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University of Groningen Vision, Pigments and Structural Colouration University of Groningen Vision, pigments and structural colouration of butterflies Pirih, Primož IMPORTANT NOTE: You are advised to consult the publisher's version (publisher's PDF) if you wish to cite from it. Please check the document version below. Document Version Publisher's PDF, also known as Version of record Publication date: 2011 Link to publication in University of Groningen/UMCG research database Citation for published version (APA): Pirih, P. (2011). Vision, pigments and structural colouration of butterflies. s.n. Copyright Other than for strictly personal use, it is not permitted to download or to forward/distribute the text or part of it without the consent of the author(s) and/or copyright holder(s), unless the work is under an open content license (like Creative Commons). The publication may also be distributed here under the terms of Article 25fa of the Dutch Copyright Act, indicated by the “Taverne” license. More information can be found on the University of Groningen website: https://www.rug.nl/library/open-access/self-archiving-pure/taverne- amendment. Take-down policy If you believe that this document breaches copyright please contact us providing details, and we will remove access to the work immediately and investigate your claim. Downloaded from the University of Groningen/UMCG research database (Pure): http://www.rug.nl/research/portal. For technical reasons the number of authors shown on this cover page is limited to 10 maximum. Download date: 11-10-2021 The research published in this book was financially supported by: University of Groningen (RUG) School of Behavioural and Cognitive Neurosciences Groningen (BCN) Japan Society for the Promotion of Science (JSPS) European Office for Air Force Research and Development (EOARD) The findings, opinions, conclusions and reccomendations expressed by the authors do not necessarily reflect the views of the funding bodies. Parts of this book served as the basis for the articles published in: Journal of Comparative Physiology A (Published by Springer, © The Authors) Journal of Experimental Biology (Published by and © The Company of Biologists Ltd) Optics Express (Published and © The Optical Society) The copyright statements of the publishers allow electronic republication of this kind. For the full list of contributors, see page 10. Editing, layout and cover design: Primož Pirih Photography: Hein L. Leertouwer & Primož Pirih P. 1 Experimentally bleached eyeshine of The Peacock Inachis io (PP) and a detail from the wing of the lycaenid Thecla marsyas (PP) P. 128 Chinese Peacock Papilio bianor (HLL) Set in Monotype Garamond and Bitstream DejaVu Sans. ISBN: 978-90-367-4850-6 (printed version) ISBN: 978-90-367-4857-5 (digital version) Interested in a printed copy of the book with additional high resolution art? Send an email to [email protected]. Vision, Pigments and Structural Colouration of Butterflies Electronic version © 2011 Primož Pirih RIJKSUNIVERSITEIT GRONINGEN Vision, Pigments and Structural Colouration of Butterflies Proefschrift ter verkrijging van het doctoraat in de Wiskunde en Natuurwetenschappen aan de Rijksuniversiteit Groningen op gezag van de Rector Magnificus, dr. E. Sterken, in het openbaar te verdedigen op maandag 28 maart 2011 om 16.15 uur door Primož Pirih geboren op 18 september 1975 te Ljubljana, Slovenië Promotor: Prof. dr. D.G. Stavenga Beoordelingscommissie: Prof. dr. K. Arikawa Prof. dr. D.G.M. Beersma Prof. dr. R.C. Hardie ISBN: 978-90-367-4850-6 (printed version) ISBN: 978-90-367-4857-5 (digital version) Thesis Abstract i n s e c t Vision, body colouration and the visual environment of an animal may be v i s i o n tuned to each other. This thesis aims at connecting the three entities by physiological studying insect vision, physiological optics of butterfly eyes and optics of o p t i c s butterfly wing colouration. p h y s i o l o g y p i g m e n t Vision is an imaging sense, used for finding food, avoiding predators, seeing s p e c t r a l mates and rivals. Many insects detect colour and polarisation of light. Body sensitivity colouration may serve to conceal or reveal, or to communicate territoriality r h o d o p s i n and gene quality. Butterfly wing patterns are formed by coloured scales. f r u i t f l y Colouration is due to pigments and due to periodic chitin structures. a r r e s t i n b u t t e r f l y First, we study the physiology of light sensing in the fruitfly Drosophila( w i n g melanogaster). We show that the ratio of the visual pigment rhodopsin to the s c a l e s controlling protein arrestin impacts the dynamic range of phototransduction. s t r u c t u r a l colouration Second, we study the physiological optics of the eye of the Clouded Yellow multilayers butterfly Colias( erate). We describe three types of red pigment-lined rhabdoms. i m a g i n g We classify the photoreceptors into nine classes with sensitivities peaking scatterometer from ultraviolet to the far red. The expanded set may be used for colour p h o t o n i c vision in intraspecific interactions, foraging or host-plant identification. c r y s t a l s s c a t t e r i n g Third, we study the optics of wings in purple-coloured, iridescent males from p a t t e r n s Coliadinae and Colotis groups (Pieridae). We relate the multilayer structure in p u r p l e the scales to the reflectance spectra. We measure the scattering patterns of colouration single scales and wing patches with an imaging scatterometer. Scale curvature iridescence determines the spatial extent of the iridescence patterns, which may influence v i s i b i l i t y the visibility of the colouration signal. Avant-propos This book is about physiology of vision, about screening pigment makes the inner layer of physiological optics of the butterfly eye and about photoreceptors to see far into the red part of the optics of butterfly wings. the spectrum. In fact, the spectral shift would be the largest found so far in insects. A big part of this book has been seeded during my stay in Hayama. I remember seeing a poster In the following three chapters we are studying there, with four kanji 生理光学. They stand for the optics of the colouration of a few iridescent physiological optics. Physiology (seiri) consists of pierid butterflies from the Colias and Colotis natural, live, raw, fresh 生 (nama) and general groups, where pigmentary colour is combined principle, logic 理 (ri). Optics (kougaku) consists with structural colour that together provide of light 光 (hikari) and knowledge, learning 学 purple colouration. We use scanning electron (gaku). The kanji for knowledge, 学, is based on microscopy (SEM) and integrating sphere spectrometry an older kanji 學, showng a child 子 under the to describe the ultrastructure of their scales, and roof of a house where good manners xx are correlate the reflectance spectra with the being embraced with both hands. University, structure. We describe an instrument, tailored not unexpectedly and historically correctly, is big for studies of spatial and spectral patterns of knowledge 大学 (daigaku). Incidentally, the fourth colouration. The instrument, an imaging scatterometer and the first kanji of physiological optics together (ISM), built around an ellipsoidal mirror, is represent a student 学生 (gakusei) – thus fresh being used for measuring spatial radiation knowledge. I sincerely hope that some of it can be patterns of materials. We use the ISM, along found on these pages. with a more conventional goniometric device, the angle-dependent reflectance measurement I start the book with a general introduction setup (ARM) to characterize the angular which is divided into two parts: the eye and the dependency of reflections from the iridescent wing. The general introduction should serve a wings. We find that the scale curvature influences non-specialist to understand better the (fresh) greatly the spatial scattering pattern of the knowledge given in six core chapters. Each of iridescence reflections. the core chapters contains its own, more specialized introduction. I round up the book with an essay, which is not directly related to the core chapters, but is The first core chapter is about the physiology of dealing broadly with imaging senses. In the short phototransduction (light detection) in the light general discussion, I am briefly touching the sensing cells – the photoreceptors – of the fruitfly, field of visual ecology, linking vision, colouration Drosophila melanogaster. We describe the interplay and the environment. between the light sensing protein, rhodopsin, and a controlling protein, arrestin, and the way how New insights into the relations between colour, their concentrations determine the sensitivity of vision, ecology, behaviour, sexual selection, and the photoreceptor. evolution are emerging from combining colouration and vision studies. By taking The next two chapters are dealing with the advantage of the diversity of species and physiological optics of the Eastern Pale Clouded environments, using a diverse set of experimental Yellow Butterfly, Colias erate. First, we study the tools and being well aware of the physics behind ultrastructure of its compound eye, and describe it, this may become integrative biology at its best. three types of elementary units of the eye, the This book is not quite there, yet I do hope that ommatidia, which use a red screening pigment to it shows a valid direction to how integrative modify the spectral sensitivities of the biology of colouration could be studied. photoreceptors. Using intracellular electro- physiological methods, we describe nine photoreceptor classes and their spectral and Primož Pirih polarisation sensitivities.
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