A M . ZOOLOCTST, 9:521-530 (19G9).
The Control of Color in Birds
CHARLES L. RALPH
Dej>arlmenl of Biology, University of Pittsburgh, Pittsburgh, Pennsylvania 15213
SYNOPSIS. The colors of birds result from deposition of pigments—mainly melanins and
carotenoids—in integumentary structures, chiefly the feathers. The plumages of birds
indicate their age, sex, and mode of living, and play important roles in camouflage,
mating, and establishment of territories. Since feathers are dead structures, change of
color of feathers is effected through divestment (molt) and replacement. The color
and pattern of a feather are determined by the interplay of genetic and hormonal
influences prevailing in its base during regeneration. Most birds replace their feathers
at least once annually. Some wear the same kind of basic plumage all the time but
others alternate a basic and breeding plumage, either in one (the male) or both sexes.
Still others may have more than two molts, adding supplemental plumage at
certain times in the plumage cycle. The varieties of patterns of molt, the kinds of
plumage, and the colors and patterns of feathers among birds apparently are the result
of several kinds of selection pressures working through evolution.
Birds are exceeded only by insects in geographical distribution. They have played
important roles in the history and folklore
of man, and all cultures have been enchanted by their astonishing variety of
colors, especially that of the plumage.
Although most colored structures of
birds are dead, they remain intriguing objects for study of the origins and maintenance of structural and color patterns. The
pigment-producing cells of feathers are
highly sensitive to changes in their environment, leaving a permanent record of
their responses to various influences that
act upon them in the course of development. Thus, feathers are excellent systems
for analysis of biological patterns (Cohen,
1966).
Pigmented external structures of birds
include feathers, beaks, combs, wattles,
skin, eyes, and scales of legs and feet. Pigments also occur in the membranes surrounding various organs and tissues, and
are secreted by the glandular wall of the
oviduct to be incorporated into egg shells.
What is said here about feathers relates
mainly to the adult-type, contour feathers;
that is, those feathers forming the bulk of
The assistance of Daniel L. Grinwich, University
of Western Ontario, London, Canada, and Dr. Kenneth C. Parkes, Carnegie Museum, Pittsburgh,
Pennsylvania in the preparation of this paper is
greatly appreciated.
the definitive garb of birds. The plumages
of young birds (natal down and juvenile
plumage) are not of great significance for
this presentation. I have attempted only to
present a sampling of the information
available about control of color in birds.
Throughout life, birds renew their
plumage periodically. Some very large
birds may molt some feathers at longer
intervals, but most adult birds undergo a
complete molt at least once annually. Additional molts, often partial, occur in many
birds. It is by the loss and replacement
that birds effect color changes of feathers if
they change colors at all. Many simply
replace old feathers with the same kind of
feathers. Others undergo dramatic seasonal
changes in plumage.
The vestures of birds indicate their age,
sex, and mode of living. Survival may be
enhanced in some whose plumage serves as
camouflage. In many species the seasonal
changes of plumage associated with molt
are importantly related to reproduction.
The nuptial (or alternate; see Humphrey
and Parkes, 1959) plumage has a function
in territorial aggression, or courtship display, or both.
FEATHER COLOR AND PATTERNS
It is obvious that feathers differ from
one region to another on the surface of
521
522
CHARLES L. RALPH
adult birds. They are arranged in distinct
units or tracts (e.g., breast, flank, wing primaries) and the feathers of a tract tend to
be similar in morphology, but do show
variation. The follicles producing the
feathers of any one tract usually are arranged in highly ordered rows or pterylae.
The feathers of the different tracts tend
to have different dvevelopmental histories
(Holmes, 1935), and when a bird molts
there is a characteristic order of feather
loss within tracts (Humphrey and Parkes,
1959). Feathers also become competent to
react to hormones at different times
(Trinkhaus, 1953).
The feather is composed largely of keratin, an undefined proteinaceous material
produced and exactly organized by epidermal cells shortly before they die. Variations in the structure of keratin to produce
optical effects, added to variations in kind
and distribution of pigments, are what
produce feather patterns. Each individual
feather pattern is subordinate to the general pattern of the entire plumage (Cohen,
1966).
Nature of Colors
No other vertebrates have the variety of
colors and shades that birds have. However, their diversity of coloration is achieved
by various combinations of a relatively
small number of pigments and structural
configurations.
Melanins. These are the most important
of the pigments and are responsible for
the dark, somber colors such as black, grey,
brown, and related tints. Melanin also
provides the dark background necessary for
the perception of blue and green resulting
from light scattering (Fox and Vevers,
1960).
Special cells of neural crest origin (Dorris, 1938), which have the potential to produce melanin, take up residence in the
feather germs (as non-pigmented cells
called melanoblasts), and as the barbs of a
developing feather are formed these cells,
now called melanocytes (Gordon, 1953),
transfer their pigment to barb cells.
Differences in oxidation of the same substance, a propigment, lead to the development of different variations of melanin.
The black and dark-brown pigments are
known as eumelanin, or simply melanin,
and the red, light-brown, and yellow melanins as phaeomelanin. Eumelanin is
known to be formed by a two-stage oxidation of tyrosine under the influence of
tyrosinase, a copper-containing enzyme
(Fitzpatrick and Kukita, 1959). The exact
cause of the difference in origin and composition of black and brown eumelanins is
not known, but Dorris (1938) suggested
that the intensity of color depends on the
stage at which oxidation of tyrosine ends,
since melanin was seen to appear first as
small yellow granules, then become larger
and simultaneously dark brown or black.
Melanins are usually in the form of
granules about 1 ^ or less in length. They
have a definite structure, as revealed by
electron microscopy (Schmidt and Ruska,
1961), but their form differs among
feathers, as between feathers of cock and
hen in domestic fowl (Carr, 1957;
Trinkaus, 1948). Melanin granules from
different breeds of fowl also differ in size,
shape, and color (Willier and Rawles,
1940). A histological and chemical investigation of the feathers of 37 breeds of domestic fowl revealed that the melanin of
black feathers was in the form of rodshaped granules (0.5 to 0.6 p by 1.0 to 1.3
fj), that of the background of blue feathers
was in spherical granules (0.5 ^ in diameter), and in buff and reddish feathers the
granules were oval (0.7 p. by 1.0 p)
(Bohren, et al, 1943; Nickerson, 1946a).
The pinkish-brown color of the breast in
the male chaffinch (Fringilla coelebs) has
been attributed to the arrangement of
phaeomelanin granules in groups with
spaces between them from which light is
reflected (Frank, 1939). Here is an example of what might be called a pigmentstructural color.
Carotenoids. The bright colors—yellow,
orange, and red—of eggs, eyes, portions of
skin and adipose tissue, and feathers generally are due to fat-soluble, nitrogen-free
CONTROL OF COLOR IN BIRDS
compounds, formerly known as "lipochromes", but now called carotenoids. In contrast to melanins, carotenoids are not the
products of special pigment cells. Their
source, genesis, and manner of infiltration
into the developing part of the feather are
largely obscure. Carotenoids and their precursors are obtained by birds from their
foods. The pigments are known to be dissolved in fat droplets in the early stages of
development and as keratinization begins
the droplets disappear, leaving carotenoids
deposited in the barbs (Voitkevitch,
1966).
Some carotenoid pigments are united
with protein. Such a union may make the
pigment water-soluble, as is the case for
the xanthophylls, lutein, and zeaxanthin,
of the hen's egg (Fox and Vevers, 1960).
Changes in the environment usually
have a greater influence on the carotenoids
than upon the melanins, but melanins
are subject to fading, especially in birds of
open areas; dark-brown feathers may fade
to buff by the time they are molted
(Parkes, K. C, personal communication).
Diet is the most important variable with
respect to carotenoids. Chickens on diets
devoid of colored carotenoids produce
nearly colorless yolks. The pink and red
feather pigments of flamingos (Phoenicopteridae), the roseate spoonbill (Ajaia
ajaja), and the scarlet ibis (Eudocimus
ruber) result from ingestion of foods containing carotenoids (Fox, 1953).
Canaries maintained on carotenoid-free
rations develop white feathers but will replace them with yellow feathers if switched
to a diet containing xanthophylls or derivatives. Red feathers can be produced by
canaries fed paprika, which contains capsanthin, and an even deeper red is produced when they are fed rhodoxanthin, a
red carotenoid (Fox and Vevers, 1960).
The display plumages of many nuptially-colored male birds, such as those of the
genus Euplectes, contain several carotenoids, whereas those in eclipse (basic)
plumage are nearly devoid of such pigments. Some male birds will retain rich
523
carotenoid stores in the liver and adipose
tissues even after they have been maintained for nearly three months on carotenoid-free diets (Kritzler, 1943).
Other Pigments. A porphyrin, protoporphyrin, is present in the egg shells of many
birds (Fischer and Linder, 1925). There
is sometimes enough of a porphyrin (coproporphyrin III) to give a pinkish color
to down feathers of owls and bustards
(Volker, 1939).
A pigment, which is a copper compound
of uroporphyrin III, called "turacin"
(Church, 1893; With, 1957), found only in
quill feathers of turacos, African birds of
the family Musophagidae, is purple-red
normally, but is reputed to turn blue or
leach out when exposed to rain. However,
Chapin (1939) refutes this color change
and never observed birds with faded
feathers even in the wettest forests. The
pigment will go into solution if the feather
is dipped in an alkaline solution such as
ammonia water. Many turacos do have a
bright green pigment (turacoverdin), the
only true green pigment known in birds.
A few feathers have pigments (probably
porphyrins) which fluoresce in ultraviolet
light. Feathers of the parakeets and some
parrots (Psittacidae) show a yellow fluorescence (Volker, 1937).
Coloration is often the result of a mixture of pigments. The beak and skin frequently contain mixtures of carotenes and
xanthophylls. An olive-green color in the
beaks of mallards (Anas) is due to carotenoids in oil droplets together with melanocytes. Olive-green in feathers is often
due to black melanins and yellow carotenoids juxtaposed (Fox and Vevers,
1960).
Structural Colors. Colors are called
structural, as opposed to pigmentary, when
the physical nature of a surface is responsible for the color. These are the
iridescent and so-called "metallic" colors.
Iridescence is characterized by glittering
with different colors that change according
to the angle from which the object is
seen. It is due to the interference of lightwaves reflected from the surfaces of very
524
CHARLES L. RALPH
thin multiple laminations, separated by
equally thin or thinner layers of material
possessing a contracting refractive index
(Fox, 1953). Colors like those produced by
soap bubbles and oil films on water are
seen in the feathers of the barnyard cock
(Gallus), starling (Sturnus vulgaris), and
head of the male merganser (Mergus).
The feathers of the peacock (Pavo cristatus) and of humming birds (Trochilidae) also show interference colors. The
surfaces which produce these effects in
some cases are attributed to the barbules
(Mason, 1923) but others claim melanin
granules are responsible for the phenomenon (Schmidt, 1952).
Blue is usually a structural color in
birds. Commonly it is Tyndall scattering that produces blue coloring. Tyndall
scattering refers to color produced when
very small particles scatter the shorter
waves in white light. This phenomenon is
a cause of the blue color of the sky. The
blue skin of the head and neck of the
turkey (Meleagris gallopavo) and guinea
fowl (Numida meleagris) are due to Tyndall scattering by protein particles.
Melanin pigments behind the particles
intensify the blue. The blue color in the
feathers of the kingfisher (Halcyon), blue
tit (Parus caeruleus), parrots, parakeets,
and many other birds is due to Tyndall
scattering by minute air-filled cavities
within the keratin of the barbs. Purple is
sometimes produced in feathers by the
combined action of Tyndall blue over a
background of reddish-brown pigment
(Fox and Vevers, 1960).
Development and Differentiation of
Feathers
The feather germ is an integrated developmental system consisting of three
components of different embryonic origin:
the epidermis of ectodermal origin, which
gives rise to the keratinized feather; the
dermal papilla, which produces the pulp;
and melanoblasts of neural crest origin
(Lillie and Wang, 1941). Following either
natural molting or plucking, a new feather
arises under the inductive influence of the
dermal papilla at the bottom of the
feather. The epidermal "collar", surrounding the upper half of the papilla, is the
formative center for the feather. On the
dorsal surface of this cylindrical structure
the rachis (or shaft) forms, and ridges
which are destined to form the barbs arise
in the ventral half; as they elongate by
proliferation from below they become oriented tangentially, so that the base of each
barb eventually is rooted in the rachis
(Lillie and Juhn, 1932). Repeated mitotic
divisions of the melanoblasts occur during
this period of barb-cell elongation, and as
the melanoblasts are transformed into melanocytes (in feathers or parts of feathers
which are to be pigmented) pigment granules and melanosomes are either injected
by melanocytes into barb cells (Strong,
1902) or blebed off and engulfed by the
developing barb cell (Watterson, 1942).
Feathers are pigmented first at the apical
ends of the barbs and as keratinization and
elongation proceed the pigmentation progresses toward the pulp and from apex to
base of the feather.
As distal portions of the feather complete their growth, the sheath splits and
the epidermal cylinder opens ventrally and
unrolls into the familiar, flat, bilateral
vane [for further details about this and
other aspects of development in feathers,
see Chap. 15, Lillie's Development of the
Chick (Hamilton, 1952)]. The finished
feather is a completely keratinized, nonliving structure, but is attached at its base
to the papilla which can repeat the entire
process of forming a new feather under
appropriate circumstances.
Genetic Contributions. Although the
melanoblasts of all birds have much in
common, as in the way they migrate and
respond to developmental processes, it is
obvious that there are difFerent phenotypic
expressions among the species and breeds.
Most information relating to genetic
determination of color and pattern comes
from studies of domestic fowl (Gallus). It
has been well established by a variety of
grafting techniques that melanocytes in-
CONTROL OF COLOR IN BIRDS
variably produce in host feathers the specific color, color pattern, or lack of color
which is characteristic of the donor breed
(Wilier and Rawles, 1940; Rawles, 1948).
Even grafts of melanogenic skin of American robin (Turdus migratorius) tissue to
White Leghorn chicken embryos produced
robin-color in feathers of the host; the
pigment was produced by donor (robin)
melanoblasts which had migrated from the
grafted tissue into the developing host
feather germs (Rawles, 1939).
There is considerable variability in genetically-determined reactivity of birds to
hormones; a few examples will serve to
illustrate this fact (see Willier, 1942). In
Brown Leghorn chickens the feather germ
of either male or female can react to female steroids but not to male steroids. On
the other hand, the Sebright bantam maintains a henny-type plumage in both sexes
in the presence of either male or female
hormones; gonadectomy of both males and
females leads to the formation of cocktype plumage (Roxas, 1926). A third type
is found in Reeves pheasant (Syrmaticus
reevesi) in which feather follicles genetically male and those genetically female
react differently to male and female hormones (Danforth, 1937). The English
sparrow (Passer domesticus) is yet another
variant where sexual differences in
plumage appear to be determined by purely genetic factors and sex hormones are
without effect (Keck, 1934). Finally, a curious situation appears to exist in Wilson's
phalarope (Steganopus tricolor) where the
male hormone, testosterone, causes brown
pigment to be deposited in feathers of
males, a pattern usually seen only in the
female of the species (Johns, 1964).
Hormonal effects. The actions of hormones on synthesis and deposition of melanin are rather well established, but in
contrast, their effects on other pigments
are largely unexplored. The differentiation
of the genetically specific melanoblast is
controlled in large part by hormones
(Trinkaus, 1953). Both the form and the
color of melanin granules have been
525
shown to be under hormonal control
(Trinkaus, 1948, 1953).
The mechanisms by which hormones induce melanogenesis by feather melanoblasts,
as a preliminary to the transfer of melanin granules to the developing barb cells are
poorly understood, There is, however,
strong evidence to suggest that hormonal
effects are mediated through the cellular
substrate surrounding the melanoblasts
and are not the result of a direct action of
the hormones on the melanoblasts themselves (Markert, 1948; Trinkaus, 1948,
1950).
The deposition of female-type salmon
pigment in feathers of male (and caponized) Brown Leghorn fowl is induced by
estrogen (Juhn, Faulkner, and Gustavson,
1931) which acts in a local manner, affecting only feathers in the vicinity of the
injection (Greenwood and Blyth, 1935;
'Espinasse, 1939). In Silver Campine fowl,
by contrast, salmon-colored feathers appear only in castrates, and administration
of either estrogens or androgens inhibits
salmon coloring and returns the plumage
to normal type. In certain other crossbreeds of fowl (Quinn and Burrows, 1935)
and in male pheasants (Vevers, 1954),
there is an increase in the amount of melanin pigment deposited in regenerating
feathers after the administration of estrogen. In African weaver birds (Ploceidae)
estrogen blocks the development of the
dark nuptial-type plumage which can be
induced by luteinizing hormone (LH) and
gonadotropin from pregnant mare's serum
(PMS) (Witschi, 1936, 1961; see below).
Androgens have been implicated both in
sexual dimorphism and seasonal plumage
changes. As noted earlier, in adult male
Wilson's phalarope, testosterone ( but not
estrogen) causes the deposition of brown
pigment in regenerating feathers (Johns,
1964). Testosterone produces a local pigmentation of the beak in the English sparrow (Pfeiffer, Hooker, and Kirchblaum,
1944) and in the bobolink (Dolichonyx
oryzivorus) (Engels, 1959). However, in
Brown Leghorn fowl testosterone (testis
hormone) has no effect on the pigmentary
526
CHARLES L. RALPH
pattern of males (Juhn and Gustavson,
1930), despite the fact that it causes explants to differentiate red melanoblasts
(Hamilton, 1941) and blocks the expression of salmon pigmentation in both sexes
of Silver Campine fowl (Nickerson,
19466). In the laughing gull (Larus atricilla) testosterone causes black head
feathering and red coloring of the beak,
features that are characteristic of both
sexes in breeding season (Noble and
Wurra, 1940). The male black-headed gull
(Larus ridibundus) fails to change its
head feathers from white to dark brown
following castration (Van Oordt and
Junge, 1933).
Sex hormones also can influence the deposition of carotenoids. In both sexes of
the starling the beak is colored black by
melanin out of breeding season, but is a
bright orange-yellow color due to carotenoid during breeding season. Castration
produces black beaks in both sexes, which
are changed to yellow by injection of androgens but not of estrogens (Witschi,
1961).
Thyroxine decreases the amount of
black pigment deposited in the English
sparrow (Miller, 1935), changes the pattern of feathers in Guinea fowl (Numida
meleagris) (Hardesty, 1935), and increases
the dark pigment in Brown Leghorn fowl
(Juhn and Barnes, 1931; Blivaiss, 1947).
In all cases concomitant structural changes
are caused by thyroxine. Thyroidectomy
of Brown Leghorn roosters is followed by
replacement of the normal black, brown,
red, and yellow melanins by a light reddishbrown pigment. The rate of growth of
feathers and degree of barbulation also are
decreased (Blivaiss, 1947).
The effects of pituitary hormones have
been found, in almost all cases, to be mediated secondarily through gonads (Van
Oordt and Junge, 1933; Hill and Parkes,
1935; Noble and Wurm, 1940) or, in a few
instances, through thyroids (Miller, 1935;
Parkes and Selye, 1937). The first indication that hormones of the pituitary gland
could extra-gonadally affect the pigmentation of feathers came from the studies by
Witschi (1936) on African weaver birds
(Euplectes). He found that castrated
males continued to undergo plumage
changes, alternating bright and dull
plumage in the manner seen in the intact
bird (Witschi, 1955). Furthermore, the
black pigmentation characteristic of males
in nuptial plumage could be produced in
normal or castrated birds (in basic
plumage) of either sex by intramuscular
injections of beef pituitary extracts. Further studies of pituitary extracts, including
that of the turkey, revealed that several
species of the so-called weaver birds (E.
franciscanus, E. afer* Quelea quelea, Steganura paradisaea**) following plucking,
would deposit dark pigment in response to
their injection (Witschi, 1937, 1940).
Fractionation and purification of extracts showed that it was the luteinizinghormone (LH) activity which had the
greatest potency in causing melanin pigmentation (Witschi, 1940). Human chorionic gonadotropin (HCG) (Segal, 1957)
and PMS gonadotropin (Witschi, 1940),
both of which have LH activity, gave positive responses. Follicle-stimulating hormone (FSH) was effective but only at very
high levels (Segal, 1957). Whereas LH
increased the activity of tyrosinase (accompanying pigmentation) in regenerating
feathers of 5. paradisaea, FSH, melanocytestimulating hormone (MSH), and adrenocorticotropic hormone (ACTH) did not
(Hall and Okazaki, 1966). Thus, this response of weavers is rather specific and has
been used as an assay for LH (ICSH)
(Witschi, 1940; Segal, 1957; Thapliyal and
Saxena, 1961). This assay is also reported
to be very sensitive, detecting as little as 5
jag of LH. However, Ortman (1967) in a
comparative study of three species of
weavers failed to confirm the levels of sensitivity claimed by Witschi and found responsiveness to be variable.
* Witschi used afra as the species name, but the
gender is wrong and is correctly afer.
" T h i s bird does not weave a nest but is in fact
a brood parasite; it is in the subfamily Viduinae of
the family Ploceidae, whereas Euplectes and Quelea
are in the subfamily Ploceinae.
CONTROL OF COLOR IN BIRDS
Pigment is deposited in feathers within
12-24 hr after injection of a threshold
amount of LH in S. paradisaea, but not
until 30-54 hr after in E. afer. In either
case the pigment appears well after the
exogenous hormone would have been removed from circulation. LH induced a
transient proliferation of melanocytes, generally not lasting more than 24 hr. PMS,
on the other hand, caused melanization to
persist for at least 72 hr in S. paradisaea
and for 96 hr in E. afer (Ralph, Grinwich,
and Hall, 1967a).
The mode of action of these agents in
causing melanization of feathers remains to
be discovered. Their effects are not mediated by way of the gonads, as noted above
(see also Thapliyal and Saxena, 1961). In
fact, estrogenic (but not androgenic) hormones inhibit the inductive action of gonadotropins on feathers in weavers (Witschi, 1936). However, very extensive attempts to demonstrate a local or direct
action of LH upon regenerating feathers
in two species of African finches (E. afer
and S. paradisaea) failed completely
(Hall, Ralph, and Grinwich, 1965). Additionally, LH does not appear to act via the
hypothalamus, adrenal, thyroid, or pineal
(Ralph, Grinwich, and Hall, 19676).
Seasonal Color Change. Many birds
show no obvious seasonal change of colors
of adult plumage. In others a semblance of
seasonal change is secondarily established
without involving a molt and replacement
of feathers; by wear or fading, the feathers
change their appearance (Witschi, 1961;
Smith, 1965). Melanin pigments seem to
give feathers mechanical strength; pale
portions of feathers abrade away, leaving
dark portions little affected, thus making
the bird appear darker (Parkes, K. C., personal communication). In some instances
the beak or iris will show a seasonal difference in color.
Humphrey and Parkes (1959) have classified the patterns of succession of adult
plumage in terms of number of molts and
plumage types per cycle as follows:
(1) One molt and one plumage per cy-
527
cle. The length of the cycle is generally a
year and there are three common variations of the basic plumage of the two
sexes: (a) males and females wear dull
basic plumage at all times (e.g., wrens,
Thryothorus and Troglodytes), (b) the
male wears bright basic plumage and the
female a dull one rather like that of the
juvenile (e.g., red-winged blackbird, Agelaius phoeniceus), or (c) both sexes wear
a bright basic plumage quite different in
appearance from that of the juvenile bird
(e.g., emperor goose, Anser canagica; European robin, Erithacus rubecula).
(2) Male with two molts and plumages
per cycle, female with one. Certain male
weaver birds (Pyromelana, Euplectes,
Quelea) are considered by Witschi (1935,
1936) to have two plumages and molts per
cycle while the females have only one, but
Humphrey and Parkes (1959) suggest
that this needs more study.
(3) One complete and one partial molt
per cycle in both sexes. This is a very
common pattern. The complete molt
varies in temporal position and duration;
the partial molt varies in extent as well as
in position and duration. The latter may
involve only a few feathers or nearly all of
them and it is generally the body feathers
that are most affected. In some species the
female may change relatively little but in
others she will be decidedly "brighter"
than is either sex in the basic plumage. In
many others the alternate plumage of both
sexes is strikingly different from the basic plumage (e.g., Podicipedidae, Alcidae).
On the other hand, both the alternate and
basic plumages in both sexes are "dull"
and practically identical in several species
of birds (e.g., some waterfowl).
(4) Two complete molts per cycle. Very
few species are known to have two complete molts per cycle. This condition is
found in the sharp-tailed sparrow (Ammospiza caudacuta), which shows little sexual
and seasonal dimorphism, and the bobolink, the male wearing a bright alternate
plumage which is replaced by a basic
plumage like that of the female; the basic
528
CHARLES L. RALPH
and alternate plumages of the female are
almost identical.
(5) Three molts and three plumages
per cycle. A few species have a third molt
and supplement or add specialized plumage. This is the case for the male of
the ruff (Philomachus pugnax) and some
species of ptarmigan (Tetraonidae).
Humphrey and Parkes (1959) believe
that the plumages of most birds probably
were not originally sexually, seasonally, or
developmentally dimorphic (or polymorphic) but were dull or subdued in color
and pattern. Species considered "primitive" have but one molt and one plumage
per year. The bright plumages are considered as "added" when acquired by partial
molts or "special" where molts occur only
in the male.
Since the plumage comprises approximately 10% of the total weight of the bird,
replacement of the plumage requires a
considerable expenditure of energy. Primitively this expense probably was budgeted
over a long period of time, and still tends
to be in certain non-migratory birds of
tropical latitudes, such as parrots. For the
majority of modern birds, however, selection pressures associated with migration,
reproduction, regulation of temperature,
or development may have made it necessary that many feathers be repaced in a
short period of time (Humphrey and
Parkes, 1959). Such pressures appear to
have been responsible for the great variety
of morphology, color, and pattern in
plumages of birds.
REFERENCES
Blivaiss, B. B. 1947. Interrelations o£ thyroid and
gonad in the development of plumage and other
sex characteristics in Brown Leghorn roosters.
Physiol. Zool. 20:67-107.
Bohren, B. B., R. M. Conrad, and D. C. Warren.
1943. A chemical and histological study o£ the
feather pigments of domestic fowl. Am. Naturalist 77:481-518.
Carr, J. G. 1957. Internal structure of avian melanin granules: an electron microscope study. Quart.
J. Microscop. Sci. 98:159-162.
Chapin, J. P. 1939. Birds of the Belgian Congo II.
Bull. Am. Mus. Natural Hist. 75:217.
Church. A. H. 1893. Turacin: a remarkable animal
pigment containing copper. Nature 48:209-211.
Cohen, J. 1966. Feathers and patterns, p. 1-38. In
M. Abercrombie and J. Brachet, [ed.], Advances
in morphogenesis, Vol. 5. Academic Press, New
York.
Danforth, C. H. 1937. An experimental study of
plumage in Reeves Pheasants J. Exp. Zool.
77:1-11.
Dorris, F. 1938. The production of pigment in vitro
by chick neural crest. Roux' Arch. Entw.mech. Org. 138:323-334.
Engels, W. L. 1959. The influence of different day
lengths on the testes of a transequatorial migrant, the bobolink (Dolichonyx oryzivorus), p.
759-766. In Photoperiodism and related phenomena in plants and animals. Publ. 55, Am. Assoc.
Adv. Sci., Washington, D. C.
'Espinasse, P. G. 1939. The developmental anatomy
of the Brown Leghorn breast feather, and its
reaction to oestrone. Proc. Zool. Soc. London
109:247-288.
Fischer, H., and F. Linder. 1925. Zur Kenntnis der
natiirlichen Porphyrine. XIV. l)ber Ooporphyrin und seine Uberfuhrung in den Ester des
Hamins. Hoppe—Seyler's Z. Physiol. Chem.
142:141-154.
Fitzpatrick, T. B., and A. Kukita. 1959. Tyrosinase
activity in vertebrate melanocytes, p. 489-524. In
M. Gordon, [ed.], Pigment cell biology. Academic Press, New York.
Fox, D. L. 1953. Animal biochromes and structural
colors. University Press, Cambridge, England.
Fox, H. M., and G. Vevers. 1960. The nature of
animal colours. Macmillan, New York.
Frank, F. 1939. Die FSrbung der Vogelfeder durch
Pigment und Struktur. J. Ornithol. (Berlin)
87:426-523.
Gordon, M., [ed.] Pigment cell growth (see preface). Academic Press, New York.
Greenwood, A. W., and J. S. S. Blyth. 1935. Variation in plumage response of Brown Leghorn
capons to oestrone I. Intramuscular injection.
Proc. Roy. Soc, London, B, 118:97-132.
Hall, P. F., and K. Okazaki. 1966. The action of
interstitial cell stimulating hormone upon avian
tyrosinase. Biochemistry 5:1202-1208.
Hall, P. F., C. L. Ralph, and D. L. Grinwich. 1965.
On the locus of action of interstitial cellstimulating hormone (ICSH or LH) on feather
pigmentation of African weaver birds. Gen.
Coinp. Endocrinol. 5:552-557.
Hamilton, H. L. 1941. Influence of adrenal and sex
hormones on the differentiation of melanophores
in the chick. J. Exp. Zool., 88:275-305.
Hamilton, H. L. 1952. Lillie's development of the
chick, 3rd ed. rev. Holt, Rinehart, and Winston,
New York. 624p.
Hardesty, M. 1935. The effect of thyroxin injections
upon the feather of the Guinea fowl. J.
Exptl. Zool. 71:389-419.
Hill, R. T., and A. S. Parkes. 1935. Hypophysectomy of birds. IV. Plumage changes in the hy-
CONTROL OF COLOR IN BIRDS
pophysectomized fowls. Proc. Roy. Soc. London,
B, 11:202-209. V. Effect of replacement therapy
on the gonads, accessory organs and secondary
sex characteristics of hypophysectomized fowls.
Ibid. 11:210-218.
Holmes, A. 1935. The pattern and symmetry of
adult plumage units in relation to the order and
locus of origin of the embryonic feather papillae.
Am. J. Anat. 56:513-537.
Humphrey, P. S., and K. C. Parkes. 1959. An
approach to the study of molts and plumages.
The Auk 76:1-31.
Johns, J. E. 1964. Testosterone-induced nuptial
feathers in phalaropes. Condor 66:449-455.
Juhn, M., and B. O. Barnes. 1931. The feather
germ as indicator for thyroid preparations. Am.
J. Physiol. 98:463-466.
Juhn, M., and R. G. Gustavson. 1930. The production of female genital subsidiary characters by
injection of human placental hormones in fowls.
J. Exptl. Zool. 56:31-61.
Juhn, M., G. H. Faulkner, and R. G. Gustavson.
1931. The correlation of rates of growth and
hormone threshold in feathers of fowls. J. Exptl.
Zool. 58:69-111.
Keck, W. N. 1934. The control of the secondary sex
characters in the English sparrow, Passer
domesticus (Linnaeus). J. Exptl. Zool. 67:315347.
Kritzler, H. 1943. Carotenoids in the display and
eclipse plumages of bishop birds. Physiol. Zool.
16:241-255.
Lillie, F. R., and M. Juhn. 1932. The physiology of
development of feathers. I. Growth-rate and pattern in the individual feather. Physiol. Zool.
5:124-184.
Lillie, F. R., and H. Wang. 1941. Physiology of
development of the feather. V. Experimental
morphogenesis. Physiol. Zool. 14:103-135.
Markert, C. L. 1948. The effects of thyroxin and
antithyroid compounds on the synthesis of pigment granules in chick melanoblasts cultured in
vitro. Physiol. Zool. 21:309-327.
Mason, C. W. 1923. Structural colors in feathers. II.
Iridescent feathers. J. Phys. Chem. 27:401-447.
Miller, D. S. 1935. Effects of thyroxin on plumage
of the English sparrow, Passer domesticus. J.
Exptl. Zool., 71:293-309.
Nickerson, M. 1946a. Relation between black and
red melanin pigments in feathers. Physiol. Zool.
19:66-77.
Nickerson, M. 1946b. Conditions modifying the expression of silver in the Silver Campine fowl.
Physiol. Zool. 19:77-83.
Noble, G. K., and M. Wurm. 1940. The effects of
hormones on the breeding of the laughing gull.
Anat. Rec. 78 (Suppl.): 50-51.
Ortman, R. 1967. The performance of the Napoleon weaver, the orange weaver, and the paradise
whydah in the weaver finch test for luteinizing
hormones. Gen. Comp. Endocrinol. 9:368-373.
529
Parkes, A. S., and H. Selye. 1937. The endocrine
system and plumage types: I. Some effects of
hypothyroidism. J. Genetics 34:297-306.
Pfeiffer, C. A., C. W. Hooker, and A. Kirchbaum.
1944. Deposition of pigment in the sparrow's bill
in response to direct applications as a specific
and quantitative test for androgen. Endocrinology 34:389-399.
Quinn, J. P., and W. H. Burrows. 1935. The
influence of female sex hormone on the expression of plumage color genes in crossbred fowls. J.
Heredity 26:299-303.
Ralph, C. L., D. L. Grinwich, and P. F. Hall.
1967a. Studies of the melanogenic response of
regenerating feathers in the weaver bird: comparison of two species in response to two gonadotrophins. J. Exptl. Zool. 166:283-288.
Ralph. C. L., D. L. Grinwich, and P. F. Hall.
1967b. Hormonal regulation of feather pigmentation in African weaver birds: The exclusion of
certain possible mechanisms. J. Exptl. Zool.
166:289-294.
Rawles, M. E. 1939. The production of robin pigment in White Leghorn feathers by grafts of
embryonic robin tissue. J. Genetics 38:517-532.
Rawles, M. E. 1948. Origin of melanophores and
their role in development of color patterns in
vertebrates. Physiol. Rev. 28:383-408.
Roxas, H. A. 1926. Gonad cross-transplantation in
Sebright and Leghorn fowls. J. Exptl. Zool.,
46:63-119.
Schmidt, W. J. 1952. Wie entstehen die Schillerfarben der Federn? Naturwissenschaft 39:313-318.
Schmidt, W. J., and H. Ruska. 1961. Electronmikroskopische Untersuchung der Pigmentgranula in den Schillernden Federstrahlen der Taube
Columba trocaz H. Z. Zellforsch. 55:379-388.
Segal, S. J. 1957. Response of weaver finch to
chorionic gonadotrophin and hypophysial luteinizing hormone. Science 126:1242-1243.
Smith, L. H. 1965. Changes in the tail feathers of
the adolescent lyrebird. Science 147:510-513. (See
note, Science 149:565).
Strong, R. M. 1902. The development of the definitive feather. Bull. Museum Comp. Zool. (Harvard) 40:145-185.
Thapliyal, J. P., and R. N. Saxena. 1961. Plumage
control in Indian weaver bird (Ploceus philippinus). Naturwissenschaften 48:741-742.
Trinkaus, J. P. 1948. Factors concerned in the
response of melanoblasts to estrogen in the
Brown Leghorn fowl. J. Exptl. Zool. 109:135-170.
Trinkaus, J. P. 1950. The role of thyroid hormone
in melanoblast differentiation in the Brown Leghorn. J. Exptl. Zool., 113:149-178.
Trinkaus, J. P. 1953. Estrogen, thyroid hormone,
and the differentiation of pigment cells in the
Brown Leghorn, p. 73-91. In M. Gordon, [ed.].
Pigment cell growth. Academic Press, New York.
Van Oordt, G. J., and G. C. A. Junge. 1933.
Die hormonal Wirkung der Gonaden auf Sommer—und Prachtkleid. I. Der Einfluss des Kastra-
530
CHARLES L. RALPH
tion bei mannlichen Lachmowen. Roux' Arch.
Entw.-mech. Org. 128:166-180.
Vevers, H G. 1954. The experimental analysis of
feather pattern in the Amherst pheasant, Chrysolophus amherstias (Leadbeater). Trans. Zool.
Soc. London 28:305-348.
Voitkevich, A. A. 1966. The feathers and plumage
of birds. October House, New York.
Volker, O. 1937. Ueber fluoreszierende gelbe Federpigmente bei Papageien eine neue Klasse von
Federfarbstoffen. J. Ornithol. (Berlin) 85:136-146.
Volker, O. 1939. Zur Kenntnis des Porphyrins in
Vogelfedern. Hoppe-Seyler's Z. Physiol. Chem.
258:1-5.
Watterson, R. L. 1942. The morphogenesis of down
feathers with special reference to the developmental histories of melanophores. Physiol.
Zool. 15:234-259.
Willier, B. H. 1942. Hormonal control of embryonic
differentiation in birds. Cold Spring Harbor
Symp. Quant. Biol. 10:135-144.
Willier, B. H., and M. Rawles. 1940. The control of
feather color pattern by melanophores grafted from one embryo to another of a different
breed of fowl. Physiol. Zool. 13:177-201.
With, T. K. 1957. Uroporphyrin from turacin: a
simplified method. Nature 179:824.
Witschi, E. 1935. Seasonal sex characters in birds
and their hormonal control. Wilson Bull.
47:177-188.
Witschi, E. 1936. Effect of gonadotrophic and oestrogenic hormones on regenerating feathers of
weaver finches (Pyromelana franciscana). Proc.
Soc. Exptl. Biol. Med. 35:484-489.
Witschi, E. 1937. Comparative physiology of the
vertebrate hypophysis (anterior and intermediate
lobes). Cold Spring Harbor Symp. Quant. Biol.
5:180-189.
Witschi, E. 1940. The quantitative determination of
follicle stimulating and Iuteinizing hormones
in mammalian pituitaries and a discussion of the
gonadotropic quotient, F/L. Endocrinology
27:437-446.
Witschi, E. 1955. Vertebrate gonadotropins. Mem.
Soc. Endocrinol. 4:149-165.
Witschi, E. 1961. Sex and secondary sexual characters, p. 115-168. In A. L. Marshall, [ed.], Biology
and comparative physiology of birds, Vol. 2.
Academic Press, New York.