AMER. ZOOL., 21:273-294 (1981)
Function and Causation of Social Signals in Lizards1
DAVID CREWS
Departments of Biology and Psychology and Social Relations and the Museum of Comparative Zoology,
Harvard University, Cambridge, Massachusetts 02138
AND
NEIL GREENBERG
Department of Zoology, University of Tennessee.
Knoxville, Tennessee 37916
SYNOPSIS. We describe here a multidisciplinary investigation of the stimuli and mechanisms controlling reproduction in the green anole lizard, Anolis carolinensis. Both environmental and social stimuli that vary seasonally are used as proximate cues to reproduction. In order for these ecological factors to initiate breeding, they must be perceived
and integrated in the central nervous system. External and internal stimuli converge upon
the hypothalamus, the major neuroendocrine integrative area of the brain, which, in turn,
directly regulates pituitary and autonomic function. In addition to their role in reproduction, the gonadal hormones are important throughout the life of the organism, acting
both peripherally and centrally, to adapt the individual to its environment. Thus, the
environment, behavior, and physiology interact in complex ways to synchronize the social
and reproductive activities of individuals.
INTRODUCTION
It is valuable to think about the function
and causation of behavior at the same time
because they are mutually illuminating:
The perspective of one often helps solve
problems in the other. Traditionally, function has been studied by ethologists concentrating on spontaneous behavior expressed in a natural setting. Problems in
causation, on the other hand, have been
explored largely by physiological and comparative psychologists using techniques in
which sources of variation are rigidly controlled if not eliminated. Thus, while
ethologists document the diversity of behavior, psychologists demonstrate the fundamental commonalities in behavior. At
times, these disciplines seemed irreconcilable: The problems of control inherent in
ethological studies were contrasted with
the lack of appreciation for environmental
constraints in comparative psychology.
Tinbergen and Schneirla were early to recognize the feasibility of a synthetic approach. They and their students, most notably Hinde and Lehrman, brought the
rigor of the laboratory to the study of
species-typical behaviors.
Our purpose in this paper is to describe
briefly: 1) some of the biologically significant stimuli impinging upon temperate climate lizards; 2) the manner in which these
stimuli are perceived and integrated in the
central nervous system; and 3) how this information regulates the hormonal milieu,
thereby influencing structures and behaviors important in social interaction and reproduction. In this pursuit we will draw on
many different disciplines which, when
combined, illustrate the power of the synthetic approach. Because we are most familiar with the green anole, much of the
information provided here will concern
Anolis carolinensis. By emphasizing the gaps
in our understanding, we hope to identify
those areas most likely to yield further insight into the function and causation of social signals.
ECOLOGICAL INFLUENCES ON
REPRODUCTIVE PHYSIOLOGY AND
SOCIAL BEHAVIOR
Much of the social behavior in temperate lizards is regulated by the conditions
From the Symposium on Social Signals—Comparative and Endocrine Aspects presented at the Annual surrounding the reproductive season.
Meeting of the American Society of Zoologists, 27— These regulatory mechanisms have evolved
30 December 1979, at Tampa, Florida.
because ultimately, such conditions reflect
1
273
274
D. CREWS AND N. GREENBERG
the availability of food, changes in preda- and agamid species (Moehn, 1974), as well
tor pressure, and a hospitable environ- as being of metabolic importance to repment for the laying of eggs and their sub- tiles (Reichenbach-Klinke and Elkan, 1965).
sequent development. The exact timing of
reproduction from year to year is finely Temperature
In most temperate areas, fluctuations \v%
tuned by specific ecological stimuli. These
include, among others, photoperiod, tem- temperature can be great. As ectotherms,
perature, moisture, and the behavior of lizards must thermoregulate behaviorally
conspecifics. These proximate factors, to accommodate their physiological needs
along with endogenous circadian or circ- (Dawson, 1975; Regal, 1978; Greenberg,
annual rhythms of sensitivities to them, 1980). The significance of thermoregulatory behavior is indicated by its many vital
determine when animals reproduce.
consequences, including maintenance of
Light
optimum activity of enzymes (Licht, 1967),
Although the seasonal change in pho- muscles (Licht et al., 1969), heart rate
toperiod is used by most birds and mam- (Licht, 1965a), digestion (Harlow et al.,
mals to cue reproduction, experiments 1976), reproductive state (Joly and St. Gihave shown that in many temperate lizard rons, 1975), and the sensitivity of target
species, temperature is the proximate stim- organs to hormones (see below).
ulus for gonadal recrudescence in the
In A. carolinensis, increasing temperaspring (Licht, 1972). The termination of tures elevate pituitary gonadotropin level
breeding activity in A. carolinensis is, how- in both males and females; the different
ever, reliant upon photoperiod as the pri- patterns of male and female emergence
mary proximate factor (Licht, 1971). The from hibernation (Gordon, 1956) suggest
fact that the photosensitivity in testicular a sex difference in temperature sensitivity.
function is restricted to a four-month This, in turn, stimulates spermiogenesis
period in the late summer and early fall (Licht, 1972) and secretion of testicular anunderscores the role of endogenous drogen in males (Pearson et al, 1976), and
periodicities in the environmental control vitellogenesis (Licht, 1973) and secretion
of seasonal reproduction in these animals. of estrogen and progesterone (Tokarz and
The brightness and spectral quality of Crews, unpublished) in females. Similarly,
light also vary predictably and may have in two species of Lacerta, the higher body
importance in the timing of reproduction. temperatures characteristic of spring activFor example, Licht (1969) demonstrated ity are necessary for final testicular matuthat bright, but not dim, white light is suf- ration and androgen secretion (Licht et al.,
ficient to accelerate testicular recrudes- 1969). High temperatures also appear to
cence in A. carolinensis. At relatively low be critical to vernal ovarian development
intensities red light is more effective than in Uta stansburiana (Tinkle and Irwin,
green, while at high intensities, red and 1965), Sceloporus undulatus (Marion, 1970),
green are equally effective; blue light is and L. sicula (Botte et al., 1976).
completely ineffective at both intensities.
In addition to its effect on pituitary goDiurnal changes in intensity of illumina- nadotropin secretion, temperature can intion have obvious implications for the ther- fluence the responsiveness of the gonads
moregulatory activities upon which most and related target tissues directly (Licht
reptiles rely. Dim light, while of little ther- and Pearson, 1969a, b; Licht, 1972, 1974;
mal significance, can be a significant cue in Pearson et al., 1976). However, maintainmorning emergence (Greenberg, 1976) ing lizards at or slightly above their
and shelter-seeking (Regal, 1967) and is species-typical preferred temperature can
therefore important in normalizing the result in marked spermatogenic damage,
pattern of daily activities.
a decline in appetite and growth, thyroid
Ultraviolet light appears to increase ag- hypertrophy and death (Cowles and Burleonistic behavior in a number of iguanid son, 1945; Wilhoft, 1958; Licht, 19656).
FUNCTION AND CAUSATION OF SOCIAL SIGNALS
275
When encountering a conspecific intruder
that
does not respond to the resident's asThe role of moisture has received little
sertion
display by either leaving the terristudy, but its importance is unquestioned.
tory
or
adopting
a submissive posture, the
Seasonal rainfalls and their effect on the
resident
will
perform
the challenge display
abundance of insect prey have long been
(Fig.
1,
bottom).
The
identifying charac•recognized as important factors in regteristics
of
the
challenge
display are the
ulating the reproductive cycles of many
extreme
lateral
compression
of the body
reptiles (reviewed in Crews and Garrick,
and
engorged
throat.
The
challenge
dis1979). There is evidence that humidity or
play,
if
answered
by
the
intruder
in
kind,
rainfall can influence reproductive functioning directly (Crews et al., 1974; Licht is the opening salvo of a confrontation that
and Gorman, 1970). Relative humidity, but establishes dominance of one male over
not the availability of drinking water, is the the other. As the encounter progresses
critical cue controlling ovarian develop- and escalates, other behavioral phenomement in A. sagrei (Brown and Sexton, na of potential signal value become apparent: Crests rise on the nuchal and dorsal
1973).
midline, the skin caudal to the eye darkBehavior also can be affected by tran- ens, and the tail may thrash or twitch.
sient variations in local conditions. A. Evenly matched lizards often will spar with
aeneus in Grenada are active and display their open jaws; if they lockjaws, both twist
throughout the rainy season. During violently in an attempt to throw the other
droughts, the frequency of display de- from the perch.
clines, but if drinking water is given, disBy the time female A. carolinensis
plays increase to pre-drought levels
emerge
from winter hibernacula the asser(Stamps, 1976a). Moisture is the primary
tion
display
is the most common display of
stimulus for oviposition behavior in A.
territorial
males;
since territorial boundaeneus. Rainfall stimulates digging behavaries
are
by
now
recognized,
challenges are
ior, but eggs are not laid until soil moisture
observed
only
occasionally
in
response to
is adequate (Stamps, 19766).
transient males. Females may establish
home ranges for feeding purposes (Stamps,
Conspecific behavior
1977), but relatively little is known about
Social organization entails the coordi- possible female-female interactions and
nation of individuals, each acting in concert their effects on the distribution of females
with the climatic variables as well as inter- throughout the habitat or on the priority
acting with each other. This conspecific of access to various ecological resources. In
behavior is a significant aspect of the ecol- A. carolinensis, it is common to find several
ogy of social lizards (Carpenter and Fer- females within a male's territory (Gordon,
guson, 1977; Stamps, 1977). Male A. car- 1956). These females defend home ranges
olinensis, stimulated by rising ambient against neighboring females and transient
temperature, emerge from winter hiber- females and males.
nacula before the females to establish
First encounters with territorial males
breeding territories (Gordon, 1956). Dur- elicit assertion displays which females reing this period, the predominant display spond to by avoiding the male or performbehaviors of males are the assertion and ing a characteristic subordination display
challenge displays. These displays are consisting of rhythmical headnods. After
species-typical and consist of rhythmical a short time, males begin to court females
bobbing movements of the forebody co- (Fig. 2, top). The courtship display begins
ordinated with extension of the gular fan in a manner similar to the assertion dis(dewlap) (Crews, 1975a; Greenberg, play, but as the dewlap retracts, the male
1977a). Typically, males patrol their terri- advances toward the female while nodding
tories, pausing on prominent perches to his head rapidly. These rapid headnods
perform the assertion display (Fig. 1, top). are the unique element of the courtship
Moisture
276
D. CREWS AND N. GREENBERG
FIG. 1. Assertion (top) and challenge (bottom) displays of the green anole, Anolis carolinensis. See text for
details.
FUNCTION AND CAUSATION OF SOCIAL SIGNALS
display of this species. At first, females respond to all male courtship by fleeing from
the approaching male. Eventually, the approach distance lessens and females stand
and allow the male to copulate. A sexuallypreceptive female assumes a characteristic
posture, the neckbend, thereby facilitating
the male's neckgrip (Fig. 2, bottom); these
changes in receptivity reflect changes in
the female's gonadal state.
The behavioral displays of male A. carolinensis have profound effects on the
physiology and behavior of conspecific females. For example, courtship behavior facilitates the stimulatory effects of the environment and, indeed, is necessary for
normal pituitary gonadotropin secretion
(Crews, 1974a). By altering the stimulus
configuration presented by the courting
male, it has been possible to determine the
critical aspect of the male's courtship display in facilitating environmentally-induced ovarian recrudescence (Crews,
1975ft). When the extension of the dewlap
is prevented by sectioning the retrobasal
process of the hyoid, courting males are
no more effective in stimulating females
than are castrated, sexually inactive males.
The second prominent feature of male
courtship, the dewlap's color, is important
but not critical. The courtship behavior of
males whose dewlap color is changed from
pink to dark blue by the injection of India
ink is initially less effective than that of
unaltered males. It is important to note
that in natural populations around New
Orleans, La., male dewlap color varies
from pink to light blue. Because of this
naturally occurring variability, it would be
of interest to determine if this experimental phenomenon occurs naturally and, if
so, the ecological consequences of retarded
ovarian growth of females courted by bluedewlapped males.
The female's perception of aggressive
behavior between males, on the other
hand, inhibits environmental stimulation
of ovarian growth. Females exposed to aggressive males challenging one another
and engaging in territorial combat will not
initiate ovarian growth despite being
housed in a stimulatory environmental
277
regimen (Crews, 1974a). The critical feature of aggression between males that is
responsible for this effect or its mechanism^) of action is not known. Variables
such as the body compression characteristic of male aggression may be important to
counteracting the stimulatory effects of
the environment. Since the courtship of
hyoidectomized males fails to facilitate
ovarian growth it is reasonable to propose
that the absence of dewlap extension in
high-intensity, challenge behavior between
males might also contribute to this effect.
The courtship behavior of males also has
a short term or releasing effect on the behavior of females. Sexually-receptive females will not stand or show the neckbend
response to the courtship of hyoidectomized males, but will mate with blue-dewlapped males (Crews, 19756).
Just as male A. carolinensis influence the
reproductive state of females, so can female A. carolinensis serve as a priming stimulus to the male. Males housed with females have heavier testes and are in a more
advanced spermatogenic stage than males
housed together in groups (Crews and
Garrick, 1980). What cues the female present to effect this physiological acceleration
is not known. Males from male-female
pairs show more rapid testicular recrudescence than males from male-female
groups. This corresponds to the pattern of
ovarian recrudescence exhibited by females (Crews et al., 1974). Thus, for both
the male and the female, gonadal recrudescence is more rapid in pairs than in
groups. However, group-housed males
and females eventually surpass those lizards that are pair-housed in their level of
gonadal activity. This suggests that the
rapid follicular growth and consequent
sexual receptivity in females is responsible
for the rapid testicular growth in the male
partner. If this is the case, then the finding
that males housed with females in groups
eventually surpass males housed in heterosexual pairs may be due to the constant
availability of receptive females in the
group; in the pair situation the females
would be receptive only for a few days
every two weeks (see below).
278
D. CREWS AND N. GREENBERG
FIG. 2. Courtship display of the male green anole, Anolis carolinensis (top). Sexually receptive females stand
and neckbend (bottom) for courting males. See text for further details.
FUNCTION AND CAUSATION OF SOCIAL SIGNALS
The females' behavior also has a releasing effect on the male. Unmated, preovulatory females (B. Greenberg and Noble,
1944; Stamps, 1976a) or ovariectomized,
estrogen-primed females will solicit courtdftiip from a male if he fails to court them
(McNicol and Crews, 1979; Tokarz and
Crews, 1980). This usually consists of the
female approaching the male and headnodding, a behavior that invariably results
in the male performing one or more courtship displays and frequently mating with
the female.
UNDERLYING NEURAL AND
NEUROENDOCRINE MECHANISMS
279
cleus which conveys somatic sensory
information to a central area of the DVR.
The remaining lateral portion of the DVR
is continuous rostrally with dorsal cortex
and may be the target of an undescribed
sensory pathway, possibly trigeminal
(Northcutt, 1978). Most projections leaving ADVR are restricted to the telencephalon. The ventral boundary of the
ADVR is the dorsal medullary lamina (Fig.
3), beneath which are the striatal structures. The principal telencephalic efferent
is the lateral forebrain bundle which arises
in the ventral striatum (Voneida and Sligar, 1979).
The posterior DVR (PDVR) is recognizable caudal to the anterior commissure. It
is not known to receive discrete thalamic
projections, but possesses the nucleus
sphericus, a terminal nucleus for afferent
vomeronasal projections, the development
of which seems to correspond to the development of the vomeronasal apparatus.
In some anoles a rudimentary n. sphericus
can be detected, but in A. carolinensis it is
absent (Greenberg, unpublished).
In order for these ecological factors to
stimulate gonadal activity and the associated reproductive behaviors, it is necessary
that they be perceived by the organism and
transduced into neural activity. Much of
this information ultimately converges on
the hypothalamus, where it influences pituitary and autonomic function and, in
turn, the target organs. Here we consider
briefly the sensory afferents in iguanid lizards, the neural sites of steroid hormone
Auditory projections. While similar in basic
uptake, and finally, the neuroendocrine organization to the ascending auditory
control of pituitary, gonadal, and adrenal pathway in mammals and birds, the repfunction.
tilian auditory system shows considerably
less nuclear differentiation, although there
The lizard forebrain and afferent influences
is reason to believe that reptiles can resolve
The lizard forebrain consists of paired different frequency components of sound
cerebral hemispheres comprised of a cor- (Foster and Hall, 1978). Nerve fibers from
tex (pallium) which overlies the lateral ven- the cochlea are conveyed in the acoustic
tricles of the brain, and a subventricular nerve to several nuclei in the brain stem.
area consisting mainly of septal, striatal, The major recipient of acoustic brain stem
and "amygdaloid" nuclei (Fig. 3). The dor- projections is the central nucleus of the tosal ventricular ridge (DVR) is a strikingly rus semicircularis, a midbrain structure
large structure of pallial origin. The an- homologous to the inferior colliculus of
terior portion of the DVR (ADVR) mammals and the nucleus mesencephalic
possesses the terminal targets of ascending lateralis pars dorsalis of birds. The central
thalamic pathways of at least three sensory nucleus of the torus then sends projections
modalities (Northcutt, 1978), a circum- by way of the dorsal thalamus to a medial
stance similar to parts of the mammalian anterior DVR site that has been identified
neocortex (Butler, 1978). These projec- as the most rostral target of the ascending
tions consist of a dorsal thalamic visual auditory system (Pritz, 1974).
projection from the optic tectum to the latOlfactory and vomeronasal projections. The
eral third of the DVR, a dorsal thalamic olfactory/vomeronasal apparatus of repauditory projection from the torus semi- tiles show considerable variation in their
circularis to the medial third, and a pro- degree of development. Compared to othjection from a more caudal thalamic nu- er lizards, A. carolinensis has an extremely
280
D. CREWS AND N. GREENBERG
Cx. dors.
,Cx, med.
Pal. membr.
A.D.V R.
Septum
Pal.
Med. inter.
N. tr. olt. lat.
A.D.V.R.
Comm. hip.
Comm. ant.
Tr. opt.
FIG. 3. Three levels of the forebrain of the green anole lizard, Anolis carolinensis. Drawings combine adjacent
sections stained for cells and fibers, respectively. A: Level at the "zero" plane, beneath the parietal eye. B:
Level of the anterior commissure, .65 mm posterior to the zero point; C: .5 mm posterior to the anterior
commissure. Abbreviations: ADVR, anterior dorsal ventricular ridge; Comm. hip., hippocampal commissure;
Comm. ant., anterior commissure; Cx. dors., dorsal cortex; Cx. med., medial cortex; DML, dorsal medullar
lamina, LFB, lateral forebrain bundle; Med. inter., medial interposition; N. ace, nucleus accumbens; N. tr. olf.
lat., nucleus of the lateral olfactory tract; Ps., paleostriatum; Pal., pallium; Pal. membr., pallia] membrane,
PDVR, posterior dorsal ventricular ridge, Tr. opt., optic tract. PDVR is sometimes regarded as amygdala.
reduced olfactory/vomeronasal apparatus.
Although there is no morphological reason to assume that chemical senses are not
utilized by Anolis (Armstrong et al., 1953),
olfaction could not be demonstrated in
prey selection (Curio and Mobius, 1978).
The olfactory bulbs in A. carolinensis are
relatively small and extended before the
forebrain on slender peduncles. The accessory olfactory bulb, which receives the
vomeronasal nerve in all lizards, is a caudal
medial extension of the main bulb.
Those olfactory projections that pass beyond an anterior olfactory nucleus are
generally divided into lateral and medial
tracts. Fibers from the accessory bulb join
the relatively larger lateral tract. The main
bulb fibers terminate in a nucleus of the
lateral tract and a lateral ("pyriform") cortical field while the accessory fibers project
to a nucleus in the PDVR. A projection to
this area exists even in Anolis which has no
recognizable terminal nuclear group
(Greenberg and Switzer, unpublished).
Visual projections. In many diurnal lizards, vision has become a dominant sensory modality. Unlike snakes and other orders of reptiles, most lizards have all cone
retinas (Prince, 1956; Underwood, 1970)
with very dense foveae and thick retinal
inner nuclear and ganglion layers that are
exceeded only slightly by some birds
(Walls, 1942).
In A. carolinensis and /. iguana most retinofugal fibers decussate in the optic
chiasm, but a few fibers to the thalamus
remain uncrossed; these species do not
show projections to the hypothalamus
(Butler and Northcutt, 1971). Lizard retinal ganglion cells project to the dorsal and
FUNCTION AND CAUSATION OF SOCIAL SIGNALS
281
Fie. 4. Visual areas in the brain of the green anole lizard, Anolis carolinensis, as demonstrated by the ("C)
deoxyglucose metabolic mapping technique. A translucent patch covered the right eye. The left eye was
stimulated by viewing another male for 45 min following a 2 fid pulse of (14C) deoxyglucose administered
i.p. Photographs A—C are autoradiographs of coronal sections (20 ptm); photographs D—F are these same
sections after staining to demonstrate neuronal cell bodies. The right side of the brain is to the right. Areas
of asymmetrical metabolic activity are apparent: (A) in part of the anterior dorsal ventricular ridge; (B) in
nucleus rotundus and the lateral geniculate nucleus (the darkened area on the dorsal surface is caused by
folding of the tissue); (C) in the superficial layer of the optic tectum. (Allen, Adler, Greenberg, and Crews,
unpublished data.)
282
D. CREWS AND N. GREENBERG
ventral thalamus, tectum and pretectum,
nucleus of the basal optic tract and the hypothalamus (Ebbesson, 1970) (Fig. 4).
Neural sites of steroid hormone uptake
interesting that lesions immediately rostral
to the AH-POA also lead to testicular atrophy in intact male A. carolinensis, presumably acting via their effect on cells that produce gonadotropin releasing hormone
located in this region (Wheeler and Crew^
1978) (see below;).
While lesions in the AH-POA/ME produce results consistent with findings in
other vertebrates, intracranial implantation studies indicate that steroid feedback
regulation of pituitary gonadotropin secretion in lizards may be unlike that of
mammals. Implantation of estrogen into
the ME or AH of female S. cyanogenys in
mid or late stages of vitellogenic growth
inhibits ovulation although follicular development with accompanying oviduct
growth is not retarded (Callard et al.,
1972). Progesterone implantation into the
AH near the end of the ovarian growth
phase has no effect on ovulation but if performed in the midvitellogenic stage, such
an implant will prevent further ovarian
growth and induce follicular atresia. These
studies suggest that in lizards, unlike mammals, estrogen acting at the level of the
hypothalamus prevents the ovulatory
surge of GTH, but not its tonic secretion,
whereas progesterone inhibits tonic GTH
secretion but not the ovulatory surge.
Sex steroids are concentrated in specific
regions of the brain where they alter neural activity. The distribution of hormone
sensitive cells is similar in all vertebrates
studied (Morrell and Pfaff, 1978). In A.
carolinensis estradiol, testosterone, and dihydrotestosterone concentrating cells are
located in the anterior hypothalamicpreoptic area (AH-POA), septum, amygdala, basal tuberal hypothalamus, torus
semicircularis, and anterior pituitary
(Morrell et al., 1979). Males and females
show the same pattern of uptake for all
three hormones, although estradiol treated animals exhibit the most intense labeling with a highly localized pattern of uptake. T h e r e are, however, areas that
selectively bind estradiol but not testosterone and dihydrotestosterone and vice versa. For example, the lateral and dorsal cortices contain cells that selectively bind
estradiol, while there are many well-labelled cells in the mesencephalic tegmentum only after administration of androgen.
It would be valuable to know the neural
concentrating sites of adrenal steroids in
the lizard brain since these hormones also Hypothalamic-adrenal axis
have profound influences on behavior as
The hypothalamic-adrenal axis is the
in mammals (Callard et al., 1973; McEwen principal means by which vertebrates reetal, 1972).
spond to acute and chronic stress. In reptiles, the homolog of the adrenal medulla
Hypothalamic-pituitary-gonadal axis
is peripherally placed relative to the "corHypothalamic control of pituitary func- tex" and is termed the "adrenal" gland
tion in reptiles is well established (reviewed while the more centrally placed cortical
in Crews, 1979a, b; Licht, 1974). Gesell and homolog is termed the "interrenal" gland
Callard (1972) have described in Dipsosau- (reviewed in Gabe, 1970).
rus dorsalis a major neurosecretory tract
The hypothalamus is also the final CNS
arising from the paraventricular and su- component of interrenal gland activation.
praoptic nuclei in the anterior hypothala- Glucocorticoids and mineralocorticoids in
mus (AH) and running through the me- reptiles are less differentiated in both their
dian eminence region (ME) where it comes controlling mechanisms and their function
in contact with capillaries of the hypothal- than in mammals (Callard et al., 1973).
amo-hypophyseal portal vessels. Radio- Other differences from the mammalian
frequency lesions in the AH-POA or the pattern include an apparent negative feedME result in testicular atrophy in sexually- back control at the hypothalamic level of
active A. carolinensis (Wheeler and Crews, both corticosterone and aldosterone and a
1978; Farragher and Crews, 1979). It is greater independence of adrenal steroido-
FUNCTION AND CAUSATION OF SOCIAL SIGNALS
genesis from pituitary control (Callard et
al., 1973). As in gonadal sensitivity to gonadotropic hormones, interrenal sensitivity
to ACTH is also temperature dependent
(Licht and Bradshaw, 1969; Callard et al,
#973).
The adrenal and interrenal glands are
in intimate anatomical association with
each other and with the reproductive ducts
in reptiles. However, this association with
reproductive structures has no known
functional significance. The adrenal chromaffin hormones epinephrine (E) and
norepinephrine (NE) have different physiological actions and the possible alteration
of their ratio may represent a significant
adaptation to chronic stress. These catecholamines are also important in body color phenomena often utilized as social signals (see below).
283
estrogens are known to influence differentiation of the reproductive ducts (reviewed by Adkins, 1980a) and probably
have far-reaching effects on other sexually-dimorphic characters. For example, in
most reptiles, the sexes are dimorphic in
body size. The male's larger size is not due
to lesser energetic demands (Gorman and
Licht, 1973) but probably to testicular hormone effects.
Different characters undergo sexual differentiation at different times. For example, hatchling A. carolinensis can be sexed
by the presence of two conspicuous postanal scales in the male, but the dimorphism in the retrobasal process of the
hyoid apparatus does not become apparent until later in life (Fig. 5). The hemipenes, which are formed between 12 and
17 days of embryonic life, appear before
the scales, which form between days 20
SEX STEROID EFFECTS OF MORPHOLOGY
and 23 (Pearson and Licht, 1974). Sexual
AND BEHAVIOR
dimorphisms have been reported also for
The gonadal hormones have major in- the femoral glands of Crotaphytus collaris
fluences on both the morphology {e.g., sec- (Cole, 19666) and body color of adult Sceondary sex characters) and behavior {e.g., loporus occidentalis (Kimball and Erpino,
facilitation of sexually dimorphic displays) 1971). Male S. occidentalis develop medial
of the organism. These effects can, in turn, stripes of dark pigment on their ventrum
be separated according to their temporal as they approach maturity; this distinct
qualities and their permanence. Organi- male pigmentation pattern can be induced
zational effects of hormones have tradi- in immature males and females with
tionally referred to morphological and administration of exogenous androgen.
psychosexual differentiation, usually as a
Many of these sexually-dimorphic strucconsequence of exposure to hormones tures undergo cycles of activity that are
during early life. Activational effects of correlated with the reproductive season,
hormones, on the other hand, refer gen- indicating an activational role of horerally to their ability to elicit or facilitate mones. Although there is no evidence for
behavior patterns characteristic of one sex an annual fluctuation in the color pattern
after physical differentiation. These phe- of adult S. occidentalis, the blue ventral
nomena do not so much represent mu- markings become more intense ( = melatually exclusive categories as they do points nophore expansion) during the breeding
of perspective.
season (Kimball and Erpino, 1971). Castration results in a decline in the level of
Peripheral action
melanophore expansion, but this can be
Hormones are responsible for the dif- prevented by simultaneous administration
ferentiation of secondary sex characters of testosterone propionate. In several
and their accessory structures. In reptiles, iguanid lizards, gravid females have orthe period of sexual differentiation is pro- ange spots on the sides and flanks which
tracted, beginning in embryonic life and they display toward the courting male.
extending post-hatching (Forbes, 1940, These spots are rapidly acquired and are
1956). Steroidogenic activity of the embry- brightest on the day of ovulation and imonic gonad has been demonstrated (Ray- mediately afterwards while the eggs are
naud and Pieau, 1971). Androgens and oviducal. This color change is under hor-
284
D. CREWS AND N. GREENBERG
75 r ADULT
55
E
Female
(n = !32)
Male
n = 115)
45
2
UJ
35 —
o
3 5 -
CO
HATCHLING
25-
I
15
10
15
20
25
30
35
LENGTH OF RETROBASAL PROCESS (mm)
FIG. 5. Sexual dimorphism of the retrobasal process of the hyoid apparatus in the green anole, Anolis
carolinensis.
monal control and can be induced by exogenous progesterone but not estradiol17/3 in ovariectomized Crotaphytus (Cooper
and Ferguson, 1972a, b; Medica et al.,
1973); however, estradiol does have a priming effect if injected before progesterone
(Cooper and Ferguson, 1973; Medica etai,
1973).
tion of testosterone propionate (Adkins
and Schlesinger, 1979). Further, male-like
mating behavior has been observed in allfemale parthenogenetic Cnemidophorus lizards (Crews and Fitzgerald, 1980). Whether hormones have an organizing influence
on adult reproductive behavior in reptiles
will require studies in which hormones are
administered early in life and their subseCentral action
quent effects on psychosexual developUnfortunately, nothing is known about ment determined.
the differentiation and development of reIt is well-established that the steroid horproductive behaviors in reptiles (reviewed mones act on specific areas of the brain to
in Adkins, 1980a, b). There is some evi- modulate reproductive behavior. In addidence though to suggest that the neural tion to being a site of hormone feedback
substrate of mating behavior may not be control of pituitary function, the anterior
sexually dimorphic. For instance, court- hypothalamus-preoptic area (AH-POA) is
ship and copulatory behavior can be elic- known to play a crucial role in the reguited in female A. carolinensis by administra- lation of male reproductive behavior in
FUNCTION AND CAUSATION OF SOCIAL SIGNALS
vertebrates (reviewed in Crews and Silver,
1980). For example, in A. carolinensis, bilateral radiofrequency lesions in the AHPOA abolish courtship and agonistic behavior; lesions in area dorsal or caudal to
^ftis area have no effect on these displays
(Wheeler and Crews, 1978). Lesions immediately rostral to the AH-POA of intact
A. carolinensis also cause a significant decline in display behavior. In this instance,
however, the effect is probably not due to
the destruction of a behavioral integrative
area but rather is due to the destruction of
gonadotropin releasing hormone producing cells located in this region. This is indicated by the fact that such animals
undergo testicular collapse following lesioning, but display behavior can be reinstated by administration of exogenous androgen. Other evidence suggesting that
display behavior is reliant both on the integrity of the AH-POA and specific hormonal conditions is that implantation of
androgen directly into the AH-POA restores courtship behavior in castrated, behaviorally inactive A. carolinensis; implants
outside this area or cholesterol implants
within the AH-POA have no effect (Morgentaler and Crews, 1978; Crews and Morgentaler, 1979).
The basal hypothalamus also appears to
be a major integrative area for regulating
male reproductive behavior in lizards. Destruction of either the anterior or posterior
basal hypothalamus results in a rapid decline in the display behavior of castrated,
androgen-treated A. carolinensis (Farragher and Crews, 1980).
INTEGRATION OF EXTERNAL CUES AND
INTERNAL STATE IN THE
CAUSATION OF BEHAVIOR
When investigating the neural control of
behavior, it is important to distinguish between behaviors that are not influenced by
hormones from those that are hormonedependent. It is clear that certain activities
of specific neural systems are influenced
by hormones (Komisaruk, 1971, 1978).
Social signals and lizard display behavior
Behavioral displays involve communication between conspecifics. Like other
285
cues of great relevance to the survival of
a species, these social signals are selectively
perceived and integrated into a complex
sequence of physiological and behavioral
events in a way that structures their outcomes and thus the ultimate social organization. Displays are both influenced by
their evolutionary origins and exert a selective pressure on the perceptive and integrative centers of animals that respond
to them. Among the sensory modalities
known to play an important role in the social behavior of lizards are audition, chemoreception, and vision.
Auditory signals. Sounds produced by
reptiles include various squeaks, hisses and
even scale scraping (Gans and Maderson,
1973), but only recently have studies been
concerned with true vocalizations, that is,
modulated vocal emissions consistent in
form (Marcellini, 1978). Frequency, intensity and pattern of vocalizations in Gekkonidae have been studied and reviewed by
Marcellini (1978), who points out that vocalizations often functionally parallel the
visual displays of iguanid lizards.
Among the iguanid lizards, the sensitivity of the anoline ear is excellent with the
best performance from A. carolinensis over
a range of 500-3,000 Hz (Wever, 1978).
Although auditory stimuli can influence
behavior particularly in the absence of visual information in Anolis (Rothblum etal,
1979), sounds emitted during social encounters do not clearly have a social function and are probably anti-predator behaviors (Milton and Jenssen, 1979).
Chemical signals. Although chemical cues
have been demonstrated to play an important role in the social behavior of snakes,
turtles, and crocodilians (reviewed in
Crews, 1980; Madison, 1977), little is
known about their function in lizards. In
many iguanid species, males have enlarged
proctodeal and femoral glands that are
seasonally active (Cole, 1966a). Reproductively active males are often seen rubbing
their vent and/or hindlegs against surfaces
in their territories. Further, tongue flicking, a prominent activity in skinks, varanids, teiids, and other lizards with forked
tongues, is also often seen in iguanid lizards (Bissinger and Simon, 1979). This be-
286
D. CREWS AND N. GREENBERG
iguana, regional differences in the frequency of responses elicited by electrical
stimulation are apparent; however, no
clear correlations with specific anatomical
structures are discernible (Distel, 1978).
Dewlap extension was elicited at most h]0
pothalamic sites at low stimulus intensities.
Head-nodding, a component of many social displays in this species, was elicited
most reliably immediately after stimulus
offset at sites caudal to the forebrain. The
few telencephalic sites where nodding was
elicited were in the striatum and septum.
In these instances, the response occurred
during stimulation, suggesting possible
disinhibition by higher neural areas of a
response organized more caudally. Components of display behavior were also elicited by electrical stimulation of the brain
of Crotaphytus collaris (Sugerman and Demski, 1978). While gular extension, a component of defensive as well as aggressive
display, is elicited by stimulation of almost
all sites from the telencephalon through
the medulla, agonistic elements were limited to stimulation of the amygdaloid complex, septum and preoptic area.
Ablation studies. Changes in social behavior and perch site preference were observed in S. occidentalis after lesions in one
of several "amygdaloid" nuclei (Tarr,
1977). While deficits in social responsiveness were attributed to an inability to process aggressive social cues, many animals
exhibited marked decreases in spontaneous activities. In A. carolinensis radiofrequency lesions in the paleostriatum have
no influence on activity levels or assertion
display behavior, but if the lesion includes
the lateral forebrain bundle, the challenge
response is eliminated or significantly reduced (Greenberg et al., 1979). Since in
this species the optic decussation is almost
complete (Butler and Northcutt, 1971), it
is possible to lesion unilaterally and then
by use of a removable eyepatch to test anForebrain mechanisms of display behavior
The function of the forebrain in inte- imals when vision is restricted to the legrating and effecting social behavior in liz- sioned or the intact hemisphere (Greenards has been studied by both stimulation berg, 1977a). In this way, the subject can
be used as its own progressive post-operand ablation experiments.
Stimulation studies. In the forebrain of /. ative control. Utilizing this model, prelimhavior is greatest when exploring new
areas (DeFazio et al., 1977). To date, however, few studies have associated the potential chemical cues provided by this activity with a socially significant response in
conspecifics. Male and female S. occidentalis display significantly more often when
presented with surfaces "labelled" with the
droppings of conspecifics than when presented with unlabelled surfaces (Duvall,
1980). That chemical cues may be utilized
for sex identification is suggested by the
behavior of male Coleonyx variegatus who
"taste" the tails of all potential mates; when
male and female tails are surgically exchanged, a courting male will address his
attention only to the animal with the female tail (B. Greenberg, 1943).
Visual signals. Visual social signals consist
of dynamic (e.g., display action patterns)
and static (e.g., postures and colors) behavioral elements. In male-male interactions, social status is a significant factor in
determining the relative access of males to
females. Status is associated in many
species with distinctive colors (e.g., Anolis
cuvieri, Rand and Andrews, 1975; A. agassizi, Rand et al., 1975; Agama agama, Harris, 1964) and as status signals, these colors
may be important in continually reinforcing the effects of decisive aggressive interactions on conspecifics. Under ecologically
realistic conditions of temperature and illumination, dominant male A. carolinensis
are characteristically green while subordinates are typically brown (Greenberg, unpublished). Since the color changes are
profoundly influenced by adrenal/interrenal hormones, it is likely that they function as an external indicator of relative
stress (see below). That these characteristic
colors are generally reversible as social relationships shift indicates further that color may function as a signal in this species.
FUNCTION AND CAUSATION OF SOCIAL SIGNALS
287
inary studies indicate a significant role for 19746; Crews et al., 1978), and in longseptal and posterior DVR nuclei in the reg- term castrates upon intracranial implanulation of social and reproductive behavior tation of hormones (Crews and Morgen(Greenberg, Crews, and Scott, unpub- taler, unpublished) (Fig. 6).
lished).
Sexual receptivity in female A. carolinensis is also controlled by a complex sequence
Neuroendocrine integration of display behavior of hormonal and neural events. In all anoLizard display behavior provides an ex- line lizards, a single follicle matures and is
cellent opportunity to study the hormonal, ovulated; in A. carolinensis, this occurs
neural, and neuroendocrine mechanisms every 2 wk in the breeding season (Crews,
underlying social interactions. The many 1973a; Hamlett, 1952; Licht, 1973). Durthreads of intraspecific interactions consti- ing this time, Anolis females will stand for
tute the fabric of social organization and a courting male (estrus) only during the
the ultimate test of its adaptiveness: repro- latter half of the follicular cycle (Crews,
ductive success. While gonadal hormones 1973a; Stamps, 1977) and, unless mated,
dominate the integrative activities con- will remain receptive for about 24 hr after
cerned with reproduction, adrenal hor- ovulation. Plasma estrogen levels are low
mones play a significant role in social or- during the early stages of follicular growth
ganization.
but increase three-fold immediately before
Gonadal hormones and behavior. Male ovulation (Tokarz and Crews, unpubcourtship behavior is dependent upon tes- lished). Progesterone levels are highest
ticular activity (androgen production) during the breeding season, but it is as yet
(Crews, 19796). If a male is presented with not known if they vary with follicular cona female (of any reproductive state) during dition.
the winter, he will ignore her. That same
Female sexual behavior is estrogen-demale in the late spring and summer, how- pendent in A. carolinensis. Ovariectomy
ever, will court energetically and, if the fe- abolishes sexual receptivity while treatmale stands and neckbends, will mate with ment with exogenous estrogen reinstates
her. Castration of sexually-active males estrus in a dose-related manner (Crews,
abolishes this behavior. The aggressive be- 1979a, b). As in many mammals, progesterhavior of males, unlike courtship, does not one plays a central role in A. carolinensis in
appear as reliant on testicular hormones. coordinating the physiological and behavMales will continue to challenge intruders ioral events during the breeding season. In
for at least two weeks following castration oviparous lizards, luteal progesterone inif returned to their home cage (Crews et fluences ovarian activity directly. The dual., 1978). If placed in a new environment, ration of egg retention is reduced followagonistic behavior declines sharply. Famil- ing lutectomy, thereby decreasing the
iarity with the environment also modulates interval between follicular cycles in both S.
the agonistic behavior of sexually-active undulatus (Roth etal., 1973) and C. uniparmales. An intact or castrated, androgen- ens (Cuellar, 1979), while administration of
treated male will not immediately defend exogenous progesterone prevents gonada new cage, especially if it is larger than his otropin-induced ovarian growth in S. cyanprevious home cage (Crews, unpublished). ogenys (Callard et al., 1972; see also Yaron
There is evidence also to suggest that and Widzner, 1978). Recent studies with
courtship and aggression have different A. carolinensis show that estrogen acts at
neural thresholds in responsiveness to an- the neural level to increase progesterone
drogen. For example, the pattern of rein- receptor in the diencephalon (McEwen,
statement of first aggression followed by Tokarz, and Crews, unpublished); estrocourtship is seen in winter dormant males gen and progesterone synergize to faciliupon environmental stimulation (Crews, tate the onset of female sexual receptivity
1974a), in castrates given subcutaneous an- (McNicol and Crews, 1979). It is significant
drogen replacement therapy (Crews, that about half of the females tested and
288
D. CREWS AND N. GREENBERG
later found to be in the middle of their
second or third follicular cycles are sexually receptive versus none of the females
at the same ovarian stage of their first follicular cycle (Crews, 1973a). Finally, there
is some evidence that progesterone can
also have an inhibitory effect on female
sexual receptivity in A. carolinensis as in
many mammalian species (Valenstein and
Crews, 1977; McNicol and Crews, 1979).
While the expression of sexual receptivity depends upon ovarian hormones, its
maintenance is liable to exteroceptive stimuli. If a preovulatory female mates, she will
not be receptive again until the next follicular cycle. Since intact, estrogen-primed
females are rendered unreceptive to male
courtship whereas ovariectomized, estrogen-primed females are once again receptive within 24 hr of mating (Valenstein and
Crews, 1977), the presence of the ovaries
(or, more likely, some change in ovarian
hormone production) is critical for this
long-term inhibition of female sexual receptivity.
Intromission by the male is the critical
stimulus initiating mating-induced inhibition of estrous behavior in A. carolinensis
(Crews, 19736). In rodents, vagino-cervical
stimulation during mating initiates a neuroendocrine reflex involving an initial release of prolactin and maintained elevations of progesterone that effectively
suppresses lordosis behavior (Adler, 1974;
Carter et al., 1976). Our evidence, although still incomplete, suggests the existence in A. carolinensis of a similar neuroendocrine reflex whereby female sexual
receptivity, induced by ovarian hormones,
is terminated by sensory stimuli. These
stimuli also alter the female's hormonal
state, maintaining nonreceptivity until the
follicle is ovulated and another follicle begins to develop.
As mentioned previously, seasonally
breeding vertebrates exhibit circannual
rhythms in sensitivity to environmental
and physiological stimuli. For example, in
A. carolinensis there is a sharp decrease in
sensitivity to temperature, social stimuli,
and exogenous gonadotropin in the late
summer and early fall, the reproductive
refractory period (Crews and Licht, 1974;
Crews and Garrick, 1980; Licht, 1971).
Whether this refractoriness is controlled at
the level of the gonads or the brain or both
is still unclear (cf., Crews and Licht, 1974;
Crews and Garrick, 1980; Cuellar and
Cuellar, 1977). The time of year is a po-^
tentially important variable in behavioral
studies as well. We have documented recently that ovariectomized A. carolinensis
are behaviorally less sensitive to estrogen
replacement therapy in the refractory period than in the breeding season (Fig. 7),
suggesting a circannual rhythm in neural
sensitivity to ovarian hormones.
Adrenal hormones and social organization.
There are several related ways in which
interrenal/adrenal function might be significant in the social behavior of lizards:
social stress, reproductive condition, and
skin color.
Social stress. Stimuli provided by conspecifics can be stressful and require physiological compensation on the part of the responding animal if homeostasis is to be
preserved. To a considerable extent the
compensation can be anticipatory, preparing an animal for imminent stress.
Acute stress elicits an "emergency" or
"fight or flight" response by means of hypothalamic activation of the sympathetic
nervous system and stimulation of adrenal
chromaffin cell secretion of the catecholamines E and NE. Sustained stress results
in increased pituitary ACTH secretion
which, in turn, stimulates release of interrenal steroids. If an animal cannot adapt
to the chronic activation of physiological
defenses, a potentially-lethal "hypersympathetic" (Wehle et al., 1978) or "general
adaptation syndrome" (Selye, 1956) develops. The specific relationship of social
stress to adrenal function requires further
study, but at least two lines of evidence indicate this to be a fruitful area. Crowding
of the iguanid lizard Dipsosaurus results in
significantly enlarged interrenal/adrenal
glands (Callard et al, 1973). In the teiid
lizard Cnemidophorus, reduced social status
is correlated with enlarged interrenal/adrenal glands (Brackin, 1978). The stress of
reproductive activity may also be reflected
in interrenal activity. In Dipsosaurus, females have larger glands, especially during
289
FUNCTION AND CAUSATION OF SOCIAL SIGNALS
the active reproductive phase (Callard et
al., 1973), an effect probably attributable
to elevated estrogen levels in the lizard, as
in mammals (Kitay, 1969).
Reproductive condition. Conditions which
^engender stress also frequently affect reproductive functions (e.g., Bliss et al.,
1972; Ramaley, 1974; Archer, 1979) although it is not clear the extent to which
these are correlated rather than causally
related phenomena. Subordinate lizards
are chronically stressed and have reduced
reproductive function (Crews, unpublished; Greenberg, unpublished) as well as
enlarged adrenal/interrenal glands (Brackin, 1978).
Skin color. Morphological color changes
involve absolute amounts of pigment,
while physiological color change refers to
the relative visibility of color as affected by
chromatophore pigment granule dispersion or aggregation (see above). Social control of the physiology underlying color
change is an excellent example of how
both internal and external environments
may combine to regulate social signals.
Both sympathetic activation and melanocyte
stimulating hormone (MSH) can affect
body color. However, A. carolinensis, in
specific social situations, exhibits chromatophore responses controlled by E and NE
(Hadley and Goldman, 1969), while MSH
may not have a significant influence (Hadley and Bagnara, 1975). Unlike most lizards, the chromatophores of A. carolinensis
have no sympathetic innervation (Kleinholtz, 1938), and thus this species provides
us with a natural experiment in which activation of adrenal catecholamines are
readily obvious. In most instances, body
color is a balance between the effects of E
and NE on and adrenergic receptors
(Hadley and Goldman, 1969) or between
the density of the receptors themselves.
This balance, however, appears to be
tipped one way for dominants (characteristically green) and the other way for subordinates (characteristically brown). Thus,
by using color, the status of males and certain of its physiological correlates can be associated (Greenberg, unpublished). There
are two other ways in which the E/NE
balance is altered: by the emergency re-
30r-
CE
O
o
to
p20
i
X
If)
10
129
X)
2
DAYS
FIG. 6. Seasonal differences in behavioral sensitivity
to estrogen in the green anole, Anolis carolinensis.
Adult females obtained in June (•) and September
(O) were ovariectomized within two weeks of arrival
in the laboratory. Two weeks following ovariectomy,
females were pretested for sexual receptivity (•). Immediately following the pretest, females were treated
with estradiol benzoate (1.4 ftg, s.c.) and tested daily
for sexual receptivity. Mean and standard error and
sample sizes are shown. (Tokarz and Crews, unpublished.)
sponse in acutely stressful situations and
by an increase in corticosterone facilitated
methylation of NE to E (Wurtman et al.,
1967) under the influence of chronic
stress.
Color as an external indication of physiological condition and status has been exploited as a social signal in several lizard
species (Harris, 1964). In A. agama, territorial dominants have a bright red head,
the sight of which elicits defensive responses in subordinates and aggression in
other dominants. Harris (1964) asserts that
the sight of the red head acts as a "suppressor" of dominance behavior in subordinate males. A dominant S. cyanogenys has
only to lift its head, revealing its blue chin,
to suppress activity in subordinates observing him (Greenberg, 19776). In A. carolinensis, subordinate animals, while display-
290
D. CREWS AND N. GREENBERG
ing some indications of physiological stress
(brown skin color) do not suffer autonomic
collapse. However, when long-term dominants are displaced, they often die after a
relatively brief period of behavioral
depression (Greenberg, unpublished data
on A. carolinensis and A. agama).
CONCLUDING REMARKS
The work reviewed here demonstrates
how the environmental and physiological
milieus are integrated in the regulation of
social displays and thus social organization.
These adaptations have evolved to synchronize reproductive activities and maximize fitness in the environment in which
the animals evolved. Because of the wealth
of information available on their ecology
and anatomy, many reptiles are uniquely
suited to the investigation of specific problems in behavior. The research with the
green anole lizard, Anolis carolinensis, in
particular, illustrates how the methodological perspective of ethology and comparative psychology and different levels of
analysis can be combined to give us a better
understanding of how internal and external stimuli interact.
Sadlier (eds.), Reproductive behavior, pp. 259-286.
Plenum Press, New York.
Archer, J. 1979. Animals under stress. University Park
Press, Baltimore, Maryland.
Armstrong, J. A., H. J. Gamble, and F. Goldby. 1953.
Observations on the olfactory apparatus and the
telencephalon of Anolis, a microsomatic lizard. J ^
Anatomy 87:288-307.
*
Bissinger, B. E. and C. A. Simon. 1979. Comparison
of tongue extrusions in representatives of six
families of lizards. J. Herpetology 13:133-139.
Bliss, E. L., A. Frischat, and L. Samuels. 1972. Brain
and testicular function. Life Sci. 2:231-238.
Botte, V., F. Angelini, O. Picariello, and R. Molino.
1976. The regulation of the reproductive cycle
of the female lizard, Lacerta sicula sicula Raf.
Monitore Zool. Ital. (N.S.) 10:119-133.
Brackin, M. 1978. The relation of rank to physiological state in Cnemidophorus sexlineatus domi-
nance hierarchies. Herpetologica 14:185—191.
Brown, K. M. and O. J. Sexton. 1973. Stimulation
of reproductive activity of female Anolis sagrei by
moisture. Physiol. Zool. 46:168-172.
Butler, A. B. 1978. Forebrain connections in lizards
and the evolution of sensory systems. In N.
Greenberg and P. D. MacLean (eds.), Behavior
and neurology of lizards, pp. 65-79. National In-
stitutes of Mental Health, Washington, D.C.
Butler, A. B. and R. G. Northcutt. 1971. Retinal projections in Iguana iguana and Anolis carolinensis.
Brain Res. 26:1-13.
Callard, 1. P., S. W. C. Chan, and G. V. Callard. 1973.
Hypothalamic-pituitary-adrenal relationships in
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Callard, I. P., J. Doolittle, W. C. Banks, and S. W. C.
ACKNOWLEDGMENTS
Chan. 1972. Recent studies on the control of the
reptilian ovarian cycle. Gen. Comp. Endocrinol.
We wish to thank Richard Tokarz for
Suppl. 3:65-75.
reading the manuscript. Unpublished re- Carpenter, C. C. and G. W. Ferguson. 1977. Varisearch supported in part by NSF BNSation and evolution of stereotyped behavior in
13796, NINCDS 15305, NICHHD 12709,
reptiles. In C. Cans and D. W. Tinkle (eds.), Biology of the Reptilia, Vol. 7, pp. 335-555. Academand NIMH Research Scientist Developic Press, New York.
ment Award MH00135 to DC, and by NIH
Biomedical Support Grant RR-07088 to the Carter, C. S., M. R. Landauer, B. M. Tierney, and T.
Jones. 1976. Regulation of female sexual beUniversity of Tennessee and a Schweppe
havior in the golden hamster: Behavioral effects
Research and Education Fund Award to
of mating and ovarian hormones. J. Comp. Physiol. Psychol. 90:839-850.
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