DOCSLIB.ORG

Optical Influence of Oil Droplets on Cone Photoreceptor Sensitivity David Wilby* and Nicholas W

Total Page：16

File Type：pdf, Size：1020Kb

Download full-text PDF Read full-text
Optical Influence of Oil Droplets on Cone Photoreceptor Sensitivity David Wilby* and Nicholas W © 2017. Published by The Company of Biologists Ltd | Journal of Experimental Biology (2017) 220, 1997-2004 doi:10.1242/jeb.152918 RESEARCH ARTICLE Optical influence of oil droplets on cone photoreceptor sensitivity David Wilby* and Nicholas W. Roberts ABSTRACT oil droplets must serve a purpose other than just spectral filtering Oil droplets are spherical organelles found in the cone photoreceptors (Walls, 1942; Hart, 2001). of vertebrates. They are generally assumed to focus incident light into Oil droplets have a relatively high refractive index, a spherical the outer segment, and thereby improve light catch because of the shape and are typically wider than the outer segment (Ives et al., droplets’ spherical lens-like shape. However, using full-wave optical 1983; Young and Martin, 1984; Wilby et al., 2015). Being able to simulations of physiologically realistic cone photoreceptors from enlarge the area of light capture without increasing the size of the birds, frogs and turtles, we find that pigmented oil droplets actually outer segment should, in theory, improve the signal-to-noise ratio drastically reduce the transmission of light into the outer segment and reduce energetic cost (Ives et al., 1983; Young and Martin, integrated across the full visible wavelength range of each species. 1984; Stavenga and Wilts, 2014). Nevertheless, the extent to which Only transparent oil droplets improve light catch into the outer oil droplets improve light capture is still unclear. Prior efforts have segments, and any enhancement is critically dependent on the proposed that oil droplets gather more light into the outer segment refractive index, diameter of the oil droplet, and diameter and length of (Govardovskiì et al., 1981; Ives et al., 1983; Young and Martin, the outer segment. Furthermore, oil droplets are not the only optical 1984; Stavenga and Wilts, 2014). However, this might not be the elements found in cone inner segments. The ellipsoid, a dense case for all oil droplets, with a recent study discovering that aggregation of mitochondria situated immediately prior to the oil the pigmented droplets in simulations of cone photoreceptors in the droplet, mitigates the loss of light at the oil droplet surface. We chicken (Gallus gallus domesticus) reduced transmission of light describe a framework for integrating these optical phenomena into into the outer segment for the regions of the spectrum to which simple models of receptor sensitivity, and the relevance of these the visual pigments were sensitive (Wilby et al., 2015). Only the observations to evolutionary appearance and loss of oil droplets is transparent oil droplet of the violet cone increased light transmission discussed. into the outer segment by approximately 50%. This raises the questions: what properties of oil droplets influence KEY WORDS: Oil droplets, Ellipsoid, Optics, Cone, Photoreceptor, light catch?; and how do oil droplets perform relative to the ‘ideal’ Vision light-coupling scenario in which all incident light within the area of the oil droplet is focused into the outer segment? INTRODUCTION In this study, we use numerical optical calculations informed by The cone photoreceptors of approximately half of the orders of morphological and optical measurements to investigate the vertebrates contain spherical structures composed of lipids and influence oil droplets have on optical power in the outer segment. carotenoid pigment, known as oil droplets (Walls, 1942; Jacobs We include the optics of the outer segment, which act as a and Rowe, 2004). Oil droplets are situated immediately prior to the waveguide to confine light to the regions of the retina containing the light-sensitive outer segment in the light path, and their role is to light-sensitive pigment. Finally, we examine the optical role of the influence the light that reaches it. Many oil droplets contain ellipsoid in conjunction with the oil droplet in the concentration of mixtures of carotenoid pigment (Johnston and Hudson, 1976; light into the outer segment. Toomey et al., 2015) and have been studied predominantly for their spectral filtering properties (e.g. Partridge, 1989; Hart, 2001) MATERIALS AND METHODS and their influence on tuning the spectral sensitivity of colour Optical simulations vision, thereby improving colour discrimination and colour Calculations were performed with the freely available finite- constancy (Vorobyev, 2003). However, the oil droplets of difference time-domain (FDTD) simulation software, MEEP (MPI ultraviolet- and violet-sensitive (UVS and VS, respectively) version 1.2; Oskooi et al., 2010), using the computational facilities cones are transparent across the visible spectrum (Bowmaker of the Advanced Computing Research Centre, University of Bristol. et al., 1997), containing no pigment. Further, numerous species Simulations took advantage of the rotational symmetry of the (Fig. 1) only have transparent oil droplets in all of their cone types. models about the z-axis, and computations were performed in Therefore, this widespread presence of transparency indicates that cylindrical polar coordinates for a thin wedge of the model (see Fig. S1). Carotenoid absorption spectra along with refractive index measurements were used to model the dielectric function of the oil Ecology of Vision Laboratory, School of Biological Sciences, Life Sciences droplets as previously described (Wilby et al., 2015). Building, Tyndall Avenue, University of Bristol, Bristol BS8 1TQ, UK. For models of oil droplets based on the three species in this *Author for correspondence ([email protected]) study [chicken, Gallus gallus domesticus (Linnaeus 1758); red- eared slider, Trachemys scripta elegansí (Wied-Neuwied 1839); D.W., 0000-0002-6553-8739 and African clawed frog, Xenopus laevis Daudin 1802], This is an Open Access article distributed under the terms of the Creative Commons Attribution calculations were performed for specific oil droplet and outer License (http://creativecommons.org/licenses/by/3.0), which permits unrestricted use, distribution and reproduction in any medium provided that the original work is properly attributed. segment dimensions. Dimensions and refractive indices were taken from the literature and are summarised in Table S2. For Received 6 November 2016; Accepted 14 March 2017 simplicity, a wavelength-invariant value of refractive index of 1.45 Journal of Experimental Biology 1997 RESEARCH ARTICLE Journal of Experimental Biology (2017) 220, 1997-2004 doi:10.1242/jeb.152918 Fig. 1. Summary tree of the pigmentation properties and Pigmented Placentals presence/absence of oil droplets in extant vertebrates. Blue Transparent Marsupials Mammals circles indicate that there are no pigmented oil droplets in any No oil droplets cone of a taxon; red circles show taxa that have at least some pigmented droplets and some transparent, most regularly in the Monotremes violet-sensitive (VS) and ultraviolet-sensitive (UVS) cones. Asterisks indicate the possible first appearance of pigmented or Birds transparent oil droplets. Question marks indicate uncertainties. Source references for oil droplet traits and more detailed Crocodiles notes are provided in the supplementary information (Table S1). Tree informed by Meyer and Zardoya (2003). Figure courtesy of Olle Lind, Lund University. Lizards Gekkos Reptiles Snakes ? Tuatara Turtles Frogs * Salamanders Amphibians Caecilians Lungfishes Lobe-finned fish ? Coelacanth * Teleosts Gars Bowfins Ray-finned fish Sturgeons Bichir Reedfish Sharks Cartilaginous fish Skates Lampreys Agnathans Hagfishes was used for the outer segment, as measured previously (Wilby absence of the oil droplet (NOD): et al., 2015). The refractive index change of the lipid membrane ÐÐ Ã across the visible spectrum is <0.01 (Roberts et al., 2009) and the ½ EðlÞ:E ðlÞdfdr DðlÞ¼ ÐÐ OD : ð1Þ visual pigment has minimal influence on the refractive index ½ EðlÞ:EÃðlÞ f d dr NOD (Stavenga and van Barneveld, 1975). Analyses of the sensitivity of the models to the refractive index of the outer segment Integrals were performed numerically in cylindrical polar demonstrated that a value of 1.45 is a conservative choice. The coordinates over the volume of the outer segment (which surrounding medium was given the refractive index 1.35, as effectively reduces to an area under cylindrical symmetry). The calculated by Enoch and Tobey (1978). Simulations that electric field vector is composed of components [Er,Eφ,Ez] along the incorporated the ellipsoid modelled it as a cylinder preceding the radial, polar and z (propagation) axes, respectively. The complex oil droplet and surrounding its front hemisphere, similarly to conjugate is indicated by *. Wilby et al. (2015). Ellipsoids were equal in radius to the oil Additionally, we define an enhancement as predicted using the μ droplet, had a refractive index of 1.43 and were 3.5 m long. Full geometry alone, DG, as the ratio of the cross-sectional areas of the details of all simulation parameters are given in Table S2. oil droplet and the outer segment, which reduces to: Following Ives et al. (1983), we define the volume-averaged E E enhancement factor, D, as the ratio of the integral of . * (as a d2 proxy for light intensity) within the outer segment in the presence of D ¼ OD ; ð2Þ G d2 an oil droplet (OD) to the integrated electric field intensity in the OS Journal of Experimental Biology 1998 RESEARCH ARTICLE Journal of Experimental Biology (2017) 220, 1997-2004 doi:10.1242/jeb.152918 where dOD and dOS are the diameter of the oil droplet and the
Load more

Recommended publications
  • Do Hummingbirds See in Ultraviolet?
    The Open Medical Informatics Journal, 2009, 3, 9-12 9 Open Access Do Hummingbirds See in Ultraviolet? M. Curé*,1 and A.G. Palacios2 1Departamento de Física y Astronomía, Facultad de Ciencias, Universidad de Valparaíso, Chile 2Centro de Neurociencia de Valparaíso, Facultad de Ciencias, Universidad de Valparaíso, Chile Abstract: We present a numerical model to fit the electroretinogram (ERG), a gross evoked eye visual potential, that originate in the retina through photons absorption by photoreceptors and then involve the contribution form others retinal neurons. We use the ERG measured in a hummingbird, to evaluate the most likely retinal mechanism - cones visual pig- ments and oil-droplets - that participate in their high dimensional tetra or pentachromatic color hyperspace. The model - a nonlinear fit - appears to be a very useful tool to predict the underlying contribution visual mechanism for a variety of retinal preparation. Keywords: Color vision, electroretinogram, non lineal model. 1. INTRODUCTION high concentrations. Double cones have L visual pigments and are screened by a variety of galloxanthin and -carotene A critical question in visual sciences is to determinate the types of photoreceptors that contribute - for a particular eye - mixtures [2, 8, 10-12]. The final cone mechanism sensitivity to the overall retinal spectral sensitivity. We have developed a is then determined by combining the cone visual pigment mathematical model that helps to answer this question. As a absorption and oil-droplet transmittance. In many birds, case study, we have used the electroretinogram results of a ultraviolet (UV) is a color that is believed to be involved in diurnal bird, the Firecrown hummingbirds.
    [Show full text]
  • Wild Hummingbirds Discriminate Nonspectral Colors
    Wild hummingbirds discriminate nonspectral colors Mary Caswell Stoddarda,b,1, Harold N. Eysterb,c,2, Benedict G. Hogana,b,2, Dylan H. Morrisa, Edward R. Soucyd, and David W. Inouyeb,e aDepartment of Ecology and Evolutionary Biology, Princeton University, Princeton, NJ 08544; bRocky Mountain Biological Laboratory, Crested Butte, CO 81224; cInstitute for Resources, Environment and Sustainability, University of British Columbia, Vancouver, BC V6T 1Z4, Canada; dCenter for Brain Science, Harvard University, Cambridge, MA 02138; and eDepartment of Biology, University of Maryland, College Park, MD 20742 Edited by Scott V. Edwards, Harvard University, Cambridge, MA, and approved April 28, 2020 (received for review November 5, 2019) Many animals have the potential to discriminate nonspectral UV- or violet-sensitive (UVS/VS), short-wave–sensitive (SWS), colors. For humans, purple is the clearest example of a nonspectral medium-wave–sensitive (MWS), and long-wave–sensitive (LWS) color. It is perceived when two color cone types in the retina (blue color cones. Indirect evidence for avian tetrachromacy comes and red) with nonadjacent spectral sensitivity curves are pre- from the general agreement of behavioral data with a model that dominantly stimulated. Purple is considered nonspectral because predicts discrimination thresholds from opponent signals stem- no monochromatic light (such as from a rainbow) can evoke this ming from four single color cone types (8, 9). More directly, simultaneous stimulation. Except in primates and bees, few color-matching experiments (10) and tests designed to stimulate behavioral experiments have directly examined nonspectral color discrimination, and little is known about nonspectral color per- specific photoreceptors (11, 12) have suggested that avian color ception in animals with more than three types of color photore- vision results from at least three different opponent mechanisms ceptors.
    [Show full text]
  • Visual Pigments and Oil Droplets from Six Classes of Photoreceptor in the Retinas of Birds J
    CORE Metadata, citation and similar papers at core.ac.uk Provided by Elsevier - Publisher Connector Vision Res., Vol. 37, No. 16, pp. 2183-2194, 1997 Pergamon © 1997 Elsevier Science Ltd. All rights reserved PH: S0042-6989(97)00026-6 Printed in Great Britain 0042-6989/97 $17.00 + 0.00 Visual Pigments and Oil Droplets from Six Classes of Photoreceptor in the Retinas of Birds J. K. BOWMAKER,*:~ L. A. HEATH,~ S. E. WILKIE,-~ D. M. HUNT~" Received 8 August 1996; in revised form 2 December 1996 Microspectrophotometric examination of the retinal photoreceptors of the budgerigar (shell parakeet), Melopsittacus undulatus (Psittaciformes) and the zebra finch, Taeniopygia guttata (Passeriformes), demonstrate the presence of four, speetrally distinct classes of single cone that contain visual pigments absorbing maximally at about 565, 507, 430-445 and 360-380 nm. The three longer-wave cone classes contain coloured oil droplets acting as long pass filters with cut-offs at about 570, 500-520 and 445 nm, respectively, whereas the ultraviolet-sensitive cones contain a transparent droplet. The two species possess double cones in which both members contain the long- wave-sensitive visual pigment, but only the principal member contains an oil droplet, with cut-off at about 420 nm. A survey of the cones of the pigeon, Columba livia (Columbiformes), confirms the presence of the three longer-wave classes of single cone, but also reveals the presence of a fourth class containing a visual pigment with maximum absorbance at about 409 nm, combined with a transparent droplet. No evidence was found for a fifth, ultraviolet-sensitive receptor.
    [Show full text]
  • Microspectrophotometry of Visual Pigments and Oil Droplets in A
    The Journal of Experimental Biology 207, 1229-1240 1229 Published by The Company of Biologists 2004 doi:10.1242/jeb.00857 Microspectrophotometry of visual pigments and oil droplets in a marine bird, the wedge-tailed shearwater Puffinus pacificus: topographic variations in photoreceptor spectral characteristics Nathan S. Hart* Vision, Touch and Hearing Research Centre, School of Biomedical Sciences, University of Queensland, Brisbane, Queensland 4072, Australia *e-mail: [email protected] Accepted 5 January 2004 Summary Microspectrophotometric examination of the retina of a only the principal member contained an oil droplet, which procellariiform marine bird, the wedge-tailed shearwater had a λcut at 413·nm. The retina had a horizontal band or Puffinus pacificus, revealed the presence of five different ‘visual streak’ of increased photoreceptor density running types of vitamin A1-based visual pigment in seven across the retina approximately 1.5·mm dorsal to the top different types of photoreceptor. A single class of rod of the pecten. Cones in the centre of the horizontal streak contained a medium-wavelength sensitive visual pigment were smaller and had oil droplets that were either with a wavelength of maximum absorbance (λmax) at transparent/colourless or much less pigmented than at the 502·nm. Four different types of single cone contained periphery. It is proposed that the reduction in cone oil visual pigments maximally sensitive in either the violet droplet pigmentation in retinal areas associated with (VS, λmax 406·nm), short (SWS, λmax 450·nm), medium high visual acuity is an adaptation to compensate for (MWS, λmax 503·nm) or long (LWS, λmax 566·nm) spectral the reduced photon capture ability of the narrower ranges.
    [Show full text]
  • Evolution, Development and Function of Vertebrate Cone Oil Droplets
    REVIEW published: 08 December 2017 doi: 10.3389/fncir.2017.00097 Evolution, Development and Function of Vertebrate Cone Oil Droplets Matthew B. Toomey* and Joseph C. Corbo* Department of Pathology and Immunology, Washington University School of Medicine, St. Louis, MO, United States To distinguish colors, the nervous system must compare the activity of distinct subtypes of photoreceptors that are maximally sensitive to different portions of the light spectrum. In vertebrates, a variety of adaptations have arisen to refine the spectral sensitivity of cone photoreceptors and improve color vision. In this review article, we focus on one such adaptation, the oil droplet, a unique optical organelle found within the inner segment of cone photoreceptors of a diverse array of vertebrate species, from fish to mammals. These droplets, which consist of neutral lipids and carotenoid pigments, are interposed in the path of light through the photoreceptor and modify the intensity and spectrum of light reaching the photosensitive outer segment. In the course of evolution, the optical function of oil droplets has been fine-tuned through changes in carotenoid content. Species active in dim light reduce or eliminate carotenoids to enhance sensitivity, whereas species active in bright light precisely modulate carotenoid double bond conjugation and concentration among cone subtypes to optimize color discrimination and color constancy. Cone oil droplets have sparked the curiosity of vision scientists for more than a century. Accordingly, we begin by briefly reviewing the history of research on oil droplets. We then discuss what is known about the developmental origins Edited by: of oil droplets. Next, we describe recent advances in understanding the function of oil Vilaiwan M.
    [Show full text]
  • Tetrachromacy, Oil Droplets and Bird Plumage Colours
    J Comp Physiol A (1998) 183: 621±633 Ó Springer-Verlag 1998 ORIGINAL PAPER M. Vorobyev á D. Osorio á A. T. D. Bennett N. J. Marshall á I. C. Cuthill Tetrachromacy, oil droplets and bird plumage colours Accepted: 3 July 1998 Abstract There is a growing body of data on avian eyes, Abbreviations LWS long-wave sensitive á MWS medium- including measurements of visual pigment and oil wave-sensitive á SWS short-wave-sensitive á UVS droplet spectral absorption, and of receptor densities ultraviolet-sensitive and their distributions across the retina. These data are sucient to predict psychophysical colour discrimina- tion thresholds for light-adapted eyes, and hence provide Introduction a basis for relating eye design to visual needs. We ex- amine the advantages of coloured oil droplets, UV vi- Bird eyes have a number of features which suggest they sion and tetrachromacy for discriminating a diverse set are well adapted for colour vision. There are four types of avian plumage spectra under natural illumination. of cone photopigment with peak sensitivities ranging Discriminability is enhanced both by tetrachromacy and from 365 nm to 565 nm (Fig. 1), and each cone contains coloured oil droplets. Oil droplets may also improve a coloured oil droplet which sharpens spectral tuning colour constancy. Comparison of the performance of a (Bowmaker 1980). Given the colourfulness of their pigeon's eye, where the shortest wavelength receptor plumage to humans, and the evolutionary importance of peak is at 410 nm, with that of the passerine Leiothrix, their visual displays, it is interesting to ask how oil where the ultraviolet-sensitive peak is at 365 nm, gen- droplets, UV sensitivity and tetrachromacy aect birds' erally shows a small advantage to the latter, but this colour vision, and how their perception of plumage advantage depends critically on the noise level in the coloration might dier from our own (Burkhardt 1989; sensitivity mechanism and on the set of spectra being Bennett et al.
    [Show full text]
  • A Complex Carotenoid Palette Tunes Avian Colour Vision Rsif.Royalsocietypublishing.Org Matthew B
    Downloaded from http://rsif.royalsocietypublishing.org/ on June 30, 2016 A complex carotenoid palette tunes avian colour vision rsif.royalsocietypublishing.org Matthew B. Toomey1, Aaron M. Collins2, Rikard Frederiksen3, M. Carter Cornwall3, Jerilyn A. Timlin2 and Joseph C. Corbo1 Research 1Department of Pathology and Immunology, Washington University School of Medicine, St Louis, MO 63110, USA 2Bioenergy and Defense Technologies, Sandia National Laboratories, Albuquerque, NM 87123, USA 3 Cite this article: Toomey MB, Collins AM, Department of Physiology and Biophysics, Boston University School of Medicine, Boston, MA 02118-2526, USA Frederiksen R, Cornwall MC, Timlin JA, Corbo MBT, 0000-0001-9184-197X; MCC, 0000-0002-0847-939X; JAT, 0000-0003-2953-1721; JCC, 0000-0002-9323-7140 JC. 2015 A complex carotenoid palette tunes avian colour vision. J. R. Soc. Interface 12: The brilliantly coloured cone oil droplets of the avian retina function as 20150563. long-pass cut-off filters that tune the spectral sensitivity of the photoreceptors http://dx.doi.org/10.1098/rsif.2015.0563 and are hypothesized to enhance colour discrimination and improve colour constancy. Although it has long been known that these droplets are pigmen- ted with carotenoids, their precise composition has remained uncertain owing to the technical challenges of measuring these very small, dense Received: 25 June 2015 and highly refractile optical organelles. In this study, we integrated results Accepted: 14 September 2015 from high-performance liquid chromatography, hyperspectral microscopy and microspectrophotometry to obtain a comprehensive understanding of oil droplet carotenoid pigmentation in the chicken (Gallus gallus). We find that each of the four carotenoid-containing droplet types consists of a complex mixture of carotenoids, with a single predominant carotenoid Subject Areas: determining the wavelength of the spectral filtering cut-off.
    [Show full text]
  • Retinal Photoreceptor Fine Structure in Some Reptiles
    The Egyptian Journal of Hospital Medicine Vol., 17 :167 – 186 Dec.2004 I.S.S.N: 12084 1687 -2002 Retinal Photoreceptor Fine Structure in some reptiles Fairoze Khattab; Fahmy I. Khattab; Nagui Fares and Aman Zaki (Department of Zoology, Faculty of Science, Ain Shams University, Abbassia, Cairo, Egypt.) Abstract The structure of the photoreceptors of four different reptiles: the homed viper Cerastes cerastes (diurnal and nocturnal), the European Chameleo chameleon (diurnal), the gold skink Eumeces schneidrii (diurnal) and the Egyptian gecko, Tarentola annularis (nocturnal) has been investigated by light and electron microscopy. The photoreceptors of diurnal reptiles were mainly of the cone type and those of nocturnal were mainly rods. The ellipsoid region of both double rods in the nocturnals and large single cones in the species having both nocturnals and diurnal activity, consist of several mitochondria arranged in a remarkable radially gradient architecture which accommodates with the specific function of this region as a focusing device helping to condense light onto the outer segments. Moreover the principle cone of double cone and single cone of diurnal reptiles possessed a large oil droplet in the region between the inner segment and outer segment. This droplet is thought to play a role in filtering light and so doing enhanced contrast reduce glare and lessen chromatic aberration. It is worth to mention that the outer segment of rods in nocturnal reptiles approaches a length of approximately four folds the length of the inner segments of the same photoreceptors cells. This character is of a particular interest, since the outer segment is the site of photopigments and the increase in its length magnifies its ability of light and consequently accommodate with the night vision.
    [Show full text]
  • Visual Acuity and Signal Color Pattern in an Anolis Lizard Leo J
    © 2017. Published by The Company of Biologists Ltd | Journal of Experimental Biology (2017) 220, 2154-2158 doi:10.1242/jeb.150458 SHORT COMMUNICATION Visual acuity and signal color pattern in an Anolis lizard Leo J. Fleishman§, Anna I. Yeo* and Carley W. Perez‡ ABSTRACT MATERIALS AND METHODS Anolis lizards communicate with colorful dewlaps that often include All applicable international and institutional guidelines for the care detailed patterns. We measured the visual acuity of Anolis sagrei. and use of animals were followed. Procedures involving live Lizards viewed a checkerboard pattern of red and yellow–green animals were in accordance with the ethical standards of Union squares that were too small to resolve, and thus appeared uniform College and were approved in advance by the IACUC committee. in color. We quickly replaced the center portion of the display with a We used adult male A. sagrei, wild-collected in Florida by a pattern of larger squares. If the new pattern could be resolved, the commercial supplier (Snakes at Sunset, Miami, FL, USA). For our lizards perceived a change in color and reflexively shifted their gaze first experiment, 10 individuals were obtained on 7 September 2013 toward the target. The acuity threshold was 1.21 cycles deg−1.We and maintained in our laboratory in a constant temperature and also calculated acuity based on published anatomical data for humidity room (28°C, 50% relative humidity) for 3 weeks prior to Anolis carolinensis. It was similar to that of A. sagrei for the visual and 7 weeks during the experiment. For our second experiment, 10 periphery.
    [Show full text]
  • Iridescent Colouration of Male Anna's Hummingbird
    Journal of Comparative Physiology A (2018) 204:965–975 https://doi.org/10.1007/s00359-018-1295-8 ORIGINAL PAPER Iridescent colouration of male Anna’s hummingbird (Calypte anna) caused by multilayered barbules Marco A. Giraldo1 · Juan L. Parra2 · Doekele G. Stavenga3 Received: 3 March 2018 / Revised: 16 September 2018 / Accepted: 26 September 2018 / Published online: 8 October 2018 © The Author(s) 2018 Abstract The male Anna’s hummingbird features a brightly reddish-pink reflecting gorget, due to large stacks of melanosomes in the feather barbules, arranged in layers separated by keratin. Direct observations together with detailed scatterometry demon- strated that the barbules reflect incident light in an approximately specular manner. The structural colouration is iridescent, i.e. varies with a changing angle of light incidence. Spectrophotometrical measurements of the barbule reflectance and absorbance can be well interpreted with calculated spectra obtained with a transfer matrix method for optical multilayers, using anatomical data and measured refractive index spectra. The organization of the reflectors as a Venetian blind presum- ably functions to create a high spectral contrast of the male’s plumage during courtship. Keywords Feather iridescence · Courtship · Spectrophotometry · Scatterometry · Optical modelling Introduction melanin-containing organelles with large air spaces (Greenewalt et al. 1960a). The barbule material thus has Among the many colourful birds, hummingbirds stand out a strongly varying refractive index, resembling that of a because of their extremely shiny feathers (Greenewalt 1960; multilayered interference reflector (Durrer 1977). Optical Stoddard and Prum 2011; Cuthill et al. 2017). Especially modelling on the Fiery topaz (Topaza pyra) and Anna’s male hummingbirds feature brilliant plumages, which they hummingbird (Calypte anna) showed that measured reflec- display during courtship toward females.
    [Show full text]
  • The Ostrich (Struthio Camelus) and Rhea (Rhea Americana)
    View metadata, citation and similar papers at core.ac.uk brought to you by CORE provided by Elsevier - Publisher Connector Vision Research 41 (2001) 1–12 www.elsevier.com/locate/visres Retinal photoreceptors of paleognathous birds: the ostrich (Struthio camelus) and rhea (Rhea americana) Mathew W. Wright, James K. Bowmaker * Department of Visual Science, Institute of Ophthalmology, Uni6ersity College London, Bath Street, London EC1V 9EL, UK Received 25 January 2000; received in revised form 16 May 2000 Abstract Microspectrophotometry was used to determine the absorbance spectra of both rod and cone visual pigments and oil droplets from the retinae of the ostrich (Struthio camelus) and rhea (Rhea americana). Light and fluorescence microscopy of whole fresh tissue mounts were used to determine the relative numbers and distribution of oil droplets in the retinae. Both species possessed l rods, double cones and four classes of single cone identified by their oil droplets. The rods had max at about 505 nm, whereas l three cone pigments were recorded with max at 570, 505 and 445 nm. The P570 pigment was located in both members of the l double cones and in a class of single cone containing an R-type oil droplet ( cut at 555 nm). The P505 and P445 cone pigments l were found in populations of single cones containing Y-type and C-type oil droplets ( cut of 500 and 420 nm, respectively). The l fourth class of single cone contained a T-type droplet and in the ostrich contained a visual pigment with max at about 405 nm. Double cones possessed a P-type droplet in the principal member and an A-type droplet in the accessory member.
    [Show full text]
  • A Novel Cellular Structure in the Retina of Insectivorous Birds Luke P
    www.nature.com/scientificreports OPEN A novel cellular structure in the retina of insectivorous birds Luke P. Tyrrell 1*, Leandro B. C. Teixeira2, Richard R. Dubielzig2, Diana Pita3, Patrice Baumhardt3, Bret A. Moore4 & Esteban Fernández-Juricic3 The keen visual systems of birds have been relatively well-studied. The foundations of avian vision rest on their cone and rod photoreceptors. Most birds use four cone photoreceptor types for color vision, a ffth cone for achromatic tasks, and a rod for dim-light vision. The cones, along with their oil droplets, and rods are conserved across birds – with the exception of a few shifts in spectral sensitivity – despite taxonomic, behavioral and ecological diferences. Here, however, we describe a novel photoreceptor organelle in a group of New World fycatchers (Empidonax spp.) in which the traditional oil droplet is replaced with a complex of electron-dense megamitochondria surrounded by hundreds of small, orange oil droplets. The photoreceptors with this organelle were unevenly distributed across the retina, being present in the central region (including in the fovea), but absent from the retinal periphery and the area temporalis of these insectivorous birds. Of the many bird species with their photoreceptors characterized, only the two fycatchers described here (E. virescens and E. minimus) possess this unusual retinal structure. We discuss the potential functional signifcance of this unique sub-cellular structure, which might provide an additional visual channel for these small predatory songbirds. Birds are widely recognized for their specialized visual abilities1, which enable them to engage in many diverse modes of life. For example, birds can be diurnal or nocturnal, predators and/or prey, and fighted or fightless.
    [Show full text]