Integumental chromatophores of a color-change, thermoregulating lizard, Phrynosoma modestum (Iguanidae, Reptilia)

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Number 2943, 14 pp., 6 figs.

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June 27, 1989

Integumental Chromatophores of a
Color-Change, Thermoregulating Lizard,
Phrynosoma modestum (Iguanidae; Reptilia)

WADE C. SHERBROOKE! AND SALLY K. FROST?

ABSTRACT

A horned lizard inhabiting the Chihuahuan Des-
ert has a dermal chromatophore architecture (ar-
rangement) significantly different from that of the
only other lizard, Anolis carolinensis, whose der-
mal chromatophore unit was previously de-
scribed. In Phrynosoma modestum, only two cell
types (rather than three) are involved in physio-
logical color change. One type, iridophores, are
organized into a thick layer overlying and engulf-
ing the second type, melanophores, which have
processes that penetrate through the iridophore
layer to the outer surface of the dermis. Iridophore
reflecting platelets lack an organized layered ar-
rangement, reflecting white light rather than colors
produced by interference phenomena. These two
cell types are the major effectors of thermoregu-
latory color change.

Xanthophores and erythrophores, uninvolved
in physiological color change for the most part,
are both widely scattered at low densities and ag-
gregated into elaborate patterns, thus contributing
to background color matching and camouflage. The
chromatophore arrangement in P. modestum may
be typical of desert lizards that utilize physiolog-
ical color change mainly for thermoregulation.

Other findings of interest include (1) the obser-
vation of mosaic chromatophores, wherein a sin-
gle cell contains organelles representative of three
chromatophore types; (2) the unreported ontoge-
netic sequence of appearance of melanophores,
followed by iridophores, and lastly by xantho-
phores, in embryonic P. modestum; and (3) elec-
tron dense material organized in concentric la-
mellae of the pterinosomes.

INTRODUCTION

Chromatophores of poikilotherm verte-
brates have captured the attention of biolo-
gists for many years. Interest in these cells
has focused on developmental origin, clas-
sification of cell types by structure, types of

organelles (development, chemistry, and re-
flective properties), architectural arrange-
ments of cells within the epidermis and der-
mis, hormonal responses and receptors,
neural innervations and receptors, and role

' Resident Director, Southwestern Research Station, American Museum of Natural History, Portal, AZ 85632;
Research Associate, Department of Herpetology and Ichthyology, American Museum of Natural History, New York.
2 Associate Professor, Department of Physiology and Cell Biology, University of Kansas, Lawrence 66045.

Copyright © American Museum of Natural History 1989

ISSN 0003-0082 / Price $2.10

2 AMERICAN MUSEUM NOVITATES

in morphological and physiological color
change (Parker, 1938, 1948; Fingerman, 1963;
Waring, 1963; Taylor and Bagnara, 1972;
Bagnara and Hadley, 1973).

Among reptiles, saurians exhibit the most
dramatic physiological color change. Three
genera of lizards have received considerable
attention from investigators interested in the
mechanisms of such change: Chamaeleo,
Anolis, and Phrynosoma (Parker, 1938, 1948;
Fingerman, 1963; Waring, 1963; Taylor and
Hadley, 1970; Bagnara and Hadley, 1973).
Previous studies on color change in horned
lizards were done many years ago (Parker,
1906, 1938, 1948; Redfield, 1916, 1918) and
were not accompanied by detailed exami-
nation of the architectural arrangement of in-
tegumental chromatophores. Our current
knowledge of lizard skin chromatophores is
based almost entirely on a single species,
Anolis carolinensis (von Geldern, 1921; Fors-
dahl, 1959; Alexander and Fahrenbach, 1969;
Taylor and Hadley, 1970; Bagnara and Had-
ley, 1973).

In this paper we consider the architectural
arrangement of the dermal chromatophores
of Phrynosoma modestum, their color-gen-
erating organelles, mosaic chromatophores,
and the sequential appearance of the various
pigment cell types during embryonic devel-
opment. A model of the integumental chro-
matophore architecture for desert lizards that
use color change mainly for thermoregulation
is proposed and compared to the dermal
chromatophore unit of A. carolinensis (Tay-
lor and Hadley, 1970) and to that of anurans
(Bagnara et al., 1968).

MATERIALS AND METHODS

Adult specimens of P. modestum were col-
lected near Portal, Cochise Co., Arizona, in
1983 and 1984. Lizards were maintained in
captivity (Sherbrooke, 1987) until sacrificed
for skin samples from various locations on
the dorsal surface of the abdomen. Individ-
uals were of various colors; this population
is polymorphic (Sherbrooke, 1981).

Eggs laid by gravid females were incubated
in vermiculite (Zweifel, 1961; Sherbrooke,
1987). At various times during development,
the integumental surface of single embryos

NO. 2943

was examined under a dissecting microscope
for evidence of developing pigment cells.

The outer surface of skin on the dorsal ab-
domen of living lizards, excised pieces of skin
in physiological saline, and skin whole mounts
(in Karo syrup) were examined and photo-
graphed under various magnifications of a
dissecting microscope. In a few cases, the epi-
dermis was removed, using a solution of 2 M
NaBr, in order to more clearly expose the
surface of the underlying pigment cells of the
upper dermis and to examine the epidermal
chromatophore pattern.

Fixation and electron microscopic exami-
nation followed the procedures of Frost and
Robinson (1984). Skin samples were fixed in
2.5 percent glutaraldehyde in 0.2 M caco-
dylate buffer (pH 7.3) for 12 hours at 4—6°C.
Samples were postfixed in 2 percent osmium
tetroxide for 1.5-—2.0 hours, rinsed, and stored
in 0.2 M cacodylate buffer. These skin sam-
ples were then dehydrated in a graded ethanol
series. Skin was embedded in Epon and sec-
tions were cut with a diamond knife on a
Sorvall MT-1 ultramicrotome. Sections were
collected on Formvar-coated and carbon-sta-
bilized grids, stained with uranyl acetate-lead
citrate, and viewed in a Philips 300 trans-
mission electron microscope. Several skin
samples were placed in 1.6 x 107? M melano-
cyte-stimulating hormone (a-MSH), a con-
centration that is physiologically effective for
color change (Sherbrooke, 1988), for 60 min-
utes prior to fixation.

RESULTS

ONTOGENETIC APPEARANCE OF
CHROMATOPHORE TYPES

Eggs from three clutches laid by different
P. modestum females were periodically
opened and the embryos were examined for
evidence of chromatophores. The types of
pigment cells observed were recorded. In all
cases, melanophores developed first, by the
26th, 27th, and 31st day of incubation of each
clutch. In all clutches iridophores were the
second chromatophore type to develop, by
the 26th, 34th, and 44th day of incubation.
In the first clutch, melanophores and irido-
phores were first noted on the same day (26th),
but the former were well established and the

yale,

Fig. 1.

SHERBROOKE AND FROST: LIZARD CHROMATOPHORES 3

a,

yo

Transmission electron micrograph of a mosaic dermal chromatophore from Phrynosoma

modestum dorsal integument treated with 1.6 <x 10- M a-MSH for 60 min prior to fixation. To the
left of the nucleus (N), the cell contains three types of color-producing organelles, pterinosomes (PT),
reflecting platelets (RP), and a few melanosomes (M). Interspersed throughout the cytoplasm are mi-

tochondria (MI). x 12,240.

latter were just beginning to appear. Irido-
phores developed in groups, forming white
“islands” on the skin. In the first two clutch-
es, xanthophores developed last, by the 40th
and 47th days. In the third clutch, xantho-
phores had not appeared by the time the last
egg was opened on the 50th day.

MOSAIC (POLYCHROMATIC) CELLS

A few mosaic or polychromatic cells were
observed. These cells contain multiple types
of color-generating organelles, each of which
is normally restricted to a specific type of
chromatophore. One such mosaic cell con-
tained organelles characteristic of all three
types of dermal chromatophores— melano-
phores, iridophores, and xanthophores. In this
cell pterinosomes were most numerous, fol-

lowed by reflecting platelets, and melano-
somes were least abundant (fig. 1). Mosaic
cells were more frequently observed in
a-MSH-treated skin samples.

MELANOPHORES

The cell bodies of dermal melanophores lie
deep within the dermis (figs. 2, 3). These cell
bodies may be surrounded both above and
below by iridophores that can be identified
under polarized light (figs. 2, 3). Elongate pro-
cesses extend through the overlying irido-
phore layer to positions below the epidermis
(figs. 2, 4A) where they extend laterally along
the upper level of the dermis (figs. 2A, 4B).
During skin darkening, melanin-containing
melanosomes move into the processes, thus
positioning black pigment granules above

4 AMERICAN MUSEUM NOVITATES NO. 2943

we

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Fig. 2. Light micrographs of Phrynosoma modestum dermis during skin darkening. A. Dermal me-
lanophore of P. modestum. Note that melanosomes occupy the cell processes that extend from the deep
perinuclear portion of the cell to the surface of the dermis. B. Dermal iridophore (reflecting platelet)
zone of cells appears as bright areas under polarized light: same view as fig. 2A. The iridophore layer
extends from below the melanophores to the surface of the dermis.

1989 SHERBROOKE AND FROST: LIZARD CHROMATOPHORES 5

Fig. 3. Light micrographs of Phrynosoma modestum dermis during skin lightening. A. Dermal me-
lanophore of P. modestum. Note that melanosomes are withdrawn from the cell process and are con-
centrated in the deep perinuclear portion of the cell. B. Dermal iridophore (reflecting platelet) zone of
cells appears as bright areas under polarized light: same view as fig. 3A. The iridophore layer extends
from below the melanophores to the surface of the dermis.

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Fig. 4. Transmission electron micrographs of melanophore processes in the dermis. A. Melanophore
(M) process extending up through iridophores (1) and collagen bundles (C) to the upper edge of the
dermal-epidermal (E) border. x 3630. B. Melanophore (M) process extending along the upper edge of
the dermis, above the iridophores (I) and collagen bundles (C), and below the epidermis (E). x 6160.

iridophores (fig. 2). When this happens there
is a reduction of melanosome numbers in the
perinuclear portion of the melanophore.
When the integument lightens in color, mela-
nosomes have been withdrawn from the me-
lanophore processes and are concentrated in
the perinuclear area (fig. 3).

IRIDOPHORES

Clearly, these are the dominant chromato-
phores of the dorsal (as well as ventral) skin,
occurring in abundance from just below the
basement membrane to the underlying con-
nective tissue layer (figs. 2, 3, 4A). Iridophore
reflecting platelets are purported to contain
crystalline guanine as a pigment (Bagnara et
al., 1988). Although the guanine content of
the reflecting platelets is lost during tissue
preparation, the size, form, and orientation
of the platelets are retained by virtue of fix-

ation of the limiting membrane of these or-
ganelles (fig. 4). Generally, platelets are rect-
angular, oblong, or ovoid in shape. Some
platelets are observed to be arranged end-to-
end in lines, and lines of platelets may occur
in several layers (fig. 5). Although this sug-
gests a degree of structural ordering between
adjacent organelles, there appears to be no
overall organized arrangement of platelets
within iridophores. Likewise, iridophores
themselves are scattered throughout the der-
mis and are thus not regularly arranged with
respect to one another (figs. 4, 5).

XANTHOPHORES

Xanthophores lie at the uppermost level of
the dermis, above even the outer iridophores
and somewhat interspersed with them (fig.
6). Thus, they are found just below the epi-
dermal/dermal boundary. Internally, xan-

SHERBROOKE AND FROST: LIZARD CHROMATOPHORES 7

Fig. 5. Transmission electron micrograph of the extensive “network” of iridophore processes in
Phrynosoma modestum dorsal skin. Note the end-to-end alignment (arrows) of many of the reflecting
platelets (RP) and the occasional stacking of end-to-end aligned platelets. x 9900.

thophores contain primarily pterinosomes,
and occasionally carotenoid vesicles, both of
which are characteristic organelles of xan-
thophores. Pterinosomes of the individuals
illustrated in figure 6 are unusually dense,
which may be indicative of the biochemical
composition of the pigments within the or-
ganelles (see Discussion).

Examination of the skin surface under a
dissecting microscope showed that xantho-
phore distribution varies greatly over the
dorsum. In most areas of dorsal skin these
cells are widely spaced; however in areas that
are distinctly patterned, xanthophores are
present in much higher densities. Often, xan-
thophores have processes that extend out to
cover the surface of the iridophore layer.

COLLAGEN FIBERS

Bundles of collagen fibers are abundant in
the dermis; this correlates well with the thick

elastic qualities of the skin. The fibers occur
immediately below the basement membrane
and are also interspersed among the dermal
chromatophores (figs. 4-6). When sectioned
longitudinally, their banding is apparent,
whereas in cross section, they appear as
groupings of solid, roundish structures lack-
ing cellular membranes (figs. 4-6).

DISCUSSION

Bagnara and Hadley (1973) have stan-
dardized the terminology associated with
vertebrate chromatophore types and their
color-generating organelles: (1) epidermal
melanophores (cytes) contain melanosomes;
(2) dermal melanophores also contain mela-
nosomes; (3) iridophores contain reflecting
platelets; and (4) xanthophores or erythro-
phores contain pterinosomes and/or carot-
enoid vesicles and, as a result, are brightly
colored (yellow, red, orange).

8 AMERICAN MUSEUM NOVITATES

NO. 2943

Fig.6. Transmission electron micrographs of xanthophores from PArynosoma modestum dorsal skin.
A. Xanthophore (X) closely apposed to the basement membrane of the epidermis (E) with iridophore
(I) processes and collagen (C) fibers below. Within the cytoplasm of these xanthophores are numerous
electron-dense pterinosomes (*) and carotenoid vesicles (arrows) as well as prominent nuclei (the X
denoting “‘xanthophore” is within the nucleus). x 3960. B. Another example of a xanthophore illustrating
the electron-dense, concentrically organized fibrous material (presumably pteridine pigment) within the

pterinosomes (PT). X 3630.

ONTOGENETIC APPEARANCE OF
CHROMATOPHORE TYPES

It has been suggested that the ontogenetic
appearance of chromatophore types in poi-
kilotherm vertebrates occurs in a definite se-
quence. In amphibians, dermal melano-
phores occur first, followed by xanthophores,
and then iridophores (Collins, 1961; Bagnara
and Hadley, 1973; Frost et al., 1984). In the
three clutches of P. modestum eggs examined
herein, a different sequence of chromato-
phore ontogeny was observed with melano-
phores appearing first, followed by irido-
phores, and lastly by xanthophores.

The shell enclosed nature of the reptilian
egg makes it likely that such a sequence sim-
ply has not been observed before. Moreover,
because of the small number of animals ex-

amined herein, we suggest that our findings
are preliminary and need to be subjected to
further verification by histological study of
chromatophore appearance not only in P.
modestum, but in other groups of reptiles as
well. Further observations may provide in-
sight into the development and differentia-
tion of chromatophore types and their re-
spective color-generating organelles.

MOSAIC (POLYCHROMATIC) CELLS

All integumental chromatophores are de-
rived from neural crest cells that migrate from
the developing neural tube to locations
throughout the embryo during development
(DuShane, 1935; Bagnara and Hadley, 1973;
LeDouarin, 1982, 1984; Bagnara, 1987). Be-
cause of this common embryonic origin, the

1989

idea that pigment cell types all form from a
common “chromatoblast” has received much
support (Bagnara et al., 1979a, 1979b; Bag-
nara, 1981, 1983). The “signal” to differen-
tiate into a particular pigment cell type is, at
present, not well understood, but the exis-
tence of mosaic chromatophores and the ob-
servation that chromatophore types can in-
terconvert in vitro (Ide, 1978) suggest that
there is plasticity in the differentiative ca-
pabilities of these cell types.

Mosaic pigment cells have been observed
in a variety of vertebrates, including reptiles
(Bagnara and Taylor, 1970; Bagnara and Fer-
ris, 1971; Bagnara, 1972; Taylor and Bag-
nara, 1972; Ferris and Bagnara, 1972; Bag-
nara et al., 1978a, 1978b, 1979a, 1979b; Frost
and Malacinski, 1980; Bagnara, 1981, 1983).
The application of a-MSH to some skins pre-
vious to fixation appears to increase the
incidence of mosaic cells. Taylor (1969) re-
ported melanization of amphibian irido-
phores in response to intermedin. The sig-
nificance of mosaic chromatophores in the
dermis of Phrynosoma is unclear. It may re-
flect an artifact produced by hormonal stim-
ulus or this may be a bona fide “‘cell in tran-
sition.”

PTERINOSOME ULTRASTRUCTURE

It is also significant that pterinosomes in
the xanthophores of P. modestum all contain
moderate to heavy amounts of fibrous, elec-
tron-dense material organized in concentric
lamellae. The electron-dense fibrous material
has been observed by numerous investigators
and is justifiably assumed to reflect the pres-
ence of pteridine pigments. Frost et al. (1984,
1986) demonstrated (in axolotls) that the
more brightly colored an animal was (in this
case a golden albino axolotl), the more dense-
ly pigmented were its pterinosomes. More-
over, axolotls with enhanced yellow back-
ground pigmentation due to guanosine
treatment have pterinosomes with signifi-
cantly more electron-dense pigment than
normal (Frost et al., 1987). In both cases, the
enhanced yellow coloration of these axolotls
was due to the presence of the yellow pter-
idine pigment, sepriapterin.

The appearance of the pterinosomes in P.
modestum (see fig. 6) suggests a similar phe-

SHERBROOKE AND FROST: LIZARD CHROMATOPHORES 9

nomenon. The intense electron density of
these organelles, together with the yellow, red,
and/or pink color of the animals themselves,
suggests the presence of sepriapterin and/or
drosopterins (red pteridine pigments) in the
integument. Whether this speculation is ac-
curate awaits further biochemical testing.

ARCHITECTURAL ARRANGEMENT OF
INTEGUMENTAL CHROMATOPHORES

The integumental architecture of color-
changing poikilotherm vertebrates is char-
acterized by two complexes of chromato-
phores, one epidermal and one dermal. The
vertebrate epidermal melanin unit consists of
melanin-synthesizing melanophores and ad-
jacent, associated Malpighian cells that are
receptor cells for melanin elaborated in the
epidermal melanophores (Hadley and Que-
vedo, 1966). In P. modestum, epidermal me-
lanophores (cytes), with typical elliptical
melanosomes, occur within the a- and 6-ker-
atin layers of the outer epidermis (Sher-
brooke, 1988), where they play a supplemen-
tary role in pattern formation, but no role in
physiological color change. A few melano-
phores (apparently dermal) appear to have
processes that extend into epidermal portions
of mechanoreceptors (Sherbrooke, 1988).

Rapid color changes are reportedly effected
by the dermal chromatophore unit (Bagnara
et al., 1968). During skin darkening this in-
volves intracellular transport (Schliwa and
Euteneuer, 1983) of melanosomes from the
melanophore cell body deep in the dermis
into melanophore processes that extend up-
ward toward the surface of the dermis. Here
the melanosomes come to lie between an up-
per layer of xanthophores and an underlying
layer of iridophores (anurans), or melano-
phore processes may overlap both layers
(Anolis) (Taylor and Hadley, 1970; Bagnara
and Hadley, 1973). Iridophores and xantho-
phores may also exhibit changes in organelle
distribution (Bagnara, 1969; Bagnara and
Hadley, 1969, 1973; Bagnara et al., 1969).
Chromatophore cell membrane receptors re-
spond to melanotropic peptides (Hadley,
1984; papers in Hadley, 1988; Sherbrooke,
1988), catecholamines of the autonomic ner-
vous system (Nilsson, 1983; Hadley, 1984;

10 AMERICAN MUSEUM NOVITATES

Sherbrooke, 1988), and other hormones
(Bagnara and Hadley, 1973).

The architectural arrangement of dermal
chromatophores of Phrynosoma has not been
studied previously. Bagnara et al. (1968) based
their concept and description of the dermal
chromatophore unit on studies of amphibi-
ans. Von Geldern (1921) described the chro-
matophore structure and arrangement of cells
in the lizard A. carolinensis, as have later
investigators (Alexander and Fahrenbach,
1969; Taylor and Hadley, 1970). Taylor and
Hadley (1970) schematically interpreted the
dermal chromatophore unit of A. carolinen-
sis, and thus postulated wider taxonomic ap-
plicability of the concept of a multicellular
chromatophore unit, consisting of three cell
type layers, to color-changing poikilotherms
(Bagnara and Hadley, 1973). In two snakes
lacking the ability for physiological color
change, Natrix natrix and Vipera ammody-
tes, this arrangement of chromatophores into
three cell-type units is absent (Miscalencu and
Ionescu, 1972, 1973).

Striking color differences are obvious be-
tween A. carolinensis and P. modestum. Ano-
lis carolinensis is uniformly green, changing
to uniform brown during darkening. Dorsal
skin of Phrynosoma modestum is darkly pat-
terned on a pale background (Sherbrooke,
1988; Sherbrooke and Montanucci, 1988).
The dorsal pattern may contain a variety of
yellow, red, pink, or other colors (Sher-
brooke, 1981, 1988; Sherbrooke and Mon-
tanucci, 1988). Phrynosoma modestum has
been called the bleached horned lizard (Sher-
brooke, 1981) because of its ability to turn
nearly white over most of its dorsum.

Surface examination of living skin or whole
mounts shows the overwhelming predomi-
nance of white light reflected from the scales.
Clearly scattered over this background are
black processes of melanophores, and yellow
or red xanthophores that may have lateral
extending processes. Brightly colored chro-
matophores vary greatly in density from one
scale to another; many scales have only a few
isolated bright-colored cells. Melanophore
processes are more numerous on the surface
of the white iridophore layer in regions that
are more darkly patterned; likewise, brightly
colored chromatophores increase in number
in areas of colored pattern. Xanthophores and

NO. 2943

melanophores are often observed to be in-
termingled in pattern-forming areas.

THERMOREGULATION AND
CHROMATOPHORE ARRANGEMENT

Studies on integumental chromatophore
architecture in reptilian species that undergo
physiological color change have focused on
Anolis carolinensis. This species utilizes
chromic adaptation mainly for cryptic back-
ground matching that requires the attainment
of green coloration to match surrounding fo-
liage (von Geldern, 1921; Alexander and
Fahrenbach, 1969; Taylor and Hadley, 1970).

Color change in P. modestum appears to
be largely associated with thermoregulation,
not background color matching (Sherbrooke,
1988). Darkening and lightening of the skin
are due to translocation of melanosomes
within dermal melanophores. During skin
lightening melanosomes vacate melanophore
processes lying on the surface of the dermis
and move into deeper-lying portions of the
cell; this is reversed during skin darkening.
Possible movement of organelles within oth-
er types of chromatophores, known in some
other vertebrates (Bagnara, 1969; Bagnara et
al., 1969; Bagnara and Hadley, 1969, 1973)
but not in A. carolinensis (Taylor and Hadley,
1970), was not studied.

The white color of P. modestum scales over
much of the lizard’s integument is attribut-
able to the thick layers of dermal iridophores
that extend upward nearly to the basement
membrane of the epidermis. The organiza-
tion of reflecting platelets in P. modestum
contrasts sharply with that found in A. car-
olinensis iridophores, where apparently the
crystal arrangement and spacing are critical
for the production of blue-green color by thin-
film interference (Land, 1972; Rohrlich and
Porter, 1972; Frost and Robinson, 1984). In
A. carolinensis, the platelets are highly or-
ganized in rows and layers, whereas in P. mo-
destum, they approach a random arrange-
ment. This near random arrangement of
platelets may be responsible for the near total
reflectance of white light (Rohrlich and Por-
ter, 1972; Menter et al., 1979). Kleese (1981)
found (in snake skin) that species with layered
iridophores have a higher dorsal integument
reflectance than do species with scattered

1989

iridophores. Thus the thick iridophore layer
of cells in P. modestum presumably serves
an important function in a lizard utilizing
color change for thermoregulation. When not
covered by overlying melanosomes, irido-
phores reduce heat gain by reflecting visible-
spectrum radiation.

Thus, the functional dermal chromato-
phore unit in P. modestum is clearly distinct
from that found in A. carolinensis, although
the basic proximal-to-distal relationship of
cell types is the same. In order to achieve
green camouflage coloration, A. carolinensis
utilizes the combined light of two cell types,
yellow reflected light from xanthophores and
blue-green refracted light from the thin-film
interference system of iridophore organelles.
Color change darkening to brown involves
movement of melanosomes to positions lying
above the xanthophores and the iridophores.
In P. modestum, there are basically only two
chromatophores involved in color change.
The iridophores reflect out all wavelengths of
visible light and play no part in mixing wave-
lengths with light reflected off the layer of
overlying xanthophores to form a cryptic col-
or. A similar difference in chromatophore ar-
chitecture was found by Bagnara et al. (1968)
between green/brown color-change frogs
(Hyla cinerea and Agalychnis dachnicolor) and
a nongreen color-change frog (Hyla areni-
color).

THERMOREGULATION-CRYPTICITY
COMPROMISE

In P. modestum, the xanthophores and
erythrophores do play an important role in
crypticity, a second consideration in dorsal
coloration. Their distribution over the ani-
mal’s back creates patterns useful for cam-
ouflage (Cott, 1940; Sherbrooke, 1988; Sher-
brooke and Montanucci, 1988) and for
blending into the colors of the surrounding
terrain (Norris and Lowe, 1964). The mela-
nophores function in relation to the irido-
phores as the regulators of skin darkening and
lightening. In effect, these two cell types func-
tion as a dermal chromatophore unit for
changing the radiation balance of the skin,
thus facilitating thermoregulation. Irido-
phores containing reflecting platelets, whose
arrangement produces reflectance of most

SHERBROOKE AND FROST: LIZARD CHROMATOPHORES 11

wavelengths of visible light, in combination
with melanophores that extend from deep
within the iridophore layer onto its surface,
may be characteristic of desert and other sau-
rian species utilizing color change for ther-
moregulation. Such physiological consider-
ations for color changes may be compromised
by background-matching considerations
leading to an adaptive compromise in the
coloration of a lizard (Norris and Lowe, 1964;
Norris, 1967).

This compromise can be visualized in the
various components of chromatophore ar-
chitecture. Considerations for the role of in-
tegumental pigment cells in influencing ther-
moregulation are addressed through two
interacting cell types: the iridophore/mela-
nophore cell complex. Needs of an animal
for crypticity are addressed by the distribu-
tion and density (color and pattern forma-
tion) of various static chromatophores locat-
ed above the iridophore layer— xanthophores
and melanophores in this case. Thus, the
structure of the entire chromatophore com-
plex graphically illustrates the adaptive com-
promises associated with these two roles of
coloration.

Striking similarities and differences can be
seen by comparing the dermal chromato-
phore architecture of anurans (Bagnara et al.,
1968), A. carolinensis (Taylor and Hadley,
1970), and P. modestum. Taylor and Hadley
(1970) have discussed the difference between
the dermal chromatophore unit of anurans
and A. carolinensis. Phrynosoma modestum
is similar to A. carolinensis in its overall ar-
rangement of the three chromatophore cell
types, surface xanthophores over irido-
phores, which are underlain by melano-
phores having processes that extend to the
iridophore upper surface and through which
melanosomes may be translocated. Appar-
ently in both species, iridophores and xan-
thophores do not change organelle distribu-
tion during physiological color change.
Phrynosoma modestum differs from A. caro-
linensis in that: (1) the chromatophore lay-
ers are not as distinctly separated, with the
outer xanthophores extending into a thick,
irregularly arranged layer of iridophores; (2)
the arrangement of reflecting platelets within
iridophores is near random, promoting wide-
spectrum reflectance; (3) the melanophore cell

12 AMERICAN MUSEUM NOVITATES

body is surrounded above and below by the
iridophore layer; and (4) the xanthophore (or
erythrophore) layer is very sparse or absent
over portions of the skin, leaving a two-layer
chromatophore unit as the basic structure ef-
fecting color change. It seems likely that this
two-layer chromatophore unit is the basic
structure for effecting color change in a va-
riety of lizards that utilize this ability mainly
for thermoregulation. The bright-colored
pigment cells, on the other hand, play a dis-
tinctly separate role, that of pattern forma-
tion and background color matching.

ACKNOWLEDGMENTS

We thank Wayne Ferris for assistance with
fixation of tissues and Scott J. Robinson for
imbedding and sectioning tissues for electron
microscopy. Mac E. Hadley suggested the
NaBr techniques for separation of dermis and
epidermis; Joseph T. Bagnara recommended
the Karo syrup slide preparation for whole
mounts of skin in which the color cells, xan-
thophores, and erythrophores are not de-
stroyed by alcohol leaching of carotenoid
pigments. Both of the latter, with Astrid Ko-
dric-Brown, Robert L. Smith, and Floyd G.
Werner, read and commented on an early
version of the manuscript that formed a dis-
sertation chapter (Sherbrooke, 1988). Col-
lecting permits were provided by the Arizona
Game and Fish Department and the New
Mexico Department of Game and Fish.

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