THE TAPHONOMY of COLOUR in FOSSIL INSECTS and FEATHERS by MARIA E

[Palaeontology, Vol. 56, Part 3, 2013, pp. 557–575]

THE TAPHONOMY OF COLOUR IN FOSSIL INSECTS AND FEATHERS by MARIA E. MCNAMARA1,2,3 1Department of Geology & Geophysics, Yale University, New Haven, CT 06520, USA 2UCD School of Geological Sciences, University College Dublin, Belﬁeld, Dublin 4, Ireland 3Current address: School of Earth Sciences, University of Bristol, Bristol, BS8 1RJ, UK; e-mail: [email protected]

Typescript received 19 October 2012; accepted in revised form 5 March 2013

Abstract: Colouration is an important multifunctional during diagenesis. Preservation of colour is controlled by a attribute of modern animals, but its evolutionary history is suite of factors, the most important of which relate to the poorly resolved, in part because of our limited ability to rec- diagenetic history of the host sediment, that is, maximum ognize and interpret fossil evidence of colour. Recent studies burial temperatures and fluid flow, and subsurface weather- on structural and pigmentary colours in fossil insects and ing. Future studies focussing on key morphological and feathers have illuminated important aspects of the anatomy, chemical aspects of colour preservation relating to cuticular taphonomy, evolution and function of colour in these fossils. pigments in insects and keratinous structures and nonmela- An understanding of the taphonomic factors that control the nin pigments in feathers, for example, will resolve outstand- preservation of colour is key to assessing the fidelity with ing questions regarding the taphonomy of colour and will which original colours are preserved and can constrain inter- enhance our ability to infer original colouration and its pretations of the visual appearance of fossil insects and functions in fossil insects and theropods. theropods. Various analytical approaches can identify anatomical and chemical evidence of colour in fossils; experi- Key words: structural colour, multilayer reflectors, mela- mental taphonomic studies inform on how colour alters nin, pigments, taphonomy, fossil preservation.

COLOUR is a phylogenetically important and multifunc- fossil colouration and its functional evolution. Key tional attribute of extant animals (Hill and McGraw discoveries include fossilized melanin-bearing organelles 2006), with important roles in inter- and intraspeciﬁc (melanosomes) in feathers (Fig. 4; Vinther et al. 2008) signalling (e.g. sexual and social display (Parker 2000; and structural colours in fossil insects from many locali- Bokony et al. 2003; Seago et al. 2009), camouﬂage (Riley ties (Figs 1, 5; McNamara et al. 2012b). Recent studies 1997), UV protection (Butler et al. 2005), thermoregula- have also contributed novel methods for analysing fossil tion (Riley 1997), sequestration of toxic metal ions colour (Figs 6, 7; Li et al. 2010; Wogelius et al. 2011; (McGraw 2003) and as a sink for free radicals (Cesarini McNamara et al. 2011, 2012a, b), provided insights into and INSERM 1996)). Visual evidence of colour associ- the taphonomy of colour (McNamara et al. 2011, 2012a, ated with fossils can be conspicuous, for example metal- b, 2013a, b), constrained interpretations of enigmatic lic colours in fossil insects (Fig. 1; Lutz 1990; Parker anatomical features (Zhang et al. 2010) and allowed and McKenzie 2003; Tanaka et al. 2010; Wedmann et al. inferences on behaviour and evolution (Clarke et al. 2010) and colour patterning in fossil molluscs (Hagdorn 2010; Li et al. 2010, 2012; Zhang et al. 2010; McNamara and Sandy 1998), insects (Fig. 2; Wang et al. 2010) and et al. 2011). Insects and feathers each have an important some feathers (Fig. 3; Vinther et al. 2008; Li et al. 2010; fossil record: insects have been important members of Wogelius et al. 2011), and can yield taxonomic and continental ecosystems since at least the Early Devonian palaeoecological information (Blodgett et al. 1983; Turek (Grimaldi and Engel 2005); feathers, a key derived avian 2009). Despite their palaeobiological potential, such ‘col- character (Bergmann et al. 2010), were diverse by the oured’ fossils have, until recently, received little atten- late Cretaceous and may extend to the base of the tion. The original colouration of most fossil organisms archosaur tree (Norell 2011). Evidence of original colour thus remains speculative (Labandeira 2005; Li et al. in fossil examples of these taxa thus has the potential to 2010; Carney et al. 2012). A profusion of recent studies inform on the evolution of colour and its functions in on the colour of ancient insects and feathers, however, important fossil groups, and the role of colour, in par- has resulted in major advances in our understanding of ticular visual signalling, in ancient ecosystems. Even

AB C

DE F

FIG. 1. Metallic colours in fossil insects. A, leaf beetle (Coleoptera: Chrysomelidae) from the middle Eocene of Eckfeld, Germany. NHMM PE1997 003a. B, weevil (Coleoptera: Curculionidae) from the middle Eocene of Messel, Germany. SMF MeI13011. C, jewel beetle (Coleoptera: Buprestidae) from Messel showing patterning on thorax and elytra. SMF MeI14586. D, partial specimen of a jewel beetle from the late Oligocene of Enspel, Germany. GDKE 1996 PE 1592. E, moth from Messel with, inset, reconstruction of original wing colours (modiﬁed from McNamara et al. 2011). SMF MeI12269. F, detail of coprolite from Messel showing well-deﬁned moth scales. SMF MeI11808. Scale bars represent: A, 2 mm; B–E, 5 mm; F, 5 mm. where evidence of colour is preserved in fossils, however, Interpretations of the colours and colour patterns of fos- it may be the result of diagenetic alteration (Klug et al. sil organisms thus require an understanding of the 2009; Turek 2009; McNamara et al. 2011, 2012a, b). processes leading to their preservation. The purpose of

FIG. 2. ABMonotonal colour patterning in fossil insects. A, leaf beetle from the late Eocene of Florissant, USA, showing symmetrical spotted patterning on elytra. UCM 51311a. B, unidentiﬁed bug (Hemiptera) from the late Miocene of Oeningen, Switzerland with, inset, detail of area indicated showing submillime- tre-scale spotted pattern. MCZ 14431. C, leaf beetle from the late Eocene of Florissant, Colorado, USA, showing banding on elytra and abdomen. UCM 51324. D, hindwing from the Neuropteran C D Limnogramma mongolicum (Kalli- grammatidae) from the Jurassic of Daohuguo, China, showing promi- nent eyespot. NIGPAS NND11021. Scale bars represent: A, C, 2 mm; B, 5 mm; D, 10 mm. MCNAMARA: FOSSIL COLOUR 559

ABCD

FIG. 3. Fossil feathers showing monotonal colour banding. A, feather from the Oliogocene Creede Formation, USA, showing proximal to distal gradation in tone. UCMP 169013. B, feather from Archaeopteryx lithographica (from Carney et al. 2012) showing proximal to distal gradation in tone. MfN MB.Av.100. C, feather from the Miocene Alvord Creek Formation, Oregon, USA, showing distal to proximal gradation in tone. UCMP 391006. D, left forelimb of the troodontid Anchiornis huxleyi from the late Jurassic Taojishan Formation, China, showing variation in tone across the wing. BMNHC PH828 (from Li et al. 2010). Scale bars represent: A, 2 mm; B, 5 mm; C, D, 10 mm. this paper is to review recent developments in the study 1959). Structural colours are generated by constructive of colour in fossil insects and feathers and summarize inference when light is scattered in the visible part of how they have transformed our understanding of how the electromagnetic spectrum by variations in tissue colour-generating mechanisms can be recognized in the nanostructure; such biophotonic nanostructures com- fossil record, how colours are modified by diagenetic prise materials of alternating high- and low-refractive processes and how ‘coloured’ fossils can shed light on index and can be organized into one-, two- or three- the ecology and evolution of ancient insects and dimensional arrays (Prum and Torres 2003). Each of theropods. these colour-generating mechanisms is discussed in Light visible to humans is represented by a narrow detail below. region of the electromagnetic spectrum characterized by wavelengths between c. 380 and 750 nm (Farrant 1997). Institutional abbreviations. BMNHC, Beijing Museum of Natu- Certain animals, including many insects and birds, are ral History, China; GDKE, Generaldirecktion Kulturelles Erbe, sensitive to colours in the ultraviolet (10–400 nm) Mainz, Germany; IVPP, Institute of Vertebrate Paleontology and regions of the spectrum (Shi and Yokoyama 2003); rare Paleoanthropology, Beijing; MCZ, Museum of Comparative € insects (e.g. Melanophila (fire bugs; Vondran et al. Zoology, Cambridge, MA, USA; MfN, Humboldt Museum fur 1995)) are sensitive to infrared radiation (750 nm– Naturkunde, Berlin, Germany; NHMM, Naturhistorische Museum Mainz, Germany; MNCN, Museo Nacional de Ciencias 300 lm). In addition, many insects are sensitive to Naturales, Madrid, Spain; NIGPAS, Nanjing Institute of Geology polarization (Land 1997). Colour-generating mechanisms and Paleontology, China; SMF, Forschungsinstitut und Natur- in the cuticle of extant insects and feathers fall into two museum Senckenberg, Frankfurt, Germany; UCM, University of broad classes (with some overlap, see below) (Farrant Colorado Museum of Natural History, Boulder, CO, USA; 1997). Pigments are chemical compounds that are effi- UCMP, University College Berkeley Museum of Paleontology, cient absorbers of specific wavelengths of light; light of USA; YPM, Yale Peabody Museum of Natural History, New reflected wavelengths produces visible colour (Cromartie Haven, CT, USA. 560 PALAEONTOLOGY, VOLUME 56

A B C D

E F G F

FIG. 4. Scanning electron micrographs of modern (A–B) and fossil (C–H) feathers. A, eumelanosomes within a barbule of a satin bowerbird (Ptilonorhynchus violaceus) feather. B, phaeomelanosomes within a barbule of a pigeon (Columba livia) feather. C, three- dimensionally preserved eumelanosomes associated with feathers in a grebe (Podicipedidae) from the early Miocene of Libros, Spain. MNCN-63817. D–F, feathers from the bird Confuciusornis from the Early Jurassic Jehol Group, China (modiﬁed from Zhang et al. 2010). IVPP-V13171. D, eumelanosomes preserved as external moulds. E, F, phaeomelanosomes preserved in three dimensions (E) and as external moulds (F). G, rod-shaped feather degrading bacteria on a decaying contour feather from an extant ﬁnch (Taeniopygia gut- tata). H, fossil feather from Paraprejica kelleri (Aves: Caprimulgiformes) from the middle Eocene of Messel, Germany, showing incompletely degraded keratinous feather matrix. SMF MeV 1635a. All scale bars represent 2 lm.

GENERATION OF COLOUR IN INSECT in these taxa for which there is fossil evidence. Chemically, CUTICLE AND FEATHERS melanins are large, inert polymers of dihydroxyindole and dihydroxyindole carboxylic acid that crosslink strongly Pigmentary colours with proteins (McGraw 2006); the precise structure is not well understood (Li et al. 2012). In addition to their con- The mechanism by which pigments produce colour is tribution to inter- and intraspecific signalling, melanins well understood. In most pigments, absorption of light fulfil essential biological functions in metal scavenging, occurs in specific chemical regions (chromophores) that radioprotection and photoprotection (Liu and Simon comprise either conjugated p-systems (i.e. alternating sin- 2003; Liu et al. 2005); they also confer resistance to abra- gle and double bonds) or metal complexes (Shawkey and sion and immune attack, including bacterial degradation Hill 2006). In each type of chromophore, empty electron (Goldstein et al. 2004; Nappi and Christensen 2005; Gun- orbitals are available for electron excitation (due to shar- derson et al. 2008). In most insects, melanins are dissemi- ing of electrons between adjacent atoms); the energy dif- nated throughout the epi- and exocuticle and are ference between the ground- and excited state for a given implicated in cuticle sclerotization (Andersen 2010). In electron is equal to the frequency of light that is feathers, melanins occur within discrete membrane-bound absorbed. lysosome-related organelles termed melanosomes that are Diverse pigments occur in insect cuticle and feathers. embedded in the feather b-keratin matrix (Marks and Melanins, carotenoids and flavonoids are common in both Seabra 2001; Fig. 4). Melanosomes are typically 470– (Hill and McGraw 2006; Ghiradella 2009); pterins, ommo- 2000 nm long and vary in morphology according to the chromes, tetrapyrroles, bilins and quinones can also occur chemical variant of melanin they contain: eumelanin in insect cuticle (Ghiradella 2009), and psittacofulvins and occurs in elongate, rod-shaped eumelanosomes (usually porphyrins, in feathers (Hill and McGraw 2006). Melanins 900–1100 nm long; Fig. 4A), and phaeomelanin, in oblate are the most abundant and phylogenetically broadly dis- to spheroidal phaeomelanosomes (c. 470 nm long; tributed pigments in extant insects (Liu and Simon 2003) Fig. 4B). Eu- and phaeomelanosomes impart black, and and feathers (McGraw 2006; Ghiradella 2009; Stoddard brown to rufous, tones in feathers, respectively; melano- and Prum 2011), and they are the only class of pigments somes that impart grey tones are intermediate in morphol- MCNAMARA: FOSSIL COLOUR 561

A BC

D E F

FIG. 5. Biophotonic nanostructures in fossil insects. A–C, scanning (A) and transmission (B–C) electron micrographs of multilayer reflectors in fossil beetles. A, fractured vertical section of cuticle from a jewel beetle (Coleoptera: Buprestidae) from the late Oligocene of Enspel, Germany, showing laminated exocuticle (ex), epicuticular multilayer reflector (m) and vertical pore canals (arrow) traversing exocuticle. GDKE ENS 2009 PE 5889. B, vertical section of cuticle from a leaf beetle from the middle Eocene of Messel, Germany, showing laminated exocuticle (ex) and epicuticular multilayer reflector (m) characterized by alternating layers of high- and low-electron contrast. r, resin; s, sediment; t, trabecula. SMF MeI 15553. C, detail of epicuticular multilayer reflector (m) preserved in an unidentified beetle from the early Miocene of Clarkia, USA. YPM 2010 P37b 005. D–G, scanning (D–E) and transmission (F–G) electron micrographs of multilayer reflectors from metallic moths from Messel; each of the nanostructures described below contribute to the observed hue of the fossils. D, dorsal surface of cover scale showing longitudinal ridges flanked by short microribs and connected by transverse cross-ribs. Internal laminae of the multilayer reflector are visible top left. E, dorsal surface of cover scale showing detail of cross-ribs, microribs and perforations in the scale surface. F, vertical transverse section of two cover scales showing concave geometry of the multilayer reflector in between ridges (arrows). SMF MeI 11808 and MeI 12269. Scale bars represent: A–C, E–F, 1 lm; D, 5 lm, G, 500 nm. ogy (Li et al. 2010). Melanosomes of different morphology signalling (Parker 2000; Seago et al. 2009) and are usu- can occur within individual feathers (Li et al. 2010) and ally associated with one or more striking optical effects, can co-occur with other pigments (e.g. carotenoids; Lucas for example iridescence (change in hue with observation and Stettenheim 1972; Hofmann et al. 2007). In Aves, angle), opalescence and reflection that is metallic (highly melanin-based plumage pigmentation (and its absence) is directional, near-100 per cent reflectance), ultraviolet or evolutionarily primitive; carotenoids are considered to polarized (Vukusic and Sambles 2003; Doucet and have several independent evolutionary origins, and other Meadows 2009). Rare matte structural colours (with key pigments, for example psittacofulvins, unique origins probable functions in crypsis) are also known (Parker (Stoddard and Prum 2011). et al. 1998a; Wilts et al. 2009). Biophotonic nanostructures in extant insects comprise three main classes: (1) diffraction gratings, that is, arrays of parallel ridges or Structural colours slits, which usually generate weak spectral iridescence; (2) two- or three-dimensional photonic crystals with hexago- Structural colours are the brightest and most intense nal, cubic, diamond or gyroid lattices that generate a colours in nature (Vukusic and Sambles 2003; Parker spectrum of visual effects from dull matte colours to and Townley 2007) and are widespread in extant insects bright opalescence; and (3) multilayer reflectors, that is, and birds (Kinoshita and Yoshioka 2005). Such colours alternating layers of high- and low-refractive index that function primarily in inter- and intraspecific visual usually generate bright metallic iridescence (Parker et al. 562 PALAEONTOLOGY, VOLUME 56

cle (Neville and Caveney 1969) or endocuticle (Hinton 1973). Brighter colours are generated in multilayer reflectors with more layers; mirror-like (near-100 per cent) reflection is achieved where there are 10 or more high refractive index layers (Land 1972). In lepidopteran scales, colour-producing nanostructures in cover scales are typically underlain by melanin-rich basal scales; the melanin absorbs light transmitted through the biophotonic array, thus preventing incoherent scattering and enhancing the spectral purity of the observed colour (Ghiradella 1998). The role of melanin in enhancing structural colours in the cuticle of other insect groups is unclear; in some beetles, melanin may be associated with the high-index layers in multilayer reflectors (Schultz and FIG. 6. Quadratic discriminant analysis of plumage colour Rankin 1985) or may occur in a discrete layer underlying based on the morphology of feather melanosomes (from Li et al. multilayer reflectors (Parker et al. 1998a). The evolution- 2010). Black, brown and grey dots represent data from extant ary origins of the various biophotonic nanostructures in birds and numbers represent samples from the troodontid insects have been considered only for beetles (Seago et al. Anchiornis huxleyi from the late Jurassic Taojishan Formation, China. The geometry of melanosomes from the fossil feathers 2009) and some Lepidoptera (Tilley and Eliot 2002; Wilts clearly lies within the range exhibited in modern birds and, in et al. 2009). Diffraction gratings and multilayer reflectors many samples, corresponds to distinct feather colours. are considered to have multiple evolutionary origins (Seago et al. 2009); there is limited evidence that multilayer reflectors are evolutionarily primitive (Tilley and 2001; Vukusic 2003; Seago et al. 2009). Multilayer reflec- Eliot 2002; Wilts et al. 2009), although this hypothesis is tors are the most common biophotonic nanostructure in controversial (Ingram and Parker 2008). insects, where they can occur within the epicuticle In feathers, structural colours originate via two distinct (Schultz and Rankin 1985; Kurachi et al. 2002), exocuti- mechanisms that are each localized to specific regions of

ABC

FIG. 7. Synchrotron rapid scanning X-ray fluorescence (SRS-XRF) mapping of the plumage of Confuciusornis sanctus from the Lower Cretaceous Jehol Group, China (from Wogelius et al. 2011). A, optical image. IVPP MGSF 315B. B, SRS-XRF map of (A) showing concentrations of Cu (red) in the plumage, Ca (blue) in the bones, and Zn (green) in the sedimentary matrix. C–E, SRS-XRF maps of the region indicated in (A) for S (C), Ca (D) and Zn (E). Scale bar represents 20 mm. MCNAMARA: FOSSIL COLOUR 563 the feather. Quasi-ordered three-dimensional nanostruc- colour-producing array is suspected to comprise a per- tures (with either a channel-type or microsphere architec- meable array of air plus another material, however, an ture) occur within the keratinous medulla of barb rami expedient alternative is to immerse the fossil in media (Shawkey et al. 2003; Shawkey and Hill 2006; Noh et al. of different refractive index; this alters the average 2010). Such keratin-air nanostructures generate bright refractive index of the colour-producing array and thus matte colours and are underlain by a thin layer of mela- the visible hue (Mason 1927). This technique has been nosomes; as in lepidopteran scales (see above), the mela- successfully applied to metallic scales in fossil lepidopter- nin absorbs incoherently scattered light within the ans from Messel, in which the nanostructure in the structure and does not serve in colour production per se scales comprises a chitin-air nanostructure. The tech- (Shawkey and Hill 2006). Sheet-like arrays of melano- nique could also be applied to metallic scales in other somes within barbules act as thin-film reflectors and gen- fossil insect taxa (e.g. weevils) and in fossil feathers erate glossy black to highly iridescent colours (Doucet where colour is generated by quasi-ordered nanostruc- et al. 2006; Yin et al. 2006; Yoshioka et al. 2007; Shawkey tures in the barbs. et al. 2011); even slight organization can produce weakly Many fossil insects exhibit monochromatic patterning iridescent, glossy visual effects (Li et al. 2012). The precise expressed as varying tones of brown (Fig. 2) but the ori- hue produced is a function of the thickness of the thin gins of this phenomenon have not been investigated. It (100–300 nm) keratin cortex that envelops the melano- is conceivable that such patterning reflects original varia- some layer(s) (Prum 2006). Quasi-ordered and thin-film tions in cuticle thickness (Rasnitsyn and Quicke, 2002) biophotonic nanostructures in birds are considered to and/or pigment concentrations, in particular, eumelanin have multiple independent origins (Stoddard and Prum (Vinther et al. 2008). Colour patterning can also occur 2011). in fossil insects with metallic colours (e.g. Fig. 1C), but has not been studied in detail. Chromatic variations in metallic hue across a specimen presumably reflect varia- FOSSIL EVIDENCE FOR COLOUR- tions in the thickness of the multilayer reflector; pattern- GENERATING MECHANISMS ing consisting of alternating metallic and black regions may reflect presence or absence of a multilayer reflector. Hand specimens and light microscopy Interpretations of patterning in fossil insects are most robust where specimens exhibit features that occur (and Fossil insects and feathers can manifest evidence for col- have known visual functions) in extant insects, for exam- our in hand specimen, for example metallic colours and/ ple symmetry systems (i.e. mirror images in paired tis- or tonal (monochromatic) patterning. Metallic reflection sues such as insect wings), disruptive markings or is evidence of structural colour (Parker et al. 1998a) and eyespots (Heads et al. 2005; Wang et al. 2010). Rare sub- is known in fossil insects from many Cenozoic localities fossil and Miocene insect specimens exhibit patches of (Fig. 1; McNamara et al. 2012b and references therein). dull red to yellow colouration when freshly exposed, but Analysis of samples of cuticle from metallic fossil insects these colours fade rapidly upon exposure to sunlight and using electron microscopy and mathematical modelling air; this process may reflect oxidation of partially confirms that the preserved colours in these specimens degraded carotenoid-based pigments (Rasnitsyn and are structural in origin (Parker and McKenzie 2003; Quicke 2002). Tanaka et al. 2010; McNamara et al. 2012b). Barbules in Tonal variation is also known in fossil feathers, both a single fossil feather from Messel (middle Eocene, Ger- within individual feathers (Fig. 3A–C; Vinther et al. 2008; many) exhibit a silvery metallic sheen (Vinther et al. Li et al. 2010; Barden et al. 2011; Wogelius et al. 2011; 2010); preserved ultrastructural evidence (see below) Carney et al. 2012) and among feathers from an individ- strongly suggests that the feather is structurally coloured ual specimen (Fig. 3D; Li et al. 2010); this patterning can (Vinther et al. 2010). The striking red-brown and violet relate, at least in part, to variation in melanin-based hues hues of the feather barbs and rami may reflect diage- (Vinther et al. 2008; Li et al. 2010, 2012; Barden et al. netic incorporation of metals, especially Fe, into feather 2011; Wogelius et al. 2011; Carney et al. 2012). Patterning melanosomes (Vinther et al. 2010). Metallic hues may within individual barbules of fossil feathers can closely also form during diagenesis of other organic tissues: fos- resemble melanin-based patterns in modern feathers and sil graptolites associated with clay minerals can exhibit can aid interpretation of feather microstructures (McKel- blue colours (U. Farrell, pers. comm. 2012), possibly lar et al. 2011). Survival of biological patterning can be due to light scattering from tectonically aligned clay reasonably inferred in fossil feathers where the margins of minerals. Whether or not preserved metallic colours are different colour bands match isochronic sections in pig- structural in origin can be tested using electron micros- mentary patterning in modern feathers (Vinther et al. copy and computer modelling (see below). Where the 2008). 564 PALAEONTOLOGY, VOLUME 56

Fossils with metallic colours and colour patterns in Electron microscopy hand specimens are obvious targets for studies of fossil colours, but monotonal fossils may also yield evidence Electron microscopic imaging of preserved anatomical of colour. Indeed, many fossil feathers lack obvious detail is critical to identification of colour-producing variations in tone but exhibit ultrastructural or chemi- structures in fossil feathers (Fig. 4) and insects (Fig. 5). cal evidence of colour (see below). Further, recent taph- Scanning electron microscopy (SEM) cannot distinguish onomic experiments using extant structurally coloured between multilayer reflectors and other laminated regions insects demonstrate that ultrastructural evidence of of cuticle in extant and fossil insects (Fig. 5A). Transmis- biophotonic nanostructures can endure the effects of sion electron microscopy (TEM) of multilayer reflectors in burial even where visible evidence of structural colour extant insects, however, reveals a characteristic ‘barcode’ is degraded (Fig. 8; McNamara et al. 2013a; see ‘The pattern of alternating layers (each c. 100–150 nm thick) of fate of original colours’, below). Fossils that lack obvi- high- and low-electron contrast (Fig. 5B–C, F–G). The ous colour thus have the potential to provide key high- and low-contrast layers are assumed to represent lay- insights into the evolution of structural colour and ers of high- and low-refractive index, but their precise behaviour. chemical composition and refractive index is notoriously difficult to assess (Noyes et al. 2007). Identification of a ‘barcode’ pattern in TEM images of a laminated structure in fossil insect cuticle is a strong indicator of a fossil mul- A BC tilayer reflector (Parker and McKenzie 2003; Tanaka et al. 2010; McNamara et al. 2011, 2012b), but unequivocal determination of this requires mathematical modelling (see below). SEM is also useful for determining the presence of other ultrastructures capable of producing or modifying colour. SEM imaging of structurally coloured scales in fossil lepidopterans from Messel revealed evidence of a fossil multilayer reflector and various colour-modifying ultrastructures (Fig. 5D–G); the latter produce visual effects D E that are ecologically significant (McNamara et al. 2011). SEM has the potential to reveal preserved remains of other biophotonic nanostructures in fossil insects, for example diffraction gratings and three-dimensional photonic crystals. Diffraction gratings with a postulated anti-reflective function are known from fossil flies hosted in amber (Par- ker et al. 1998b; Tanaka et al. 2009) and have been reported in arthropods from the Cambrian (Parker 1998), but examples of three-dimensional photonic crystals have F H not yet been reported in the fossil record. Scanning electron microscopy imaging of many fossil feathers reveals ovoid to rod-shaped microstructures that can be closely spaced and aligned parallel to the barb or barbule long axis (Fig. 4B–F; Vinther et al. 2008). Such microstructures were originally interpreted as the fossil- G ized remains of keratinophilic decay bacteria preserved in three dimensions via rapid replacement by authigenic minerals (Wuttke 1983), but were reinterpreted recently as the decay-resistant remains of feather melanosomes FIG. 8. Maturation experiments using the jewel beetle Chrys- (Vinther et al. 2008). Melanosomes and many bacteria ochroa raja (Coleoptera: Buprestidae; modified from McNamara (e.g. Fig. 4G) are similar in gross morphology and size et al. 2013a). A, untreated specimen. B–E, light micrographs of cuticle from untreated (B) and experimentally decayed (C) spec- (Davis and Briggs 1995; Vinther et al. 2008; Zhang et al. imens, and specimens experimentally matured at 200°C, 500 bar 2010; Knight et al. 2011); reinterpretation of the fossil (D) and 270°C, 500 bar (E). F–G, transmission electron micro- microstructures as preserved melanosomes is therefore graphs of untreated (F) cuticles and cuticles matured at 270°C, based on several arguments relating to their spatial orga- 500 bar (G). H, reflectance spectra for cuticles in (A), (D) and nization and location within the feather. A melanosome (E). Scale bars represent: A, 10 mm; B–E, 1 mm; F–G, 1 lm. interpretation is supported where the fossil microstruc- MCNAMARA: FOSSIL COLOUR 565 tures exhibit most or all of the following features: (1) tance spectra generated using this technique are compared location within, or envelopment by, an organic matrix with observed reflectance spectra measured from the sur- (presumably the degraded remains of the feather keratin), face of the fossil to assess whether the putative biophotonic that is, the structures are internal to the feather and are nanostructure in the fossil can produce the observed hue. not external films of decay bacteria that grew on the The 2D Fourier transform uses direct observations of feather tissue during diagenesis (Zhang et al. 2010); (2) spatial variation in refractive index rather than idealized or preferential location, or at least high abundance, within average values and can be applied to all types of biopho- dark regions of fossil feathers (Vinther et al. 2008; Barden tonic nanostructure, not just laminar arrays (Prum and et al. 2011); (3) dense packing, forming a discrete uni- Torres 2003); it has been used to analyse colour-producing form surficial layer (e.g. Vinther et al. 2010) as in the structures in extant insects, birds and mammals (Prum barbules of extant birds (Shawkey et al. 2006); and (4) and Torres 2003; Shawkey et al. 2009; Noh et al. 2010). diagnostic nanoscale organizations, for example alignment Digital TEM micrographs of cuticle are analysed using a parallel to the barb long axis (Knight et al. 2011) that 2D Fourier tool that is freely available (http://www.yale. cannot be generated by bacteria (Vinther et al. 2010; Li edu/eeb/prum/fourier.htm) and implemented in the et al. 2012). Despite increasing evidence for the preserva- matrix algebra program MATLAB. The tool uses the distri- tion of melanosomes and melanin within theropods and bution of lighter and darker areas in the TEM image (and other fossil groups (Glass et al. 2012; Lindgren et al. therefore the distribution of materials of different refractive 2012), interpretation of the fossil microstructures as pre- index) to estimate the average refractive index of the struc- served feather melanosomes (and thus survival of the pig- ture. 2D fast Fourier transform analyses of spatial variation ment melanin on geological timescales) is not universally in refractive index generate radial averages of Fourier accepted on the basis of microstructure alone (Schweitzer power spectra (useful for assessing whether a particular 2011; Glass et al. 2012). Some authors have proposed that structure can produce visible wavelengths) and predicted the fossil microstructures represent melanosomes released reflectance spectra. This technique has been applied suc- from the skin of the animals during decay (Lingham- cessfully to cuticular nanostructures in fossil insects from Soliar and Plodowski 2010) or the degraded remains of several localities (McNamara et al. 2011, 2012b). structural collagen or keratin (Lingham-Soliar 2011). Studies of the colouration of fossil feathers have used Interpretations of fossil melanosomes may be more reli- statistical analysis of the morphology of fossil melano- able where they are supported by chemical evidence of somes to predict colour within certain confidence inter- melanin survival (Schweitzer 2011; Wogelius et al. 2011; vals (Clarke et al. 2010; Li et al. 2010, 2012; Carney et al. see below). Some fossil feathers retain three-dimensional 2012). These analyses were based on a data set of melano- details of keratinous feather structures (e.g. Fig. 4H), somes from a phylogenetically diverse sample of extant which are obvious targets for the recovery of nonmelanin bird feathers with melanin pigmentation (Li et al. 2010, feather pigments and biophotonic nanostructures. 2012; Clarke et al. 2010). The data set included parameters such as long-axis, short-axis, long- and short-axis skew, long- and short-axis variation, aspect ratio and Modelling and statistics ‘density’ (i.e. number of melanosomes per unit area). Data on these aspects of the morphology and packing of Identification of biophotonic nanostructures in fossil fossil melanosomes were compared with the data set of insects is contingent upon optical modelling of nanostruc- modern samples using quadratic discriminant analysis, a tures within the cuticle. In extant insects, coherent scatter- statistical technique that estimates the probability with ing can be analysed using various techniques, in particular, which unknown samples can be classified correctly using the matrix method of Macleod (1969) and applications of data on known samples (Li et al. 2012). In each study, the discrete 2D Fourier transform (Prum and Torres forward stepwise analysis was used to determine which 2003). The matrix method is a powerful technique that melanosome parameters contributed significantly to the calculates the optical properties of laminar nanostructures; analysis. Different combinations of parameters were sig- average values for the thickness of each layer (measured nificant in different studies (aspect ratio and density in from TEM images), and estimates of each layer’s refractive the troodontid paravian Anchiornis (Fig. 6; Li et al. index, are used to generate a characteristic matrix for each 2010); long-axis variation, short-axis skew, aspect ratio lamina (Macleod 1969). Matrices are then analysed using and density in the fossil penguin Inkayacu (Clarke et al. purpose-built software, for example TFCalc (Software 2010); and aspect ratio, long-axis, short-axis, long- and Spectra, Inc., Portland, OR, USA). This approach is rou- short-axis variation, and aspect ratio skew in the paravian tinely used in thin-film optics and has been applied to bee- Microraptor (Li et al. 2012)), but the importance of these tles from Messel (Parker and McKenzie 2003) and from the differences is unclear. The data from modern feathers Pleistocene of Japan (Tanaka et al. 2010). Predicted reflec- treated melanosomes from barb rami and barbules sepa- 566 PALAEONTOLOGY, VOLUME 56 rately (presumably to account for known intrafeather var- Recent SRS-XRF analyses of fossil feathers indicate that iation in melanosome geometry; Prum 2006), but not all certain trace elements (especially organic-bound Cu) in analyses of fossil feathers made this distinction (e.g. Li fossil tissues rich in spheroidal and rod-shaped micro- et al. 2010). The results of the statistical analyses were structures have melanin affinities and may act as biomar- used to predict the colours of fossil feathers from differ- kers for melanin-derived compounds in fossils (Fig. 7; ent plumage regions with probabilities ranging from 56 to Wogelius et al. 2011). This technique allows rapid, non- 100 per cent. destructive chemical mapping of entire fossil specimens at concentrations in the ppm range (Wogelius et al. 2011). Some authors consider the resulting chemical data Chemistry superior to morphological data in studies of melanin- based colour mechanisms in fossils as the effects of dia- The chemistry of structurally coloured fossil insects is genesis on the geometry of melanosomes is poorly incompletely resolved. Electron dispersive spectroscopy resolved (Norell 2011; Wogelius et al. 2011; but see (EDS) of structurally coloured cuticle in specimens from McNamara et al. 2013b, and ‘The fate of original col- Messel, Enspel (late Oligocene, Germany), Eckfeld (middle ours’, below). Other analytical techniques that could be Eocene, Germany), Clarkia (middle Miocene, USA) and applied to studies of fossil melanin in theropods include Randecker Maar (early Miocene, Germany) confirm that ToF-SIMS, which allows simultaneous identification and the cuticle is invariably organically preserved (McNamara mapping of molecules and their structures at high spatial et al. 2011, 2012b). The extent to which original biochemi- resolution (Lindgren et al. 2012). Recent studies of fossil cal components of the lipid-rich cuticle are preserved could squid and fish using ToF-SIMS confirm that chemical be determined using techniques such as pyrolysis–gas chro- evidence of melanin is restricted to micron-sized melano- matography–mass spectrometry (py-GC-MS) and nuclear some-like bodies in tissues where melanin was probably a magnetic resonance (NMR), which inform on macromo- major constituent in life (Glass et al. 2012; Lindgren lecular complexes and proteinaceous moieties, respectively. et al. 2012). In contrast, several recent studies have investigated the chemistry of fossil feathers (most of which are organically preserved; Davis and Briggs 1995) using techniques that THEFATEOFORIGINALCOLOURS provide insights into their elemental composition (EDS), functional groups (Fourier transform infrared spectroscopy Morphological evidence of colour (FTIR)), involatile macromolecular complexes (py-GC- MS), organic free radicals (electron paramagnetic Insects. The taphonomy of colour-producing nanostruc- resonance (EPR)), spatial distribution of elements tures in insects is reasonably well understood. Multi- (synchrotron rapid scanning X-ray fluorescence (SRS- layer reflectors in Cenozoic insects have a similar XRF)) or local structure of specific metallic elements preservation potential to other cuticular nanostructures (extended X-ray absorption fine structure (EXAFS) and (McNamara et al. 2012b). The suite of ultrastructural X-ray absorption near-edge structure (XANES)) (Barden features preserved in fossil cuticles is therefore key to et al. 2011; Wogelius et al. 2011; Carney et al. 2012). assessing whether black colours are a taphonomic arte- Combination of several such techniques is a powerful fact; the preservation of diverse cuticular ultrastructures, approach to investigating the structural properties of but not biophotonic structures, indicates that biopho- organic constituents, especially melanin and its degrada- tonic nanostructures were originally absent. This does tion products, within fossils (Glass et al. 2012), and can not necessarily imply, however, that the cuticle was test interpretations of melanin fossilization based on black in vivo; nonmelanin pigments may have been morphological evidence for preserved melanosomes present originally, but visual evidence thereof is not (Schweitzer 2011; Wogelius et al. 2011). EPR is a useful preserved. technique for studies of eumelanin-based colouration in Despite widespread preservation of multilayer reflectors fossils as eumelanin possess a unique free radical signature in metallic fossil beetles, original hues are not preserved (Glass et al. 2012). However, despite successful identifica- (McNamara et al. 2011, 2012b); observed reflectance tion of eumelanin and its derivatives in the ink sac of fossil spectra of the fossils are redshifted from spectra pre- squid using this technique (Glass et al. 2012), application dicted using the preserved biophotonic nanostructure. of EPR to fossil feathers has met with only limited success; This phenomenon was attributed to alteration of the analyses have demonstrated different free radical signatures refractive index of the cuticle; changes in periodicity can in fossil feathers and the surrounding sedimentary matrix, also effect colour change in multilayer reflectors (Adachi but have not yielded diagnostic spectra for melanin 2007), but cuticular features in the fossils lack clear evi- (Barden et al. 2011). dence of volume change, for example buckling, pull-apart MCNAMARA: FOSSIL COLOUR 567 structures and desiccation cracks (McNamara et al. mechanisms in extant insects: multilayer reflectors are the 2012b). In contrast to these results, high-pressure/high- most common biophotonic nanostructure in animals temperature maturation experiments using extant struc- (Parker 2002), including beetles (Seago et al. 2009). Alter- turally coloured beetles resulted in a blueshift in natively, the high abundance of fossil multilayer reflectors observed hue (Fig. 8; McNamara et al. 2013a). The may be taphonomic in origin. All published examples of experiments used the extant jewel beetle Chrysochroa fossil multilayer reflectors are hosted within organic-rich raja, which generates metallic colour using an epicuticu- lacustrine sediments with significant volcaniclastic input lar multilayer reflector; specimens were matured for (McNamara et al. 2012a); pore waters from such sedi- 24 hours using various pressure–temperature regimes ments would be expected to have a slightly acidic pH. (117 bar, 200°C; 250 bar, 200°C; 500 bar, 200°C; and Epicuticular lipids are insoluble in acidic media, and thus, 500 bar, 270°C). The hue of the beetles changed progres- the composition and chemistry of host sediments may sively (decreasing wavelength) with increasing pressure. influence the preservation potential of multilayer reflec- This change resulted from alteration of both the refrac- tors. Maturation experiments on 3D photonic crystals tive index and periodicity of the multilayer reflector; the show that they have similar preservation potential to mul- dimensions of the reflector and of various other cuticular tilayer reflectors. The absence of 3D photonic crystals in structures were altered without obvious distortion. The the fossil record (at least in biotas of Miocene age and colour change had two discrete components: a large older) is thus considered to represent a real, evolutionary blueshift caused by a decrease in periodicity of the multi- absence (McNamara et al. 2013a). Critically, maturation layer reflector, partly offset by a smaller redshift relating experiments also demonstrate that physical evidence of to considerable alteration of the chemistry of the epicuti- colour-producing nanostructures survives in insects even cle and, in turn, an increase in its refractive index. The where visual evidence of colour is lost (McNamara et al. redshift is identical in magnitude and direction to the 2013a). Structural colour may thus have an extensive discrepancy in wavelength between observed and pre- cryptic fossil record in insect specimens that lack obvious dicted data for the fossil beetles, supporting the hypothe- metallic colouration. sis that the fossil redshift results from a change in refractive index. The chemistry of structurally coloured Feathers. Despite intense interest in the colour of fossil fossil insects has yet to be investigated comprehensively feathers, the taphonomy of colour-producing mechanisms (but see Parker and McKenzie 2003; Tanaka et al. 2010), in feathers has not been a focus of investigation. None- but it is clear that both chemical and morphological data theless, it is clear that the fidelity of preservation of fossil are critical to future attempts to reconstruct original feathers, and their melanosomes, varies considerably. Fos- structural colours in fossil insects. sil melanosomes can be preserved as three-dimensional As with fossil beetle colours, the hues produced by bodies (Fig. 4C, E) or as external moulds embedded in multilayer reflectors in fossil lepidopterans also alter dur- amorphous organic material or diagenetic minerals ing diagenesis (McNamara et al. 2011); unlike the fossil (Fig. 4D, F; Clarke et al. 2010; Li et al. 2010, 2012; Zhang beetles, however, predicted colours for the lepidopterans et al. 2010); both preservational modes can occur within are blueshifted from preserved hues. This difference could a single feather (Zhang et al. 2010). The nature of the plausibly relate to differences in the chemistry of the bio- organic matrix surrounding some mouldic melanosomes photonic tissues in each taxon: in extant insects, beetle may represent degraded feather keratin (Zhang et al. epicuticle comprises lipid and protein (i.e. chitin is 2010) or melanin (Clarke et al. 2010; Li et al. 2010). Fur- absent; Neville 1975), whereas lepidopteran scales com- ther, dark visual tones in fossil feathers can (Li et al. prise predominantly chitin (Powell 2003). Regardless of 2010), but do not always (Li et al. 2012), correspond to a the extent to which original colours have been altered, high abundance of melanosomes and do not correlate however, certain aspects of the visual ecology of structur- with the mode of melanosome preservation (Li et al. ally coloured insects may be inferred using anatomical 2010). Dark tones (i.e. a high absorbance of visible light) evidence preserved in fossils. For instance, the colour- commonly originate in organometal- or conjugated bonds producing nanostructures in the fossil moths described in modern pigments (Farrant 1997). The precise chemical above are associated with other ultrastructural features in structure, and taphonomy, of the chromophore in fossil the scales that modify the visual signal (the inherent feathers is, as yet, uncertain. iridescence and specular reflection of the multilayer In structurally coloured fossil feathers, reconstructions reflector are suppressed), implying a defensive function of original hue are precluded by degradation of the kera- for the colour (McNamara et al. 2011). tin cortex that envelops the melanosomes in vivo; this All fossil examples of structurally coloured insects cortex is responsible for the exact hue produced by the contain multilayer reflectors. This may be a function of highly ordered melanosome array (Vinther et al. 2010; Li the relative abundance of different colour-producing et al. 2012). In other fossil feather examples, however 568 PALAEONTOLOGY, VOLUME 56

(i.e. those lacking structural colour), accurate predictions Some authors have suggested that original organic of precise hue are contingent upon the geometry of mel- material has survived in metallic beetles from the mid- ansomes (Li et al. 2010). Reconstructions of original dle Eocene of Messel, but this hypothesis is supported plumage colouration in fossil theropods have assumed only by bulk elemental analysis (Parker and McKenzie that the original geometry of melanosomes is preserved 2003). Where fossil cuticles contain an epicuticular in the fossils (Clarke et al. 2010; Li et al. 2010, 2012; multilayer reflector, lipid extracts may be a useful proxy Knight et al. 2011). Fossil melanosomes, however, vary for the chemistry of the epicuticle and thus of the col- in the mode of preservation: melanosomes preserved as our-producing structure. Lipid extracts of thermally moulds and three-dimensional bodies from the same matured cuticle from extant beetles analysed via py-GC- feather region differ in size (Clarke et al. 2010) and yield MS are dominated by lipid–protein complexes. These differing colour predictions (Li et al. 2010, 2012). Matu- complexes are absent in fresh cuticle and represent ration experiments on feathers from extant birds reveal reaction products of functionalized epicuticular lipids that melanosome geometry is altered by the effects of with proteinaceous moieties from the epi- or exocuticle elevated pressure and temperature (McNamara et al. (McNamara et al. 2013a). The composition of structur- 2013b). These experiments used melanosome-bearing ally coloured fossil cuticles has yet to be investigated feathers from 12 extant taxa; feathers encompassed using techniques that inform on the structure of pre- diverse hues and melanosome types (eu- and phaeomela- served components. nosomes, solid and hollow melanosomes). The experi- Unequivocal traces of melanin have been reported in ments used two different pressure–temperature regimes fossil squid (Glass et al. 2012) and fish (Lindgren et al. (200°C, 250 bar; 250 bar, 250°C) and lasted 24 hours; 2012) but have not been identified in fossil feathers (Bar- melanosomes in all feathers altered progressively in den et al. 2011). Recent synchrotron-aided analyses using geometry (both long and short axes reduced in length) X-ray fluorescence (XRF) show that distribution maps of between the 200°C, 250 bar experiment and that using certain trace elements with a melanin affinity, for example 250°C, 250 bar. Survival of original melanosome geome- Cu, in fossil feathers may help reconstruct colour patterns tries in fossils is thus most likely where the host sedi- in fossil plumage (Wogelius et al. 2011). EXAFS and ments experienced limited burial. Not all feather- XANES analyses demonstrate that Cu is present in fossils containing fossil deposits, however, meet this criterion in organometallic form, possibly derived from original (McNamara et al. 2013b). Some studies of melanin-based melanin (Wogelius et al. 2011). The spatial distribution colouration in fossil feathers have considered that contri- of trace elements in fossil specimens, however, may also butions by other pigmentary and structural colouration result (at least in part) from taphonomic modification of mechanisms to the visible hue in vivo would have been original colouration signals. Trace metal concentrations masked by melanin (Carney et al. 2012; Li et al. 2012), could increase in tissues as a result of adsorption by but this is likely only in feather regions with very abun- microorganisms during decay (Hitchcock et al. 2009) or dant melanosomes. Feathers in many extant birds con- chelation during later diagenesis (Shock and Koretsky tain melanosomes but the visible hue derives from 1993). Studies of melanin in fossil fish suggest that it may nonmelanin pigments or biophotonic architectures be concentrated in the dark regions of fossils during dia- (McNamara et al. 2013b and references therein). Matura- genesis due to preferential degradation of more labile tion experiments on such feathers reveal that melano- organic molecules (Lindgren et al. 2012). This process somes are retained in degraded feathers even where does not, however, preclude diagenetic migration of mela- visual evidence of all other colouration mechanisms has nin from source tissues. Diagnostic biomarkers for mela- degraded completely. Given this preferential preservation nin were recovered from sediment adjacent to the ink of melanosomes, attempts to reconstruct colour in fossil sacs of fossil squid (Glass et al. 2012), although this may feathers should be integrated with anatomical and geo- reflect minor leakage of ink and/or intact melanosomes chemical data on the preservation of other pigments and from the ink sac during decay rather than later diagenesis. biophotonic structures. Trace elements within fossil feathers could also derive from endogenous sources other than melanin, for example keratin–Cu complexes in feathers (Wogelius et al. Chemistry 2011)), or from external, that is, sedimentary, sources. Preservation of intact chemical moieties of the melanin Traces of original cuticular biomolecules, for example molecule may result from thermally induced polymeriza- chitin and amino acids, are preserved in subfossil bee- tion reactions during diagenesis (Glass et al. 2012). In situ tles with epicuticular multilayer reflectors (Tanaka et al. polymerization may also explain, at least in part, the ali- 2010). Less is known about the chemical fidelity with phatic composition of some fossil feathers (Barden et al. which older structurally coloured insects are preserved. 2011). MCNAMARA: FOSSIL COLOUR 569

CONTROLS ON THE PRESERVATION Structurally coloured fossils can be abundant in biotas OF COLOUR that experienced limited burial, for example Messel, Ens- pel, Eckfeld, but absent in biotas buried to greater depths, Patterns in the fossil record of structural colour in insects for example Green River (McNamara et al. 2012a). Matu- relate to a hierarchy of taphonomic controls, including ration experiments confirm that increasing pressure alters decay, burial pressure, burial temperature, the nature of insect structural colours, but the effect of pressure is sec- diagenetic fluids, weathering and the mode of curation of ondary to that of temperature, which is the primary agent fossil specimens (McNamara et al. 2012a). These factors of colour change during burial (McNamara et al. 2013a). are also likely to govern the preservation of colour in fos- Structural colours alter progressively with increasing tem- sil feathers, although the relative importance of different perature but are lost beyond a temperature threshold; the taphonomic factors in preserving feather and insect col- value of this threshold temperature is likely to vary with our may differ. Statistical analyses of the fidelity of the the chemistry of the tissue and host sediment. Feathers preservation of structural colours in various insect taxa experimentally treated to elevated pressures and tempera- from Cenozoic biotas revealed that age and taxonomic tures lose visual and ultrastructural evidence of all compositions do not control taphonomy; age may, how- colour-producing mechanisms save for melanosomes; ever, be more important in older material as it serves as a progressive loss of anatomical detail occurs in tandem proxy for more extensive or complex diagenesis. with loss of visual colour with increasing temperature (McNamara et al. 2013b). As with insects, temperature may be the primary determinant of colour (i.e. melano- Decay some) survival in fossils.

Laboratory decay experiments on extant structurally coloured beetles at room temperatures and pressures did Diagenetic fluids and weathering not induce colour change (Fig. 8; McNamara et al. 2013a). Some fossil insect cuticles in which metallic col- Other factors that influence biota-scale patterns in the fossil ours are poorly preserved or absent, however, exhibit evi- record of colour (at least for structurally coloured fossil dence for decay by fossil or modern microbes insects) include the nature of diagenetic fluid flow and the (McNamara et al. 2012a); the latter have a particularly extent of weathering (McNamara et al. 2012a). Reactive negative impact on the fidelity of preservation. Decay hydrothermal fluids can degrade insect cuticle and lead to may also affect colours in fossil feathers, especially where precipitation of authigenic minerals within colour-produc- these are structurally coloured: the keratin cortex and ing nanostructures, resulting in loss of visible colour medulla (which house various colour-producing nano- (McNamara et al. 2012a). Extensive oxidative degradation structures) are less resistant to decay than melanin (Gold- of cuticles during weathering may also destroy structural stein et al. 2004). The high preservation potential of colours. The absence of structurally coloured insects in the melanin (Hollingworth and Barker 1991) does not, how- late Eocene of Florissant (USA), and their high abundance ever, imply that it (or melanosomes) is immune to alter- in other Cenozoic biotas (i.e. Messel, Clarkia (early Mio- ation during decay. Laboratory decay experiments on cene, USA), Enspel and Eckfeld), has been attributed to extant birds showed that decay-induced rupture of feath- variations in the extent of Recent weathering among these ers can liberate melanosomes from the keratin matrix, biotas (McNamara et al. 2012a). Host sediments at Floris- obliterating original packing arrangements (McNamara sant are exposed subaerially, but those from the other local- unpub. data). ities are located beneath the water table; sediments from Messel comprise approximately 40 per cent water (Schaal and Ziegler 1992). Variations in the extent of weathering Burial depth can also explain patterns in the fidelity of preservation of colour within an individual biota. Specimens from Eckfeld The maximum depth to which fossil insects and feathers (middle Eocene, Germany) show a statistically significant are buried during diagenesis is an important control on correlation between poor preservation of structural colours the preservation of colour. It determines the maximum and preservation in extensively weathered host sediment pressures and temperatures to which most fossils are (McNamara et al. 2012a). exposed and influences the fidelity of preservation of ana- Deep burial, exposure to diagenetic fluids, and subaer- tomical features (McNamara et al. 2012a, 2013a); it may ial or subsurface weathering may also be responsible for also influence biomolecular preservation (Hoss€ et al. certain taphonomic features in fossil feathers. Melano- 1996). Burial depth contributes to broad-scale inter-biota somes are frequently preserved as external moulds, yet the patterns in the fossil record of structural colour in insects. origin of this phenomenon is unclear. Melanin is resistant 570 PALAEONTOLOGY, VOLUME 56 to microbial and chemical attack (Goldstein et al. 2004), Striking colour patterns and glossy iridescence in vari- but heat treatment can induce chemical changes in its ous feathered dinosaurs suggest that sexual display or molecular structure, rendering the molecule soluble in defence was important in the early evolution of plumage strongly oxidizing fluids and various acids and bases (Fox and feather colour (Li et al. 2010, 2012). This is sup- 1976). Degradation of three-dimensional fossil melano- ported by variations in colour within individual penna- somes could therefore result from the effects of elevated ceous fossil feathers in Anchiornis, a basal paravian, temperatures and reactive pore fluids during diagenesis, indicating that melanin-based intrafeather patterns or from oxidative weathering during exhumation and evolved before powered flight (Li et al. 2010). Some fossil exposure. Indeed, the last of these factors is considered to feathers exhibit evidence for the involvement of melanin be an important agent of colour loss in other pigmented in nonvisual roles. Several authors have observed trends fossils (Hagdorn and Sandy 1998). in the intensity of dark tones within individual fossil feathers and related these to the degree of melanization and hence feather function. As in modern feathers (Lucas Mode of curation and Stettenheim 1972; Hill and McGraw 2006), visual tone can be pale in down feathers (McKellar et al. 2011) The mode of curation of structurally coloured fossils can and in basal regions of contour feathers (Li et al. 2010) affect also the long-term stability of the colour-producing and darkest at the distal tip of contour feathers (Fig. 3B; mechanism and the resulting hue after collection. Metallic Clarke et al. 2010; Carney et al. 2012) and in distal bar- colours in insect specimens can degrade following dehy- bules (which overlap their proximal counterparts). Such dration in air (Parker and McKenzie 2003; Schweizer increased melanization has been suggested to confer et al. 2006). Loss of colour via dehydration and microbial increased mechanical strength (Li et al. 2010; Carney degradation (Toporski et al. 2002) is usually, but not et al. 2012). Other fossil feathers exhibit dark tones in always (McNamara et al. 2012a), prevented by storing proximal regions (e.g. Fig. 3C; Wogelius et al. 2011, such specimens in liquid media, for example brine, etha- fig. 3A). Some authors have suggested that specific mela- nol or glycerine. Indeed, loss of nanostructural definition nosome geometries and configurations may affect the and visible colour can occur after only several months’ material properties of fossil feathers (Clarke et al. 2010), storage in brine (McNamara et al. 2012a). but these hypotheses are largely untested in modern material. Identification of colour-producing structures in some FUNCTIONAL AND EVOLUTIONARY fossil theropods has significant implications for our SIGNIFICANCE OF FOSSIL COLOURS understanding of the evolution of feathers. Discoveries of melanosomes in integumentary filaments of the tail of Identification of evidence of colour (and accurate recon- Sinosauropteryx (Zhang et al. 2010) refute claims that the structions of original colours) in fossils can inform on the filaments are partially decayed dermal collagen fibres function of colour, especially visual signalling mecha- (Lingham-Soliar 2003; Feduccia et al. 2005; Lingham- nisms. Iridescent metallic colours in modern insects can Soliar et al. 2007) and support interpretations of the fila- be cryptic in foliage but conspicuous in direct sunlight ments as feather homologues, that is, precursors of true and thus may function in both camouflage and sexual feathers. Although the function of colouration in such selection, especially in environments characterized by structures is still unclear, the filaments themselves are uneven dappled light, for example forest (Doucet and considered to occur in sufficient densities to have had Meadows 2009; Seago et al. 2009). Metallic colours in important nonvisual functions in thermoregulation and fossil insects may have had similar functions, particularly protection (McKellar et al. 2011). in specimens from palaeolakes surrounded by forest (e.g. Messel (Schaal and Ziegler 1992), Clarkia (Smiley 1985)) and in specimens with original green hues. Many struc- FUTURE DIRECTIONS turally coloured fossil insects exhibit blue hues; given that structural colours are blueshifted during fossilization Certain aspects of the taphonomy of colour in insects and (McNamara et al. 2013a), at least some of these blue fos- feathers are poorly understood, not least that of pigmentary sil cuticles are likely to have been originally green. Some colours in fossil insects. Some common insect pigments fossil insects preserve anatomical evidence for modifica- (e.g. carotenoids and pterins) are also abundant in plants; tion of iridescence to enhance defensive signals, that is, the degraded remains of plant-derived pigments are often camouflage and aposematism (Fig. 1E; McNamara et al. preserved in sedimentary organic matter and are the basis 2011); cryptic functions have been inferred from mono- of many studies of lake productivity (e.g. Romero-Viana tonal colour patterns (Wang et al. 2010). et al. 2009). It is therefore reasonable to hypothesize that MCNAMARA: FOSSIL COLOUR 571 evidence of some insect pigments may survive in the fossil consider factors that may contribute to alteration of record. Resolving the taphonomy of insect pigments will melanosome geometry and packing arrangement in fos- require extensive chemical analysis of fossil insect remains sils. Additional maturation experiments will constrain the and taphonomic experiments. By providing insights into range of pressure–temperature conditions capable of the relative preservation potential of different insect pig- inducing morphological change and may allow the extent ments, and into the nature of any diagnostic biomarkers of diagenetic alteration of melanosomes to be predicted. for such pigments when they decay, such experimental and The keratinous feather matrix is the basis of several col- chemical studies are likely to prove critical to our under- our-producing nanostructures, yet little is known about its standing of the origins of monotonal patterning in fossil physical taphonomy. Recent maturation experiments using insects and will test previous suggestions (Vinther et al. structurally coloured feathers revealed that decay of quasi- 2008) that such patterning reflects the distribution of eu- ordered nanostructures generates diagnostic ultrastructures melanin. (McNamara et al. 2013b). Such textures could serve as a Loss of structural colour via oxidative weathering has proxy for the former presence of quasi-photonic nano- been invoked to explain inter- and intrabiota patterns in structures in fossils. The chemical taphonomy of keratin the presence or absence of metallic colours, and even has been studied in detail in various fossil reptiles (Man- within individual specimens, but the chemical processes ning et al. 2009; Edwards et al. 2011) and, to a lesser involved are uncertain. Chemical analysis of structurally extent, in fossil birds. Immunological evidence of keratin coloured cuticles at various stages of oxidative degrada- has been reported in feathers and claw sheaths from Creta- tion could inform on this phenomenon and could also ceous theropods (Schweitzer et al. 1999a, b). Amide peaks help to explain patterns in the fidelity of preservation of in FTIR spectra of fossil feathers may derive, in part, from pigments in fossil insects and feathers. feather b-keratin (Barden et al. 2011). Keratin-chelated Cu The chemistry of melanin in fossil feathers is not fully released during decay may bind to melanin during later understood. Chemical techniques such as EPR and ToF- diagenesis, enhancing Cu concentrations in fossil feathers SIMS have proved critical to our understanding of the (Wogelius et al. 2011). Sulphur associated with fossil feath- taphonomy of melanin in fossil squid (Glass et al. 2012) ers may derive from feather keratin (Wogelius et al. 2011). and fish (Lindgren et al. 2012), but have not been applied Future chemical analyses of fossil feathers will inform on to fossil feathers. Doing so will test whether taxonomic or the taphonomy of the keratin molecule and will constrain tissue-related factors influence the chemical fidelity of the extent to which it is linked to the taphonomy of feather preservation of melanin in fossils. SRS-XRF analyses have melanin and melanosomes. yielded intriguing insights into the elemental composition of fossil fish, squid and, in particular, feathers (Wogelius et al. 2011). The ability of this technique to resolve ques- CONCLUSIONS tions regarding the preservation of melanin in fossil feathers could be tested by comparing data on the distribution Understanding the taphonomic processes that influence and abundance of various trace elements for specimens of the preservation of pigmentary and structural colour is of various taxa (including those that do not possess mela- fundamental importance to palaeobiologists interested in nin) from a single biota. the evolutionary history of colour and its functions. Fos- Other unresolved aspects of the taphonomy of colour sils with obvious colour and colour patterns, and those in feathers are also amenable to experimental testing. lacking visible colour, have the potential to retain physical Some authors have surmised that eumelanosomes and and chemical evidence of colour-generating mechanisms. phaeomelanosomes may differ in their resistance to dia- Preservation of colour is controlled by a suite of tapho- genetic alteration (Clarke et al. 2010). The relative pres- nomic factors that are, at present, not fully resolved; key ervation potential of the different melanosome types factors identified to date include the depth of burial and could be investigated via conventional decay- and matu- the extent of hydrothermal alteration and weathering. ration experiments; decay experiments could also assess Additional taphonomic data from fossils and from whether autolytic and microbial decay processes affect controlled laboratory experiments are critical in unravel- melanosome geometry. Morphological and chemical anal- ling the taphonomic history of colour in different taxa, yses of degraded feather tissues could inform on the depositional environments and diagenetic regimes. This taphonomic processes that influence the preservation of will inform interpretations of original colour in fossils melanosomes as external moulds; such studies could also and of the role of colour in visual signalling through help resolve the nature of melanin (and its derivatives), time. and the chromophore responsible for visual dark colouration, in feathers preserving mouldic melanosomes. Acknowledgements. My research on the taphonomy of colour in Future studies of melanosome taphonomy should also fossils was funded by an Irish Research Council – Marie Curie 572 PALAEONTOLOGY, VOLUME 56

International Mobility Fellowship. I thank Derek Briggs and Pat- VINTHER, J., DEVRIES, T. J. and BABY, P. 2010. Fossil rick Orr for their advice, collaboration and many fruitful discus- evidence for evolution of the shape and color of penguin sions of taphonomy. I also thank Mike Benton, Hui Cao, Daniel feathers. Science, 330, 954–957. Field, Neal Gupta, Stuart Kearns, Emma Locatelli, Laura Meyer, CESARINI, J. P. and INSERM 1996. Melanins and their pos- Heeso Noh, Lin Qiu, Sonja Wedmann and Hong Yang for their sible roles through biological evolution. Advances in Space significant contributions to published and ongoing collaborative Research, 18,35–40. studies. I am grateful to Gunter€ Bechly, Susan Butts, Thomas CROMARTIE, R. I. T. 1959. Insect pigments. Annual Review Engel, Larry Gall, David Grimaldi, Kristof Kristoffersen, Herbert of Entomology, 4,59–76. Lutz, Leonard Munsterman, Markus Poschmann, Michael Ras- DAVIS, P. G. and BRIGGS, D. E. G. 1995. Fossilization of ser, Greg Watkins-Colwell and Michael Wuttke for access to fos- feathers. Geology, 23, 783–786. sil and extant specimens, and to Daniel Field, Zhenting Jiang, DOUCET, S. M. and MEADOWS, M. G. 2009. Iridescence: Robert Patalano, Barry Piekos, Vinod Saranathan, Elizabeth a functional perspective. Journal of the Royal Society Interface, Savrann, Jess Utrup, Robert Young and Shuang Zhang for assis- 6, S115–S132. tance with laboratory techniques. Thanks also to Antonia -SHAWKEY, M. D., HILL, G. E. and MONTGOM- Monteiro, Paul Nash, Jeffrey Oliver, Rick Prum, Jakob Vinther ERIE, R. 2006. Iridescent plumage in satin bowerbirds: struc- and the members of the G&G Paleo group and the staff of the ture, mechanisms and nanostructural predictors of individual Peabody Museum Entomology Division for their insights into variation in colour. Journal of Experimental Biology, 209, 380– taphonomy, evolution and the colours of extant organisms. 390. EDWARDS, N. P., BARDEN, H. E., VAN DONGEN, B. Editor. Patrick Orr E., MANNING, P. L., LARSON, P. L., BERGMANN, U., SELLERS, W. I. and WOGELIUS, R. A. 2011. Infrared mapping resolves soft tissue preservation in 50 million year- REFERENCES old reptile skin. Proceedings of the Royal Society B, 278, 3209– 3218. ADACHI, E. 2007. Unexpected variability of millennium FARRANT, P. A. 1997. Color in nature: a visual and scientific green: structural color of Japanese jewel beetle resulted from exploration. Blandford Press, London, 208 pp. thermosensitive porous organic multilayer. Journal of Morphol- FEDUCCIA, A., LINGHAM-SOLIAR, T. and HINCH- ogy, 268, 826–829. LIFFE, J. R. 2005. Do feathered dinosaurs exist? Testing the ANDERSEN, S. O. 2010. Insect cuticular sclerotization: a hypothesis on neontological and paleontological evidence. review. Insect Biochemistry and Molecular Biology, 40, 166–178. Journal of Morphology, 266, 125–166. BARDEN, H. E., WOGELIUS, R. A., LI, D., MANNING, FOX, D. L. 1976. Animal biochromes and structural colours, Sec- P. L., EDWARDS, N. P. and VAN DONGEN, B. E. 2011. ond edition. University of California Press, Berkeley and Los Morphological and geochemical evidence of eumelanin preser- Angeles, California, 450 pp. vation in the feathers of the Early Cretaceous bird, Gansus yu- GHIRADELLA, H. 1998. Hairs, bristles, and scales. 637–645. menensis. PLoS One, 6, e25494. In LOCKE, M. (ed.). Microscopic anatomy of invertebrates, BERGMANN, U., MORTON, R. W., MANNING, P. L., Vol. 11A: Insecta. Wiley-Liss, New York, 496 pp. SELLERS, W. I., FARRAR, S., HUNTLEY, K. G., -2009. Coloration. 213–220. In RESH, V. H. and CARDE, WOGELIUS, R. A. and LARSON, P. 2010. Archaeopteryx R. T. (eds). Encyclopedia of insects, Second edition. Elsevier, feathers and bone chemistry fully revealed via synchrotron New York, 1024 pp. imaging. Proceedings of the National Academy of Sciences, 107, GLASS, K., ITO, S., WILBY, P. R., SOTAD, T., NAKAM- 9060–9065. URAD, A., BOWERS, C. R., VINTHER, J., DUTTAG, BLODGETT, R. B., BOUCOT, A. J. and FERRILL, B. A. S., SUMMONS, R., BRIGGS, D. E. G., WAKAMATSU, 1983. A color-banded Beachia (Brachiopoda; Terebratulida) K. and SIMON, J. D. 2012. Direct chemical evidence for eu- from the Oriskany equivalent (mid-Early Devonian) of central melanin pigment from the Jurassic period. Proceedings of the Alabama. Journal of Paleontology, 57, 865–869. National Academy of Sciences, 109, 10218–10223. BOKONY, V., LIKER, A., SZEKELY, T. and KIS, J. 2003. GOLDSTEIN, G., FLORY, K. R., BROWNE, B. A., MAJ- Melanin-based plumage coloration and flight displays in plo- ID, S., ICHIDA, J. M. and BURTT, E. H. 2004. Bacterial vers and allies. Proceedings of the Royal Society of London B: degradation of black and white feathers. Auk, 121, 656–659. Biological Sciences, 270, 2491–2497. GRIMALDI, D. and ENGEL, M. S. 2005. Evolution of the BUTLER, M. J., GARDINER, R. B. and DAY, A. W. 2005. insects. Cambridge University Press, Cambridge, 755 pp. Fungal melanin detection by the use of copper sulfide-silver. GUNDERSON, A. R., FRAME, A. M., SWADDLE, J. P. Mycologia, 97, 312–319. and FORSYTH, M. H. 2008. Resistance of melanised feath- CARNEY, R. M., VINTHER, J., SHAWKEY, M. D., ers to bacterial degradation: is it really so black and white? D’ ALBA, L. and ACKERMANN, J. 2012. New evidence Journal of Avian Biology, 39, 539–545. on the colour and nature of the isolated Archaeopteryx feather. HAGDORN, H. and SANDY, M. R. 1998. Color banding in Nature Communications, 3, 637–643. the Triassic terebratulid brachiopod Coenothyris from the Mu- CLARKE, J. A., KSEPKA, D. T., SALAS-GISMONDI, R., schelkalk of Central Europe. Journal of Paleontology, 72,11– ALTAMIRANO, A. J., SHAWKEY, M. D., D’ ALBA, L., 27. MCNAMARA: FOSSIL COLOUR 573

HEADS, S., MARTILL, D. M. and LOVERIDGE, R. 2005. LI, Q., GAO, K.-Q., VINTHER, J., SHAWKEY, M. D., An exceptionally preserved antlion (Insecta: Neuroptera) with CLARKE, J. A., D’ ALBA, L., MENG, Q., BRIGGS, colour pattern preservation from the Cretaceous of Brazil. Pal- D. E. G. and PRUM, R. O. 2010. Plumage color patterns of aeontology, 48, 1409–1417. an extinct dinosaur. Science, 327, 1369–1372. HILL, G. E. and MCGRAW, K. J. 2006. Bird coloration. vol. -- MENG, Q., CLARKE, J. A., SHAWKEY, M. D., 1: Mechanisms and measurements. Harvard University Press, D’ ALBA, L., PEI, R., ELLISON, M., NORELL, M. A. Cambridge, MA, 589 pp. and VINTHER, J. 2012. Reconstruction of Microraptor and HINTON, H. 1973. Natural deception. 97–159. In GREG- the evolution of iridescent plumage. Science, 335, 1215–1219. ORY, R. L. and GOMBRICH, E. H. (eds). Illusion in nat- LINDGREN, J., UVDAL, P., SJOVALL,€ P., NILSSON, ure and art. Duckworth, London, 288 pp. D. E., ENGDAHL, A., SCHULTZ, B. P. and THIEL, V. HITCHCOCK, A. P., DYNES, J. J., LAWRENCE, J. R., 2012. Molecular preservation of the pigment melanin in fossil OBST, M., SWERHONE, G. D. W., KORBER, D. R. and melanosomes. Nature Communications, 3, 824–831. LEPPARD, G. G. 2009. Soft X-ray spectromicroscopy of LINGHAM-SOLIAR, T. 2003. The dinosaurian origin of nickel sorption in a natural river biofilm. Geobiology, 7, feathers: perspectives from dolphin (Cetacea) collagen fibres. 432–453. Naturwissenschaften, 90, 563–567. HOFMANN, C. M., MCGRAW, K. J., CRONIN, T. W. -2011. The evolution of the feather: Sinosauropteryx, a col- and OMLAND, K. E. 2007. Melanin coloration in New orful tail. Journal of Ornithology, 152, 567–577. World orioles I: carotenoid masking and pigment dichroma- -and PLODOWSKI G. 2010. The integument of Psittaco- tism in the orchard oriole complex. Journal of Avian Biology, saurus from Liaoning Province, China: taphonomy, epidermal 38, 163–171. patterns and color of a ceratopsian dinosaur. Naturwissens- HOLLINGWORTH, N. T. J. and BARKER, M. J. 1991. chaften, 97, 479–486. Colour pattern preservation in the fossil record: taphonomy -FEDUCCIA, A. and WANG, X. 2007. A new Chinese and diagenetic significance. 105–119. In DONOVAN, S. K. specimen indicates that ‘protofeathers’ in the early Cretaceous (ed.). The processes of fossilization. Columbia University Press, theropod dinosaur Sinosauropteryx are degraded collagen fibres. New York, NJ, 303 pp. Proceedings of the Royal Society of London B, 274, 1823–1829. HOSS,€ M., DILLING, A., CURRANT, A. and PA€ ABO,€ S. LIU, Y. and SIMON, J. D. 2003. Isolation and biophysical 1996. Molecular phylogeny of the extinct ground sloth Myl- studies of natural eumelanins: applications of imaging tech- odon darwinii. Proceedings of the National Academy of Sciences, nologies and ultrafast spectroscopy. Pigment Cell Research, 16, 93, 181–185. 606–618. INGRAM, A. L. and PARKER, A. R. 2008. A review of the - HONG, L., WAKAMATSU, K., ITO, S., ADH- diversity and evolution of photonic structures in butterflies, YARU, B., CHENG, C.-Y., BOWERS, C. R. and incorporating the work of John Huxley (The Natural History SIMON, J. D. 2005. Comparison of structural and chemical Museum, London from 1961 to 1990). Philosophical Transac- properties of black and red human hair melanosomes. Photo- tions of the Royal Society B, 363, 2465–2480. chemistry and Photobiology, 81, 135–144. KINOSHITA, S. and YOSHIOKA, S. 2005. Structural colors LUCAS, A. M. and STETTENHEIM, P. R. 1972. Avian in biological systems: principles and applications. Osaka Univer- anatomy: integument. Agriculture handbook 362, US Depart- sity Press, Osaka, 351 pp. ment of Agriculture, Washington, DC, 750 pp. KLUG, C., SCHULZ, H. and DE BAETS, K. 2009. Red LUTZ, H. 1990. Systematische und paleokologische€ Untersuch- Devonian trilobites with green eyes from Morocco and the ungen an Insekten aus dem Mittel-Eoz€an der Grube Messel bei silicification of the trilobite exoskeleton. Acta Palaeontologica Darmstadt. Courier Forschungsinstitut Senckenberg, 124,1–165. Polonica, 54, 117–123. MACLEOD, H. A. 1969. Thin film optical filters. Adam Hilger, KNIGHT, T. K., BINGHAM, S., LEWIS, R. D. and SAV- London, 519 pp. RDA, C. E. 2011. Feathers of the Ingersoll Shale, Eutaw For- MANNING, P. L., MORRIS, P. M., MCMAHON, A., mation (Upper Cretaceous), Eastern Alabama: the largest JONES, E., GIZE, A., MACQUAKER, J. H. S., WOLFF, collection of feathers from North American Mesozoic Rocks. G., THOMPSON, A., MARSHALL, J., TAYLOR, K. G., Palaios, 26, 364–376. LYSON, T., GASKELL, S., REAMTONG, O., SELL- KURACHI, M., TAKAKU, Y., KOMIYA, Y. and HARIY- ERS, W. I., VAN DONGEN, B., BUCKLEY, M. and AMA, T. 2002. The origin of extensive colour polymorphism WOGELIUS, R. 2009. Mineralized soft-tissue structure and in Plateumaris sericea (Chrysomelidae, Coleoptera). Naturwis- chemistry in a mummified hadrosaur from the Hell Creek senschaften, 89, 295–298. Formation, North Dakota (USA). Proceedings of the Royal LABANDEIRA, C. 2005. Recent and exciting developments in Society B: Biological Sciences, 276, 3429–3437. understanding fossil insects and their terrestrial relatives. MARKS, M. S. and SEABRA, M. C. 2001. The melanosome: American Paleontologist, 13,8–11. membrane dynamics in black and white. National Review of LAND, M. F. 1972. The physics and biology of animal Molecular and Cellular Biology, 2, 738–748. reflectors. Progress in Biophysical and Molecular Biology, 24, MASON, C. W. 1927. Structural colors in insects. II. Journal of 75–106. Physical Chemistry, 31, 321–354. -1997. Visual acuity in insects. Annual Review of Entomol- MCGRAW, K. 2003. Melanins, metals, and mate quality. Oi- ogy, 42, 147–177. kos, 102, 402–406. 574 PALAEONTOLOGY, VOLUME 56

-2006. Mechanics of melanin-based coloration. 243–294. In contrasting examples. Journal of Experimental Biology, 201, HILL, G. E. and MCGRAW, K. J. (eds). Bird coloration: 1307–1313. Vol. 1: mechanisms and measurements. Harvard University -HEGEDUS, Z. and WATTS, R. A. 1998b. Solar-absorb- Press, Cambridge, MA, 589 pp. er antireflector on the eye of an Eocene fly (45 Ma). Proceed- MCKELLAR, R. C., CHATTERTON, B. D. E., WOLFE, ings of the Royal Society B, 265, 811–815. A. P. and CURRIE, P. J. 2011. A diverse assemblage of Late - MCPHEDRAN, R. C., MCKENZIE, D. R., BOT- Cretaceous dinosaur and bird feathers from Canadian amber. TEN, L. C. and NICOROVICI, N.-A. P. 2001. Aphrodite’s Science, 333, 1619–1622. iridescence. Nature, 409,36–37. MCNAMARA, M. E., BRIGGS, D. E. G., ORR, P. J., POWELL, J. A. 2003. Lepidoptera (Moths, Butterflies). 631– WEDMANN, S., NOH, H. and CAO, H. 2011. Fossilized 663. In RESH, V. H. and CARDE, R. T. (eds). Encyclopedia biophotonic nanostructures reveal the original colors of 47- of insects. Academic Press, Burlington, MA, 1024 pp. million-year-old moths. PLoS Biology, 9, e1001200. PRUM, R. O. 2006. Anatomy, physics, and evolution of struc- --- 2012a. The controls on the preservation of tural colors. 295–353. In HILL,G.E.andMCGRAW,K.J. structural color in fossil insects. Palaios 27, 443–454. (eds). Bird coloration. Vol 1: mechanisms and measurements. --- NOH, H. and CAO, H. 2012b. The original Harvard University Press, Cambridge, MA, 589 pp. colours of fossil beetles. Proceedings of the Royal Society B, -and TORRES R. H. 2003. A Fourier tool for the analysis 279, 1114–1121. of coherent light scattering by bio-optical nanostructures. Inte- --- GUPTA, N. S., LOCATELLI, E. R., QIU, grative and Comparative Biology, 43, 591–602. L., YANG, H., WANG, Z., NOH, H. and CAO, H. 2013a. RASNITSYN, A. P. and QUICKE, D. L. J. 2002.History of The fossil record of insect color illuminated by maturation insects. Kluwer Academic Publishers, Dordrecht, 517 pp. experiments. Geology, published online 20 February 2013. doi: RILEY, P. A. 1997. Melanin. International Journal of Biochemis- 10.1130/G33836.1. try and Cell Biology, 29, 1235–1239. --- FIELD, D. and WANG, Z. 2013b. Experi- ROMERO-VIANA, L., KEELY, B. J., CAMACHO, A., mental maturation of feathers: implications for reconstructions VICENTE, E. and MIRACLE, M. R. 2009. Photoautotro- of fossil feather colour. Biology Letters, 9, published online phic community changes in Lagunillo del Tejo (Spain) in March 2013. doi: 10.1098/rsbl.2013.0184. response to lake level fluctuation: two centuries of sedimentary NAPPI, A. J. and CHRISTENSEN, B. M. 2005. Melanogen- pigment records. Organic Geochemistry, 40, 376–386. esis and associated cytotoxic reactions: applications to insect SCHAAL, S. and ZIEGLER, W. 1992. Messel: an insight into innate immunity. Insect Biochemistry and Molecular Biology, the history of life and of the Earth. Clarendon Press, Oxford, 35, 443–459. 328 pp. NEVILLE, A. C. 1975. Biology of the arthropod cuticle. SCHULTZ, T. D. and RANKIN, M. A. 1985. The ultrastruc- Springer, New York, 458 pp. ture of the epicuticular interference reflectors of tiger beetles -and CAVENEY S. 1969. Scarabaeid beetle exocuticle as (Cicindela). Journal of Experimental Biology, 117,87–110. an optical analogue of cholesteric liquid crystals. Biological SCHWEITZER, M. H. 2011. Soft tissue preservation in terres- Reviews, 44, 531–562. trial Mesozoic vertebrates. Annual Reviews of Earth and Plane- NOH, H., LIEW, S. F., SARANATHAN, V., MOCHRIE, tary Sciences, 39, 187–216. S. G. J., PRUM, R. O., DUFRESNE, E. R. and CAO, H. -WATT, J. A., AVCI, R., FORSTER, C. A., KRAUSE, 2010. How noniridescent colors are generated by quasi- D. W., KNAPP, L., ROGERS, R. R., BEECH, I. and ordered structures of bird feathers. Advanced Materials, 22, MARSHALL, M. 1999a. Keratin immunoreactivity in the 2871–2880. Late Cretaceous bird Rahonavis ostromi. Journal of Vertebrate NORELL, M. A. 2011. Fossilized feathers. Science, 333, 1590– Paleontology, 19, 712–722. 1591. --- KNAPP, L., CHIAPPE, L., NORELL, M. NOYES, J. A., VUKUSIC, P. and HOOPER, I. R. 2007. and MARSHALL, M. 1999b. Beta-keratin specific immuno- Experimental method for reliably establishing the refractive logical reactivity in feather-like structures of the Cretaceous index of buprestid beetle exocuticle. Optics Express, 15, 4351– alvarezsaurid, Shuvuuia deserti. Journal of Experimental Zool- 4358. ogy, 285, 146–157. PARKER, A. R. 1998. Colour in Burgess Shale animals and the SCHWEIZER, M. K., WOOLLER, M. J., TOPORSKI, J., effect of light on evolution in the Cambrian. Proceedings of the FOGEL, M. L. and STEELE, A. 2006. Examination of an Oli- Royal Society B, 265, 965–971. gocene lacustrine ecosystem using C and N stable isotopes. Pal- -2000. 515 Million years of structural colour. Journal of aeogeography, Palaeoclimatology, Palaeoecology, 230, 335–351. Optics A: Pure and Applied Optics, 2, R15–R28. SEAGO, A. E., BRADY, P., VIGNERON, J.-P. and -2002. Natural photonic engineers. Materials Today, 5,26–31. SCHULTZ, T. D. 2009. Gold bugs and beyond: a review of -and MCKENZIE D. R. 2003. The cause of 50 million- iridescence and structural colour mechanisms in beetles (Cole- year-old colour. Biology Letters, 270, S151–S153. optera). Journal of the Royal Society Interface, 6, S165–S184. -and TOWNLEY H. E. 2007. Biomimetics of photonic SHAWKEY, M. D. and HILL, G. E. 2006. Significance of a nanostructures. Nature Nanotechnology, 2, 347–353. basal melanin layer to production of non-iridescent structural -MCKENZIE, D. R. and LARGE, M. C. J. 1998a. Multi- plumage color: evidence from an amelanotic Steller’s jay (Cya- layer reflectors in animals using green and gold beetles as nocitta stelleri). Journal of Experimental Biology, 209, 1245–1250. MCNAMARA: FOSSIL COLOUR 575

-ESTES, A. M., SIEFFERMAN, L. M. and HILL, G. E. VINTHER, J., BRIGGS, D. E. G., PRUM, R. O. and 2003. Nanostructure predicts intraspecific variation in ultravi- SARANATHAN, V. 2008. The colour of fossil feathers. olet-blue plumage colour. Proceedings of the Royal Society B, Biology Letters, 4, 522–525. 270, 1455–1460. -- CLARKE, J., MAYR, G. and PRUM, R. O. 2010. -HAUBER, M. E., ESTEP, L. K. and HILL, G. E. 2006. Structural coloration in a fossil feather. Biology Letters, 6, 128– Evolutionary transitions and mechanisms of matte and irides- 131. cent plumage coloration in grackles and allies (Icteridae). VONDRAN, T., APEL, K. H. and SCHMITZ, H. 1995. Journal of the Royal Society Interface, 3, 777–786. The infrared receptor of Melanophila acuminata De Geer -SARANATHAN, V., PALSDOTTIR, H., CRUM, J., (Coleoptera: Buprestidae): ultrastructural study of a unique ELLISMAN, M., AUER, M. and PRUM, R. O. 2009. insect thermoreceptor and its possible descent from a hair Electron tomography, three-dimensional Fourier analysis and mechanoreceptor. Tissue and Cell, 27, 645–658. colour prediction of a three-dimensional amorphous biopho- VUKUSIC, P. 2003. Natural coatings. 1–34. In KAISER, N. tonic nanostructure. Journal of the Royal Society Interface, 6, and PULKER, H. (eds). Optical interference coatings. S213–S220. Springer, Berlin, 500 pp. SHAWKEY, M., MAIA, R. and D’ ALBA, L. 2011. Proxi- -and SAMBLES J. R. 2003. Photonic structures in biology. mate bases of silver colour in anhinga (Anhinga anhinga) Nature, 424, 852–855. feathers. Journal of Morphology, 272, 1399–1407. WANG, Y., LIU, Z., WANG, X., SHIH, C., ZHAO, Y., SHI, Y. and YOKOYAMA, S. 2003. Molecular analysis of the ENGEL, M. S. and REN, D. 2010. Ancient pinnate leaf evolutionary significance of ultraviolet vision in vertebrates. mimesis among lacewings. Proceedings of the National Acad- Proceedings of the National Academy of Sciences, 100, 8308– emy of Sciences, 107, 16212–16215. 8313. WEDMANN, S., POSCHMANN, M. and HORNSCHE-€ SHOCK, E. L. and KORETSKY, C. M. 1993. Metal-organic MEYER, T. 2010. Fossil insects from the Late Oligocene complexes in geochemical processes: calculation of standard Enspel Lagerst€atte and their palaeobiogeographic and palaeo- partial molal thermodynamic properties of aqueous acetate climatic significance. Palaeobiology and Palaeoenvironments, complexes at high pressures and temperatures. Geochimica et 90,49–58. Cosmochimica Acta, 57, 4899–4922. WILTS, B. D., LEERTOUWER, H. L. and STAVENGA, SMILEY, J. 1985. Late Cenozoic history of the Pacific northwest. D. G. 2009. Imaging scatterometry and microspectropho- American Association for the Advancement of Science, San tometry of lycaenid butterfly wing scales with perforated Francisco, 417 pp. multilayers. Journal of the Royal Society Interface, 6, S185– STODDARD, M. C. and PRUM, R. O. 2011. How colorful S192. are birds? Evolution of the avian plumage color gamut. WOGELIUS, R. A., MANNING, P. L., BARDEN, H. E., Behavioural Ecology, 22, 1042–1052. EDWARDS, N. P., WEBB, S. M., SELLERS, W. I., TANAKA, G., PARKER, A. R., SIVETER, D. J., MAEDA, TAYLOR, K. G., LARSON, P. L., DODSON, P., YOU, H. and FURUTANI, M. 2009. An exceptionally well-pre- H., DA-KING, L. and BERGMANN, U. 2011. Trace met- served Eocene dolichopodid fly eye: function and evolutionary als as biomarkers for eumelanin pigment in the fossil record. significance. Proceedings of the Royal Society of London B, 276, Science, 333, 1622–1626. 1015–1019. WUTTKE, M. 1983. ‘Weichteil-Erhaltung’ durch lithifizierte -TANIGUCHI, H., MAEDA, H. and NOMURA, S. Mikroorganismen bei mittel-eoz€anen Vetebraten aus den 2010. Original structural colour preserved in an ancient leaf Olschiefern€ der ‘Grube Messel’ bei Darmstadt. Senckenbergiana beetle. Geology, 38, 127–130. Lethaea, 64, 509–527. TILLEY, R. J. D. and ELIOT, J. N. 2002. Scale microstructure YIN, H., SHI, L., SHA, J., LI, Y., QIN, Y., DONG, B., and its phylogenetic implications in lycaenid butterflies (Lepi- MEYER, S., LIU, X., ZHAO, L. and ZI, J. 2006. Irides- doptera, Lycaenidae). Transactions of the Lepidopteran Society cence in the neck feathers of domestic pigeons. Physical of Japan, 53, 153–180. Review E, 74, 051916. TOPORSKI, J. K. W., STEELE, A., WESTALL, F., AVCI, YOSHIOKA, S., NAKAMURA, E. and KINOSHITA, S. R., MARTILL, D. M. and MCKAY, D. S. 2002. Morpho- 2007. Origin of two-color iridescence in rock dove’s feather. logic and spectral investigation of exceptionally well preserved Journal of the Physical Society of Japan, 76, 013801 1–4. bacterial biofilms from the Oligocene Enspel formation, Ger- ZHANG, F., KEARNS, S. L., ORR, P. J., BENTON, M. J., many. Geochimica et Cosmochimica Acta, 66, 1773–1791. ZHOU, Z., JOHNSON, D., XU, X. and WANG, X. TUREK, V. 2009. Colour patterns in Early Devonian cephalo- 2010. Fossilized melanosomes and the colour of Cretaceous pods from the Barrandian area: taphonomy and taxonomy. dinosaurs and birds. Nature, 463, 1075–1078. Acta Palaeontologica Polonica, 54, 491–502.