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University of Groningen Spectral Tuning of Amazon Parrot Feather Coloration by Psittacofulvin Pigments and Spongy Structures

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University of Groningen Spectral Tuning of Amazon Parrot Feather Coloration by Psittacofulvin Pigments and Spongy Structures University of Groningen Spectral tuning of Amazon parrot feather coloration by psittacofulvin pigments and spongy structures Tinbergen, Jan; Wilts, Bodo D.; Stavenga, Doekele G. Published in: Journal of Experimental Biology DOI: 10.1242/jeb.091561 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: 2013 Link to publication in University of Groningen/UMCG research database Citation for published version (APA): Tinbergen, J., Wilts, B. D., & Stavenga, D. G. (2013). Spectral tuning of Amazon parrot feather coloration by psittacofulvin pigments and spongy structures. Journal of Experimental Biology, 216(23), 4358-4364. https://doi.org/10.1242/jeb.091561 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). 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: 24-09-2021 4358 The Journal of Experimental Biology 216, 4358-4364 © 2013. Published by The Company of Biologists Ltd doi:10.1242/jeb.091561 RESEARCH ARTICLE Spectral tuning of Amazon parrot feather coloration by psittacofulvin pigments and spongy structures Jan Tinbergen*, Bodo D. Wilts and Doekele G. Stavenga† Computational Physics, Zernike Institute for Advanced Materials, University of Groningen, NL-9747 AG Groningen, The Netherlands *Deceased †Author for correspondence ([email protected]) SUMMARY The feathers of Amazon parrots are brightly coloured. They contain a unique class of pigments, the psittacofulvins, deposited in both barbs and barbules, causing yellow or red coloured feathers. In specific feather areas, spongy nanostructured barb cells exist, reflecting either in the blue or blue-green wavelength range. The blue-green spongy structures are partly enveloped by a blue-absorbing, yellow-colouring pigment acting as a spectral filter, thus yielding a green coloured barb. Applying reflection and transmission spectroscopy, we characterized the Amazons’ pigments and spongy structures, and investigated how they contribute to the feather coloration. The reflectance spectra of Amazon feathers are presumably tuned to the sensitivity spectra of the visual photoreceptors. Supplementary material available online at http://jeb.biologists.org/cgi/content/full/216/23/4358/DC1 Key words: barbs, barbules, melanin, thin films, vision. Received 28 May 2013; Accepted 20 August 2013 INTRODUCTION Instead of the carotenoids, parrot feathers contain a special class Parrots are well known for their striking, bright coloration (Berg of pigment, called the psittacofulvins, after the family name, the and Bennett, 2010). When at rest, most Amazon parrots show a psittacines or Psittaciformes (McGraw and Nogare, 2004; McGraw predominantly green colour (Fig. 1), but feathers with bright yellow, and Nogare, 2005; McGraw, 2006b; Berg and Bennett, 2010). Both red or blue colours are also widespread. The feather colours result the carotenoids and psittacofulvins have rather narrow-band from the cumulative reflections from the feather components, the absorbance spectra, with absorption bands restricted to the violet, barbs and barbules (Prum, 2006), which in Amazon parrots are often blue or blue-green wavelengths, yielding (pale-)yellow or red differently coloured. The yellow and red colours are commonly pigmentary colours. The carotenoids and psittacofulvins are easily referred to as pigmentary colours, as they are caused by pigments confused in spectral measurements, but detailed chemical and that selectively absorb short-wavelength light. As a consequence, Raman spectroscopical research has clearly documented their only the long-wavelength part of broad-band incident light remains differences (Veronelli et al., 1995; Stradi et al., 2001). The as back-scattered, reflected light. However, the colour of blue psittacofulvins are probably enzymatically derived from carotenoids feathers is called a structural colour, because it originates from (McGraw and Nogare, 2004; McGraw, 2006b), but the parrot unpigmented, nano-sized, spongy-structured cells that selectively pigments seem to be an independent evolutionary development reflect short-wavelength light by constructive interference (Shawkey (Stoddard and Prum, 2011). Why this has occurred, that is, what et al., 2003; Prum, 2006; Kinoshita et al., 2008; Berg and Bennett, special benefit is provided by the psittacofulvins, is somewhat 2010; Stavenga et al., 2011b). The green feathers also have spongy enigmatic. cells, which reflect blue-green light. A blue-absorbing pigment, To gain insight into these questions we have performed a which functions as a short-wavelength filter, restricts the wavelength quantitative study of the different coloration techniques employed range of the reflected light, resulting in green coloured feathers (Berg by the Amazon parrots. We measured the absorbance spectra and and Bennett, 2010; D’Alba et al., 2012; Saranathan et al., 2012). density of various psittacofulvins and investigated how they are The most common pigments of birds are melanins and combined with melanin pigmentation as well as with different carotenoids (McGraw, 2006a; McGraw, 2006b). The melanins are spongy structures that together produce the Amazons’ colourful usually incorporated in pigment granules, the melanosomes. plumage. We furthermore compared the feather coloration, i.e. the Their very broad absorbance spectrum causes a black or brownish feather reflectance, with the spectral sensitivity of the birds’ visual pigmentary coloration (McGraw, 2006c). In many bird species, photoreceptors. the melanosomes of barbules are arranged in orderly arrays, which then cause structural colorations ranging from violet to purple- MATERIALS AND METHODS red to broad-band whitish (Greenewalt et al., 1960; Durrer, 1977; Amazon parrot feathers Osorio and Ham, 2002; Prum, 2006; Stavenga et al., 2011a). We obtained feathers of various Amazon parrots [Natterer’s However, in parrots, melanosome-based structural colours are Amazon, Amazona ochrocephala nattereri (Finsch 1865); Panama unknown. yellow-headed Amazon, Amazona ochrocephala panamensis THE JOURNAL OF EXPERIMENTAL BIOLOGY Amazon parrot feather coloration 4359 (Bowmaker et al., 1997). The spectral sensitivities (S) of the cone photoreceptors were calculated using the following equation: S(λ)=To(λ)Td(λ){1–exp[–dκmaxP(λ)]}, where λ is the wavelength, To(λ) is the transmittance of the ocular media, Td(λ) is the oil droplet transmittance, d is the cone photoreceptor length, κmax is the peak absorption coefficient of the visual pigment and P(λ) is the normalized visual pigment absorption spectrum. For To(λ) we used the transmittance spectrum of the ocular lens of a parrot closely related to the Amazons, the crimson rosella, Platycercus elegans (Carvalho et al., 2011); this spectrum is very similar to the transmittance spectrum of the ocular media of the starling, Sturnus vulgaris, considered to be applicable for the budgerigar (Hart et al., 1998). The transmittance of the transparent oil droplet was assumed to be Td(λ)=1, and the other oil droplet transmittances were approximated by Td(λ)=exp{–exp[–b(λ–λ0)]}, with values of b and λ0 for the C-, Y- and R-type oil droplets of b=0.086, 0.033 and 0.054, and λ0=425, 537 and 587 nm, respectively [table 1 in Hart and Vorobyev (Hart and Vorobyev, 2005)]. We took d=16 μm and −1 κmax=0.035 μm [equivalent to a decadic absorbance coefficient of Fig. 1. A Panama Amazon parrot, Amazona ochrocephala panamensis. 0.014 μm−1 (see Hart and Vorobyev, 2005)], and we calculated P(λ) using λmax and a rhodopsin template (Govardovskii et al., 2000). (Cabanis 1874); and orange-winged Amazon, Amazona amazonica (Linnaeus 1766)] from the parrot rescue centre Stichting RESULTS Papegaaienhulp (Erica, The Netherlands; assistant curator Nathalie Pigmentary coloration van der Vechte). As a first example of Amazon feather coloration, Fig. 2A shows a feather of a Natterer’s Amazon, which has white, yellow and red Spectroscopy parts. The red feather area, observed with incident and transmitted Reflectance spectra of the wings were measured with an Avaspec light, reveals the barbs and its branches, the barbules (Fig. 2B,C). 2048-2 CCD detector array spectrometer using a bifurcated probe Measurement of the feather reflectance with a bifurcated probe (Avantes FCR-7UV200; Avantes, Eerbeek, The Netherlands) or a microspectrophotometer (MSP) constructed from a Leitz Ortholux microscope (see Stavenga et al., 2011b). In the MSP, the microscope A B C objective was an Olympus 20×, NA 0.46 (Tokyo, Japan). The light 3 source was a deuterium/halogen [AvaLight-D(H)-S, Avantes, Eerbeek, The Netherlands] or xenon arc lamp (Osram XBO 150W, 2 Munich, Germany). The reference was a diffuse white reflectance tile (Avantes WS-2). The absorbance spectra of the pigments were 1 determined by transmission microspectrophotometry on barbules immersed in refractive index fluids (Cargille Labs,
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