2010), 342–348.
Welch, V.L., Van Hooijdonk, E., Intrater, N., Vigneron, J.-P., Fluorescence in insects. Proc. SPIE, 8480, 2012, 848004.
Lagorio, M.G., Cordon, G.B., Iriel, A., Reviewing the relevance of fluorescence in biological systems. Photochem. Photobiol. Sci. 14 (2015), 1538–1559.
Gruber, D.F., Gaffney, J.P., Mehr, S., DeSalle, R., Sparks, J.S., Platisa, J., Pieribone, V.A., Adaptive evolution of eel fluorescent proteins from fatty acid binding proteins produces bright fluorescence in the marine environment. PLoS One, 10(11), 2015, e0140972.
Gruber, D.F., Loew, E.R., Deheyn, D.D., Akkaynak, D., Gaffney, J.P., Smith, W.L., Davis, M.P., Stern, J.H., Pieribone, V.A., Sparks, J.S., Biofluorescence in catsharks (Scyliorhinidae): fundamental description and relevance for elasmobranch visual ecology. Sci. Rep. 6:24751 (2016), 1–16.
Mouchet, S.R., Lobet, M., Kolaric, B., Kaczmarek, A.M., Van Deun, R., Vukusic, P., Deparis, O., Van Hooijdonk, E., Controlled fluorescence in a beetle's photonic structure and its sensitivity to environmentally induced changes. Proc. R. Soc. Lond. B Biol. Sci., 283(1845), 2016.
Marshall, J., Johnsen, S., Fluorescence as a means of colour signal enhancement. Philos. Trans. R. Soc. Lond. B Biol. Sci., 372(1724), 2017.
Deschepper, P., Jonckheere, B., Matthys, J., A light in the dark: the discovery of another fluorescent frog in the Costa Rican rainforests. Wilderness Environ. Med. 29:3 (2018), 421–422.
Mouchet, S.R., Kaczmarek, A.M., Mara, D., Van Deun, R., Vukusic, P., Colour and fluorescence emission of Euchroea auripigmenta beetle. Proc. SPIE 10965 (2019), 72–82.
Ladouce, M., Barakat, T., Su, B.-L., Deparis, O., Mouchet, S.R., Scattering of ultraviolet light by avian eggshells. Faraday Discuss. 223 (2020), 63–80.
Ladouce, M., Barakat, T., Su, B.-L., Deparis, O., Mouchet, S.R., UV scattering by pores in avian eggshells. Proc. SPIE 11481 (2020), 101–109.
Mohd Top, M., Puan, C.L., Chuang, M.-F., Othman, S.N., Borzée, A., First record of ultraviolet fluorescence in the bent-toed gecko Cyrtodactylus quadrivirgatus taylor, 1962 (Gekkonidae: Sauria). Herpetol. Notes 13 (2020), 211–212.
Croce, A.C., Light and autofluorescence, multitasking features in living organisms. Photochemistry 1:2 (2021), 67–124.
Reinhold, L., Mammals with fluorescent fur: observations from the wet tropics. North Queensl. Nat. 51 (2021), 1–8.
Toussaint, S.L.D., Ponstein, J., Thoury, M., Métivier, R., Kalthoff, D.C., Habermeyer, B., Guilard, R., Bock, S., Mortensen, P., Sandberg, S., Gueriau, P., Amson, E., Fur glowing under ultraviolet: in situ analysis of porphyrin accumulation in the skin appendages of mammals. Integr. Zool. 0 (2021), 1–12.
Stoddart, P.R., Cadusch, P.J., Boyce, T.M., Erasmus, R.M., Comins, J.D., Optical properties of chitin: surface-enhanced Raman scattering substrates based on antireflection structures on cicada wings. Nanotechnology, 17(3), 2006, 680.
Sun, M., Liang, A., Zheng, Y., Watson, G.S., Watson, J.A., A study of the anti-reflection efficiency of natural nano-arrays of varying sizes. Bioinspiration Biomimetics, 6(2), 2011, 026003.
Dellieu, L., Sarrazin, M., Simonis, P., Deparis, O., Vigneron, J.-P., A two-in-one superhydrophobic and anti-reflective nanodevice in the grey cicada Cicada orni (Hemiptera). J. Appl. Phys., 116(2), 2014, 024701.
Deparis, O., Mouchet, S.R., Dellieu, L., Colomer, J.-F., Sarrazin, M., Nanostructured surfaces: bioinspiration for transparency, coloration and wettability. Mater. Today Proc. 1S (2014), 122–129.
Verstraete, C., Mouchet, S.R., Verbiest, T., Kolaric, B., Linear and nonlinear optical effects in biophotonic structures using classical and nonclassical light. J. Biophot., 2019, e201800262.
Yoshida, A., Motoyama, M., Kosaku, A., Miyamoto, K., Nanoprotuberance array in the transparent wing of a hawkmoth, Cephonodes hylas. Zool. Sci. 13:4 (1996), 525–526.
Yoshida, A., Motoyama, M., Kosaku, A., Miyamoto, K., Antireflective nanoprotuberance array in the transparent wing of a hawkmoth, Cephonodes hylas. Zool. Sci. 14:5 (1997), 737–741.
Yoshida, A., Antireflection of the butterfly and moth wings through microstructure. Forma 17:2 (2002), 75–89.
Hooper, I.R., Vukusic, P., Wootton, R.J., Detailed optical study of the transparent wing membranes of the dragonfly Aeshna cyanea. Opt Express 14:11 (2006), 4891–4897.
Deparis, O., Khuzayim, N., Parker, A., Vigneron, J.-P., Assessment of the antireflection property of moth wings by three-dimensional transfer-matrix optical simulations. Phys. Rev. E, 79, 2009, 041910.
Stavenga, D.G., Thin film and multilayer optics cause structural colors of many insects and birds. Mater. Today Proc. 1S (2014), 109–121.
Siddique, R., Gomard, G., Hölscher, H., The role of random nanostructures for the omnidirectional anti-reflection properties of the glasswing butterfly. Nat. Commun., 6, 2015, 6909.
Mouchet, S.R., Verstraete, C., Mara, D., Cleuvenbergen, S.V., Finlayson, E.D., Van Deun, R., Deparis, O., Verbiest, T., Maes, B., Vukusic, P., Kolaric, B., Nonlinear optical spectroscopy and two-photon excited fluorescence spectroscopy reveal the excited states of fluorophores embedded in a beetle's elytra. Interface Focus, 9(1), 2019, 20180052.
Bernhard, C.G., The insect corneal nipple array. a biological, broad-band impedance transformer that acts as an antireflection coating. Acta Physiol. Scand. 63:243 (1965), 1–79.
Stavenga, D.G., Foletti, S., Palasantzas, G., Arikawa, K., Light on the moth-eye corneal nipple array of butterflies. Proc. R. Soc. Lond. B Biol. Sci. 273:1587 (2006), 661–667.
Xie, G., Zhang, G., Lin, F., Zhang, J., Liu, Z., Mu, S., The fabrication of subwavelength anti-reflective nanostructures using a bio-template. Nanotechnology, 19(9), 2008, 095605.
Zada, I., Zhang, W., Sun, P., Imtiaz, M., Abbas, W., Zhang, D., Multifunctional, angle dependent antireflection, and hydrophilic properties of SiO2 inspired by nano-scale structures of cicada wings. Appl. Phys. Lett., 111(15), 2017, 153701.
Zhang, G., Zhang, J., Xie, G., Liu, Z., Shao, H., Cicada wings: a stamp from nature for nanoimprint lithography. Small 2:12 (2006), 1440–1443.
Sun, M., Watson, G.S., Zheng, Y., Watson, J.A., Liang, A., Wetting properties on nanostructured surfaces of cicada wings. J. Exp. Biol. 212:19 (2009), 3148–3155.
Wisdom, K.M., Watson, J.A., Qu, X., Liu, F., Watson, G.S., Chen, C.-H., Self-cleaning of superhydrophobic surfaces by self-propelled jumping condensate. Proc. Natl. Acad. Sci. USA 110:20 (2013), 7992–7997.
Román-Kustas, J., Hoffman, J.B., Reed, J.H., Gonsalves, A.E., Oh, J., Li, L., Hong, S., Jo, K.D., Dana, C.E., Miljkovic, N., Cropek, D.M., Alleyne, M., Molecular and topographical organization: influence on cicada wing wettability and bactericidal properties. Adv. Mater. Interfac., 7(10), 2020, 2000112.
Kelleher, S.M., Habimana, O., Lawler, J., O'Reilly, B., Daniels, S., Casey, E., Cowley, A., Cicada wing surface topography: an investigation into the bactericidal properties of nanostructural features. ACS Appl. Mater. Interfaces 8:24 (2016), 14966–14974.
Cockayne, E., I. The distribution of fluorescent pigments in Lepidoptera. Trans. R. Entomol. Soc. Lond. 72:1–2 (1924), 1–19.
Kumazawa, K., Tanaka, S., Negita, K., Tabata, H., Fluorescence from wing of Morpho sulkowskyi butterfly. Jpn. J. Appl. Phys. 33:1;4A (1994), 2119–2122.
Trzeciak, T.M., Wilts, B.D., Stavenga, D.G., Vukusic, P., Variable multilayer reflection together with long-pass filtering pigment determines the wing coloration of papilionid butterflies of the nireus group. Opt. Express 20:8 (2012), 8877–8890.
Wilts, B.D., Trzeciak, T.M., Vukusic, P., Stavenga, D.G., Papiliochrome II pigment reduces the angle dependency of structural wing colouration in nireus group papilionids. J. Exp. Biol. 215:5 (2012), 796–805.
Vigneron, J.-P., Kertész, K., Vértesy, Z., Rassart, M., Lousse, V., Bálint, Z., Biró, L.P., Correlated diffraction and fluorescence in the backscattering iridescence of the male butterfly Troides magellanus (Papilionidae). Phys. Rev. E, 78, 2008, 021903.
Van Hooijdonk, E., Barthou, C., Vigneron, J.-P., Berthier, S., Detailed experimental analysis of the structural fluorescence in the butterfly Morpho sulkowskyi (Nymphalidae). J. Nanophotonics, 5(1), 2011, 053525.
Van Hooijdonk, E., Barthou, C., Vigneron, J.-P., Berthier, S., Angular dependence of structural fluorescent emission from the scales of the male butterfly Troïdes magellanus (Papilionidae). J. Opt. Soc. Am. B 29:5 (2012), 1104–1111.
Gorb, S.N., Serial elastic elements in the damselfly wing: mobile vein joints contain resilin. Naturwissenschaften 86:11 (1999), 552–555.
Appel, E., Gorb, S.N., Resilin-bearing wing vein joints in the dragonfly Epiophlebia superstes. Bioinspiration Biomimetics, 6(4), 2011, 046006.
Appel, E., Heepe, L., Lin, C.-P., Gorb, S.N., Ultrastructure of dragonfly wing veins: composite structure of fibrous material supplemented by resilin. J. Anat. 227:4 (2015), 561–582.
Chuang, C.-J., Liu, C.-D., Patil, R.A., Wu, C.-C., Chang, Y.-C., Peng, C.-W., Chao, T.-K., Liou, J.-W., Liou, Y., Ma, Y.-R., Impact of cuticle photoluminescence on the color morphism of a male damselfly Ischnura senegalensis (Rambur, 1842). Sci. Rep., 6, 2016, 38051.
Burrows, M., Shaw, S.R., Sutton, G.P., Resilin and chitinous cuticle form a composite structure for energy storage in jumping by froghopper insects. BMC Biol. 6:41 (2008), 1–16.
Guillermo-Ferreira, R., Therézio, E.M., Gehlen, M.H., Bispo, P.C., Marletta, A., The role of wing pigmentation, UV and fluorescence as signals in a neotropical damselfly. J. Insect Behav. 27:1 (2014), 67–80.
Spurr, A.R., A low-viscosity epoxy resin embedding medium for electron microscopy. J. Ultra. Res. 26:1 (1969), 31–43.
Gullion, J.D., Gullion, T., Solid-state NMR study of the cicada wing. J. Phys. Chem. B 121:32 (2017), 7646–7651.
Hai, T.A.P., Sugimoto, R., Fluorescence control of chitin and chitosan fabricated via surface functionalization using direct oxidative polymerization. RSC Adv. 8 (2018), 7005–7013.
Azofeifa, D.E., Arguedas, H.J., Vargas, W.E., Optical properties of chitin and chitosan biopolymers with application to structural color analysis. Opt. Mater. 35 (2012), 175–183.
Andersen, S.O., Characterization of a new type of cross-linkage in resilin, a rubber-like protein. Biochim. Biophys. Acta 69 (1963), 249–262.
Lakowicz, J., Principles of Fluorescence Spectroscopy. 1999, Kluwer Academic/Plenum Publishers, New York, NY.
Ramanan, C., Hoon Kim, C., Marks, T.J., Wasielewski, M.R., Excitation energy transfer within covalent tetrahedral perylenediimide tetramers and their intermolecular aggregates. J. Phys. Chem. C 118 (2014), 16941–16950.
Kolaric, B., Vallée, R.A.L., Dynamics and stability of DNA mechano-nanostructures: energy-transfer investigations. J. Phys. Chem. C 114:3 (2010), 1430–1435.
Rabasović, M.D., Pantelić, D.V., Jelenković, B.M., Ćurčić, S.B., Rabasović, M.S., Vrbica, M.D., Lazović, V.M., Ćurčić, B.P., Krmpot, A.J., Nonlinear microscopy of chitin and chitinous structures: a case study of two cave-dwelling insects. J. Biomed. Opt., 20(1), 2015, 016010.
Verbiest, T., Clays, K., Rodriguez, V., Second-order Nonlinear Optical Characterization Techniques: an Introduction. 2009, CRC press.
Peitsch, D., Fietz, A., Hertel, H., de Souza, J., Ventura, D.F., Menzel, R., The spectral input systems of hymenopteran insects and their receptor-based colour vision. J. Comp. Physiol. 170:1 (1992), 23–40.
Stavenga, D.G., Colour in the eyes of insects. J. Comp. Physiol. 188:5 (2002), 337–348.
Stavenga, D.G., Surface colors of insects: wings and eyes. Functional Surfaces in Biology: Little Structures with Big Effects, 1, 2009, Springer Netherlands, Dordrecht, 285–306.
Lunau, K., Visual ecology of flies with particular reference to colour vision and colour preferences. J. Comp. Physiol. 200:6 (2014), 497–512.
Moan, J., Visible light and UV radiation. Brune, A., Hellborg, R., Persson, B., Pääkkönen, R., (eds.) Radiation at Home, Outdoors and in the Workplace Oslo), 2001, Scandinavian Science Publisher, 69–85.