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Seeking carotenoid pigments in amber-preserved fossil feathers

Published on May 1, 2015in Scientific Reports 4.12
· DOI :10.1038/srep05226
Daniel B. Thomas11
Estimated H-index: 11
,
Paul C. Nascimbene13
Estimated H-index: 13
+ 2 AuthorsHelen F. James28
Estimated H-index: 28
Abstract
Animal colours can be richly informative about aspects of behaviour such as foraging ecology and mate preference. Birds in particular display many striking hues and complex patterns of pigmentation. Examples of plumage adaptations include brightly coloured feathers for enticing potential mates, as well as cryptic patterns that allow a bird to hide in plain sight1,2,3. By analogy with modern birds, the behaviours and habitats of ancient birds and other feathered dinosaurs may be inferred from pigments in fossil plumage. Methods for describing one class of plumage pigment (melanins) have recently been developed for ancient feathers4,5. Modern birds display six chemically-distinct classes of feather pigment, of which carotenoids are the most common after melanins; carotenoids mostly confer yellow, orange and red colours to feathers6,7. The two key challenges for describing carotenoids in ancient plumage are 1) to find an environment that preserves molecular evidence for carotenoids, and 2) to ascertain a technique that provides unequivocal evidence for carotenoids. We focused on feathers in amber because encapsulation within amber may insulate carotenoid molecules against diagenetic alteration, and such preserved pigments could be detected with Raman spectroscopy. Carotenoids have an unequivocal Raman spectral signal that is greatly enhanced by a resonance effect, allowing trace amounts to be detected8. Furthermore, Raman spectroscopy can be performed without sample preparation or destruction. Edwards and colleagues9 showed that inclusions in amber can be studied with minimal or no interference from the amber matrix when Raman spectra are collected with confocal optics and 1064 nm excitation. With conventional Raman microscopy, laser light is channeled through a microscope objective towards a sample, and then scattered light is channeled back through the same objective towards a detector. Light scatters from the entire sample volume that is penetrated by incident light, and the greatest concentration of scattered photons are typically returned from the focal plane of the incident light. Accordingly, light is scattered from both the surface and internal volume of a translucent sample. Confocal Raman microscopy differs from conventional Raman microscopy by the inclusion of a confocal pinhole above the microscope objective. The pinhole allows only the photons scattered from the focal plane to reach the detector. For a translucent sample with an inclusion (e.g. amber containing a fossil feather), the inclusion can be positioned in the focal plane of the incident light and only the light scattered from the inclusion will reach the detector. Hence, confocal Raman microscopy usefully provides chemical information about an inclusion with minimal or no interference from the surface or surrounding matrix. Near infrared excitation wavelengths are typically less sensitive than visible wavelengths when studying pigments with Raman spectroscopy. However, visible excitation wavelengths tend to induce fluorescence when interacting with amber9. Thus, from a signal vs. noise perspective, a Raman spectrum of an inclusion in amber collected with a near infrared wavelength can be substantially more informative than a Raman spectrum of the same inclusion collected with a visible wavelength. A confocal Raman microscope with a near infrared (NIR) laser is thus an ideal tool for seeking carotenoids preserved in amber. We first conducted a pilot study to determine if the carotenoid pigments of a modern feather could be detected through an amber matrix. A yellow and black wing feather from a greenfinch (Carduelis chloris) was placed underneath a polished piece of amber and analysed with Raman spectroscopy. In a second series of experiments, we analysed six fossil feathers preserved in amber using Raman spectroscopy and light microscopy. Evidence for pigmentation in the fossil feathers was sought with Raman spectroscopy, and the preservation of fine-scale morphology was studied with light microscopy. Finally, we collected Raman spectra and scanning electron microscopy images from an ancient feather preserved as a carbonised compression fossil. Compression fossils have previously provided evidence for melanin pigmentation4,5, and here we compared Raman spectral evidence from two types of fossil feather (1: preserved in amber; 2: preserved in lake sediment) with spectra from a modern feather.
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References17
Newest
Published on Jan 1, 2014in Analytical Methods 2.07
Daniel B. Thomas11
Estimated H-index: 11
(National Museum of Natural History),
Kevin J. McGraw51
Estimated H-index: 51
(ASU: Arizona State University)
+ 1 AuthorsOdile Madden5
Estimated H-index: 5
(Museum Conservation Institute)
Chemical analyses of pigments in skin, scales, feathers and fur have provided deep insight into the colouration and visual communication strategies of animals. Carotenoid pigments in particular can be important colour signals in birds and other animals. Chromatographic analyses of plumage carotenoids require the destruction of one or more feathers, which has made pigment research on threatened species or museum specimens challenging. Here we show that Raman spectroscopy, coupled with multivariat...
14 Citations Source Cite
Published on Mar 27, 2013in Biology Letters 3.35
Maria E. McNamara12
Estimated H-index: 12
(Yale University),
Derek E. G. Briggs62
Estimated H-index: 62
(Yale University)
+ 2 AuthorsZhengrong Wang21
Estimated H-index: 21
(Yale University)
Fossil feathers often preserve evidence of melanosomes—micrometre-scale melanin-bearing organelles that have been used to infer original colours and patterns of the plumage of dinosaurs. Such reconstructions acknowledge that evidence from other colour-producing mechanisms is presently elusive and assume that melanosome geometry is not altered during fossilization. Here, we provide the first test of this assumption, using high pressure–high temperature autoclave experiments on modern feathers to ...
38 Citations Source Cite
Published on Mar 20, 2013in Journal of the Royal Society Interface 3.35
Daniel B. Thomas11
Estimated H-index: 11
(Smithsonian Institution),
Cushla M. McGoverin18
Estimated H-index: 18
(TU: Temple University)
+ 2 AuthorsOdile Madden5
Estimated H-index: 5
(Smithsonian Institution)
Many animals extract, synthesize and refine chemicals for colour display, where a range of compounds and structures can produce a diverse colour palette. Feather colours, for example, span the visible spectrum and mostly result from pigments in five chemical classes (carotenoids, melanins, porphyrins, psittacofulvins and metal oxides). However, the pigment that generates the yellow colour of penguin feathers appears to represent a sixth, poorly characterized class of feather pigments. This pigme...
19 Citations Source Cite
Published on Sep 16, 2011in Science 41.06
Roy A. Wogelius22
Estimated H-index: 22
(University of Manchester),
P. M. Manning55
Estimated H-index: 55
(University of Manchester)
+ 9 AuthorsHai-Lu You20
Estimated H-index: 20
Well-preserved fossils of pivotal early bird and nonavian theropod species have provided unequivocal evidence for feathers and/or downlike integuments. Recent studies have reconstructed color on the basis of melanosome structure; however, the chemistry of these proposed melanosomes has remained unknown. We applied synchrotron x-ray techniques to several fossil and extant organisms, including Confuciusornis sanctus , in order to map and characterize possible chemical residues of melanin pigments....
89 Citations Source Cite
Published on Nov 1, 2010in Journal of Evolutionary Biology 2.54
T.-L. Gluckman1
Estimated H-index: 1
(University of Melbourne),
Gonçalo C. Cardoso18
Estimated H-index: 18
(University of Melbourne)
A commonly held principle in visual ecology is that communication compromises camouflage: while visual signals are often conspicuous, camouflage provides concealment. However, some traits may have evolved for communication and camouflage simultaneously, thereby overcoming this functional compromise. Visual patterns generally provide camouflage, but it was suggested that a particular type of visual pattern – avian barred plumage – could also be a signal of individual quality. Here, we test if the...
22 Citations Source Cite
Published on Mar 12, 2010in Science 41.06
Quanguo Li5
Estimated H-index: 5
,
Ke-Qin Gao20
Estimated H-index: 20
+ 6 AuthorsRichard O. Prum46
Estimated H-index: 46
For as long as dinosaurs have been known to exist, there has been speculation about their appearance. Fossil feathers can preserve the morphology of color-imparting melanosomes, which allow color patterns in feathered dinosaurs to be reconstructed. Here, we have mapped feather color patterns in a Late Jurassic basal paravian theropod dinosaur. Quantitative comparisons with melanosome shape and density in extant feathers indicate that the body was gray and dark and the face had rufous speckles. T...
145 Citations Source Cite
Howell G. M. Edwards44
Estimated H-index: 44
(University of Bradford),
Dennis W. Farwell28
Estimated H-index: 28
(University of Bradford),
Susana E. Jorge Villar20
Estimated H-index: 20
(UBU: University of Burgos)
Abstract Raman microscope spectra of specimens of Baltic and Mexican amber resins containing insect inclusions have been analysed using near-infrared excitation to assess the potential for discrimination between the keratotic remains of the insects and the terpenoid matrix. For the Mexican amber specimen the insect spectra exhibit evidence of significant protein degradation compared with the insect remains in the Baltic amber specimen. In both cases the Raman spectra of the insect remains are st...
20 Citations Source Cite
Published on Mar 1, 2005in Biopolymers 1.99
Hartwig Schulz28
Estimated H-index: 28
,
Malgorzata Baranska31
Estimated H-index: 31
(Jagiellonian University),
Rafal Baranski17
Estimated H-index: 17
This paper demonstrates the special advantages of FT-Raman spectroscopy for in situ studies of several carotenoids that occur ubiquitously in the plant kingdom. Spectra obtained from various tissues of a range of plant species indicate that the wavenumber location of CC stretching vibrations is mainly influenced both by the length as well as by the terminal substituents of the polyene chain of carotenoids and by their interaction with other plant constituents. The obtained results show also the ...
161 Citations Source Cite
Published on Aug 1, 2002in Botanical Journal of the Linnean Society 3.12
George Poinar1
Estimated H-index: 1
(OSU: Oregon State University)
Five palm flowers in Dominican amber and one in Baltic amber are described or characterized. Palaeoraphe dominicanagen. et sp. nov. in the subtribe Livistoninae, is described from one perfect flower in Dominican amber. Roystonea palaeasp. nov. is described from one staminate and one pistillate flower in Dominican amber. Three other palm flowers, two perfect flowers from Dominican amber and one staminate flower from Baltic amber, are briefly characterized and figured. © 2002 The Linnean Society o...
24 Citations Source Cite
Published on Mar 1, 2002in American Museum Novitates 0.98
David A. Grimaldi40
Estimated H-index: 40
,
Michael S. Engel36
Estimated H-index: 36
,
Paul C. Nascimbene13
Estimated H-index: 13
Abstract Amber from Kachin, northern Burma, has been used in China for at least a millennium for carving decorative objects, but the only scientific collection of inclusion fossils, at the Natural History Museum, London (NHML), was made approximately 90 years ago. Age of the material was ambiguous, but probably Cretaceous. Numerous new records and taxa occur in this amber, based on newly excavated material in the American Museum of Natural History (AMNH) containing 3100 organisms. Without having...
449 Citations Source Cite
Cited By14
Newest
Published on Jun 1, 2019in Trends in Ecology and Evolution 15.94
Source Cite
Published on Feb 16, 2019in Journal of Systematic Palaeontology 2.33
Ekaterina A. Sidorchuk9
Estimated H-index: 9
(RAS: Russian Academy of Sciences),
Andre V. Bochkov14
Estimated H-index: 14
+ 1 AuthorsO. F. Chernova5
Estimated H-index: 5
(RAS: Russian Academy of Sciences)
Tetrapods are rarely recovered from fossil resins, such as amber, and fossils of parasites are even rarer. We describe the first pre-Quaternary co-occurrence of ectoparasitic mites with hairs of their mammalian hosts, preserved in life-like detail from a piece of Eocene (∼ 40 Ma) Baltic amber. The mites, representing the oldest fossils of the family Myobiidae (Acari: Prostigmata: Eleutherengona), are described as Protohylomysobia erinaceophilus Sidorchuk & Bochkov gen. et sp. nov. and belong to ...
2 Citations Source Cite
Published on Dec 1, 2018in Journal of Palaeogeography
Lida Xing18
Estimated H-index: 18
(China University of Geosciences),
Pierre F.D. Cockx1
Estimated H-index: 1
(University of Regina)
+ 1 AuthorsJingmai K. O’Connor9
Estimated H-index: 9
(CAS: Chinese Academy of Sciences)
Over the last 20 years, compression fossils of feathers surrounding dinosaurs have greatly expanded our understanding of the origin and evolution of feathers. One of the most peculiar feather morphotypes discovered to date are rachis dominated feathers (RDFs), which have also been referred to as proximally ribbon-like pennaceous feathers (PRPFs). These elongate feathers are only found in the tail plumage, typically occurring in pairs with both streamer (not proximally ribbon-like) and racket-plu...
Source Cite
Published on Jul 1, 2018in Science Advances
Lida Xing18
Estimated H-index: 18
(China University of Geosciences),
Michael W. Caldwell32
Estimated H-index: 32
(U of A: University of Alberta)
+ 9 AuthorsHongliang Shi1
Estimated H-index: 1
(BFU: Beijing Forestry University)
We present the first known fossilized snake embryo/neonate preserved in early Late Cretaceous (Early Cenomanian) amber from Myanmar, which at the time, was an island arc including terranes from Austral Gondwana. This unique and very tiny snake fossil is an articulated postcranial skeleton, which includes posterior precloacal, cloacal, and caudal vertebrae, and details of squamation and body shape; a second specimen preserves a fragment of shed skin interpreted as a snake. Important details of sk...
3 Citations Source Cite
Published on Mar 1, 2017in Earth-Science Reviews 7.49
Paul A. Selden28
Estimated H-index: 28
(KU: University of Kansas),
David Penney17
Estimated H-index: 17
(University of Manchester)
Spiders are the most diverse and important terrestrial predators in modern ecosystems. Therefore, fossil spiders are fundamental to understanding past terrestrial ecosystems, especially coevolution with their principal prey, the insects. Being generally soft bodied, spiders have a poor fossil record, but where they do occur, it is in the exceptional circumstance of a Fossil-Lagerstatte. By far the greatest number of fossil spider specimens are found in amber (fossilized tree resin), but earlier ...
1 Citations Source Cite
Published on Dec 1, 2016in Current Biology 9.25
Lida Xing18
Estimated H-index: 18
(China University of Geosciences),
Ryan C. McKellar5
Estimated H-index: 5
(University of Regina)
+ 11 AuthorsAlexander P. Wolfe47
Estimated H-index: 47
(U of A: University of Alberta)
Summary In the two decades since the discovery of feathered dinosaurs [1–3], the range of plumage known from non-avialan theropods has expanded significantly, confirming several features predicted by developmentally informed models of feather evolution [4–10]. However, three-dimensional feather morphology and evolutionary patterns remain difficult to interpret, due to compression in sedimentary rocks [9, 11]. Recent discoveries in Cretaceous amber from Canada, France, Japan, Lebanon, Myanmar, an...
32 Citations Source Cite
Published on Nov 1, 2016in Nature Communications 12.35
Lida Xing18
Estimated H-index: 18
(China University of Geosciences),
Ryan C. McKellar5
Estimated H-index: 5
(University of Regina)
+ 10 AuthorsMartinGLockley38
Estimated H-index: 38
(University of Colorado Denver)
Our knowledge of Cretaceous plumage is limited by the fossil record itself: compression fossils surrounding skeletons lack the finest morphological details and seldom preserve visible traces of colour, while discoveries in amber have been disassociated from their source animals. Here we report the osteology, plumage and pterylosis of two exceptionally preserved theropod wings from Burmese amber, with vestiges of soft tissues. The extremely small size and osteological development of the wings, co...
23 Citations Source Cite
Published on Jul 7, 2016in PeerJ 2.12
Gustavo M.E.M. Prado2
Estimated H-index: 2
(USP: University of São Paulo),
Luiz Eduardo Anelli8
Estimated H-index: 8
(USP: University of São Paulo)
+ 1 AuthorsGuilherme Raffaeli Romero3
Estimated H-index: 3
(USP: University of São Paulo)
Here we describe three fossil feathers from the Early Cretaceous Santana Formation of the Araripe Basin, Brazil. Feathers are the most complex multiform vertebrate integuments; they perform different functions, occurring in both avian and non-avian dinosaurs. Despite their rarity, fossil feathers have been found across the world. Most of the Brazilian feather fossil record comes from the Santana Formation. This formation is composed of two members: Crato (lake) and Romualdo (lagoon); both of whi...
4 Citations Source Cite
Published on Jan 12, 2016
Malgorzata Baranska31
Estimated H-index: 31
(Jagiellonian University),
Jan Cz. Dobrowolski20
Estimated H-index: 20
,
Grzegorz Zajac6
Estimated H-index: 6
(Jagiellonian University)
Source Cite
Published on Oct 6, 2015in Analytical Chemistry 6.04
Naiara Cipriano Oliveira2
Estimated H-index: 2
,
João Hermínio da Silva5
Estimated H-index: 5
+ 6 AuthorsAmauri J. Paula14
Estimated H-index: 14
We used here a scanning electron microscopy approach that detected backscattered electrons (BSEs) and X-rays (from ionization processes) along a large-field (LF) scan, applied on a Cretaceous fossil of a shrimp (area ∼280 mm2) from the Araripe Sedimentary Basin. High-definition LF images from BSEs and X-rays were essentially generated by assembling thousands of magnified images that covered the whole area of the fossil, thus unveiling morphological and compositional aspects at length scales from...
5 Citations Source Cite