Quantitative characterization of iridescent colours in biological studies: a novel method using optical theory

Iridescent colours are colours that change with viewing or illumination geometry. While they are widespread in many living organisms, most evolutionary studies on iridescence do not take into account their full complexity. Few studies try to precisely characterize what makes iridescent colours special: their angular dependency. Yet, it is likely that this angular dependency has biological functions and is therefore submitted to evolutionary pressures. For this reason, evolutionary biologists need a repeatable method to measure iridescent colours as well as variables to precisely quantify the angular dependency. In this study, we use a theoretical approach to propose five variables that allow one to fully describe iridescent colours at every angle combination. Based on the results, we propose a new measurement protocol and statistical method to reliably characterize iridescence while minimizing the required number of time-consuming measurements. We use hummingbird iridescent feathers and butterfly iridescent wings as test cases to demonstrate the strengths of this new method. We show that our method is precise enough to be potentially used at intraspecific level while being also time-efficient enough to encompass large taxonomic scales.

[1]  S. Berthier,et al.  Morphological structure and optical properties of the wings of Morphidae , 2006 .

[3]  R. Wootton,et al.  Remarkable iridescence in the hindwings of the damselfly Neurobasis chinensis chinensis (Linnaeus) (Zygoptera: Calopterygidae) , 2004, Proceedings of the Royal Society of London. Series B: Biological Sciences.

[4]  L. Biró,et al.  Variability of the Structural Coloration in Two Butterfly Species with Different Prezygotic Mating Strategies , 2016, PloS one.

[5]  Olimpia D. Onelli,et al.  Development of structural colour in leaf beetles , 2017, Scientific Reports.

[6]  Pierre-Paul Bitton,et al.  Plumage characteristics, reproductive investment and assortative mating in tree swallows Tachycineta bicolor , 2008, Behavioral Ecology and Sociobiology.

[7]  Chad M. Eliason,et al.  A photonic heterostructure produces diverse iridescent colours in duck wing patches , 2012, Journal of The Royal Society Interface.

[8]  D. Stavenga,et al.  Structural coloured feathers of mallards act by simple multilayer photonics , 2017, Journal of The Royal Society Interface.

[9]  S. Vignolini,et al.  Genetic manipulation of structural color in bacterial colonies , 2018, Proceedings of the National Academy of Sciences.

[10]  R. Montgomerie,et al.  Multiple sexual ornaments in satin bowerbirds: ultraviolet plumage and bowers signal different aspects of male quality , 2003 .

[11]  D. Stavenga,et al.  Shiny wing scales cause spec(tac)ular camouflage of the angled sunbeam butterfly, Curetis acuta , 2013 .

[12]  M. Rankin,et al.  The Ultrastructure of the Epicuticular Interference Reflectors of Tiger Beetles (Cicindela) , 1985 .

[13]  K. McGraw,et al.  Two ways to display: male hummingbirds show different color-display tactics based on sun orientation , 2018 .

[14]  M. Land,et al.  Rapid colour changes in multilayer reflecting stripes in the paradise whiptail, Pentapodus paradiseus , 2003, Journal of Experimental Biology.

[15]  Shuichi Kinoshita,et al.  Origin of Two-Color Iridescence in Rock Dove's Feather(Cross-disciplinary physics and related areas of science and technology) , 2007 .

[16]  S. Weiner,et al.  Structural Basis for the Brilliant Colors of the Sapphirinid Copepods. , 2015, Journal of the American Chemical Society.

[17]  Jeremy J. Baumberg,et al.  Pointillist structural color in Pollia fruit , 2012, Proceedings of the National Academy of Sciences.

[18]  S. Weiner,et al.  Light‐Induced Color Change in the Sapphirinid Copepods: Tunable Photonic Crystals , 2016 .

[19]  T. Mignot,et al.  A unique self-organization of bacterial sub-communities creates iridescence in Cellulophaga lytica colony biofilms , 2016, Scientific Reports.

[20]  Large-scale geographic variation in iridescent structural ornaments of a long-distance migratory bird , 2012 .

[21]  Yasuharu Takaku,et al.  The origin of extensive colour polymorphism in Plateumaris sericea (Chrysomelidae, Coleoptera) , 2002, Naturwissenschaften.

[22]  S. Nishida,et al.  Spectral patterns of the iridescence in the males of Sapphirina (Copepoda: Poecilostomatoida) , 1999, Journal of the Marine Biological Association of the United Kingdom.

[23]  A. Møller,et al.  Different roles of natural and sexual selection on senescence of plumage colour in the barn swallow , 2009 .

[24]  S. Weiner,et al.  The structural basis for enhanced silver reflectance in Koi fish scale and skin. , 2014, Journal of the American Chemical Society.

[25]  Chad M. Eliason,et al.  How hollow melanosomes affect iridescent colour production in birds , 2013, Proceedings of the Royal Society B: Biological Sciences.

[26]  Richard O Prum,et al.  Contribution of double scattering to structural coloration in quasiordered nanostructures of bird feathers. , 2010, Physical review. E, Statistical, nonlinear, and soft matter physics.

[27]  Ullrich Steiner,et al.  Disorder in convergent floral nanostructures enhances signalling to bees , 2017, Nature.

[28]  Dietary protein level affects iridescent coloration in Anna's hummingbirds, Calypte anna , 2012, Journal of Experimental Biology.

[29]  L. D’Alba,et al.  Iridescent colour production in hairs of blind golden moles (Chrysochloridae) , 2012, Biology Letters.

[30]  R. Wootton,et al.  Limited-view iridescence in the butterfly Ancyluris meliboeus , 2002, Proceedings of the Royal Society of London. Series B: Biological Sciences.

[31]  D. Stavenga,et al.  Sparkling feather reflections of a bird-of-paradise explained by finite-difference time-domain modeling , 2014, Proceedings of the National Academy of Sciences.

[32]  N. Ogihara,et al.  Wing Scale Orientation Alters Reflection Directions in the Green Hairstreak Chrysozephyrus smaragdinus (Lycaenidae; Lepidoptera) , 2016, Zoological Science.

[33]  D. J. Brink,et al.  Iridescent colors on seashells: an optical and structural investigation of Helcion pruinosus. , 2002, Applied optics.

[34]  J. Huxley,et al.  The basis of structural colour variation in two species of Papilio , 2009 .

[35]  R. Montgomerie,et al.  Structural plumage colour and parasites in satin bowerbirds Ptilonorhynchus violaceus: implications for sexual selection , 2003 .

[36]  D. Stavenga,et al.  Variable multilayer reflection together with long-pass filtering pigment determines the wing coloration of papilionid butterflies of the nireus group. , 2012, Optics express.

[37]  Female blue tits with brighter yellow chests transfer more carotenoids to their eggs after an immune challenge , 2013, Oecologia.

[38]  J. T. Lumeij,et al.  Sexual Dichromatism in the European Magpie Pica pica. Not as Black and White as Expected , 2007 .

[39]  Shuichi Kinoshita,et al.  Phase-Adjusting Layers in the Multilayer Reflector of a Jewel Beetle , 2012 .

[40]  A. Charmantier,et al.  Colour ornamentation in the blue tit: quantitative genetic (co)variances across sexes , 2016, Heredity.

[41]  F. Pelletier,et al.  The influence of iridescent coloration directionality on male tree swallows’ reproductive success at different breeding densities , 2016, Behavioral Ecology and Sociobiology.

[42]  D. J. Brink,et al.  Structural colours from the feathers of the bird Bostrychia hagedash , 2004 .

[43]  R. Montgomerie,et al.  Eye for an eyespot: how iridescent plumage ocelli influence peacock mating success , 2013 .

[44]  N. Marshall,et al.  Dramatic colour changes in a bird of paradise caused by uniquely structured breast feather barbules , 2011, Proceedings of the Royal Society B: Biological Sciences.

[45]  S. Weiner,et al.  The mechanism of color change in the neon tetra fish: a light-induced tunable photonic crystal array. , 2015, Angewandte Chemie.

[46]  G. Hill,et al.  The effect of coccidial infection on iridescent plumage coloration in wild turkeys , 2005, Animal Behaviour.

[47]  Mckenzie,et al.  Multilayer reflectors in animals using green and gold beetles as contrasting examples , 1998, The Journal of experimental biology.

[48]  Male-specific Iridescent Coloration in the Pipevine Swallowtail (Battus philenor) is Used in Mate Choice by Females but not Sexual Discrimination by Males , 2013, Journal of Insect Behavior.

[49]  Chad M. Eliason,et al.  Structural color change following hydration and dehydration of iridescent mourning dove (Zenaida macroura) feathers. , 2011, Zoology.

[50]  D. Stavenga,et al.  Unique wing scale photonics of male Rajah Brooke’s birdwing butterflies , 2016, Frontiers in Zoology.

[51]  Chad M. Eliason,et al.  Modular color evolution facilitated by a complex nanostructure in birds , 2015, Evolution; international journal of organic evolution.

[52]  S. Gorb,et al.  Effects of cuticle structure and crystalline wax coverage on the coloration in young and old males of Calopteryx splendens and Calopteryx virgo. , 2011, Zoology.

[53]  R. Maia,et al.  Iridescent structural colour production in male blue-black grassquit feather barbules: the role of keratin and melanin , 2009, Journal of The Royal Society Interface.

[54]  I. Cuthill,et al.  Ultraviolet plumage colors predict mate preferences in starlings. , 1997, Proceedings of the National Academy of Sciences of the United States of America.

[55]  Diann E. Gaalema,et al.  Iridescent ultraviolet signal in the orange sulphur butterfly (Colias eurytheme): spatial, temporal and spectral properties , 2007, Biological Journal of the Linnean Society.

[56]  Now you see me, now you don’t: iridescence increases the efficacy of lizard chromatic signals , 2014, Naturwissenschaften.

[57]  D. Stavenga,et al.  High refractive index of melanin in shiny occipital feathers of a bird of paradise , 2015, Light: Science & Applications.

[58]  K. McGraw,et al.  Quantifying iridescent coloration in animals: a method for improving repeatability , 2011, Behavioral Ecology and Sociobiology.

[59]  R. Macedo,et al.  Coccidian oocyst parasitism in the blue-black grassquit: influence on secondary sex ornaments and body condition , 2005, Animal Behaviour.

[60]  P. Wong,et al.  Effects of a butterfly scale microstructure on the iridescent color observed at different angles. , 1999, Optics express.

[61]  Tom D. Schultz,et al.  Structural colours create a flashing cue for sexual recognition and male quality in a Neotropical giant damselfly , 2009 .

[62]  L. D’Alba,et al.  What makes a feather shine? A nanostructural basis for glossy black colours in feathers , 2011, Proceedings of the Royal Society B: Biological Sciences.

[63]  V. Meyer-Rochow,et al.  A closer look at the feather coloration in the male purple sunbird, Nectarinia asiatica. , 2016, Micron.

[64]  D. Kemp Heightened phenotypic variation and age-based fading of ultraviolet butterfly wing coloration , 2006 .

[65]  P. Vukusic,et al.  Measuring and modelling the reflectance spectra of male Swinhoe's pheasant feather barbules , 2015, Journal of The Royal Society Interface.

[66]  Lei Shi,et al.  Iridescence in the neck feathers of domestic pigeons. , 2006, Physical review. E, Statistical, nonlinear, and soft matter physics.

[67]  T. Goldsmith,et al.  Four spectral classes of cone in the retinas of birds , 1986, Journal of Comparative Physiology A.

[68]  R. Rutowski,et al.  Warning Color Changes in Response to Food Deprivation in the Pipevine Swallowtail Butterfly, Battus philenor , 2013, Journal of insect science.

[69]  L. Plattner Optical properties of the scales of Morpho rhetenor butterflies: theoretical and experimental investigation of the back-scattering of light in the visible spectrum , 2004, Journal of The Royal Society Interface.

[70]  S. Sugita,et al.  The Weak Iridescent Feather Color in the Jungle Crow Corvus macrorhynchos , 2012 .

[71]  F. Pelletier,et al.  A reliable technique to quantify the individual variability of iridescent coloration in birds , 2016 .

[72]  Shuichi Kinoshita,et al.  Direct determination of the refractive index of natural multilayer systems. , 2011, Physical review. E, Statistical, nonlinear, and soft matter physics.

[73]  T. Mignot,et al.  Glitter-Like Iridescence within the Bacteroidetes Especially Cellulophaga spp.: Optical Properties and Correlation with Gliding Motility , 2012, PloS one.

[74]  D. Rubenstein,et al.  Selection, constraint, and the evolution of coloration in African starlings , 2016, Evolution; international journal of organic evolution.

[75]  J. Zi,et al.  Coloration strategies in peacock feathers , 2003, Proceedings of the National Academy of Sciences of the United States of America.

[76]  Pierre-Paul Bitton,et al.  Plumage brightness and age predict extrapair fertilization success of male tree swallows, Tachycineta bicolor , 2007, Animal Behaviour.

[77]  M F Land,et al.  The physics and biology of animal reflectors. , 1972, Progress in biophysics and molecular biology.

[78]  Chad M. Eliason,et al.  Decreased hydrophobicity of iridescent feathers: a potential cost of shiny plumage , 2011, Journal of Experimental Biology.

[79]  Sébastien R Mouchet,et al.  Photonic scales of Hoplia coerulea beetle: any colour you like , 2017 .

[80]  J. Ornelas,et al.  Molecular and iridescent feather reflectance data reveal recent genetic diversification and phenotypic differentiation in a cloud forest hummingbird , 2016, Ecology and evolution.

[81]  Doekele G Stavenga,et al.  Butterfly wing colors: glass scales of Graphium sarpedon cause polarized iridescence and enhance blue/green pigment coloration of the wing membrane , 2010, Journal of Experimental Biology.

[82]  G. Borgia,et al.  Blue, not UV, plumage color is important in satin bowerbird Ptilonorhynchus violaceus display , 2011 .

[83]  R. Sambles,et al.  Sculpted-multilayer optical effects in two species of Papilio butterfly. , 2001, Applied optics.

[84]  Shuichi Kinoshita,et al.  Physics of structural colors , 2008 .

[85]  A. Møller,et al.  Structural coloration and sexual selection in the barn swallow Hirundo rustica , 2002 .

[86]  L. D’Alba,et al.  Relative contributions of pigments and biophotonic nanostructures to natural color production: a case study in budgerigar (Melopsittacus undulatus) feathers , 2012, Journal of Experimental Biology.

[87]  R. S. Hunter,et al.  Methods of determining gloss , 1937 .

[88]  D. Kemp,et al.  Multimodal signalling: structural ultraviolet reflectance predicts male mating success better than pheromones in the butterfly Colias eurytheme L. (Pieridae) , 2007, Animal Behaviour.

[89]  S. Doucet,et al.  Iridescence: a functional perspective , 2009, Journal of The Royal Society Interface.

[90]  P. Rudall,et al.  Structural colour in Chondrus crispus , 2015, Scientific Reports.

[91]  J. L. Parra COLOR EVOLUTION IN THE HUMMINGBIRD GENUS COELIGENA , 2010, Evolution; international journal of organic evolution.

[92]  D. Stavenga,et al.  Magnificent magpie colours by feathers with layers of hollow melanosomes , 2018, Journal of Experimental Biology.

[93]  D. Osorio,et al.  Spectral reflectance and directional properties of structural coloration in bird plumage. , 2002, The Journal of experimental biology.

[94]  Shinichi Nakagawa,et al.  Repeatability for Gaussian and non‐Gaussian data: a practical guide for biologists , 2010, Biological reviews of the Cambridge Philosophical Society.

[95]  D. Kemp,et al.  Signal design and courtship presentation coincide for highly biased delivery of an iridescent butterfly mating signal , 2014, Evolution; international journal of organic evolution.

[96]  A. Parker,et al.  Structural origin of the green iridescence on the chelicerae of the red-backed jumping spider, Phidippus johnsoni (Salticidae: Araneae). , 2011, Arthropod structure & development.

[97]  Chad M. Eliason,et al.  Morphological basis of glossy red plumage colours , 2016 .

[98]  David W. Lee Ultrastructural basis and function of iridescent blue colour of fruits inElaeocarpus , 1991, Nature.

[99]  Leon Poladian,et al.  Exaggeration and suppression of iridescence: the evolution of two-dimensional butterfly structural colours , 2006, Journal of The Royal Society Interface.

[100]  E. Font,et al.  Iridescent (angle-dependent reflectance) properties of dorsal coloration in Podarcis muralis (Laurenti, 1768) , 2016 .

[101]  M. Evans,et al.  A quantitative analysis of objective feather color assessment: Measurements in the laboratory do not reflect true plumage color , 2016, The Auk.

[102]  Sang-im Lee,et al.  Multiple Structural Colors of the Plumage Reflect Age, Sex, and Territory Ownership in the Eurasian Magpie Pica pica , 2016, Acta Ornithologica.

[103]  D. Stavenga,et al.  Spatial reflection patterns of iridescent wings of male pierid butterflies: curved scales reflect at a wider angle than flat scales , 2011, Journal of Comparative Physiology A.

[104]  D. Kemp,et al.  Diversity in structural ultraviolet coloration among female sulphur butterflies (Coliadinae, Pieridae). , 2007, Arthropod structure & development.

[105]  X. H. Liu,et al.  Structural color change in longhorn beetles Tmesisternus isabellae. , 2009, Optics express.

[106]  M. Breed Animal Signals.Oxford Series in Ecology and Evolution.ByJohn Maynard Smithand, David Harper.Oxford and New York: Oxford University Press. $99.50 (hardcover); $44.50 (paper). ix + 166 p; ill.; index. ISBN: 0–19–852684–9 (hc); 0–19–852685–7 (pb). 2003. , 2005 .

[107]  Bodo D Wilts,et al.  Polarized iridescence of the multilayered elytra of the Japanese jewel beetle, Chrysochroa fulgidissima , 2011, Philosophical Transactions of the Royal Society B: Biological Sciences.

[108]  Shuichi Kinoshita,et al.  Structural colors in nature: the role of regularity and irregularity in the structure. , 2005, Chemphyschem : a European journal of chemical physics and physical chemistry.

[109]  Andrew R. Parker,et al.  515 million years of structural colour , 2000 .

[110]  M. Théry,et al.  Iridescent structurally based coloration of eyespots correlates with mating success in the peacock , 2007 .

[111]  R. Montgomerie,et al.  Iridescent plumage in satin bowerbirds: structure, mechanisms and nanostructural predictors of individual variation in colour , 2006, Journal of Experimental Biology.

[112]  R. Dudley,et al.  Molecular Phylogenetics and the Diversification of Hummingbirds , 2014, Current Biology.

[113]  D. Kemp,et al.  Potential direct fitness consequences of ornament-based mate choice in a butterfly , 2008, Behavioral Ecology and Sociobiology.

[114]  B. Sheldon,et al.  Age, sex and beauty: methodological dependence of age- and sex-dichromatism in the great tit Parus major , 2010 .

[115]  G. R. Kulkarni,et al.  Study of nano-architecture of the wings of Paris Peacock butterfly , 2013, Photonics West - Biomedical Optics.

[116]  Feng Liu,et al.  Inconspicuous structural coloration in the elytra of beetles Chlorophila obscuripennis (Coleoptera). , 2008, Physical review. E, Statistical, nonlinear, and soft matter physics.

[117]  Peter Vukusic,et al.  Stress-mediated covariance between nano-structural architecture and ultraviolet butterfly coloration , 2006 .

[118]  Pierre-Paul Bitton,et al.  Age-related differences in plumage characteristics of male tree swallows Tachycineta bicolor: hue and brightness signal different aspects of individual quality , 2008 .

[119]  S. Motreuil,et al.  Reduced sexual dichromatism, mutual ornamentation, and individual quality in the monogamous Zenaida dove Zenaida aurita , 2017 .

[120]  Geoffrey I N Waterhouse,et al.  A nanostructural basis for gloss of avian eggshells , 2015, Journal of The Royal Society Interface.

[121]  Dietrich Mossakowski,et al.  Reflection Measurements Used In The Analysis Of Structural Colours Of Beetles , 1979 .

[122]  Nicola J Nadeau,et al.  Wing scale ultrastructure underlying convergent and divergent iridescent colours in mimetic Heliconius butterflies , 2018, Journal of The Royal Society Interface.

[123]  D. Kemp,et al.  CONDITION DEPENDENCE, QUANTITATIVE GENETICS, AND THE POTENTIAL SIGNAL CONTENT OF IRIDESCENT ULTRAVIOLET BUTTERFLY COLORATION , 2007, Evolution; international journal of organic evolution.

[124]  I. Cuthill,et al.  Mutual ornamentation, age and reproductive performance in the European starling , 2005 .

[125]  J. Macedonia,et al.  Pterin pigments amplify iridescent ultraviolet signal in males of the orange sulphur butterfly, Colias eurytheme , 2005, Proceedings of the Royal Society B: Biological Sciences.

[126]  G. Hill,et al.  Evolutionary transitions and mechanisms of matte and iridescent plumage coloration in grackles and allies (Icteridae) , 2006, Journal of The Royal Society Interface.

[127]  R. Macedo,et al.  Achieving luster: prenuptial molt pattern predicts iridescent structural coloration in Blue-black Grassquits , 2011, Journal of Ornithology.

[128]  B. Seymoure,et al.  A bird's eye view of two mimetic tropical butterflies: coloration matches predator's sensitivity , 2016 .

[129]  D. Osorio,et al.  Morphology and Ornamentation in Male Magnificent Frigatebirds: Variation with Age Class and Mating Status , 2007, The American Naturalist.

[130]  J. Macedonia,et al.  Iridescent hindwing patches in the Pipevine Swallowtail: differences in dorsal and ventral surfaces relate to signal function and context , 2010 .

[131]  D. Kemp,et al.  Female mating preferences and male signal variation in iridescent Hypolimnas butterflies , 2014, Animal Behaviour.

[132]  Matthew D. Shawkey,et al.  pavo: an R package for the analysis, visualization and organization of spectral data , 2013 .

[133]  J. Endler,et al.  Experimental evidence suggests that specular reflectance and glossy appearance help amplify warning signals , 2017, Scientific Reports.

[134]  K. McGraw Multiple UV reflectance peaks in the iridescent neck feathers of pigeons , 2004, Naturwissenschaften.

[135]  K. McGraw,et al.  It's not just what you have, but how you use it: solar-positional and behavioural effects on hummingbird colour appearance during courtship. , 2018, Ecology letters.

[136]  J. Watanabe,et al.  Unique Reflection Property Due to Bumpy Multilayer Structure in Elytra of Rhomborrhina unicolor , 2010 .

[137]  Yasuharu Takaku,et al.  The Origin of the Iridescent Colors in Coleopteran Elytron , 2002 .

[138]  S. Leclaire,et al.  Feather bacterial load affects plumage condition, iridescent color, and investment in preening in pigeons , 2014 .

[139]  Serge Berthier,et al.  Iridescences: The Physical Colors of Insects , 2006 .

[140]  Chad M. Eliason,et al.  Rapid, reversible response of iridescent feather color to ambient humidity. , 2010, Optics express.

[141]  Michael F. Land,et al.  A Multilayer Interference Reflector in the Eye of the Scallop, Pecten Maximus , 1966 .

[142]  M. Théry,et al.  Condition dependence of iridescent wing flash-marks in two species of dabbling ducks , 2010, Behavioural Processes.

[143]  D. Rubenstein,et al.  Key ornamental innovations facilitate diversification in an avian radiation , 2013, Proceedings of the National Academy of Sciences.

[144]  D. Kemp,et al.  Female mating biases for bright ultraviolet iridescence in the butterfly Eurema hecabe (Pieridae) , 2008 .