A.M. ZOOLOCIST, 12:63-76 (1972).
Functional Significance of Vertebrate Integumental Pigmentation
MAC E. HADLEY
Department of Biological Sciences, University of Arizona,
Tucson, Arizona 85721
SYNOPSIS. Pigment cells and their synthesized products play an important functional
role in the skin of most all vertebrates, from cyclostomes to man. Both dermal and
epidermal pigment cells function in physiological and morphological color changes and
provide the cellular basis for vertebrate pigment patterns and differences in racial
coloration. Epidermal melanization is of particular importance in homeotherms in the
regulation of seasonal pelage and feather color changes. In addition, melanin pigmentation may: have a photoprotective function, influence vitamin D synthesis in the skin,
protect or influence nervous system function, affect heat absorption and conservation,
play an intracellular homeostatic role in the skin and (by leucocytic transport)
elsewhere in the body, and provide a structural element to the integument. A
consideration of the comparative evolution of the vertebrate integumental pigmentary
system may be necessary for a proper interpretation of the supposed roles ot melanin
and other integumental pigments.
"The color-relations of earth, sky, water,
and vegetation are practically the same
the world over, and one may read on an
animal's coat the main facts of his habits
and habitat, without ever seeing him in his
home."
will be shown to play a number of diverse
physiological roles. A number of older
monographs (Poulton, 1890; Beddard,
1892; Thayer, 1909; Pycraft, 1925; Parker,
1948; Cott, 1957; Portmann, 1959) have discussed the functions of animal pigmentation. The recent nature of the references
provided in the present review suggests,
however, that much more observation and
experimentation is needed to fully appreciate the multiplicty of integumental pigment function in vertebrates.
Abbott H. Thayer, 1909
INTRODUCTION
Pigments are common to the integuments of most vertebrates whether they be
haired, feathered, scaled, or smooth
skinned. These pigments are generally localized in the skin within cellular components referred to as chromatophores.
The functioning of these chromatophores
and their contained chromatic components
is the topic of tills review.
Animal pigmentation is adaptive in
nature and has undoubtedly been selected
for to better fit the species to the particular
environment. Integumental pigmentation
NATURE OF INTEGUMENTAL PIGMENTATION
General Nature of Skin Coloration
The color of the vertebrate integument
is due to the presence of pigments which
include the hemoglobins found within the
vascularity of the dermis and other pigments which are generally localized within
specialized cells referred to as chromatophores (Parker, 1948). These pigment
cells may contain one or a number of pigments: carotenoids, pteridines, guanine
and related compounds, melanins, and
others. Pigment deposits of a diverse
nature may be present in the skin under
I would like to thank Dr. R. D. Guthrie and R.
G. Petocz of the University of Alaska and the
University of Calgary, respectively, for the use ot
Figures 1 and 2 used in the text. These figures
appeared in The American Naturalist 104:585-588,
and permission for the use of these figures was
granted by the University of Chicago Press.
63
64
MAC E. HADLEY
certain pathological conditions or may appear during certain drug administrations
(Rubin, 1968). Structural coloration (not
due to pigments) may result from the refraction and reflection of light from the
surface of the skin, as in feathers or in the
tail of some lizards. The present discussion
will mainly concern itself with chromatophore pigments. The biochemistry and
nature of animal pigmentation is discussed
in detail by Fox and Vevers (1960).
Source, Synthesis, and Control
Pigment cells are of neural crest origin
(DuShane, 1935; Rawles, 1948). The prospective
chromatophores
(propigment
cells) migrate to either or both the dermis
or epidermis where as chromatoblasts they
then embark upon specific synthetic processes to become either melanophores
(containing melanins), iridophores (reflecting cells containing either guanine,
hypoxanthine, or adenine or a combination of these), or yellow- (xanthophores)
or red- (erythrophores) colored cells (containing either or both yellow- to redcolored carotenoid or pteridine pigments
(Bagnara, 1966).
Almost without exception, the red or
yellow pigment cells and the reflecting
cells are restricted to the dermis. The melanophores may be present in either the
dermis or the epidermis. It is the special
attribute of the epidermal melanophores
that they not only synthesize melanin but
that they may release (by what has been
referred to as a cytocrine process; Masson,
1948) this melanin into surrounding epidermal cells (e.g., keratinocytes). This melanin may then play an important role as a
sun screen or in the development of the
specific patterns of epidermal melanization
characteristic of most vertebrates.
Whereas the red and yellow pigment
cells and iridophores of poikilotherms play
important functional roles in skin coloration, the epidermal melanocytes of homeotherms by virtue of the fact that they can
produce a number of variously-colored melanins (brown to black eumelanins and
yellow to red phaeomelanins) provide the
basis for the array of red, yellow, brown, or
black feathers or hairs that are characteristic of warm-blooded vertebrates.
Hormonal stimuli from a number of endocrine sources (pituitary, thyroid, gonads,
adrenals) play a dominant role in the
control of chromatophores and skin coloration (Snell, 1967). Nervous stimuli directly
innervating chromatophores and/or regulating the release of hormones play an important role in some poikilotherms (Bagnara and Hadley, 1969). Whether some
pigment patterns in adult reptiles (such as
snakes) are solely under a genetic rather
than an additional endocrine or other control has not been determined.
Seasonal alterations in pigment cell activity are an important aspect of the ability
of an animal to conform to the seasonal
changes in environmental conditions. Control of integumental pigmentation is generally a dynamic rather than a static process and this accounts for the ability of
such an animal as the varying hare (Lepus
americanus) to be able to make a color
change from a brown summer pelage to a
white winter coat (Grange, 1932; Lyman,
1943). Sun tanning in humans is another
example. Ontogenic changes in integumental pigmentation are important as in
the development of the nuptial coloration
of the skin associated with the sexual activity of some vertebrates. The greying of
hair of man and other mammals is a common phenotypic characteristic of older
age, but its particular physiological role or
basis is not understood.
Comparative Morphology and Phylogeny
The presence and anatomical distribution of pigment cells within the vertebrate
integument is somewhat variable (Elias
and Bortner, 1957). Xanthophores or erythrophores, or both, are present in elasmobranchs, teleosts, amphibians, and reptiles
but are absent in birds and mammals. The
reflecting cells may have a similar distribution and although present in the irises
of some birds (Chiasson et al., 1968) are
SIGNIFICANCE OF VERTEBRATE PIGMENTATION
absent from the integument of homeotherms. Dermal melanophores are present
in the integument of representatives of all
vertebrate groups but may be absent (at
least in some anatomical sites) in some
specific species (e.g., the sea turtle, Caretta
caretta; Hadley, personal observations).
Epidermal melanophores are present in
the epidermis of some members of each
vertebrate class. They have but seldom
been described in the epidermis of teleosts
(Parker, 1940) and are clearly absent from
the epidermis of certain hylid frogs. It is
not known whether in all species their
presence is always associated with an active
cytocrine activity (Masson, 1948). Whether epidermal melanophores are seasonally
inactive in the feather follicles of certain
species of birds (e.g., Great Horned Owl,
ptarmigan) which, like the varying hare,
have a winter plumage color change from
brown to white is unknown.
CONCEALING COLORATION
The ability of animals to adjust the color of their skin to match the general color
of the environment is referred to as color
resemblance or protective or cryptic coloration. It may be a fast color change response involving the rapid movements of
pigment organelles within chromatophores
(Bagnara et al., 1968; Hadley and Bagnara, 1969) or a slower color change resulting from a change in the amount of pigment present in the integument. The rapid
physiological color changes or slower morphological color changes allow, therefore,
for both immediate as well as seasonally
oriented integumentary pigment changes.
Where background matching may not appear to be an adaptive necessity, some species may have lost all or certain components of their chromatic display. Totally
albinistic forms of fish and salamanders
are common to a cavernous existence
where light is completely absent (Eigenmann, 1909). Teleosts and chondrichthians from deep marine waters lack reflecting crystals (of guanine) in their skin.
Two species of closely related chimaerids
65
form an interesting contrast in this respect:
Hydrolaugus afjinis from deep water has a
dull-colored integument, whereas H. colliei from shallow water has a brightlyreflective skin (Nicol and van Baalen,
1968). In very deep waters the light is
apparently entirely luminescent.
Many diverse animals have evolved a
"common cryptic coloration" (Cott, 1957;
syncryptic coloration, Poulton 1890)
where all have a very similar skin color.
Many hylid frogs, tree snakes, lizards (e.g.,
Anolis carolinensis) and birds possess a
very bright green skin which well adapts
them for concealment in the green forest
foilage. Although mammals never have
green coats, the South and Central American two-toed sloth is said to overcome this
". . . handicap by allowing green algae to
take root in its fur" (Portmann, 1959). In
addition to the ability to background
adapt, some species possess elaborate integumentary pigment patterns. These patterns have their cellular basis in the specific anatomical distributions of the various
types of chromatophores present in the
skin. The patterns have been described as
obliterative or disruptive in nature (Cott,
1957). Obliterative shading involves a
counter lightening and darkening which
abolishes the appearance of roundness or
relief. Disruptive coloration is a superimposed pattern of contrasting colors and
tones serving to blur the outline and to
break up the real surface form.
Physiological Color Changes
These rapid chromatic adjustments to
the background environment are common
to nearly all poikilotherms except cyclostomes. In certain species, all chromatophore types may participate to some degree in the response. Sumner (1934,
]9S5a,b) clearly demonstrated the protective value of adaptive color change in the
mosquito fish, Gambusia patruelis, against
predatory birds and fishes. These small fish
were first adapted for long periods of time
over either a white or a black colored
background. Subsequently, they were
66
MAC E. HADLEY
transferred to a similarly colored tank or
to a contrastingly colored tank in the
presence of a predator (either a Galapagos
Penguin, a Night Heron, or a fish). Since
they had been adapted for a long period to
the previous background (and had undergone morphological color change) they
were not able to readjust their color rapidly
to the new environmental backgrounds.
Taken together, these experiments revealed that the mortality rate was about
66% for the fish that were more conspicuous because they could not readily adapt,
whereas it was only 34% for the less conspicuous background-adapted fish (Cott, 1957).
Morphological Color Changes
Morphological color changes are generally manifested in response to seasonal
changes in background conditions. Rabbits
(Grange, 1932; Lyman, 1943) and ptarmigans, for example, have white winter
coats in conformity with the snow of the
winter habitat. During the spring and summer, a dark pelage or feather change accompanies the melting of the snows. Similar results can be obtained in the laboratory by altering the day length to which the
animals are subjected (Lyman, 1943).
Morphological color changes involve
changes in the amount of pigment present
within the skin and may result from changes
in the number or synthetic activity of
the integumentary pigment cells (Sumner,
1944; Dawes, 1941; Hadley and Quevedo,
1967). Usually the color change is permanent until the animal has shed its hair or
feathers.
Concealing Coloration in Nature
Dice (1929, 1930) was apparently the
first to record the similarity in color which
exists between some races of mammals and
their variously colored environments.
Dice (1929) described a nearly white
pocket mouse from an area of white sand,
and a black wood rat and a black pocket
mouse from a nearby black lava flow.
Bradt (1932) further emphasized the close
correlation in color between the dark
races of mice and the dark-colored lava
beds upon which they lived. Dice's (1930)
suggestion that climatic factors appear to
have nothing to do with the development
of color in black and white rodents was
further confirmed by Benson (1933) in his
monograph on concealing coloration
among desert rodents. None of the physical factors of the environment, save that of
color, appeared to be correlated with the
colors of the animals. He hypothesized that
the color of the background and the process of natural selection, together with the
factor of isolation, may be important in
determining the color of mammals.
Similar correlations between pelage coloration of mammals and environment have
been made by numerous other workers
(Dice and Blossom, 1937; Stebler, 1939;
Dice, 1940; Blair, 1941, 1947; Hooper,
1941; Hall and Hoffmeester, 1942; Hardy,
1945; Baker, 1960). It is interesting that
Sumner (1921; Sumner and Swarth, 1924),
who did so much in demonstrating the
biological effectiveness of protective coloration, originally failed to come to such a
conclusion in his earlier studies on mammals. The White Sands of New Mexico
provide further striking examples of concealing coloration in both lizards and frogs
(Stroud, 1949). The gaiter snakes (Thamnophis sirlalis) of Wizard Island, Crater
Lake, Oregon, are jet black (Blanchard
and Blanchard, 1941) in conformity with the
nature of the black lava upon which they
live; they contrast with the brightly striped
members of the same species that live in
and around the surrounding shores of the
lake (Fitch, 1941).
The fidelity with which most species of
animals color-match has been clearly determined by objective measurements (Hutchinson and Larimer, I960; Norris and
Lowe, 1964). The "effectiveness of selection
by owls of deer mice (Pcromyscus rnanicu-
latus) which contrast in color with their
background" has been demonstrated in the
studies by Dice (1947).
According to Allee et al. (1919), however, the brilliant colors of the coral snake
SIGNIFICANCE OF VERTEBRATE PIGMENTATION
FIG. 1. Imitation canines of three artiodaclyl species. (From Guthrie and I'etocz, 1971.)
(Micruriis) are not readily explainable in
terms of prevailing theories of cryptic or
warning coloration. "Here mutation pressures that affect color patterns reign, little
controlled by environmental checks."
Gloger's rule states that animals in
warm, humid regions tend to be more
darkly pigmented than those in arid or
cool climates. A number of studies on birds
(Johnston, 1966, 1969; Barlow and
Williams, 1971) have been directed toward
determining whether color differences
vary as predicted by the ecogeographic
rule of Gloger. These and other studies
have failed to clearly rule out the possibility that the color differences noted are not
examples of protective coloration rather
than responses to a precipitation gradient.
Certainly, the studies of Dice (1947) on
deer mice (Peromyscus maniculatus) have
demonstrated, as did earlier studies, that
coloration in animals can be explained in
terms of concealment from predators
rather than by any differences in humidity.
CONSPICUOUS COLORATION
Many animals utilize skin color to advertise themselves rather than for any cryptic
purpose. Integumental pigmentation may
function to intimidate a predator or intruder or to secure a mate. Some warning
colors as in skunks or brightly colored
frogs may serve to "remind" the would-be
predator of their particularly undesirable
odoriferous or unpalatable qualities (Cott,
1957) . Some of the most interesting functions of vertebrate skin color fall within
this discussion and are still in need of further investigation (see Guthrie, 1970).
Weapon Automimicry
Guthrie (1970, 1971a,fc) and Guthrie
and Petocz (1970) have described how,
from an understanding of comparative
anatomy and behavior, it is possible to
speculate about the possible evolution of
body markings (color patterns) and behavioral gestures in vertebrates. For example, the use of the canine teeth in the
earlier phylogeny of some cervid species
can explain the occurrence of the dark
labial spot pattern in a number of contemporary deer species (Guthrie, 1970). A
dark labial spot, may have originally increased the threat value of the canine that
protruded from the lower lip. The retention of such body markings may still give
the impression that large protruding canines are present. Indeed, these black markings may have taken on threatening qualities of their own (Guthrie, 1970). The
white whisker tufts of the warthog
(Phacochoerus aethiopicus, Fig. 1-1) may
represent mimics of the elongated canines.
Similar tufts (Fig. 1-3; the Chinese water
deer, Hydropotes inermis) or light stripes
(Fig. 1-2; the chevrotain, Hyemoschus
aqunlicus) in certain artiodactyl species
68
MAC E. HADLEY
FIG. 2. Pattern similarities between ears, facial
markings, and horns of some artiodactyls. 1. Artilocapra americana; 2. Acelaphus buselaphus; 3. Hippotragus equinus; 4. Oryx beisa; 5. Pelea capreo-
lus; 6. Sylvicapra grimmia; 7. Oreamnos americanus; 8. Oreotragus orcotragus; 9. Ovibos moschatus. (From Guthrie and Petocz, 1971.)
may also suggest enlarged canines.
Thus, some mammalian species have
color patterns, or other structures, or both,
that resemble and reinforce the intraspecific weaponry (Fig. 2). This "automimicry" has probably been selected for "because duplication of the signal form results
in increased signal strength." Thus, there
has been an evolutionary "opportunity" to
modify the ears or other structures to
strengthen the visual threat of the horns
and antlers. Pigmentation of the ears (Fig.
2-1 to 2-5) or of tufts of hair (Fig. 2-6)
are common features that have evolved.
The large white patch of hair on the forehead of the musk oxen (Fig. 2-9), for
example, reinforces the large, light-colored
horn bases of older animals.
In contrast to the use of pigment markings to reinforce the specialized organs of
aggression concentrated at the anterior
end, it has been suggested (Guthrie,
1971fo) that the white rump patch of many
mammals functions as an organ of submission, a visual communication of subordination.
Guthrie (1970) has provided a most interesting discussion of the possible "evolution of human threat display organs." For
example, the human beard is considered to
have evolved as an artificial enlargement
of the jaw to increase its apparent size. It
is interesting that black seems to be considered (by Guthrie, 1970) a threat coloration, and that where there is a sexual dimorphism in body color, the male mammal is darkest. According to Guthrie
(1970), sexual differences in skin color in
human subgroups may have resulted from
selection for light skin in the female.
Hulse (1967) has determined that there is
a selection for skin color among the Japanese.
Eye Marks as Aids to Vision
Ficken et al. (1971) have presented evidence that the patterns of circles and lines
about the eyes of vertebrates may enhance
their vision and enable predaceous species
to locate and capture prey more readily.
Dark lines leading forward from the eye
SIGNIFICANCE OF VERTEBRATE PIGMENTATION
may function as aiming sites in some small
vertebrates. Light-colored circles around
the eyes may aid as light-gathering devices
for birds that feed in reduced light. Dark
patches around the eyes probably act as
reducers of glare for diurnal birds living in
bright environments. A posteroventral
black orbital spot has been noted (Nakamura and Magnuson, 1965) in a number
of scombrid fish. The possible function of
this spot was also suggested to reduce the
glare or amount of light reflected up into
the eye from the ventral rim of the orbit.
Warning (Aposematic) Coloration
Many species of fish and some frogs
(Noble, 1954) have conspicuous eye-spots
on various parts of the body, but usually
toward the tail end. Possibly, these conspicuous elements may serve to intimidate or
misdirect attack and thus facilitate escape.
Other animals utilize flash coloration to
confuse their enemies. The conspicuous,
brightly colored areas of the body are in
general normally concealed during rest but
become brightly revealed during escape
movements. Localized conspicuous colors
used for flash devices are found in some
lizards (Draco) and frogs (Hylids) and
have been well described for insects (Cott,
1957).
According to Nicol (1960) some fish
have special warning markings in association with certain poisonous properties.
Some puffer fishes possess poisonous flesh
and are brightly colored. The weaver fish
(Trachinus vipera) has poisonous glands
associated with modified fin rays and bears
a conspicuous dark "warning" mark on its
dorsal fin. The sole, Solea solea, although
itself harmless, has a similar dark patch
and shares a similar habitat and distribution.
Magnuson (1971) has suggested that the
transient coloration of the pilotfish, Naucrates ductor, is part of an agonistic display and may be aposematic. An association with an animal (in this case, a shark)
potentially dangerous to its predators is
common to some other fish which are also
69
conspicuously colored.
There may be a reversal of the normal
countershading pattern in some mammals,
such as skunks, wherein the ventrum is
dark-colored and the dorsal hair is light or
white in color. At night, white would be
the more likely warning color in those animals that are nocturnal (Searle, 1968). In
diurnal mammals, on the contrary, black is
most often used for threat display. Black
areas are often present on the appendages,
such as the ears or tail, and are displayed
under conditions of alarm. The skunk, in
contrast, has a conspicuous white tail. This
type of display has been referred to as
"dynamic" or "startling" coloration by
Young (1957).
A lluring Colors
A Brazilian chelonian, Chelus fimbriata,
has about the mouth and beneath the
throat a series of red filaments, flattened
and fleshy, which are movable and, due to
their conspicuous color and worm-like
form, may serve to lure other aquatic animals (Cott, 1957). The orange-red crown
of the King Bird, Tyrannus tyrannus, may
lure certain insects by being mistaken for a
flower (see Cott, 1957, for reference to
Keeler, 1893). According to Pycraft (1925),
the colored tails of certain snakes (Agkistrodon contortrix, A. piscivorus, and Bothrops atrox) may be used for a similar function. In contrast, although the bright dorsal
stripes of some snakes (Fitch, 1941), especially fast-moving snakes (Klauber, 1931),
are conspicuous, they have an effect of producing "color continuity" which disguises
motion. For a more complete description of
similar uses of bright colors in vertebrates,
the reader is referred to the monograph by
Cott (1957).
Color as a Social Releaser
That some bright colors of animals may
function as social releasers is a suggestion
often discussed in the literature. "A social
releaser is a device — either a property of
colour, and or shape, or a special sequence
70
MAC E. HADLEY
of movements, or, for that matter, of
sounds, or scent — specifically differentiated
to the function of eliciting a response in a
fellow member of a species" (Lorenz,
1950) . Generally speaking, conspicuous
coloration may either intimidate other
males of the species or may function to
initiate mating behavior. In many fish "the
degree of their emotion can be measured
by their coloring, which also shows whether aggressiveness, sexual excitement or the
flight urge is uppermost" (Lorenz, 1966).
The colors of these fish are their means of
social expression, apparently only appearing when they are needed.
Neil (1964) has described (and quantitated) the color changes involved in the
courtship ritual of the teleost, Tilapia
mossambica. Criteria were established to
predict the subsequent behavior of Tilapia
from its color patterns and its subsequent
color patterns from its behavior. Both color pattern and mating behavior were
found to be highly ritualized. Clark (1959,
1965) has shown that the hermaphroditic
marine teleost, Serranus subligarius, may
function as a male, or female, or both
sexes simultaneously, depending upon the
environmental situation. During spawning,
the "male fish" that chases the "female"
has bold, broad, dark, vertical bands on its
body. The fish in the female phase is unbanded and is usually larger. These fish
are capable of changing their behavorial
roles and chromatic characteristics. Many
other studies dealing with the releaser hypothesis of innate behavior in teleosts have
been described (see Tavolga, 1956, for
references). Peterman (1971) has suggested that conspicuous markings may help
coordinate movements such as schooling
and feeding. In the tuna (Euthynnus
affinis Cantor) there are three transient
color patterns or markings. These color
features are observable during feeding. It
was suggested that they might act as social
releasers to signal the presence of food to
other members of the school (Magnuson
and Prescott, 1966). Dolphins also change
color just after reacting to food (Murchison and Magnuson, 1966).
Adult males of such lizards as Eumeces
fasciatus (Fitch, 1954) or Crotophytus collaris collaris (Greenberg, 1945; Fitch,
1956) develop orange-colored jaws during
the breeding season, and it is possible that
this coloration may again function as a
social releaser among mutually aggressive
males (Fitch, 1956).
It has been suggested that the bright tail
color of lizards, such as the skinks, Eumeces fasciatus, E. laticeps, E. inexpectatus,
and others, coupled with the ease with
which the member is lost, is of definite
survival value (Poulton, 1890). This "expendable" part of the body has been considered to function as a decoy in diverting
predators from more vulnerable parts of
the body. Since the blue tail is found only
in juvenile E. fasciatus and disappears in
the adult, it is difficult to understand why
it should not be equally advantageous
throughout the life cycle. Clark and Hall
(1970) have suggested that the blue tail
color of young skinks plays an intraspecific
role, that of inhibiting attack by aggressive adult males. The red breast of the
robin is (as in lizards; Pearse, 1926) usually well hidden but is used as a threat display for other intruding robins (Lack,
1943).
THERMOREGULATORY ROLE OF INTEGUMENTAL
PIGMENTATION
As earlier described for the lizards, Anolis carolinensis (Parker and Starratt, 1904;
Wilson, 1940) and Phyrnosoma blainvillii
(Parker, 1938), most lizards that have
been studied (Atsatt, 1939; Mayhew, 1963;
Brattstrom, 1971) become light in color
in response to high temperature and take
on a dark color phase in response to low
temperature. These responses are considered to play a thermoregulatory role (Atsatt, 1939).
The continuing argument of whether
black pigmentation is an adaptation for
concealment or for heat conservation has
been discussed on several occasions by
Cowles (1958, 1959, 1967) and others
(Hutchison and Larimer, 1960; Norris and
SIGNIFICANCE OF VERTEBRATE PIGMENTATION
Lowe, 1964). Such an argument would
seem, however, to be unnecessary "unless
the presence of one function is taken to
mean that the other is excluded" (Hutchison and Larimer, 1960). Under certain environmental conditions protective color and
"protective reflectivity" (Klauber, 1939)
may be mutually beneficial; where the
chromatic conditions tend to produce opposite effects, protective coloration appears
to dominate, at least throughout the optimal activity range of the reptile. As suggested by Norris and Lowe (1964), there
may of necessity be an adaptive compromise
wherein individual animals may have to
achieve a general chromatic compromise.
Stullken and Helstand (1953) found
that the oxygen requirements of albino
mice increased at low temperatures and
this was especially so for albino mice that
were dyed black or for mice that were
naturally black (C-57 strain). This suggested that mammals bearing a darkcolored pelage would be at a thermal
disadvantage in such areas as the far
North, whereas a white pelage or plumage
would be of value in retarding heat loss.
Svihla (1956), however, found that at low
temperatures there was no difference with
respect to heat conservation between white
and dark colored rats. It was suggested
that any relationship between white coloration and white background is best explained on the basis of natural selection
for concealing coloration. Hamilton and
Heppner (1967) found that zebra finches
(Poephila castanotis) used an average of
22.9 percent less energy after they were
dyed black and exposed to artificial sunlight. Apparently, a warming of the outer
feathers of a dark bird reduces the temperature gradient from the skin of the bird to
feather surface ". . . and thus slows the loss
of metabolic heat to cold surroundings".
Cowles (1967) has suggested that it is just
as reasonable that a heated surface might
reverse the normal thermal gradient and,
therefore, place a barrier to an otherwise
excessive heat loss. Hamilton and Heppner
(1967) suggested that the color of homeothermic animals might be of considerable
71
importance in their energy budget in
nature by ". . . reducing the metabolic cost
of maintaining a constant body temperature".
Ohmart and Lasiewski (1971), in an interesting study on energy conservation in
roadrunners (Geococcyx californianus),
found that these birds could elevate their
body temperatures to normal levels, at a
reduced metabolic cost, by sunning. The
sunning behavior involves the erecting of
the cervical plumage to expose the black
skin of the interscapular apterium and the
soft black plumage of the dorsal spinal
tract. These exposed areas apparently absorb solar radiation directly due to their
dark pigmentation.
PHOTOPROTECTIVE FUNCTION OF MELANIN
The proposed role of melanin pigment
as a sun screen against the damging effects
of ultraviolet radiation has been discussed
in a number of articles (Blum, 1961; Pathak, 1967; Szabo, 1967, 1969). There is a
definite correlation between the incidence
of cancer and the geographic location and
skin color of an individual. Skin cancer is
much more likely to occur in the lightskinned rather than the darker-skinned individual. Melanin pigment in the epidermis is assumed to play a photoprotective
role in protecting against the harmful effects of actinic radiation. Mason et al.
(1960) have stated that "melanin may act
in some organisms as a biological electron
exchange polymer" and in this capacity
protect against reducing or oxidizing conditions resulting from free radical formation
induced by ultraviolet radiation. Few
workers now accept the earlier thesis of
Blum (1961) that there is little merit to
the suggestion that melanin pigment in
human skin protects against sunlight.
Melanin Pigmentation and the Synthesis of
Vitamin D
Loomis (1967) has also raised the interesting question of whether indeed the degree of skin pigmentation in the human is
72
MAC E. HADLEY
not more related to vitamin D requirements than to a photoprotetcive function.
Since the biosynthesis of vitamin D is dependent upon the activation of provitamin
present in the skin by ultraviolet rays, it
was suggested that under conditions of
meager solar radiation there has been a
natural selection for lighter-colored skins
in some geographical races of man. The
ability to become suntanned in these lightskinned groups, such as some Europeans,
during the summer would then be for protection against too great a production of
vitamin D, which in excess, he claims, is
detrimental physiologically. Similarly, the
darker skins of tropical races of man have
evolved, according to this theory, in relation to a protection against an overproduction of vitamin D.
Tropical Disease and the Homeostatic
Hole of Melanin
Wassermann (1965a) has presented a
hypothesis that tropical disease rather than
tropical climate was the major selective
factor leading to racial pigmentation. He
suggests that a primary adaptation involved an increased activity of the reticuloendothelial system (in defense against
tropical disease) resulting from a decreased adrenocortical activity. This, then,
resulted in an increased release of ACTH
and MSH with resulting hyperpigmentation.
Wassermann (1965a) has further suggested that melanin may play a role in
regulating intracellular homeostasis in the
skin and elsewhere in the body. Melanin,
acting as a stable free radical, may protect
a melanin-containing or associated tissue
against reducing or oxidizing conditions
resulting from metabolic activity (Mason
et al., 1960). Wassermann (19656) observed that in South African blacks there is
a circulation of melanin throughout the
body by an intracellular leucocytic melanin
transport. Thus, the suggested intracellular
homeostatic function of melanin can be ex-
erted elsewhere in the body. Similar observations of pigmented leucocytes were
made on blood of amphibians and reptiles
(Wassermann, 1965c).
OTHER ROLES OF INTEGUMENTAL
PIGMENTATION
Melanin and other integumentary pigments may function in a number of other
diverse and less well recognized roles.
Many fishes, for example, are silvery because of shiny layers of reflecting crystals
of guanine or related compounds (e.g., hypoxanthine, uric acid). These reflecting
layers diminish the visibility of the fish
from most fields of view because they
reflect light approximately equal to the
background light against which the fish is
seen (Denton and Nicol, 1965, 1966).
Why some salmonoids undergo a smoltification (a silvering of the skin) on their
migration to the sea is unknown. Some
insects (the Pieridae) have evolved a metabolic mechanism whereby pteridines are
deposited in the integument as a dry storage excretory product. Whether pteridines
as excretory products function primarly or
only secondarily in cuticular ornament is
unresolved (Harmson, 1966). One wonders whether the deposition of purine or
related crystals in the teleost scale might
not serve some similar physiological function during the increased metabolic activity which precedes smoltification.
Tanning of the cuticle of flies and other
insects involves deposition of a melaninlike product in the cuticle and is under
hormonal control (Fraenkel and Hsiao,
1965). This cuticular melanization may
function to strengthen the integument.
Possibly the synthesis and deposition of
melanin into epidermal cells may play a
similar role as a structural element of the
skin of vertebrates. Possibly such a function is still retained in the feather and the
hair or as a component of the integumental protuberances of some anurans (Elias
and Bortner, 1957; Elias and Shapiro,
1957).
SIGNIFICANCE OF VERTEBRATE PIGMENTATION
EVOLUTIONARY CONSIDERATIONS OF MELANIN
PIGMENT FUNCTION
It would appear that a number of theories have evolved relative to the proposed
roles of integumental pigmentation. Melanin pigmentation of the skin may have
evolved: (1) to serve as a sun screen
against the deleterious effects of ultraviolet
light, (2) to protect against an over production of vitamin D (or in the absence of
melanin to allow for the synthesis of vitamin D),
(3)
as a thermoregulatory
mechanism, (4) to provide a means for
color concealment, (5) as a consequence of
adaptation to tropical disease. Although
not mutually exclusive, the presumed roles
are considered by the various authors to
have evolved quite independently.
What is needed is a clearer understanding of the evolution of integumental pigment function. Melanin is apparently
present within the epidermis of some cyclostomes. Young (1935) noted that the
melanin pigment of the epidermis of Lampetra planeri may function as a light
screen over the central nervous system of
this cyclostome. Removal of the epidermal
melanin pigment resulted in a photosensitiveness of the underlying nerve cord. It is
interesting that in the sea urchin Diadema
(Millott, 1957) both locomotion and
spine responses vary with the degree of
dispersion of melanin in the melanophores
which lie just above the underlying photosensitive nerves which regulate spine and
body movements. Possibly, melanin pigment in early vertebrates played a role in
regulating central nervous system activity
as it does now in the invertebrate and
vertebrate retina. Melanosome movements
within integumentary melanophores is
known to regulate photophore function
(luminescence) in certain teleosts (Badcock, 1969). Secondarily, it may have
evolved other roles such as protective coloration.
REFERENCES
Allee, W. C, A. E. Emerson, O. Park, T. Park, and
73
K. P. Schmidt. 1949. Principles of animal ecology.
W. B. Saunders Co., Philadelphia.
Atsatt, S. R. 1939. Color changes as controlled by
temperature and light in the lizards of the desert
regions of southern California. Univ. Calif.
Publ. Biol. Sci. 1:237-276.
Badcock, J. 1969. Colour variation in two mesopelagic fishes and its correlation with ambient
light conditions. Nature 221:383-385.
Bagnara, J. T. 1966. Cytology and cytophysiology of
non-melanophore pigment cells. Int. Rev. Cytol. 20:173-205.
Bagnara, J. T., and M. E. Hadley. 1969. The
control of bright colored pigment cells of fishes
and amphibians. Amer. Zool. 9:465-478.
Bagnara, J. T., J. D. Taylor, and M. E. Hadley.
1968. The dermal chromatophore unit. J. Cell
Biol. 38:67-79.
Baker, R. H. 1960. Mammals of the Guadiana lava
fields Durango, Mexico. Mich. State Univ. Mus.
Publ. Biol. Ser. 1:305-327.
Barlow, J. C, and N. Williams. 1971. Colorimetric
analysis of the dorsal plumage of the red-eyed
vireo (Aves: Vireonidae) in Canada. Can. J.
Zool. 49:417.
Beddard, F. E. 1892. Animal coloration. Hazell,
Watson, and Viney, Ltd., London.
Benson, S. B. 1933. Concealing coloration among
some desert rodents of the southwestern United
States. Univ. Calif. Publ. Zool. 40:1-70.
Blair, W. F. 1941. Color variation in the spotted
ground squirrels of the Tularosa Basin, New
Mexico. Contrib. Lab. Vertebrate Genet. Univ.
Mich. 16:1-16.
Blair, W. F. 1947. Variations in shade of pelage of
local populations of the cactus-mouse (Peromyscus eremicus) in the Tularosa Basin and
adjacent areas of southern New Mexico. Contrib.
Lab. Vertebrate Biol. Univ. Mich. 37:1-7.
Blanchard, F. N., and F. C. Blanchard. 1941. The
inheritance of melanism in the garter snake
Thamnophis sirtalis sirtalis (Linnaeus), and
some evidence of effective autumn mating. Pap.
Mich. Acad. Sci. Arts Lett. 26:177-193.
Blum, H. F. 1961. Does the melanin pigment of
human skin have adaptive value? An essay in
human ecology and the evolution of race. Quart.
Rev. Biol. 36:50-63.
Bradt, G. W. 1932. The mammals of the Malpais,
an area of black lava rock in the Tularosa Basin,
New Mexico. J. Mammalogy 13:321-329.
Brattstrom, B. H. 1971. Social and thermoregulatory behavior of the bearded dragon, Amphibolurus barbatus. Copeia 1971:484-497.
Chiasson, R. B., M. E. Hadley, and S. M. Russell.
1968. Adrenergic and cholinergic mechanisms
controlling color changes of the Inca Dove
(Scardafella inca) iris. Amer. Zool. 8:818.
Clark, D. R., and R. J. Hall. 1970. Function of the
blue tail-coloration of the five-lined skink (Eumeces fasciatus) . Herpetologica 26:271-274.
Clark, E. 1959. Functional hermaphroditism and
74
MAC E. HADLEY
self-fertilization in serranid fish. Science 129:215216.
Clark, E. 1965. Mating of groupers. Natur. Hist.
74:22-25.
Cott, H. B. 1957. Adaptive coloration in animals.
Methuen and Co., London.
Cowles, R. B. 1958. Possible origin of dermal temperature regulation. Evolution 12:347-357.
Cowles, R. B. 1959. Some ecological factors bearing
on the origin and evolution of pigment in the
human skin. Amer. Natur. 93:283-293.
Cowles, R. B. 1967. Black pigmentation: adaptation
for concealment or heat conservation? Science
158:1340-1341.
Dawes, B. 1941. The melanin content of the skin of
Rana temporaria under normal conditions and
after prolonged light- and dark-adaptation. A
photometric study. J. Exp. Biol. 18:26-49.
Denton, E. J., and J. A. C. Nicol. 1965. Polarization
of light reflected from the silvery exterior of
the bleak, Alburnus alburnus. J. Mar. Biol. Ass.
U. K. 45:705-709.
Denton. E. J., and J. A. C. Nicol. 1966. A survey of
reflectivity in silvery teleosts. J. Mar. Biol. Ass.
U.K. 46:685-722.
Dice, L. R. 1929. Description of two new pocket
mice and a new woodrat from New Mexico.
Occas. Pap. Mus. Zool. Univ. Mich. 203:1-4.
Dice, L. R. 1930. Mammal distribution in the
Alamogordo region, New Mexico. Occas Pap.
Mus. Zool. Univ. Mich. 213:1-32.
Dice, L. R. 1940. The Tularosa malpais. Sci.
Month. 50:419-424.
Dice, L. R. 1947. Elfectiveness of selection by owls
of deer mice (Peromyscus maniculatus) which
contrast in color with their background. Contrib.
Lab. Vertebrate Biol. Univ. Mich. 34:1-20.
Dice, L. R., and P. M. Blossom. 1937. Studies of
mammalian ecology in southwestern North
America with special attention to the colors of
desert mammals. Carnegie Inst. Wash. Publ. No.
485.
Dushane, G. P. 1935. An experimental study of the
origin of pigment cells in Amphibia. J. Exp.
Zool. 72:1-31.
Eigenmann, C. H. 1909. Cave vertebrates of America. Carnegie Inst. Wash. Publ. No. 104.
Elias, H., and S. Bortner. 1957. On the phylogeny
of hair. Amer. Mus. Novitates 1820:1-15.
Elias, H., and J. Shapiro. 1957. Histology of the
skin of some toads and frogs. Amer. Mus. Novitates 1819:1-27.
Ficken, R. W., P. E. Matthiae, and R. Horwich.
1971. Eye marks in vertebrates: aids to vision.
Science 173:936-939.
Fitch, H. S. 1941. Geographic variation in garter
snakes of the species Thomnophis sirtalis in the
Pacific Coast region of North America. Am. Midland Natur. 26:570-592.
Fitch, H. S. 1954. Life history and ecology of the
five-lined skink, Eumcces fasciatus. Univ. Kansas
Publ. Mus. Nat. Hist. 8:1-156.
Fitch, H. S. 1956. An ecological study of the collared lizard (Crotaphytus collaris). Univ. Kans.
Mus. Nat. Hist. Publ. 8:213-274.
Fox, H. M., and G. Vevers. 1960. The nature of
animal colours. Sedgwick and Jackson, London.
Fraenkel, G.. and C. Hsiao. 1965. Bursicon, a hormone which mediates tanning of the cuticle in
the adult fly and other insects. J. Insect Physiol.
11:513-556.
Grange, W. B. 1932. The pelages and color changes
of the snowshoe hare, Lepus americanns phaeonotus Allen. J. Mammalogy 13:99-116.
Greenberg, B. 1945. Notes on the social behavior of
the collared lizard. Copeia 1945:225-230.
Guthrie, R. D. 1970. Evolution of human threat
display organs. Evol. Biol. 4:257-300.
Guthrie, R. D. 1971a. The evolutionary significance
of the cervid labial spot. J. Mammalogy
52:209-212.
Guthrie, R D. 1971 &. A new theory of mammalian
rump patch evolution. Behavior 38:132-145.
Guthrie, R. D., and R. G. Petocz. 1970. Weapon
automimicry among mammals. Amer. Natur.
104:585-588.
Hadley, M. E., and J. T. Bagnara. 1969. Integrated
nature of chromatophore responses in the in
vitro frog skin bioassay. Endocrinology 84:69-82.
Hadley, M. E., and W. C. Quevedo, Jr. 1967. The
role of epidermal melanocytes in adaptive color
changes in amphibians. Advan. Biol. Skin
8:337-359.
Hall, E. R., and D. F. Hoffmeester. 1942. Geographic variation in the canyon mouse. Peromyscus
crinitus. J. Mammalogy 23:57-65.
Hamilton, W. J., III. and F. Heppner. 1967. Radiant solar energy and the function of black homeotherm pigmentation: an hypothesis. Science
155:196-197.
Hardy, R. 1945. The influence of types of soil upon
the local distribution of some mammals in
southwestern Utah. Ecol. Monogr. 15:71-108.
Harmson, R. 1966. The excretory role of pteridines
in insects. J. Exp. Biol. 45:1-13.
Hooper, E. T. 1941. Mammals of the lava fields and
adjoining areas in Valencia County, New
Mexico. Misc. Publ. Mus. Zool. Univ. Mich. No.
51.
Hulse, F. S. 1967. Selection for skin color among
the Japanese. Amer. J. Phys. Anthropol.
27:143-155.
Hutchinson, V. H., and J. L. Larimer. 1960. Reflectivity of the integuments of some lizards from
different habitats. Ecology 41:199-209.
Johnston, R. F. 1966. The adaptive basis of geographic variation in color of the purple martin.
Condor 68:219-228.
Johnston, R. F. 1969. Character variation and adaptation in European sparrows. Syst. Zool.
18:206-231.
Klauber, L. M. 1931. A statistical survey of the
snakes of the southern border of California. Bull.
Zool. Soc. San Diego 8:1-87.
SIGNIFICANCE OF VERTEBRATE PIGMENTATION
Klauber, L. M. 1939. Studies o£ reptile life in the
southwest, Part II. Speculations on protective
coloration and protective reflectivity. Bull. Zool.
Soc. San Diego 14.65-79.
Lack, D. 1943. The life of the robin. Penguin
Books, London.
Lorenz, K. 1950. The comparative method in studying innate behavior patterns. Symp. Soc. Exp.
Biol. 4:221-268.
Lorenz, K. 1966. On aggression. Harcourt, Brace
and World, Inc., New York.
Loomis, W. F. 1967. Skin-pigment regulation of
vitamin-D biosynthesis in man. Science 157:501506.
Lyman, C. P. 1943. Control of coat color on the
varying hare, Lepus americanus Erxleben. Bull.
Mus. Comp. Zool. Harvard 93:393-461.
Magnuson. J. J. 1971. Color patterns of pilotfish
{Naucrates ductor) and their possible significance. Copeia 1971:314-316.
Magnuson, J. J., and J. H. Prescott. 1966. Courtship, locomotion, feeding and miscellaneous behavior of Pacific bonilo (Sarda chilrensis).
Anim. Behav. 14:54-67.
Mason, H. S., D. J. E. Ingram, and B. Allen. 1960.
The free radical property of melanins. Arch.
Biochem. Biophys. 86:225-230.
Masson, P. 1948. Pigment cells in man, p. 15-37. In
The biology of melanomas. Spec. Publ. New York
Acad. Sci. 4.
Mayhew, W. W. 1963. Observations on captive Amphibolurus pictus, an Australian agamid lizard.
Herpetologica 19:81-88.
Murchison, A. E., and J. J. Magnuson. 1966. Notes
on the coloration and behavior of the common
dolphin, Coryphaena hippurus. Pac. Sci. 20:515517.
Nakamura, E. L., and J. J. Magnuson. 1965. Coloration of the scombrid fish Euthynnus affinis (Cantor). Copeia 1965:234-235.
Millott, N. 1957. Animal photosensitivity, with special reference to eyeless forms. Endeavour
16:19-28.
Neil, E. H. 1964. An analysis of color changes and
social behavior of Tilapia mossambica. Univ. Calif. Publ. Zool. 75:1-58.
Nicol, J. A. C. 1960. The biology of marine animals. Interscience Publ. Inc., New York.
Nicol, J. A. C, and C. van Baalen. 1968. Studies on
the reflecting layers of fishes. Contrib. Mar. Sci.
Univ. Tex. 13:65-88.
Noble, G. K. 1954. The biology of the amphibia.
Dover Publ. Inc., New York.
Norris, K. S., and C. H. Lowe. 1964. An analysis of
background color-matching in amphibians and
reptiles. Ecology 45:565-580.
Ohmart, R. D., and R. C. Lasiewski. 1971.
Roadrunners: energy conservation by hypothermia and absorption of sunlight. Science 172:6769.
Parker, G. H. 1938. The colour changes in lizards,
particularly in Phrynosoma. J. Exp. Biol.
15:48-73.
75
Parker, G. H. 1940. The chromatophore system in
the catfish Ameiurus. Biol. Bull. 79:237-251.
Parker, G. H. 1948. Animal colour changes and
their neurohumours. Univ. Press, Cambridge, England.
Parker, G. H., and S. A. Starratt. 1904. The effect
of heat on the color changes in the skin of
Anolis carolinensis Cuv. Proc. Amer. Acad. Arts
Sci. 40:457-466.
Pathak, M. A. 1967. Photobiology of melanogenesis:
biophysical
aspects.
Advan.
Biol. Skin
8:397-420.
Pearse, A. S. 1926. Animal ecology. McGraw-Hill,
Inc., New York.
Peterman, R. M. 1971. A possible function of coloration in coral reef fishes. Copeia 1971:330-331.
Poulton, E. B. 1890. The colours of animals. Int.
Sci. Ser. 68, London.
Portmann, A. 1959. Animal camouflage. Univ.
Michigan Press, Ann Arbor.
Pycraft, W. P. 1925. Camouflage in nature.
Hiuchinson and Co., Ltd., London.
Rawles. M. E. 1948. Origin of melanophores and
their role in development of color patterns in
vertebrates. Physiol. Rev. 28:383-408.
Rubin, M. 1968. The antimalarials and the tranquilizers. Dis. Nerv. Syst. 29:67-76.
Searle, A. G. 1968. Comparative genetics of coat
colour in mammals. Academic Press, New York.
Snell, R. S. 1967. Hormonal control of pigmentation
in man and other mammals. Advan. Biol.
Skin 8:447-466.
Stebler, A. M. 1939. An ecological study of the
mammals of the Badlands and Black Hills of
South Dakota and Wyoming. Ecology 20:382-393.
Stroud, C. P. 1949. A white spade-foot toad from
the New Mexico White Sands. Copeia 1949:232.
Stullken, D. E., and W. A. Helstand. 1953. An
experimental study of the influence of pelage
pigmentation on metabolic rate and its possible
relationship to body temperature control and
ecological distribution. Ecology 34:610-613.
Sumner, F. B. 1921. Desert and lava-dwelling mice,
and the problem of protective coloration in
mammals. J. Mammalogy 2:75-86.
Sumner, F. B. 1934. Does "protective coloration"
protect? Results of some experiments with fishes
and birds. Proc. Nat. Acad. Sci. U.S. 20:559-564.
Sumner, F. B. 1935a. Studies of protective color
change. III. Experiments with fishes both as
predators and prey. Proc. Nat. Acad. Sci. U.S.
21:345-353.
Sumner, F. B. 19356. Evidence for the protective
value of changeable coloration in fishes. Amer.
Natur. 49:245-266.
Sumner, F. B. 1944. Vision and guanine production
in fishes. Proc. Nat. Acad. Sci. U.S.
30.285-294.
Sumner, F. B., and H. S. Swarth. 1924. The supposed effects of the color tone of the background
upon the coat color o£ mammals. J.
Mammalogy 5:81-113.
Svihla, A. 1956. The relation of coloration in mam-
76
MAC E. HADLEY
mals to low temperature. J. Mammalogy
37:378-381.
Szab6, G. 1967. Photobiology of melanogenesis: cytological aspects with special reference to differences in racial coloration. Advan. Biol. Skin
8:379-396.
Szabd, G. 1969. The biology of the pigment cell.
Biol. Basis Med. 6:59-91.
Thayer, A. H. 1909. Concealing coloration in the
animal kingdom. Macmillan Co., New York.
Tavolga, W. N. 1956. Visual, chemical, and sound
stimuli as cues in the sex discriminatory behavior
of the gobiid fish, Bathygobius soporator.
Zoologica 41:49-65.
Wassermann, H. P. 1965a. Human pigmentation
and environmental adaptation. Arch. Environ.
Health 11:691-694.
Wassermann, H. P. 1965b. The circulation of melanin. Its clinical and physiological significance. S.
Afr. Med. J. 39:711-716.
Wassermann, H. P. 1965c. Leucocytes and melanin
pigmentation I. Demonstration of pigmented leucocytes in blood of amphibians, reptiles and normal man. J. Invest. Dermatol. 45:104-109.
Wilson, F. H. 1940. Color changes in blindfolded
anoles. Copeia 1939:151-153.
Voung, J. Z. 1935. The photoreceptors of lampreys.
I. Light-sensitive fibres in the lateral line nerves.
J. Exp. Biol. 12:229-238.
Young, ]. Z. 1957. The life of mammals. Clarendon
Press, Oxford.