Considerations in the Conservation of Feathers

Considerations in the Conservation of Feathers and Hair, Particularly their Pigments Jocelyn Hudon

Abstract

Introduction

Feathers are amongst the most complex epidermal derivatives found in vertebrates. They have complex branched structures, grow from their bases by a unique mechanism, and come in a wide variety of sizes, shapes, structures, and colours. Not only do feathers impart cover, insulation, waterproofing of the body, contribute to flight, tactile sensations or protection of sensory organs, even storing water, they are also involved in myriad aspects of communication and display in birds, and characteristically rather ornately. Underlying this diversity of colours and patterns found in birds is a variety of pigments (melanins, carotenoids, psittacofulvins, porphyrins, etc.), pigment-bearing structures and molecules, and complex micro- and macrostructures. Given the great structural and functional diversity of feathers it should come as no surprise that their conservation should require a multifaceted approach. Accordingly, a brief review of feather anatomy, including the arrangement of feathers on the skin (pterylosis), chemical composition, even the native fauna of feathers (e.g., lice, mites, bacteria)will be provided, emphasizing aspects of feathers that may be of relevance to conservators. Since cleaning methods are well covered by other speakers, my focus will be on the preventive conservation of feather and fur colour from light. I will show how even pigment systems that seem biochemically homogenous—like the melanins of mammals—show surprisingly complex and species-specific responses to light. For example, in pilot fading experiments, mink, but not marten, fur darkened initially upon exposure to light. Attempts to quench free radicals likely generated by light irradiation did not appear to slow fading down.

Feathers are among the most complex integumentary appendages found in any vertebrate (Lucas and Stettenheim, 1972). They have complex branched structures, grow from their bases by a unique mechanism (Prum and Brush, 2002), and come in an astonishing variety of shapes, sizes, structures, and colours. Feather follicles can alternatively form feathers of different types in each skin area in an arrangement that is precisely determined to form a coherent plumage that conveys information about the bearer’s species, age, sex, and, sometimes, even condition. From their humble origins as structures that probably functioned in defence, thermal insulation or water repellency (Prum and Brush, 2002), feathers diversified into structures that provided cover, permitted active flight, carried tactile sensation, protected sensory organs, produced sound, and, even, stored water. More importantly, feathers became highly patterned and ornate, involved in myriad aspects of display and communication in birds, a highly visual group of vertebrates. Perhaps not surprisingly, feathers have been repeatedly borrowed as ornaments by another highly visual species, Homo sapiens, in countless cultural settings and periods, at times incorporated into headdresses, diadems, cloaks, capes, wristbands, earrings, and sceptres, even European fashion, notably millinery. Feathers have also been used in the fletching of arrows, bedding, ornamentation in millinery, as quill pens, powderpuffs, even the making of artificial flies for fishing. Feathers still attached to skin, like whole birds, whole skins and parts of skins and bird’s bodies, are also represented in various collections (Rae and Wills, 2002). However, the use of bird skins for practical purposes is less common, being strongest in cultures that were more reliant on birds for their survival, like people of the Arctic, where the skins of fur trade legacy workshop

127

marine birds were used to make parkas, overslippers, stockings, bonnets and bags (Oakes and Riewe, 1996). In those instances where mammalian skins were available, they were usually preferred as more durable (Rae and Wills, 2002). For an exposition on the conservation of feathered skins, as opposed to the feathers themselves, the reader is referred to Rae and Wills (2002). Feathered skins are also of course widespread in natural history collections. Although, in a museum context, attack by insects, deposition of dust and soiling, and poor storage conditions are the most damaging to artifacts incorporating feathers, these topics are largely covered by other speakers. My focus here will be to provide information on the “natural history” of feathers and on the effect of light of these brightly-coloured integumentary derivatives.

Feather Composition Like the epidermal appendages of other amniotes (reptiles, birds and mammals), feathers are composed mostly of keratin(s), an intermediate filament protein produced by epidermal cells that forms a hard, flexible, and insoluble polymer (Brush, 1978a). Unlike the α-keratins of the epidermis and the hairs of mammals, which naturally form α-helices, the keratins of feathers, scutate scales, claws and beak, rather adopt a beta-pleated sheet structure, where hydrogen bonds are formed between adjacent parallel or antiparallel polypeptide strands, yielding a markedly different high angle X-ray diffraction pattern (Brush, 1978a). The feathers, scutate scales, claws and beak of birds (and a few reptiles) are composed of a subclass of β-keratins that are referred to as feather keratins, or φ-keratins (Brush, 1978a). The keratins of feathers are polypeptides of about 100 amino acid residues (Presland et al., 1989a, 1989b; Takahashi et al., 2003), with a molecular weight of approximately 10.4 kD [one Dalton (D) is the mass of an atom of hydrogen]. Avian scutate scales, beak, and claw are composed of another subclass of filament-

128

cac / accr 31 st annual conference, jasper 2005

forming φ-keratins that are slightly larger (13.4 kD). The α-keratins are comparatively much larger at about 56.5 to 60 kD. Feather keratins are relatively high in glycine, serine, proline, leucine, and glutamic acid. Acidic amino acids exceed the basis residues, and the overall pattern differs quantitatively from other fibrous proteins (Brush, 1978a). When compared to mammalian hair keratins, feathers have relatively lower methionine and lysine and a higher proline content (Brush, 1978a). Feather keratins are produced by several families of closely related genes, occurring as tandem repeats throughout the bird genome. It has been estimated that there may be as many as 100-240 φ-keratin genes in the chick genome alone (Kemp, 1975). The flexural stiffness of the rachis does not appear to be controlled by the material properties of feather keratins, but rather by their crosssectional morphology (Bonser and Purslow, 1995). The X-ray diffraction pattern of the intact feather calamus indicates a high degree of crystallinity which can be deformed by stretching and is affected by heating in water or aqueous butanol (Brush, 1978a). Crooks in feathers can usually be removed with a stream of water vapour (steam). Much of the following information about types, structures and arrangement of feathers—including several illustrations—is taken from Lucas and Stettenheim (1972).

Pterylosis In most birds, but excluding ratite birds (kiwis, cassowaries, emu, rheas, and ostrich) and penguins, feathers are not distributed uniformly over a bird’s body, but rather segregated into tracts or groups, interspersed with featherless spaces over the body (Fig. 1). The areas covered by contour feathers, which are visible on the external surface of the plumage, are called pterylae (Fig. 1). The areas of the skin without feathers, or with only down or semiplume feathers, are called apteria.

Pterylography, or more commonly pterylosis, describes the pattern of feather tracts (or feather follicles) in birds, while ptilosis is used to describe the plumage associated with these follicles.

Moult From the time a bird hatches until it becomes an adult, its feathering passes through several changes in appearance. These changes are due largely to a periodic replacement of feathers. In most birds, the shape of each feather is established during its growth and does not change thereafter except through wear. All feathers of fully-grown birds are replaced at least once annually by moulting, in a stereotypical manner and following a rather strict schedule of feather replacement, which may vary from species to species, even populations of a single species. The single generation of feathers that is brought in by each moult is known as a plumage. Feathers may change in appearance as they are replaced as a function of the bird’s age, gender, and seasonal changes. In birds of temperate locales, feathers grown in the Fall (the Basic plumage) may differ markedly from those grown in the Spring (the Alternate plumage) just before the breeding season. The quantity and quality of nutrition and other factors affecting the health of a bird can affect the appearance of growing feathers, especially the flight feathers. Malnutrition, for example, may result in the presence of a series of V-shaped grooves across the vane. These grooves are caused by the poor development of the barbules and are known as growth bars (Pyle, 1997).

Feather Structure Figure 1. Pterylosis of a male Single Comb White Leghorn Chicken. From Lucas and Stettenheim, 1972.

The main parts of a body contour feather, which form the outer cover of feathers, are the shaft, the plates or vanes on either side of it and, in most birds, an aftershaft on the undersurface (Fig. 2).

fur trade legacy workshop

129

The shaft (or quill) is the longitudinal axis, and it is composed of two segments, the barb-less calamus and the rachis. The calamus (or barrel) is the short, unpigmented tubular base, largely implanted into the feather follicle. It is approximately circular in cross-section and often tapered toward the end. The rachis is the long, essentially solid portion of the shaft above the skin. On each side of the shaft is a set of closely knit, fine branches that are known individually as barbs and collectively as a vane. Proximally (closest to the body) each vane is fluffy, while distally (away from the body) it is firm and flat. The shaft serves as the scaffold, while the vanes provide the surface for an airfoil or for covering and insulating the body. The aftershaft is a structure attached to the underside of a feather at the base of the feather, including featherlike structures composed of an axis with barbs on each side.

Figure 2. Main parts of a typical contour feather, exemplified by a feather from the middle of the dorsal tract of a Single Comb White Leghorn Chicken. From Lucas and Stettenheim, 1972.

130


Vane The vane provides the surface for an airfoil or for covering and insulating the body. It consists of barbs (Fig. 2). The vane of contour feathers varies in texture from base to tip as a function of the structure of the barbs (and function of the feather). The proximal portion of the vanes has a soft, loose, fluffy texture designated as plumulaceous or downy. This portion, concealed by other feathers, gives a feather its property of insulation. The remaining portion of the vanes has firm, compact, closely knit texture designated pennaceous. It is a thin sheet of barbs that covers the body, and gives the feather its airfoil. The proportion of downy and pennaceous texture varies and is one of the criteria for defining certain types of feathers. Remiges and rectrices have entirely pennaceous vanes, whereas semiplumes are entirely plumulaceous. Barbs do not attach to opposite sides of the shaft at exactly the same level, yet the total number of barbs is very nearly equal in both vanes. The bare primary branch of barbs is called the ramus, the term barb being reserved for the ramus and its vanules, the barbules on one side of a barb.

Figure 3 (above). Plumulaceous barbules of a Common Pigeon. From Lucas and Stettenheim, 1972. Figure 4 (right). Pennaceous barbules from the middle of a secondary remix of a Single Comb White Leghorn Chicken. Both have been turned on their long axes so that they can be shown in side view. From Lucas and Stettenheim, 1972. Figure 5 (below). Segments of two pennaceous barbs from a contour feather of a Single Comb White Leghorn Chicken, showing the interlocking mechanism. The barbs are seen obliquely from the distal end to show interlocking of parts. From Lucas and Stettenheim, 1972.


131

The ramus has the shape of a somewhat compressed filament that tapers in height from base to tip. The branches of a barb are the barbules, also known as radii. Plumulaceous barbules are characterized by a relatively short, straplike base and long, slender pennulum (Fig. 3). In spite of their simplicity, plumulaceous barbules have distinctive characteristics in many orders or birds, even lower taxonomic groups of birds, and are very useful to identify feathers. Because plumulaceous barbules are less variable than those on the pennaceous portion of a vane (particularly the barbules on the inner portion of the distal vanule of the basal barbs), they are very useful to identify isolated feathers. Identification keys have been produced based strictly on the characteristics of plumulaceous barbules [see Chandler (1916) and Day (1966)]. The dimensions of a feather (length, width, calamus length, downy part, aftershaft length) as well as its curvature (including lateral curvature) can assist identifying from which species of bird or tract they originated. A feather’s outer surface can always be told by the smooth side of the shaft, which faces away from the body except in certain coverts on the underside of the wings. One of the most distinctive features of a feather is its coloration and patterning. Of course, this characteristic is of little utility when the feather is white or has been dyed. Pennaceous barbules make up the flat, closely knit portions of the vanes. They are differentiated on both sides of a barb; even the ramus is asymmetrical (Fig. 4). The side of a ramus facing the distal end (tip) of a feather is flatter than the side facing the proximal end (base), and may even be concave (Fig. 5). Pennaceous barbs are held together by a flexible, self-adjusting mechanism that is complex in details yet simple in essence. The distal barbules of one barb cross over the proximal barbules of the next barb on the distal side. Hooklets of the former grasp the dorsal flanges of the latter, thereby interlocking them (Fig. 5). Dishevelled vanes with intact barbules can usually be straightened by running fingers through the vane. One has to look no further for the origin of Velcro! 132


Feather Types A single bird bears a wide variety of feathers, including (1) large, stiff remiges and rectrices; (2) moderate-sized, partly-firm feathers that cover the body (contour feathers); (3) small, fluffy down feathers; (4) hair-like filoplumes; and (5) tiny bristles on the face. Contour feathers These are the main feathers on a bird’s body, which have already been described above. Contour feathers are also known as pennae (singular: penna). Remiges and rectrices Remiges and rectrices are characterized by large size, stiffness, asymmetry, vanes that are almost entirely pennaceous, and the absence of an aftershaft. Remiges and rectrices comprise most of the airfoil necessary for flying, often referred to as flight feathers. Semiplumes Semiplumes are sometimes combined with the downs, but they are considered by Lucas and Stettenheim (1972) as a category between the contour feathers and the downs, combining features of both rather than any unique feature. Semiplumes have a long rachis (exceeding the longest barbs) and have entirely plumulaceous vanes. Semiplumes are distributed along the margins of tracts of contour feathers and in the tracts themselves. Down feathers There are two main categories of down feathers: natal down and definite down. The natal down is present on a bird when it hatches or shortly afterward, while the definite down occurs in later generations of feathers. Down feathers are wholly plumulaceous, the rachis being either absent or relatively short. The texture of down feathers results primarily from their slender flexible rami that bear long, segmented, filamentous barbules without hooklets. Down feathers occur at various places on the

body, as a function of the need for insulation. The patterns of distribution of definite down feathers vary between groups of birds. Powder down Feathers of many birds are dusted with a very fine substance that resembles talcum powder. Small amounts of this powder are shed by ordinary plumules and contour feathers. However, the powder is chiefly produced by special feathers, the powder downs which are commonly dispersed over the body among the ordinary downs and contour feathers. The powder is composed entirely of keratin. The powder down is derived from cells on the surface and in the middle of each of the many ridges of barbforming tissue within a feather germ, not normally incorporated in the barbs but lost. Bristles Bristles are characterized by stiff, tapered rachis and the absence of barbs except at the proximal end. They are virtually all found on the head. Filoplumes Filoplumes are hair-like, consisting of a very fine shaft with a tuft of short barbs or barbules at its tip. Filoplumes do not have a tapered rachis and have barbs only at the tip when fully grown. They are always situated beside other feathers, and may serve as an indirect yet very sensitive means for recording slight movements of the larger feathers nearby.

Coloration Birds show an exquisite variety of colours and patterns of coloration, including many bold and showy ones. The patterns are often speciesspecific and may vary within a species with gender, age and season. All colours are produced by one of two physical processes: the absorption of specific wavelengths of light by natural pigments (pigmentation), or the interference of light reflected by biological nanostructures of contrasting refractive indices (structural colours) (Frank, 1939).

Pigments Biochemicals deposited in feathers during their elaboration are varied and include melanins, carotenoids, psittacofulvins, porphyrins, and a few unknown pigments (Frank, 1939; Völker, 1944; Brush, 1978b). Coloration may also be acquired by grown feathers from the environment, like ferrous oxides present in mud or sand. Finally, a wide variety of natural or artificial dyes may be applied by humans to light-coloured feathers. The emphasis here will be on pigments in native feathers. Pigments (also called biochromes) differ in their chemical make-up, absorption properties (colours), mode of formation, mode of incorporation and display in feathers, as well as in their response to various physico-chemical treatments. Melanins Melanins are the most common and widely distributed class of pigments in bird feathers, and almost the only one in mammals. Melanins also occur widely among plants, animals, fungi, and bacteria. Melanins give the feather a black, reddish-brown, brown or yellow colour (Frank, 1939; Lubnow, 1963; Brush, 1978b). Generally the colours produced by melanins lack saturation (i.e., are relatively dull) because most wavelengths of visible light are absorbed, at least to some extent. Still, when combined with other pigments or structural modifications melanins can create bright, even stunning colours (see Structural Colours below). Melanin is a heterogenous polymer synthesized through the oxidation of the amino acid tyrosine by a process that is in part autocatalytic involving free radicals, but initially requiring the enzymatic activity of the copper-containing oxidase tyrosinase. Tyrosinase catalyzes the conversion of the amino acid tyrosine to 3,4-dihydroxyphenylalanine (dopa), then to dopaquinone, and so on (Brush, 1978b; Körner and Pawelek, 1982). Eumelanin is formed through subsequent intramolecular rearrangements and polymerizations (Fig. 6). In the presence of sulfhydryl compounds such as cysteine and glutathione there is production of fur trade legacy workshop

133

Figure 6. Presumed pathways of melanin biosynthesis. From Brush, 1978b.

134


cysteinyldopas which oxidize, cyclize and polymerise to form another type of melanin, phaeomelanin (Fig.6; Brush, 1978b). Most melanins are insoluble and chemically intractable, though some are somewhat soluble in alkali. Melanin is synthesized in specific cytoplasmic organelles, known as melanin granules, by specialized stellate pigment cells called melanophores (melanocytes, when they lack organelle motility). Melanophores do not develop in the growing feather per se, but rather lie at the base of the growing feather (epithelial layer), actively producing and transferring melanin granules to the keratinocytes that will make up the feather proper. These pigment cells ultimately derive from neural crest cells that form beside the neural tube early in development, which have migrated to those parts of the body that are to be pigmented (Le Douarin, 1982). Melanin granules deposited on the surface of the keratinocytes enter the deeper layers of the cytoplasm. With subsequent keratinization the pigment granules become embedded in the horny substance of the epithelial cells (Lucas and Stettenheim, 1972). The colours produced by melanins depend on the type of melanin involved, and secondarily on the number of granules laid down. Four types of melanins are known in birds: (1) the eumelanins produce black or dark brown; eumelanin granules are typically rod-shaped (0.5-1.2 µm). (2) the phaeomelanins produce light brown, reddish-brown, or yellow granules. Granules of phaeomelanin are spheroid or ovoid and smaller than those of eumelanin, the smallest granules giving rise to rusty-brown to pale yellow colours (Lucas and Stettenheim, 1972). Phaeomelanins differ in solubility, as well as spectrally and chemically, from eumelanins (Lubnow, 1963). Unlike eumelanins, phaeomelanins are soluble in alkali and can be extracted with cold 0.25 % NaOH solution (Lubnow, 1963). (3) An iron pigment closely related to, or possibly identical to, trichosiderin—the iron pigment of human red hair—has also been

isolated from red, brown and buff feathers of chickens, turkeys, junglefowl and Bobwhites (Lucas and Stettenheim, 1972). (4) Erythromelanins produce chestnut red, and have been hypothesized to occur in birds mainly on genetic grounds, but have never been characterized adequately chemically. Feathers, or parts of feathers, that contain melanin are usually more resilient and less subject to wear than the unpigmented feathers or parts of feathers (Burtt, 1986). Carotenoids Carotenoids are found in the feathers of birds from at least 10 orders (and 19 families) (Brush, 1981). Carotenoids produce most of the bright red, orange and yellow hues of feathers, though not those seen in parrots, where psittacofulvins are involved instead (see below). When combined with structural elements, especially blue, carotenoids also produce shades of green. Carotenoids are highly unsaturated hydrocarbons that are readily soluble in fats and organic solvents. For many years carotenoids were labelled as lipochromes, a designation which no longer is desirable as other groups of pigments (like the psittacofulvins) are also fat-soluble. Birds, as all animals, cannot synthesize carotenoid pigments de novo and ultimately must obtain these pigments from their diet, directly or indirectly from plants (Goodwin, 1984). However, many organisms, like birds, can modify the ingested pigment to some extent (Goodwin, 1984). Both carotenes, made up of only carbon and hydrogen, and xanthophylls, which also contain oxygen, can be obtained in the diet, though birds tend to absorb xanthophylls preferentially (one exception being the flamingoes which absorb preferentially dietary carotenes) (Fox, 1976; Brush, 1981). Though carotenes turn up in feathers only rarely, they can act as precursors of pigments that are deposited in feathers. Several carotenoids have now been identified in the feathers of birds (Völker, 1944; Fox, 1976; Brush, 1981; Hudon, 1991). Feather colour usu-

ally correlates with the types of carotenoids deposited, particularly the number of conjugated double bonds that they bear. It is not uncommon for feathers to contain mixtures of several related carotenoids (Hudon and Brush, 1990; Hudon, 1991). Feather carotenoids include: (1) dietary carotenoids: lutein, zeaxanthin, sometimes deposited unaltered in feathers to produce orange-yellow to orange colours (Fig. 7). (2) red 4-oxo-carotenoids, produced through the enzymatic addition of one or two oxo (=O) functions at carbon 4 of the carotenoid end-rings, extending the central chain of double bonds of dietary carotenoids and shifting the colour toward red. Examples: astaxanthin, canthaxanthin, adonirubin, etc. (Fig.7). (3) yellow carotene-3-ones produced through the migration of a double bond on the carotenoid end-rings from position 5,6 to 4,5, shortening the chain of double bonds by one or two double bonds yielding bright yellow pigments. Examples: canary xanthophylls (Fig.7; Goodwin, 1980; Hudon, 1991). (4) light yellow picofulvins produced through hydrogenation of the double bond 7,8 to produce 7,8-dihydro-carotenoids, in several woodpeckers (Stradi et al., 1998). (5) an unusual, bright red, retrodehydro carotenoid, rhodoxanthin, presumed to be acquired directly from the diet, responsible for blue, violet and red feather colours in several fruit pigeons, and dark red colours of cotingas (Völker, 1952, 1953). During feather development the carotenoids are dissolved in lipoid droplets. In the first stage of keratinisation the fat droplets disappear, and the carotenoids are absorbed by the viscous keratin substance; sometimes they are precipitated in the shape of fine particles which later dissolve in the keratin (Desselberger, 1930).


135

Figure 7. Examples of carotenoids found in the diet (top four) and feathers of birds (all except β-carotene and β-cryptoxanthin).

136


The colorfastness of feather displays involving carotenoids varies tremendously between taxa, from vanishing quickly after the death of a bird, even in complete darkness [e.g., the pink or yellow blush, also called flush, wash, tint, etc. of white feathers of several gulls, terns, ducks, pelicans and ptarmigans (Stresemann, 1927; Höhn and Singer, 1980; Hudon and Brush, 1990)], to disappearing under filtered natural light over a period of several months [e.g., the red feathers of Crested Quetzal (Pharomachrus antisianus)], to being able to withstand display in museum exhibits for extended periods of time, and retain their colour almost indefinitely in darkness (e.g., Northern Cardinal, Cardinalis cardinalis) (Völker, 1964). Feathers containing carotenoids also differ markedly in the ease with which they release their carotenoids to organic solvents, from being easily washed away by organic solvents with little penetrating power, like petroleum ethers, hexane, acetone (Hudon and Brush, 1990), to quickly (in a few minutes) releasing them almost completely to a solution of methanol at room temperature (Crested Quetzal), to even being resistant to organic solvents like methanol (most birds, including the Cardinal) (Völker, 1964; Hudon and Brush, 1992). Since the same carotenoids are involved in many of these examples, the variation in colourfastness and binding strength must be related to the strength and specificity of binding of the pigments to feather proteins, and not to the nature of the carotenoids themselves (Völker, 1964): it has been suggested that some blushes may be applied to the surface as a component of the preen gland secretion (Stegmann, 1954), while carotenoids in feathers may be bound more or less strongly and specifically to feather proteins (Hudon, unpublished observation.). Carotenoids in the Northern Cardinal (and the psittacofulvins of parrots; see below) are bound to feather proteins of large size (> 200 kD) different from feather keratins (Hudon, unpublished obs.). These proteins alter the absorption properties of the pigments, shifting their peak of absorption to longer, less energetic wavelengths (which can be demonstrated by heating the feathers in an oven), and dramatically extending

the pigment’s stability and half-life, which would only be a few hours in solution at room temperature (Hudon, unpublished obs.). Traditionally, carotenoids in feathers have been extracted in strong bases like alkaline ethanol (e.g., 10% NaOH) over a steam bath, because of the relative stability of most carotenoids in bases (though acidogenic carotenoids, like astaxanthin, are often oxidized to respective acid derivatives in these conditions), but these methods lead to the complete dissolution of the feather matrix. Extraction without feather destruction is effected using acidified pyridine (Hudon and Brush, 1990), permitting an examination of the remaining pigments (e.g., eumelanins), structural colours and other morphological features. This method has proved useful to remove pigments from fresh feathers (including those of parrots) to match badly faded ethnographic artifacts (Hudon, unpublished obs.). Extraction with acidified pyridine also provides an easy and convenient means to determine whether carotenoids are involved (McGraw et al., 2005). Where carotenoid pigments are heavily concentrated, the ramus or rachis is frequently swollen, there is no differentiation into cortex and pith, and the barbules are much reduced or altogether absent (Desselberger, 1930). Psittacofulvins The bright red, orange, and yellow colours in the plumage of parrots are produced by a class of pigment altogether different from carotenoids, which parrots also circulate in their blood, but seemingly do not use for pigmentary purposes (McGraw and Nogare, 2004). Parrots instead deposit psittacofulvins, until recently a structurally unelucidated family of pigments (Völker, 1936, 1937; Hudon and Brush, 1992). Like the carotenoids, the psittacofulvins are hydrophobic molecules. Unlike carotenoids, however, they are synthesized endogenously by parrots and do not appear first in lipoid droplets in growing feathers but are dissolved directly in the keratinising cytoplasm of the cells (Völker, 1937; Driesen, 1953).

Amerindians of the Amazon drainage and the Guianas apparently had developed a means to reprogram the feather follicles of live parrots to produce yellow or red feathers instead of the normal green ones by a process of “tapirage” which involved rubbing plucked areas of the skin with a concoction containing the blood or skin toxin of Dendrobates tinctorius, a member of the group of poison-arrow frogs (Métraux, 1944). Recently, the psittacofulvins found in the red feathers of the Scarlet Macaw (Ara macao) were chemically identified as consisting of four linear polyenal structures: tetradecahexenal, hexadecaheptenal, octadecaoctonal and eicosanonenal CH3 - (CH + CH)n - CHO, where n varies from 6 to 9 (Stradi et al., 2001). Psittacofulvins can be extracted with acidified pyridine (Völker, 1936, 1937; Hudon and Brush, 1992). They change colour dramatically upon initial exposure to this solvent, though the colour change is reversible if heating is not applied (Völker, 1937; Hudon, personal obs.). It is not known how these pigments are synthesized by parrots. Porphyrins Unconjugated porphyrins are present in red and brown feathers of birds from 13 orders, notably in the downy plumage and adult feathers of owls and bustards (Völker, 1938; With, 1978). Porphyrins also occur in the hair of mammals. Porphyrins characteristically produce an intense red fluorescence under ultraviolet light. Porphyrins are unstable and fade rapidly upon exposure to light, and thus tend to be restricted to those areas of the body protected from direct sunlight (Völker, 1964; Lucas and Stettenheim, 1972). Porphyrins are derived from the catabolism of the heme moiety of hemoglobin by the liver (which is another pigment used for the pigmentation of the skin of birds, though not of their feathers) (Thiel, 1968). fur trade legacy workshop

137

Pigmentary porphyrins consist of four pyrrole rings united by methane bridges into a super-ring. Feather porphyrins consist mainly in coproporphyrin III, but include also protoporphyrin IX and uroporphyrin I, which also appear in the eggshells of birds (Völker, 1938; With, 1978). Members of the family of touracos (Musophagidae) deposit a unique porphyrin, turacin, a copper-containing derivative of uroporphyrin III, responsible for the rich red to purple-red colour of their remiges and head feathers (Moreau, 1958; With, 1957). Turacin changes colour (turns blue) upon exposure to rain, but reverses to its former colour upon drying. Turacin is soluble in a weak alkaline solution and can easily leach out of feathers. Considerable care should be taken when washing these feathers to prevent leaching of the pigment. Yet turacin is considerably more stable to light exposure than the free porphyrins discussed above. The green feathers of touracos and species from several orders of birds [Blood Pheasant (Ithaginis cruentus), Roulroul (Rollulus roulroul), Jaçanas (Jacana spp.), etc.] contain a porphyrin whose chemical relationship to turacin is not well understood, called turacoverdin (Dyck, 1992). An unknown green pigment is found in the green feathers of eider ducks (Somateria spp.) (Dyck, 1992; Hudon, unpublished obs.). Adventitious coloration Red and yellow colours in several species of waterfowl and some birds of prey (e.g., the Bearded Vulture, Gypaetus barbatus) are the result of the deposition of ferrous oxides picked up from the environment (mud, sand) (Kennard, 1918; Höhn, 1955; Berthold, 1967). These colours are relatively stable as they are an integral part of the plumage coloration. The same could probably be said of pigments like ochre that are applied by indigenous cultures.

Structural Colours Structural colours in feathers are broadly classified as either iridescent or non-iridescent, based on whether they change with the angle of view138


ing or illumination, or not. Until recently, these two classes of structural colours were believed to arise from distinct physical processes, coherent or incoherent scattering, respectively. In coherent scattering, colour production is described in terms of the phase relationships among light waves scattered by multiple scatterers, for example the interfaces afforded by rows of melanin granules in a keratinised matrix. Scattered waves that are out of phase destructively interfere and cancel each other, whereas scattered waves that are in phase constructively reinforce one another. In incoherent scattering, in contrast, colour production arises as a result of the differential scattering of wavelengths of light by the individual light-scattering elements, through Rayleigh scattering (erroneously known as Tyndall scattering) or Mie scattering, with no relation to the phase relationships between the scattered waves. It has become apparent in recent years that quasi-ordered arrays of light-scattering elements in non-iridescent feathers also produce biological structural colours through coherent scattering and interference (Dyck, 1971, 1976; Prum et al., 1998, 1999; Osorio and Ham, 2002). The scatterers are sufficiently spatially ordered at the nanoscale level to produce the observed hues by coherent scattering but are not ordered enough at larger spatial scales to be strongly or at all iridescent (Prum et al., 1998). Iridescent colours Iridescent colours are produced overwhelmingly in the barbules of feathers. Iridescent colours are always associated with melanin granules, the granules being deposited in highly ordered layers parallel to the upper surface of a barbule or one of its sections, keratin/melanin granule or air-vacuoles in melanin granules affording interfaces of contrasting refractive indices for reflection (Lucas and Stettenheim, 1972). The colour of the iridescence will vary as a function of the thickness of the granules, intervening keratin layers, and/or air-filled cavities, number of layers and spacing of light-scattering interfaces, as well as with the angle of viewing and light incidence on the feather (Dyck, 1976).

Figure 8. Coloured barbules in the pennaceous part of a humeral feather from a Bronze Turkey. From Lucas and Stettenheim, 1972.


139

Figure 9. Rami that are coloured entirely or partly by interference in cloudy cells. These cells are shown in blue because they are the source of this colour in whole feathers, although they do not actually appear blue in cross-section, i.e., without a background of melanin. A and B, Green Magpie (Cissa chinensis), head feathers; C, Vulturine Guineafowl (Acryllium vulturinum) outer vane of remix; D, Red-rumped Paradise Tanager (Tangara chilensis), abdominal feathers; E, Gouldian Finch (Poephilia gouldiae), dorsal feather; F, Masked Tanager (Tangara nigrocincta), head feather. From Lucas and Stettenheim, 1972; redrawn after Frank, 1939. In some species, like the wild turkey, the pennula of iridescent barbules become highly modified: broadened, flattened, and twisted so that they lie in the plane of the vane (instead of perpendicular to it). As a result, the vane presents a very smooth surface, not unlike a closed venetian blind (Fig. 8). Barbs in the iridescent zone contain such a large amount of melanin that separate granules can no longer be made out (Lucas and Stettenheim, 1972). In hummingbirds, the melanin granules instead contain gas-filled air vacuoles in single or multiple layers, causing iridescence through interference of light reflected from the upper and lower surfaces of the vacuoles (Lucas and Stettenheim, 1972; Dyck, 1976). Non-iridescent Colours Non-iridescent colours (most blues and violets, many greens) are produced by modified rami or shafts, except in blue fruit pigeons (Alectroenas spp.), crowned pigeons (Goura spp.) and a few other taxa, where they are 140


produced in the barbules (Lucas and Stettenheim, 1972; Dyck, 1976). In these systems the reflections responsible for colour-production occur at keratin-air interfaces, in the spongy structure of large, polygonal medullary cells of the barbs and shafts (Fig. 9). Electron microscopic studies show the spongy structure to be a complicated network of interconnected keratin rods of fairly constant diameter separated by air-filled channels (Dyck, 1971, 1976), where colour is determined by the diameters of the rods, which vary from 200 to 400 nm. Melanin granules, when present, function primarily to absorb the transmitted light, not reflect light as in iridescent colours (Dyck, 1976). In white feathers, there is no underlying pigment and the rods of keratin are of a larger diameter and reflect all wavelengths of light about equally. In structurally coloured rami, the cortex is unpigmented and generally thin, usually referred to as cuticle. Combined with the presence of yellow carotenoids or psittacofulvins the cortical layer will appear green (Fig. 9).

Feather Fauna The feathers of live birds provide cover and food for a wide variety of organisms, besides the clothes moths that are the bane of museum collections. Chewing feather lice (Mallophaga) Chewing feather lice are small (mostly less than 5 mm long) wingless, flattened insects, armed with chewing mandibles that are ectoparasites of birds, feeding on the feathers (or hair) of their host. Chewing lice spend their entire life on their host. Transmission from one host to another usually occurs when hosts come in contact, since lice are unable to survive long off a host. Each species attacks one or a few related species of hosts, and lives on a particular part of a host’s body. Eggs are laid on the host, usually attached to hair and feathers. Chewing lice can be quite irritating to their hosts. Heavily infested animals are often emaciated (Borror and Delong, 1989). Mites Mites are very small. Their small bodies allow them to exploit habitats too cramped and food sources too meager for insects, and their life histories are often many times more rapid. Not all bird-associated mites are parasitic; some may even be beneficial. At least 2500 species of mites from 40 families are closely associated with birds, occupying all conceivable habitats on the bodies and nests of their hosts (Proctor and Owens, 2000). Even taxa that lack feather mites, such as penguins, are attacked by ticks. Feathers provide a habitat for the greatest diversity of bird-associated mites, some of which live on feather surfaces (plumicoles), while others live inside the quills (syringicoles) (Proctor and Owens, 2000). Unlike feather lice, which consume feathers, plumicolous mites consume mainly uropygial-gland oil (predominantly waxes and fatty acids) and scurf, pollen and fungi that adhere to the feather barbs. The mites’ mouthparts are designed for scraping not chewing.

Bacteria A soil bacterium, Bacillus licheniformis, was described recently as capable of degrading feathers in poultry waste (Williams et al., 1990), and found to be present in the plumage of many North American birds (Burtt and Ichida, 1999). Burtt and Ichida (2004) hypothesized that Gloger’s rule of ecogeographic variation, whereby populations living in climates with high relative humidity tend to be darker than those living in climates with low relative humidity, might find an explanation in the increased resistance to bacterial degradation of feathers laden with melanin pigmentation (Burtt, 1986). However, even when applied liberally to the plumage of live birds housed outdoors, even in humid conditions, B. licheniformis does not appear to degrade feathers (Cristol et al., 2005), raising the question as to whether this and other keratin-degrading microbes have any effect on the feathers of live birds.

Effect of Light on the Colour of Integumentary Derivatives There have been surprisingly few studies of the effect of light on the epidermal appendages of wild species of vertebrates, e.g., range of natural pigments and packages (scales, feathers, fur) (Cato et al., 2001), and there are no published data about fading rates and acceptable exposure levels for different types of feathers (Solajic et al., 2002). Moreover, studies carried out so far, and some currently in progress at the British Museum, have been concerned mainly with the feathers of parrots (Horie, 1990; Solajic et al., 2002), which contain an unusual suite of pigments, the psittacofulvins, and so cannot be generalized to other more common pigment systems, though they might be some of the most susceptible to fading (Solajic et al., 2002). Unfortunately, the small size of feathers, complex patterning and difficulty to acquire large amounts of material greatly impede a systematic study of the effect of light on a wide range of feathers. By contrast, furs fur trade legacy workshop

141

are often readily available and often of large enough size to allow for a study, with controls and replicates. Moreover, furs also come in a variety of colours, including colour morphs or variants, which might permit evaluation of the effect of pigment composition on rates of fading. With that in mind I set out to compare the effect of light on the fur of three species of carnivorous mammals (the marten, mink and otter); specifically I set out to: 1) gather quantitative data on rates of fading of furs known to be sensitive to light in museum displays; 2) compare fading in species of different colours and mane structures; 3) evaluate the remedial effects of an antioxidant (butylated hydroxytoluene) on fading. Methods Tanned skins of Mink (Mustela vison), Marten (Martes americana) and River Otter (Lutra canadensis) were acquired from Halford Hide & Leather Co. Ltd, Edmonton and cut into many 6.2 cm-long strips spanning the area between the dorsal and ventral midlines (except for the otter strips which ran along the dorsal midline). Strips that differed noticeably in appearance were set aside. The remaining (similar) strips were drawn randomly and subjected to different treatments or used as controls. Most experiments were represented by at least two strips, except for the methanol control, and the otter samples, where there was only one sample for each treatment. One set of samples was treated with an antioxidant, butylated hydroxytoluene (Sigma Chemical Co.; 1% in methanol), for 50 or 100 hours; a control strip was bathed in methanol for 100 hours. The fur strips were stapled on individual Atlas Electric Devices Fadeometer test masks (No. SL-8A-3T) with a 6 cm x 6 cm window, ensuring that the samples from a single skin visually matched in appearance (the hair always pointed in the same direction). AATCC Blue Wool Lightfastness Standards (L2 to L7) were also mounted and run concurrently

142


to monitor light exposure levels. All samples were exposed to light in an Atlas Weather-O-meter, Model Ci35 equipped with a continuous water-cooled xenon-arc lamp shielded by a Soda Lime outer filter and borosilicate inner filter (Option E in AATCC Test Method 16-1993; AATCC Technical Manual, 1998). Colorimetric and spectral readings were taken of all samples (N = 26) after 0, 5, 10, 20, 40, 80, and 160 hours in the weatherometer. Colorimetric determinations were made with a HunterLab ScanLab XE spectrocolorimeter (0°/45° geometry; 50 mm diameter aperture) connected to a Dell Latitude C800 laptop (and driven by HunterLab Universal software v. 4.10). Each sample was read twice. An Ocean Optics USB2000 spectrophotometer operated with OOIBase32 v. 2.0.1.4 was used to obtain visible spectra of smaller areas of each sample (10.32 mm diameter) using a ISPREF illuminated integrating sphere; sampling was done at the centre of the plate, as well as at 15 mm above, below and to the left and right of the centre. By the end of the experiment, 364 readings had been taken on the colorimeter and more than 1092 spectra were acquired. Fading was estimated by determining ∆ECIELAB and ∆L* for CIELAB illuminant D65 and 10° observer data.

Results and Discussion The three furs examined differed significantly in their reaction to exposure to light in a fade-ometer. Both mink and otter fur darkened initially (L* decreased) upon exposure to light, then slowly lightened. The marten fur, in contrast, lightened rather monotonously through that time interval (Fig. 10). After 160 hours of light exposure in the fade-ometer, the lightness of the mink fur, but not of the otter, had returned to near the level when the experiment started. The otter fur gained only about half the lightness it had lost on initial exposure to light (Fig. 10). The fur coloration also changed in a species-specific way, reddening in the otter and mink, but initially becoming less red in the marten before getting redder as in the other species (Fig. 10).

Figure 10. Fading rate curves for tanned marten, mink and otter fur (one example each; colour and lightness variables are CIELAB units; error bars are ±SD). Exposed to light in an Atlas Weather-O-meter, Model Ci35 equipped with a continuous water-cooled xenon-arc lamp shielded by a Soda Lime outer filter and borosilicate inner filter (Option E in AATCC Test Method 16-1993; AATCC Technical Manual 1998).

Figure 11. Fading rate curves for otter fur with and without 1% BHT, an antioxidant (and methanol wash control). AFU’s are AATCC Fading Units or hours of exposure calibrated using AATCC blue wool standards (AATCC Technical Manual 1998).


143

Unfortunately, the species differ in hair length, pigment arrangement, concentration and presumably composition; so the source of the speciesspecificity of reaction to light cannot be completely ascertained. In another experiment we tested whether scavenging free radicals, generated either directly from exposure to light, or indirectly from photochemical processes set afoot by light irradiation (Feller, 1994), using an antioxidant (1% butylated hydroxytoluene), might impede or slow down the photo-oxidation of pigments, particularly since melanins can sometimes act as free radical traps (Geremia et al., 1984). Surprisingly, however, addition of an anti-oxidant did not affect the direction nor the rate of change of coloration, for example in the otter skin (Fig. 11). In conclusion, conservators need to be aware that integumentary colour systems, even those with only a single pigmentary or structural system, may vary markedly in sensitivity and response to exposure to light from one species to another. Future efforts should attempt to document the effects of light on a wide variety of sources of colours and types of feathers and to carry out controlled fading experiments on a wide variety of organic materials (feather, fur, scales, etc.).

Literature Cited American Association of Textile Chemists and Colorists. (1998). Colorfastness to light. Pp. 24-35 in: AATCC Technical Manual, Volume 73. AATCC, Research Triangle Park, North Carolina. Berthold, P. (1967). Über Haftfarben bei Vögeln: Rostfärbung durch Eisenoxid beim Bartgeier (Gypaetus barbatus) und bei anderen Arten. Zoologisches Jahrbuch, Abteilung für Systematik 93: 507-595. Bonser, R.H.C., and P.P. Purslow. (1995). The Young’s modulus of feather keratin. J. Experimental Biology 198: 1029-1033. Borror, D.J., and D.M. Delong. (1989). An introduction to the study of insects. Sixth Edition. Saunders College Publishing.

144


Brush, A.H. (1978a). Feather keratins (Chapter 4). Pp. 117-139 in: M. Florkin and B.T. Scheer (eds.), Chemical Zoology. Volume 10. Aves. Academic Press, New York. ———. (1978b). Avian pigmentation (Chapter 5). Pp. 141-164 in: M. Florkin and B.T. Scheer (eds.), Chemical Zoology. Volume 10. Aves. Academic Press, New York. ———. (1981). Carotenoids in wild and captive birds. Pp. 539-562 in: J.C. Bauernfeind (ed.), Carotenoids as Colorants and Vitamin A Precursors. Academic Press, New York. Burtt, E.H., Jr. (1986). An analysis of physical, physiological and optical aspects of avian coloration with emphasis on wood warblers. AOU Ornithological Monographs 38: 1-126. ———, and J.M. Ichida. (1999). Occurrence of feather-degrading bacilli in the plumage of birds. Auk 116: 364-372. ———, and J.M. Ichida. (2004). Gloger’s rule, feather-degrading bacteria, and color variation among Song Sparrows. Condor 106: 681-686. Cato, P.S., D.H. Dicus, and D. von Endt. (2001). Priorities for natural history collections conservation research: results of a survey of the SPNHC membership. Collection Forum 15: 1-25. Chandler, A.C. (1916). A study of the structure of feathers, with reference to their taxonomic significance. Univ. California Publications in Zoology 13: 243-446. Cristol, D.A., J.L. Armstrong, J.M. Whitaker, and M.H. Forsyth. (2005). Feather-degrading bacteria do not affect feathers on captive birds. Auk 122: 222-230. Day, M.G. (1966). Identification of hair and feather remains in the gut and faeces of stoats and weasels. J. Zoology 148: 201-217. Desselberger, H. (1930). Ueber das Lipochrom der Vogelfeder. J. für Ornithologie 78: 328-376. Driesen, H.H. (1953). Untersuchungen über die Einwanderung diffuser Pigmente in die Federanlage, insbesondere beim Wellensittich (Melopsittacus undulatus [Shaw]). Zeitschrift für Zellforschung 39: 121-151.

Dyck, J. (1971). Structure and colour-production of the blue barbs of Agapornis roseicollis and Cotinga maynana. Zeitschrift für Zellforschung 115: 17-29. ———. (1976). Structural colours. Pp. 426-437 in: Proceedings of the 16th International Ornithological Congress. Australian Academy of Science, Canberra City. ———. (1992). Reflectance spectra of plumage areas colored by green feather pigments. Auk 109: 293-301. Frank, F. (1939). Die Färbung der Vogelfeder durch Pigment und Struktur. J. für Ornithologie 87: 426-523. Feller, R.L. (1994). Accelerated Aging. Photochemical and Thermal Aspects. Research in Conservation. Getty Conservation Institute. Fox, D. (1976). Animal Biochromes and Structural Colours. University of California Press, Berkeley. Geremia, E., C. Corsaro, R. Bonomo, R. Giardinelli, P. Pappalardo, A. Vanelle and G. Sichel. (1984). Eumelanins as free radicals trap and superoxide dismutase activities in amphibia. Comparative Biochemistry and Physiology 79B: 67-19. Goodwin, T. W. (1984). The Biochemistry of Carotenoids. Volume II. Animals. Chapman and Hall, New York. Höhn, E.O. (1955). Evidence of iron staining as the cause of rusty discoloration of normally white feathers in anserine birds. Auk 72: 414. ———, and P. Singer. (1980). Über die Rostfärbung bei Schneehühnern. J. für Ornithologie 121: 282-286. Horie, C.V. (1990). Fading of feathers by light. ICOM-CC 9th Triennal Meeting, 26-31 August, 1990, Dresden. pp. 431-435. Hudon, J. (1991). Unusual carotenoid use by the Western Tanager (Piranga ludoviciana) and its evolutionary implications. Canadian J. Zoology 69: 2311-2320. ———, and Brush, A.H. (1990). Carotenoids produce flush in the Elegant Tern plumage. Condor 92: 798-801. ———, and Brush, A.H. (1992). Identification of carotenoid pigments in birds. Methods in Enzymology 213: 312-321.

Kemp, D.J. (1975). Unique and repetitive sequences in multiple genes for feather keratin. Nature 254: 573-577. Kennard, F.H. (1918). Ferruginous stains on waterfowl. Auk 35: 123-132. Körner, A., and J. Pawelek. (1982). Mammalian tyrosinase catalyzes three reactions in the biosynthesis of melanin. Science 217: 1163-1165. Le Douarin, N. (1982). The Neural Crest. Cambridge University Press, Cambridge. Lubnow, E. (1963). Melanine bei Vögeln und Säugetieren. J. für Ornithologie 104: 69-81. Lucas, A.M., and Stettenheim, P.R. (1972). Avian Anatomy. Integument. Agriculture Handbook 362. US Department of Agriculture, Washington, D.C. McGraw, K.J., J. Hudon, G.E. Hill and R.S. Parker. (2005). A simple and inexpensive chemical test for behavioural ecologists to determine the presence of carotenoid pigments in animal tissues. Behavioural Ecology and Sociobiology 57: 391-397. McGraw, K.J., and M.C. Nogare. (2004). Carotenoid pigments and the selectivity of psittacofulvin-based coloration systems in parrots. Comparative Biochemistry and Physiology 138B: 229-233. Métraux, A. (1944). “Tapirage” a biological discovery of South American Indians. Proc. Washington Academy of Science 34: 252-254. Moreau, R.E. (1958). Some aspects of the Musophagidae. Part 3. Ibis 100: 238-270. Oakes, J., and R. Riewe. (1996). Our Boots: An Inuit Woman’s Art. Thames and Hudson, London and New York. Osorio, D., and A.D. Ham. (2002). Spectral reflectance and directional properties of structural coloration in bird plumage. J. Experimental Biology 205: 2017-2027. Presland, R.B., K. Gregg, P.L. Molloy, C.P. Morris, L.A. Crocker and G.E. Rogers. (1989a). Avian keratin genes. I. A molecular analysis of the structure and expression of a group of feather keratin genes. J. Molecular Biology 209: 549-559.


145

Presland, R.B., L.A. Whitbread and G.E. Rogers. (1989b). Avian keratin genes. II. Chromosomal arrangement and close linkage of three gene families. J. Molecular Biology 209: 561-576. Proctor, H., and I. Owens. (2000). Mites and birds: diversity, parasitism and coevolution. TREE 15: 358-364. Prum, R.O., and A.H. Brush. (2002). The evolutionary origin and diversification of feathers. Quarterly Review of Biology 77: 261-295. Prum, R.O., R.H. Torres, S. Williamson and J. Dyck. (1998). Coherent light scattering by blue feather barbs. Nature 396: 28-29. ———, R.H. Torres, S. Williamson and J. Dyck. (1999). Two-dimensional Fourier analysis of the spongy medullary keratin of structurally coloured feather barbs. Proc. Royal Society of London, Series B, Biological Sciences 266:13-22. Pyle, P. (1997). Identification Guide to North American Birds. Part 1. Columbidae to Ploceidae. Slate Creek Press, Bolinas, California. Rae, A., and B. Wills. (2002). Love a duck: the conservation of feathered skins. Pp. 43-61 in: M.M. Wright (ed.), The Conservation of Fur, Feather and Skin. Archetype Publications Ltd., London. Solajic, M.R., M. Cooper, T. Seddon, J. Ruppel, J. Ostapkowicz and T. Parker. (2002). Colourful feathers. Pp. 69- 78 in: M.M. Wright (ed.), The Conservation of Fur, Feather and Skin. Archetype Publications Ltd., London. Stegmann, B. (1956). Über die Herkunft des flüchtigen rosenroten Federpigments. J. für Ornithologie 97: 204-205. Stradi, R., J. Hudon, G. Celentano and E. Pini. (1998). Carotenoids in bird plumage: the complement of yellow and red pigments in true woodpeckers (Picinae). Comparative Biochemistry and Physiology 120B: 223-230. Stradi, R., E. Pini, and G. Celentano. (2001). The chemical structure of the pigments in Ara macao plumage. Comparative Biochemistry and Physiology B 130: 57-63.

146


Stresemann, E. (1927-1934). Aves.–Vögel. in: W. Kükenthal and T. Krumbach (eds.), Handbuch der Zoologie. Vol. 7. Part 2. Walter de Gruyter, Berlin. Takahashi, R., K. Akahane and K. Arai. (2003). Nucleotide sequences of pigeon feather keratin genes. DNA Sequence 14: 205-210. Thiel, H. (1968). Die Porphyrine der Vogelfeder. Untersuchungen über ihre Herkunft und Einlagerung. Zoologisches Jahrbuch, Abteilung für Systematik. 95: 147-188. Völker, O. (1936). Ueber den gelben Federfarbstoff des Wellensittichs (Melopsittacus undulatus [Shaw]). J. für Ornithologie 84: 618-630. ———. (1937). Ueber Fluoreszierende, gelbe Federpigmente bei Papageien, eine neue Klasse von Federfarbstoffen. J. für Ornithologie 85: 136-146. ———. (1938). Porphyrin in Vogelfedern. J. für Ornithologie 86: 436-456. ———. (1944). Die Stofflichen Grundlagen der Pigmentierung der Vögel. Biologisches Zentralblat 64: 184-235. ———. (1952). Die Lipochrome in der Federn der Cotingiden. J. für Ornithologie 93: 122-129. ———. (1953). Das Farbkleid der Flaumfußtauben (Ptilinopodinae). J. für Ornithologie 94: 263-273. ———. (1964). Federn, die am Licht ausbleichen. Natur und Museum 94: 10-14. Williams, C.M., C.S. Richter, J.M. Mackenzie, Jr., and J.C.H. Shih. (1990). Isolation, identification, and characterization of a featherdegrading bacterium. Applied and Environmental Microbiology 56: 1509-1515. With, T.K. (1957). Turacin is a copper compound of uroporphyrin III. Nature 179: 824. ———. (1978). On porphyrins in feathers of owls and bustards. International J. Biochemistry 9: 893-895.

Author Jocelyn Hudon PhD Curator of Ornithology Provincial Museum of Alberta 12845 – 102 Avenue Edmonton, Alberta T5N 0M6 Tel: (780) 453-9179 Fax: (780) 454-6629 [email protected]


147