the-colour-of-fossil-feathers-2jtb35ncqt
the-colour-of-fossil-feathers-2jtb35ncqt
the-colour-of-fossil-feathers-2jtb35ncqt
1. INTRODUCTION 3. RESULTS
In contrast to most mammals, birds are able to see a The pennaceous contour feather from the Crato
broad range of colours. This colour vision complexity Formation of Brazil (figure 1a) shows striking black
has led to the evolution of coloured plumage for and white bands. The margins of the bands match
sexual display and camouflage. A number of pigments isochronic sections in melanin pigment patterning in
and nanostructures produce plumage colours. Black modern feathers (Prum & Williamson 2001, 2002),
and brown feather colours are generated by eumela- indicating that these colour bands are not preser-
nins and phaeomelanins, respectively. Melanins are vation artefacts. Relief on the fossil defines the rachis,
complex cross-linked oligomeric to polymeric barbs and rarely barbules, and reveals places where
structures composed of units of dihydroxyindole and the barbules were ‘unzipped’.
dihydroxyindole carboxylic acid (Liu & Simon 2003). Under the ESEM, the dark bands of the Crato
Melanins are the most common and broadly distrib- feather showed masses of elongate, oblate bodies
uted pigments in feathers (McGraw et al. 2005; 1–2 mm long, aligned along the barbs and barbules
McGraw 2006) as well as in the rest of the animal (figure 1b). Energy dispersive analysis (EDS) of the
kingdom (Liu & Simon 2003; Liu et al. 2005). dark bands showed that these structures are composed
Melanins are synthesized within membrane-bound, mainly of carbon, as are most fossil feathers (Davis &
lysosome-like organelles called melanosomes inside pig- Briggs 1995). By contrast, in the light bands, the relief
ment cells called melanocytes (Marks & Seabra 2001). on the specimen is less pronounced. Furthermore, no
The melanosomes are then transferred to keratinocytes oblate structures were evident under the ESEM, which
during feather morphogenesis to create pigmentation revealed only the texture of the rock matrix (figure 1c).
patterning (Durrer 1986; Prum & Williamson 2001, EDS of the light bands detected no carbon residue.
Received 3 June 2008 This journal is q 2008 The Royal Society
Accepted 17 June 2008
2 J. Vinther et al. Fossil feather colour
(a) (b)
(c)
(d )
Figure 1. Cretaceous feather ultrastructure compared with that in a living bird. (a) Feather from the Crato Formation, Early
Cretaceous, Brazil (Leicester University, UK, Geology Department, LEIUG 115562) showing colour bands; margins of
colour bands are similar to those found in living birds and barbules are clearly preserved. (b) Dark bands, composed of
aligned eumelanosomes, contrast with (c) light areas that reveal only the rock matrix. (d ) A broken barbule from a modern
Red-winged Blackbird (Agelaius phoeniceus, Aves: Icteridae, Yale Peabody Museum 1047) reveals eumelanosomes aligned
along the barbule enclosed in a keratin matrix. Scale bars, (a) 3 mm, insert 1 mm; (b) 1 mm; (c) 10 mm; (d ) 1 mm.
The feathers associated with the skull of the Early (Bingham et al. 2008) and the Eocene of Grube
Eocene bird (figure 2a) are preserved as aligned Messel, Germany (Wuttke 1983). As in the feather
oblate bodies in the same size range as those in the analysed here, it is clear that these structures are fossil
Crato fossil (figure 2b,c). The organic material of the melanosomes. Likewise structures in a feather from
feathers in both specimens consists entirely of aligned the Oligocene of Cereste interpreted by Davis &
oblate bodies. Briggs (1995, fig. 1b) as bacteria surrounded by glyco-
The oblate structures from the dark bands in the calyx can now be identified as melanosomes sur-
fossil Crato feather are strikingly similar in size, shape rounded by the remains of b-keratin fibres. The
and orientation to eumelanosomes from the barbules structures in a decaying osprey feather illustrated by
of a black-pigmented contour feather from a Red- Davis & Briggs (1995, fig. 1a) for comparison are also
winged Blackbird (figure 1d ), and to eumelanosomes presumably melanosomes. Feathers in dinosaurs may
from other modern bird feathers (Durrer 1986; Zi also preserve melanosomes, although they have yet
et al. 2003). to be investigated; colour banding has been reported
in feathers of the Cretaceous theropod dinosaur
Caudipteryx zoui (Ji et al. 1998).
4. DISCUSSION
Phaeomelanosomes are distinct morphologically
We interpret the oblate structures in the fossil feathers
as fossilized eumelanosomes based primarily on their from eumelanin-containing melanosomes in both
similarity to these structures in modern feathers. There birds (McGraw 2006) and mammals (Liu et al.
is no reason for bacteria to be preserved on the dark 2005) and are generally more globular in shape.
bands alone and not on the light bands of the fossil Their chemical composition, however, is somewhat
feather. Rather, eumelanin is resistant to chemical different (Liu et al. 2005) and their preservation
degradation (Liu & Simon 2003), and the presence of potential remains to be assessed. Their preservation
eumelanin in dark feathers makes them less prone to in fossil feathers would also be of interest as they
bacterial decay than white feathers (Goldstein et al. produce rusty red to buff yellow colours.
2004). This supports the interpretation of the carbon Many melanin-bearing structures are preserved in
residue found in the Crato feather and other fossil fossils. The eye of the Eocene bird (figure 2d )
feathers (Davis & Briggs 1995) as a result of the appears to preserve retinal eumelanosomes based on
preservation of eumelanin-containing melanosomes. a comparison with a modern bird (figure 2e). Similar
Similar oblate structures, previously interpreted structures have been reported in the eyes of fossil fish
as feather-degrading bacteria, have been revealed from the Cretaceous of Spain (Gupta et al. 2008,
by SEM of feathers from the Cretaceous of Alabama fig. 3c) and from the Eocene of Grube Messel (Liebig
Biol. Lett.
Fossil feather colour J. Vinther et al. 3
(a) (b)
(c)
(e) (d)
Figure 2. (a) Skull of undescribed bird from the Fur Formation, Early Eocene, Denmark (Danekræ 200, MGUH 28.929),
preserving feathers and the eye as an organic film. (b,c) Details of the feather region showing aligned eumelanosomes.
(d ) Detail of the eye showing elongate and oblate eumelanosomes. (e) TEM of a section through the retina of a Whip-poor-
will (Caprimulgus vociferus, Caprimulgidae). Scale bars, (a) 10 mm; (b) 1 mm; (c) 5 mm; (d ) 1 mm; (e) 5 mm.
1998, Pl. 5, fig. 6). Structures preserving the fur and the carbon coating has presumably been lost
of mammals from Messel are strikingly similar to due to oxidation, except in the single isolated
melanosomes (e.g. in the bat Palaeochiropteryx: feather, which is still carbonaceous. Different shapes
Wuttke 1983, Pl. 2, fig. 4). It has also been suggested and arrangements of melanosomes in bird feathers are
that the organic imprint of the integument of ichthyo- associated with different colours, including black,
saurs could be composed of melanocytes (Whitear brown, red, buff and even iridescent structural colours
1956). Thus, the preservation of eumelanin may (Prum & Williamson 2002; McGraw 2006; Prum
be important in the preservation of soft tissue 2006). Our discovery of melanosomes in a fossil
outlines in animal fossils from a number of localities. feather therefore opens up the possibility of predicting
Fossil squids preserve the ink sac as an organic feather colour in ancient birds and perhaps in other
mass composed of fossilized eumelanin granules theropod dinosaurs, with obvious implications for
(Doguzhaeva et al. 2004). The colour bands in some understanding their ecology and behaviour.
fossil insects presumably also reflect the distribution
of eumelanin, but as insects do not generate melano- We are grateful to Kay Hawkins, Leicester and Sten
somes, such structures are unlikely to be evident Jakobsen, David Harper and Arne Nielsen, Copenhagen for
under the ESEM. the loan of specimens and Kristof Zyskowski, Yale Peabody
Our observations indicate that the structures on Museum, for providing access to the bird collection. Tim
Quinn took the TEMs of the bird retina. Zhenting Jiang
fossil feathers previously reported as bacteria are and Barry Piekos assisted with SEM. Michael Wuttke
melanosomes, and that the Cretaceous feather offered valuable comments. The research was funded by
described here (figure 1) was originally banded with a NSF EAR-0720062 to D.E.G.B. and R.O.P. and completed
black and white eumelanin pattern. It is likely that while D.E.G.B. was a Humboldt Award holder at the
melanosomes are the source of the carbon in fossil University of Bonn.
feathers, as the eumelanin inside the melanosomes
remains even after the keratin that encloses them has
degraded. The absence of carbon in other feathers, such
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