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 mecha-nisms controlling reproduction in the green anole lizard, Anolis carolinensis. Both envi-ronmental and social stimuli that vary seasonally are used as proximate cues to repro-duction. In order for these ecological factors to initiate breeding, they must be perceivedand integrated in the central nervous system. External and internal stimuli converge uponthe hypothalamus, the major neuroendocrine integrative area of the brain, which, in turn,directly regulates pituitary and autonomic function. In addition to their role in repro-duction, the gonadal hormones are important throughout the life of the organism, actingboth peripherally and centrally, to adapt the individual to its environment. Thus, theenvironment, behavior, and physiology interact in complex ways to synchronize the socialand reproductive activities of individuals.

INTRODUCTION

It is valuable to think about the functionand causation of behavior at the same timebecause they are mutually illuminating:The perspective of one often helps solveproblems in the other. Traditionally, func-tion has been studied by ethologists con-centrating on spontaneous behavior ex-pressed in a natural setting. Problems incausation, on the other hand, have beenexplored largely by physiological and com-parative psychologists using techniques inwhich sources of variation are rigidly con-trolled if not eliminated. Thus, whileethologists document the diversity of be-havior, psychologists demonstrate the fun-damental commonalities in behavior. Attimes, these disciplines seemed irreconcil-able: The problems of control inherent inethological studies were contrasted withthe lack of appreciation for environmentalconstraints in comparative psychology.Tinbergen and Schneirla were early to rec-ognize the feasibility of a synthetic ap-proach. They and their students, most no-tably Hinde and Lehrman, brought the

1 From the Symposium on Social Signals—Compar-ative and Endocrine Aspects presented at the AnnualMeeting of the American Society of Zoologists, 27—30 December 1979, at Tampa, Florida.

rigor of the laboratory to the study ofspecies-typical behaviors.

Our purpose in this paper is to describebriefly: 1) some of the biologically signifi-cant stimuli impinging upon temperate cli-mate lizards; 2) the manner in which thesestimuli are perceived and integrated in thecentral nervous system; and 3) how this in-formation regulates the hormonal milieu,thereby influencing structures and behav-iors important in social interaction and re-production. In this pursuit we will draw onmany different disciplines which, whencombined, illustrate the power of the syn-thetic approach. Because we are most fa-miliar with the green anole, much of theinformation provided here will concernAnolis carolinensis. By emphasizing the gapsin our understanding, we hope to identifythose areas most likely to yield further in-sight into the function and causation of so-cial signals.

ECOLOGICAL INFLUENCES ONREPRODUCTIVE PHYSIOLOGY AND

SOCIAL BEHAVIOR

Much of the social behavior in temper-ate lizards is regulated by the conditionssurrounding the reproductive season.These regulatory mechanisms have evolvedbecause ultimately, such conditions reflect

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274 D. CREWS AND N. GREENBERG

the availability of food, changes in preda-tor pressure, and a hospitable environ-ment for the laying of eggs and their sub-sequent development. The exact timing ofreproduction from year to year is finelytuned by specific ecological stimuli. Theseinclude, among others, photoperiod, tem-perature, moisture, and the behavior ofconspecifics. These proximate factors,along with endogenous circadian or circ-annual rhythms of sensitivities to them,determine when animals reproduce.

Light

Although the seasonal change in pho-toperiod is used by most birds and mam-mals to cue reproduction, experimentshave shown that in many temperate lizardspecies, temperature is the proximate stim-ulus for gonadal recrudescence in thespring (Licht, 1972). The termination ofbreeding activity in A. carolinensis is, how-ever, reliant upon photoperiod as the pri-mary proximate factor (Licht, 1971). Thefact that the photosensitivity in testicularfunction is restricted to a four-monthperiod in the late summer and early fallunderscores the role of endogenousperiodicities in the environmental controlof seasonal reproduction in these animals.

The brightness and spectral quality oflight also vary predictably and may haveimportance in the timing of reproduction.For example, Licht (1969) demonstratedthat bright, but not dim, white light is suf-ficient to accelerate testicular recrudes-cence in A. carolinensis. At relatively lowintensities red light is more effective thangreen, while at high intensities, red andgreen are equally effective; blue light iscompletely ineffective at both intensities.Diurnal changes in intensity of illumina-tion have obvious implications for the ther-moregulatory activities upon which mostreptiles rely. Dim light, while of little ther-mal significance, can be a significant cue inmorning emergence (Greenberg, 1976)and shelter-seeking (Regal, 1967) and istherefore important in normalizing thepattern of daily activities.

Ultraviolet light appears to increase ag-onistic behavior in a number of iguanid

and agamid species (Moehn, 1974), as wellas being of metabolic importance to rep-tiles (Reichenbach-Klinke and Elkan, 1965).

Temperature

In most temperate areas, fluctuations \v%temperature can be great. As ectotherms,lizards must thermoregulate behaviorallyto accommodate their physiological needs(Dawson, 1975; Regal, 1978; Greenberg,1980). The significance of thermoregula-tory behavior is indicated by its many vitalconsequences, including maintenance ofoptimum activity of enzymes (Licht, 1967),muscles (Licht et al., 1969), heart rate(Licht, 1965a), digestion (Harlow et al.,1976), reproductive state (Joly and St. Gi-rons, 1975), and the sensitivity of targetorgans to hormones (see below).

In A. carolinensis, increasing tempera-tures elevate pituitary gonadotropin levelin both males and females; the differentpatterns of male and female emergencefrom hibernation (Gordon, 1956) suggesta sex difference in temperature sensitivity.This, in turn, stimulates spermiogenesis(Licht, 1972) and secretion of testicular an-drogen in males (Pearson et al, 1976), andvitellogenesis (Licht, 1973) and secretionof estrogen and progesterone (Tokarz andCrews, unpublished) in females. Similarly,in two species of Lacerta, the higher bodytemperatures characteristic of spring activ-ity are necessary for final testicular matu-ration and androgen secretion (Licht et al.,1969). High temperatures also appear tobe critical to vernal ovarian developmentin Uta stansburiana (Tinkle and Irwin,1965), Sceloporus undulatus (Marion, 1970),and L. sicula (Botte et al., 1976).

In addition to its effect on pituitary go-nadotropin secretion, temperature can in-fluence the responsiveness of the gonadsand related target tissues directly (Lichtand Pearson, 1969a, b; Licht, 1972, 1974;Pearson et al., 1976). However, maintain-ing lizards at or slightly above theirspecies-typical preferred temperature canresult in marked spermatogenic damage,a decline in appetite and growth, thyroidhypertrophy and death (Cowles and Burle-son, 1945; Wilhoft, 1958; Licht, 19656).

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FUNCTION AND CAUSATION OF SOCIAL SIGNALS 275

Moisture

The role of moisture has received littlestudy, but its importance is unquestioned.Seasonal rainfalls and their effect on theabundance of insect prey have long been

•recognized as important factors in reg-ulating the reproductive cycles of manyreptiles (reviewed in Crews and Garrick,1979). There is evidence that humidity orrainfall can influence reproductive func-tioning directly (Crews et al., 1974; Lichtand Gorman, 1970). Relative humidity, butnot the availability of drinking water, is thecritical cue controlling ovarian develop-ment in A. sagrei (Brown and Sexton,1973).

Behavior also can be affected by tran-sient variations in local conditions. A.aeneus in Grenada are active and displaythroughout the rainy season. Duringdroughts, the frequency of display de-clines, but if drinking water is given, dis-plays increase to pre-drought levels(Stamps, 1976a). Moisture is the primarystimulus for oviposition behavior in A.aeneus. Rainfall stimulates digging behav-ior, but eggs are not laid until soil moistureis adequate (Stamps, 19766).

Conspecific behavior

Social organization entails the coordi-nation of individuals, each acting in concertwith the climatic variables as well as inter-acting with each other. This conspecificbehavior is a significant aspect of the ecol-ogy of social lizards (Carpenter and Fer-guson, 1977; Stamps, 1977). Male A. car-olinensis, stimulated by rising ambienttemperature, emerge from winter hiber-nacula before the females to establishbreeding territories (Gordon, 1956). Dur-ing this period, the predominant displaybehaviors of males are the assertion andchallenge displays. These displays arespecies-typical and consist of rhythmicalbobbing movements of the forebody co-ordinated with extension of the gular fan(dewlap) (Crews, 1975a; Greenberg,1977a). Typically, males patrol their terri-tories, pausing on prominent perches toperform the assertion display (Fig. 1, top).

When encountering a conspecific intruderthat does not respond to the resident's as-sertion display by either leaving the terri-tory or adopting a submissive posture, theresident will perform the challenge display(Fig. 1, bottom). The identifying charac-teristics of the challenge display are theextreme lateral compression of the bodyand engorged throat. The challenge dis-play, if answered by the intruder in kind,is the opening salvo of a confrontation thatestablishes dominance of one male overthe other. As the encounter progressesand escalates, other behavioral phenome-na of potential signal value become appar-ent: Crests rise on the nuchal and dorsalmidline, the skin caudal to the eye dark-ens, and the tail may thrash or twitch.Evenly matched lizards often will spar withtheir open jaws; if they lockjaws, both twistviolently in an attempt to throw the otherfrom the perch.

By the time female A. carolinensisemerge from winter hibernacula the asser-tion display is the most common display ofterritorial males; since territorial bound-aries are by now recognized, challenges areobserved only occasionally in response totransient males. Females may establishhome ranges for feeding purposes (Stamps,1977), but relatively little is known aboutpossible female-female interactions andtheir effects on the distribution of femalesthroughout the habitat or on the priorityof access to various ecological resources. InA. carolinensis, it is common to find severalfemales within a male's territory (Gordon,1956). These females defend home rangesagainst neighboring females and transientfemales and males.

First encounters with territorial maleselicit assertion displays which females re-spond to by avoiding the male or perform-ing a characteristic subordination displayconsisting of rhythmical headnods. Aftera short time, males begin to court females(Fig. 2, top). The courtship display beginsin a manner similar to the assertion dis-play, but as the dewlap retracts, the maleadvances toward the female while noddinghis head rapidly. These rapid headnodsare the unique element of the courtship

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276 D. CREWS AND N. GREENBERG

FIG. 1.details.

Assertion (top) and challenge (bottom) displays of the green anole, Anolis carolinensis. See text for

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FUNCTION AND CAUSATION OF SOCIAL SIGNALS 277

display of this species. At first, females re-spond to all male courtship by fleeing fromthe approaching male. Eventually, the ap-proach distance lessens and females standand allow the male to copulate. A sexually-

preceptive female assumes a characteristicposture, the neckbend, thereby facilitatingthe male's neckgrip (Fig. 2, bottom); thesechanges in receptivity reflect changes inthe female's gonadal state.

The behavioral displays of male A. car-olinensis have profound effects on thephysiology and behavior of conspecific fe-males. For example, courtship behavior fa-cilitates the stimulatory effects of the en-vironment and, indeed, is necessary fornormal pituitary gonadotropin secretion(Crews, 1974a). By altering the stimulusconfiguration presented by the courtingmale, it has been possible to determine thecritical aspect of the male's courtship dis-play in facilitating environmentally-in-duced ovarian recrudescence (Crews,1975ft). When the extension of the dewlapis prevented by sectioning the retrobasalprocess of the hyoid, courting males areno more effective in stimulating femalesthan are castrated, sexually inactive males.The second prominent feature of malecourtship, the dewlap's color, is importantbut not critical. The courtship behavior ofmales whose dewlap color is changed frompink to dark blue by the injection of Indiaink is initially less effective than that ofunaltered males. It is important to notethat in natural populations around NewOrleans, La., male dewlap color variesfrom pink to light blue. Because of thisnaturally occurring variability, it would beof interest to determine if this experimen-tal phenomenon occurs naturally and, ifso, the ecological consequences of retardedovarian growth of females courted by blue-dewlapped males.

The female's perception of aggressivebehavior between males, on the otherhand, inhibits environmental stimulationof ovarian growth. Females exposed to ag-gressive males challenging one anotherand engaging in territorial combat will notinitiate ovarian growth despite beinghoused in a stimulatory environmental

regimen (Crews, 1974a). The critical fea-ture of aggression between males that isresponsible for this effect or its mecha-nism^) of action is not known. Variablessuch as the body compression characteris-tic of male aggression may be important tocounteracting the stimulatory effects ofthe environment. Since the courtship ofhyoidectomized males fails to facilitateovarian growth it is reasonable to proposethat the absence of dewlap extension inhigh-intensity, challenge behavior betweenmales might also contribute to this effect.

The courtship behavior of males also hasa short term or releasing effect on the be-havior of females. Sexually-receptive fe-males will not stand or show the neckbendresponse to the courtship of hyoidecto-mized males, but will mate with blue-dew-lapped males (Crews, 19756).

Just as male A. carolinensis influence thereproductive state of females, so can fe-male A. carolinensis serve as a priming stim-ulus to the male. Males housed with fe-males have heavier testes and are in a moreadvanced spermatogenic stage than maleshoused together in groups (Crews andGarrick, 1980). What cues the female pres-ent to effect this physiological accelerationis not known. Males from male-femalepairs show more rapid testicular recru-descence than males from male-femalegroups. This corresponds to the pattern ofovarian recrudescence exhibited by fe-males (Crews et al., 1974). Thus, for boththe male and the female, gonadal recru-descence is more rapid in pairs than ingroups. However, group-housed malesand females eventually surpass those liz-ards that are pair-housed in their level ofgonadal activity. This suggests that therapid follicular growth and consequentsexual receptivity in females is responsiblefor the rapid testicular growth in the malepartner. If this is the case, then the findingthat males housed with females in groupseventually surpass males housed in hetero-sexual pairs may be due to the constantavailability of receptive females in thegroup; in the pair situation the femaleswould be receptive only for a few daysevery two weeks (see below).

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FIG. 2. Courtship display of the male green anole, Anolis carolinensis (top). Sexually receptive females standand neckbend (bottom) for courting males. See text for further details.

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FUNCTION AND CAUSATION OF SOCIAL SIGNALS 279

The females' behavior also has a releas-ing effect on the male. Unmated, preovu-latory females (B. Greenberg and Noble,1944; Stamps, 1976a) or ovariectomized,estrogen-primed females will solicit court-

dftiip from a male if he fails to court them(McNicol and Crews, 1979; Tokarz andCrews, 1980). This usually consists of thefemale approaching the male and head-nodding, a behavior that invariably resultsin the male performing one or more court-ship displays and frequently mating withthe female.

UNDERLYING NEURAL ANDNEUROENDOCRINE MECHANISMS

In order for these ecological factors tostimulate gonadal activity and the associ-ated reproductive behaviors, it is necessarythat they be perceived by the organism andtransduced into neural activity. Much ofthis information ultimately converges onthe hypothalamus, where it influences pi-tuitary and autonomic function and, inturn, the target organs. Here we considerbriefly the sensory afferents in iguanid liz-ards, the neural sites of steroid hormoneuptake, and finally, the neuroendocrinecontrol of pituitary, gonadal, and adrenalfunction.

The lizard forebrain and afferent influences

The lizard forebrain consists of pairedcerebral hemispheres comprised of a cor-tex (pallium) which overlies the lateral ven-tricles of the brain, and a subventriculararea consisting mainly of septal, striatal,and "amygdaloid" nuclei (Fig. 3). The dor-sal ventricular ridge (DVR) is a strikinglylarge structure of pallial origin. The an-terior portion of the DVR (ADVR)possesses the terminal targets of ascendingthalamic pathways of at least three sensorymodalities (Northcutt, 1978), a circum-stance similar to parts of the mammalianneocortex (Butler, 1978). These projec-tions consist of a dorsal thalamic visualprojection from the optic tectum to the lat-eral third of the DVR, a dorsal thalamicauditory projection from the torus semi-circularis to the medial third, and a pro-jection from a more caudal thalamic nu-

cleus which conveys somatic sensoryinformation to a central area of the DVR.The remaining lateral portion of the DVRis continuous rostrally with dorsal cortexand may be the target of an undescribedsensory pathway, possibly trigeminal(Northcutt, 1978). Most projections leav-ing ADVR are restricted to the telen-cephalon. The ventral boundary of theADVR is the dorsal medullary lamina (Fig.3), beneath which are the striatal struc-tures. The principal telencephalic efferentis the lateral forebrain bundle which arisesin the ventral striatum (Voneida and Sli-gar, 1979).

The posterior DVR (PDVR) is recogniz-able caudal to the anterior commissure. Itis not known to receive discrete thalamicprojections, but possesses the nucleussphericus, a terminal nucleus for afferentvomeronasal projections, the developmentof which seems to correspond to the de-velopment of the vomeronasal apparatus.In some anoles a rudimentary n. sphericuscan be detected, but in A. carolinensis it isabsent (Greenberg, unpublished).

Auditory projections. While similar in basicorganization to the ascending auditorypathway in mammals and birds, the rep-tilian auditory system shows considerablyless nuclear differentiation, although thereis reason to believe that reptiles can resolvedifferent frequency components of sound(Foster and Hall, 1978). Nerve fibers fromthe cochlea are conveyed in the acousticnerve to several nuclei in the brain stem.The major recipient of acoustic brain stemprojections is the central nucleus of the to-rus semicircularis, a midbrain structurehomologous to the inferior colliculus ofmammals and the nucleus mesencephaliclateralis pars dorsalis of birds. The centralnucleus of the torus then sends projectionsby way of the dorsal thalamus to a medialanterior DVR site that has been identifiedas the most rostral target of the ascendingauditory system (Pritz, 1974).

Olfactory and vomeronasal projections. Theolfactory/vomeronasal apparatus of rep-tiles show considerable variation in theirdegree of development. Compared to oth-er lizards, A. carolinensis has an extremely

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280 D. CREWS AND N. GREENBERG

Pal. membr.

Septum

Cx. dors. ,Cx, med.

A.D.V R.

Pal.Med. inter.

N. tr. olt. lat.

Comm. hip.

Comm. ant.

A.D.V.R.

Tr. opt.

FIG. 3. Three levels of the forebrain of the green anole lizard, Anolis carolinensis. Drawings combine adjacentsections 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 anteriorcommissure. Abbreviations: ADVR, anterior dorsal ventricular ridge; Comm. hip., hippocampal commissure;Comm. ant., anterior commissure; Cx. dors., dorsal cortex; Cx. med., medial cortex; DML, dorsal medullarlamina, 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 rea-son to assume that chemical senses are notutilized by Anolis (Armstrong et al., 1953),olfaction could not be demonstrated inprey selection (Curio and Mobius, 1978).The olfactory bulbs in A. carolinensis arerelatively small and extended before theforebrain on slender peduncles. The ac-cessory olfactory bulb, which receives thevomeronasal nerve in all lizards, is a caudalmedial extension of the main bulb.

Those olfactory projections that pass be-yond an anterior olfactory nucleus aregenerally divided into lateral and medialtracts. Fibers from the accessory bulb jointhe relatively larger lateral tract. The mainbulb fibers terminate in a nucleus of thelateral tract and a lateral ("pyriform") cor-tical field while the accessory fibers project

to a nucleus in the PDVR. A projection tothis area exists even in Anolis which has norecognizable terminal nuclear group(Greenberg and Switzer, unpublished).

Visual projections. In many diurnal liz-ards, vision has become a dominant sen-sory modality. Unlike snakes and other or-ders of reptiles, most lizards have all coneretinas (Prince, 1956; Underwood, 1970)with very dense foveae and thick retinalinner nuclear and ganglion layers that areexceeded only slightly by some birds(Walls, 1942).

In A. carolinensis and /. iguana most ret-inofugal fibers decussate in the opticchiasm, but a few fibers to the thalamusremain uncrossed; these species do notshow projections to the hypothalamus(Butler and Northcutt, 1971). Lizard reti-nal ganglion cells project to the dorsal and

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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 wasstimulated by viewing another male for 45 min following a 2 fid pulse of (14C) deoxyglucose administeredi.p. Photographs A—C are autoradiographs of coronal sections (20 ptm); photographs D—F are these samesections after staining to demonstrate neuronal cell bodies. The right side of the brain is to the right. Areasof asymmetrical metabolic activity are apparent: (A) in part of the anterior dorsal ventricular ridge; (B) innucleus rotundus and the lateral geniculate nucleus (the darkened area on the dorsal surface is caused byfolding of the tissue); (C) in the superficial layer of the optic tectum. (Allen, Adler, Greenberg, and Crews,unpublished data.)

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282 D. CREWS AND N. GREENBERG

ventral thalamus, tectum and pretectum,nucleus of the basal optic tract and the hy-pothalamus (Ebbesson, 1970) (Fig. 4).

Neural sites of steroid hormone uptake

Sex steroids are concentrated in specificregions of the brain where they alter neu-ral activity. The distribution of hormonesensitive cells is similar in all vertebratesstudied (Morrell and Pfaff, 1978). In A.carolinensis estradiol, testosterone, and di-hydrotestosterone concentrating cells arelocated in the anterior hypothalamic-preoptic area (AH-POA), septum, amyg-dala, basal tuberal hypothalamus, torussemicircularis, and anterior pituitary(Morrell et al., 1979). Males and femalesshow the same pattern of uptake for allthree hormones, although estradiol treat-ed animals exhibit the most intense label-ing with a highly localized pattern of up-take. There are, however, areas thatselectively bind estradiol but not testoster-one and dihydrotestosterone and vice ver-sa. For example, the lateral and dorsal cor-tices contain cells that selectively bindestradiol, while there are many well-la-belled cells in the mesencephalic tegmen-tum only after administration of andro-gen.

It would be valuable to know the neuralconcentrating sites of adrenal steroids inthe lizard brain since these hormones alsohave profound influences on behavior asin mammals (Callard et al., 1973; McEwenetal, 1972).

Hypothalamic-pituitary-gonadal axis

Hypothalamic control of pituitary func-tion in reptiles is well established (reviewedin Crews, 1979a, b; Licht, 1974). Gesell andCallard (1972) have described in Dipsosau-rus dorsalis a major neurosecretory tractarising from the paraventricular and su-praoptic nuclei in the anterior hypothala-mus (AH) and running through the me-dian eminence region (ME) where it comesin contact with capillaries of the hypothal-amo-hypophyseal portal vessels. Radio-frequency lesions in the AH-POA or theME result in testicular atrophy in sexually-active A. carolinensis (Wheeler and Crews,1978; Farragher and Crews, 1979). It is

interesting that lesions immediately rostralto the AH-POA also lead to testicular atro-phy in intact male A. carolinensis, presum-ably acting via their effect on cells that pro-duce gonadotropin releasing hormonelocated in this region (Wheeler and Crew^1978) (see below;).

While lesions in the AH-POA/ME pro-duce results consistent with findings inother vertebrates, intracranial implanta-tion studies indicate that steroid feedbackregulation of pituitary gonadotropin se-cretion in lizards may be unlike that ofmammals. Implantation of estrogen intothe ME or AH of female S. cyanogenys inmid or late stages of vitellogenic growthinhibits ovulation although follicular de-velopment with accompanying oviductgrowth is not retarded (Callard et al.,1972). Progesterone implantation into theAH near the end of the ovarian growthphase has no effect on ovulation but if per-formed in the midvitellogenic stage, suchan implant will prevent further ovariangrowth and induce follicular atresia. Thesestudies suggest that in lizards, unlike mam-mals, estrogen acting at the level of thehypothalamus prevents the ovulatorysurge of GTH, but not its tonic secretion,whereas progesterone inhibits tonic GTHsecretion but not the ovulatory surge.

Hypothalamic-adrenal axis

The hypothalamic-adrenal axis is theprincipal means by which vertebrates re-spond to acute and chronic stress. In rep-tiles, the homolog of the adrenal medullais peripherally placed relative to the "cor-tex" and is termed the "adrenal" glandwhile the more centrally placed corticalhomolog is termed the "interrenal" gland(reviewed in Gabe, 1970).

The hypothalamus is also the final CNScomponent of interrenal gland activation.Glucocorticoids and mineralocorticoids inreptiles are less differentiated in both theircontrolling mechanisms and their functionthan in mammals (Callard et al., 1973).Other differences from the mammalianpattern include an apparent negative feed-back control at the hypothalamic level ofboth corticosterone and aldosterone and agreater independence of adrenal steroido-

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FUNCTION AND CAUSATION OF SOCIAL SIGNALS 283

genesis from pituitary control (Callard etal., 1973). As in gonadal sensitivity to gon-adotropic hormones, interrenal sensitivityto ACTH is also temperature dependent(Licht and Bradshaw, 1969; Callard et al,#973).

The adrenal and interrenal glands arein intimate anatomical association witheach other and with the reproductive ductsin reptiles. However, this association withreproductive structures has no knownfunctional significance. The adrenal chro-maffin hormones epinephrine (E) andnorepinephrine (NE) have different phys-iological actions and the possible alterationof their ratio may represent a significantadaptation to chronic stress. These cate-cholamines are also important in body col-or phenomena often utilized as social sig-nals (see below).

SEX STEROID EFFECTS OF MORPHOLOGYAND BEHAVIOR

The gonadal hormones have major in-fluences on both the morphology {e.g., sec-ondary sex characters) and behavior {e.g.,facilitation of sexually dimorphic displays)of the organism. These effects can, in turn,be separated according to their temporalqualities and their permanence. Organi-zational effects of hormones have tradi-tionally referred to morphological andpsychosexual differentiation, usually as aconsequence of exposure to hormonesduring early life. Activational effects ofhormones, on the other hand, refer gen-erally to their ability to elicit or facilitatebehavior patterns characteristic of one sexafter physical differentiation. These phe-nomena do not so much represent mu-tually exclusive categories as they do pointsof perspective.

Peripheral action

Hormones are responsible for the dif-ferentiation of secondary sex charactersand their accessory structures. In reptiles,the period of sexual differentiation is pro-tracted, beginning in embryonic life andextending post-hatching (Forbes, 1940,1956). Steroidogenic activity of the embry-onic gonad has been demonstrated (Ray-naud and Pieau, 1971). Androgens and

estrogens are known to influence differ-entiation of the reproductive ducts (re-viewed by Adkins, 1980a) and probablyhave far-reaching effects on other sexual-ly-dimorphic characters. For example, inmost reptiles, the sexes are dimorphic inbody size. The male's larger size is not dueto lesser energetic demands (Gorman andLicht, 1973) but probably to testicular hor-mone effects.

Different characters undergo sexual dif-ferentiation at different times. For exam-ple, hatchling A. carolinensis can be sexedby the presence of two conspicuous post-anal scales in the male, but the dimor-phism in the retrobasal process of thehyoid apparatus does not become appar-ent until later in life (Fig. 5). The hemi-penes, which are formed between 12 and17 days of embryonic life, appear beforethe scales, which form between days 20and 23 (Pearson and Licht, 1974). Sexualdimorphisms have been reported also forthe femoral glands of Crotaphytus collaris(Cole, 19666) and body color of adult Sce-loporus occidentalis (Kimball and Erpino,1971). Male S. occidentalis develop medialstripes of dark pigment on their ventrumas they approach maturity; this distinctmale pigmentation pattern can be inducedin immature males and females withadministration of exogenous androgen.

Many of these sexually-dimorphic struc-tures undergo cycles of activity that arecorrelated with the reproductive season,indicating an activational role of hor-mones. Although there is no evidence foran annual fluctuation in the color patternof adult S. occidentalis, the blue ventralmarkings become more intense ( = mela-nophore expansion) during the breedingseason (Kimball and Erpino, 1971). Cas-tration results in a decline in the level ofmelanophore expansion, but this can beprevented by simultaneous administrationof testosterone propionate. In severaliguanid lizards, gravid females have or-ange spots on the sides and flanks whichthey display toward the courting male.These spots are rapidly acquired and arebrightest on the day of ovulation and im-mediately afterwards while the eggs areoviducal. This color change is under hor-

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75 r -

55

E 45

2UJ

oCO

3 5 —

3 5 -

2 5 -

15

ADULT

Female(n = !32)

Malen = 115)

HATCHLING

I10 15 20 25 30

LENGTH OF RETROBASAL PROCESS (mm)35

FIG. 5. Sexual dimorphism of the retrobasal process of the hyoid apparatus in the green anole, Anoliscarolinensis.

monal control and can be induced by ex-ogenous progesterone but not estradiol-17/3 in ovariectomized Crotaphytus (Cooperand Ferguson, 1972a, b; Medica et al.,1973); however, estradiol does have a prim-ing effect if injected before progesterone(Cooper and Ferguson, 1973; Medica etai,1973).

Central action

Unfortunately, nothing is known aboutthe differentiation and development of re-productive behaviors in reptiles (reviewedin Adkins, 1980a, b). There is some evi-dence though to suggest that the neuralsubstrate of mating behavior may not besexually dimorphic. For instance, court-ship and copulatory behavior can be elic-ited in female A. carolinensis by administra-

tion of testosterone propionate (Adkinsand Schlesinger, 1979). Further, male-likemating behavior has been observed in all-female parthenogenetic Cnemidophorus liz-ards (Crews and Fitzgerald, 1980). Wheth-er hormones have an organizing influenceon adult reproductive behavior in reptileswill require studies in which hormones areadministered early in life and their subse-quent effects on psychosexual develop-ment determined.

It is well-established that the steroid hor-mones act on specific areas of the brain tomodulate reproductive behavior. In addi-tion to being a site of hormone feedbackcontrol of pituitary function, the anteriorhypothalamus-preoptic area (AH-POA) isknown to play a crucial role in the regu-lation of male reproductive behavior in

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vertebrates (reviewed in Crews and Silver,1980). For example, in A. carolinensis, bi-lateral radiofrequency lesions in the AH-POA abolish courtship and agonistic be-havior; lesions in area dorsal or caudal tof̂tis area have no effect on these displays

(Wheeler and Crews, 1978). Lesions im-mediately rostral to the AH-POA of intactA. carolinensis also cause a significant de-cline in display behavior. In this instance,however, the effect is probably not due tothe destruction of a behavioral integrativearea but rather is due to the destruction ofgonadotropin releasing hormone produc-ing cells located in this region. This is in-dicated by the fact that such animalsundergo testicular collapse following le-sioning, but display behavior can be rein-stated by administration of exogenous an-drogen. Other evidence suggesting thatdisplay behavior is reliant both on the in-tegrity of the AH-POA and specific hor-monal conditions is that implantation ofandrogen directly into the AH-POA re-stores courtship behavior in castrated, be-haviorally inactive A. carolinensis; implantsoutside this area or cholesterol implantswithin the AH-POA have no effect (Mor-gentaler and Crews, 1978; Crews and Mor-gentaler, 1979).

The basal hypothalamus also appears tobe a major integrative area for regulatingmale reproductive behavior in lizards. De-struction of either the anterior or posteriorbasal hypothalamus results in a rapid de-cline in the display behavior of castrated,androgen-treated A. carolinensis (Farrag-her and Crews, 1980).

INTEGRATION OF EXTERNAL CUES ANDINTERNAL STATE IN THE

CAUSATION OF BEHAVIOR

When investigating the neural control ofbehavior, it is important to distinguish be-tween behaviors that are not influenced byhormones from those that are hormone-dependent. It is clear that certain activitiesof specific neural systems are influencedby hormones (Komisaruk, 1971, 1978).

Social signals and lizard display behavior

Behavioral displays involve communi-cation between conspecifics. Like other

cues of great relevance to the survival ofa species, these social signals are selectivelyperceived and integrated into a complexsequence of physiological and behavioralevents in a way that structures their out-comes and thus the ultimate social orga-nization. Displays are both influenced bytheir evolutionary origins and exert a se-lective pressure on the perceptive and in-tegrative centers of animals that respondto them. Among the sensory modalitiesknown to play an important role in the so-cial behavior of lizards are audition, che-moreception, and vision.

Auditory signals. Sounds produced byreptiles include various squeaks, hisses andeven scale scraping (Gans and Maderson,1973), but only recently have studies beenconcerned with true vocalizations, that is,modulated vocal emissions consistent inform (Marcellini, 1978). Frequency, inten-sity and pattern of vocalizations in Gekkoni-dae have been studied and reviewed byMarcellini (1978), who points out that vo-calizations often functionally parallel thevisual displays of iguanid lizards.

Among the iguanid lizards, the sensitiv-ity of the anoline ear is excellent with thebest performance from A. carolinensis overa range of 500-3,000 Hz (Wever, 1978).Although auditory stimuli can influencebehavior particularly in the absence of vi-sual information in Anolis (Rothblum etal,1979), sounds emitted during social en-counters do not clearly have a social func-tion and are probably anti-predator behav-iors (Milton and Jenssen, 1979).

Chemical signals. Although chemical cueshave been demonstrated to play an impor-tant role in the social behavior of snakes,turtles, and crocodilians (reviewed inCrews, 1980; Madison, 1977), little isknown about their function in lizards. Inmany iguanid species, males have enlargedproctodeal and femoral glands that areseasonally active (Cole, 1966a). Reproduc-tively active males are often seen rubbingtheir vent and/or hindlegs against surfacesin their territories. Further, tongue flick-ing, a prominent activity in skinks, vara-nids, teiids, and other lizards with forkedtongues, is also often seen in iguanid liz-ards (Bissinger and Simon, 1979). This be-

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havior is greatest when exploring newareas (DeFazio et al., 1977). To date, how-ever, few studies have associated the po-tential chemical cues provided by this ac-tivity with a socially significant response inconspecifics. Male and female S. occiden-talis display significantly more often whenpresented with surfaces "labelled" with thedroppings of conspecifics than when pre-sented with unlabelled surfaces (Duvall,1980). That chemical cues may be utilizedfor sex identification is suggested by thebehavior of male Coleonyx variegatus who"taste" the tails of all potential mates; whenmale and female tails are surgically ex-changed, a courting male will address hisattention only to the animal with the fe-male tail (B. Greenberg, 1943).

Visual signals. Visual social signals consistof dynamic (e.g., display action patterns)and static (e.g., postures and colors) be-havioral elements. In male-male interac-tions, social status is a significant factor indetermining the relative access of males tofemales. Status is associated in manyspecies with distinctive colors (e.g., Anoliscuvieri, Rand and Andrews, 1975; A. agas-sizi, Rand et al., 1975; Agama agama, Har-ris, 1964) and as status signals, these colorsmay be important in continually reinforc-ing the effects of decisive aggressive inter-actions on conspecifics. Under ecologicallyrealistic conditions of temperature and il-lumination, dominant male A. carolinensisare characteristically green while subordi-nates are typically brown (Greenberg, un-published). Since the color changes areprofoundly influenced by adrenal/inter-renal hormones, it is likely that they func-tion as an external indicator of relativestress (see below). That these characteristiccolors are generally reversible as social re-lationships shift indicates further that col-or may function as a signal in this species.

Forebrain mechanisms of display behavior

The function of the forebrain in inte-grating and effecting social behavior in liz-ards has been studied by both stimulationand ablation experiments.

Stimulation studies. In the forebrain of /.

iguana, regional differences in the fre-quency of responses elicited by electricalstimulation are apparent; however, noclear correlations with specific anatomicalstructures are discernible (Distel, 1978).Dewlap extension was elicited at most h]0pothalamic sites at low stimulus intensities.Head-nodding, a component of many so-cial displays in this species, was elicitedmost reliably immediately after stimulusoffset at sites caudal to the forebrain. Thefew telencephalic sites where nodding waselicited were in the striatum and septum.In these instances, the response occurredduring stimulation, suggesting possibledisinhibition by higher neural areas of aresponse organized more caudally. Com-ponents of display behavior were also elic-ited by electrical stimulation of the brainof Crotaphytus collaris (Sugerman and Dem-ski, 1978). While gular extension, a com-ponent of defensive as well as aggressivedisplay, is elicited by stimulation of almostall sites from the telencephalon throughthe medulla, agonistic elements were lim-ited to stimulation of the amygdaloid com-plex, septum and preoptic area.

Ablation studies. Changes in social behav-ior and perch site preference were ob-served in S. occidentalis after lesions in oneof several "amygdaloid" nuclei (Tarr,1977). While deficits in social responsive-ness were attributed to an inability to pro-cess aggressive social cues, many animalsexhibited marked decreases in sponta-neous activities. In A. carolinensis radio-frequency lesions in the paleostriatum haveno influence on activity levels or assertiondisplay behavior, but if the lesion includesthe lateral forebrain bundle, the challengeresponse is eliminated or significantly re-duced (Greenberg et al., 1979). Since inthis species the optic decussation is almostcomplete (Butler and Northcutt, 1971), itis possible to lesion unilaterally and thenby use of a removable eyepatch to test an-imals when vision is restricted to the le-sioned or the intact hemisphere (Green-berg, 1977a). In this way, the subject canbe used as its own progressive post-oper-ative control. Utilizing this model, prelim-

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inary studies indicate a significant role forseptal and posterior DVR nuclei in the reg-ulation of social and reproductive behavior(Greenberg, Crews, and Scott, unpub-lished).

Neuroendocrine integration of display behavior

Lizard display behavior provides an ex-cellent opportunity to study the hormonal,neural, and neuroendocrine mechanismsunderlying social interactions. The manythreads of intraspecific interactions consti-tute the fabric of social organization andthe ultimate test of its adaptiveness: repro-ductive success. While gonadal hormonesdominate the integrative activities con-cerned with reproduction, adrenal hor-mones play a significant role in social or-ganization.

Gonadal hormones and behavior. Malecourtship behavior is dependent upon tes-ticular activity (androgen production)(Crews, 19796). If a male is presented witha female (of any reproductive state) duringthe winter, he will ignore her. That samemale in the late spring and summer, how-ever, will court energetically and, if the fe-male stands and neckbends, will mate withher. Castration of sexually-active malesabolishes this behavior. The aggressive be-havior of males, unlike courtship, does notappear as reliant on testicular hormones.Males will continue to challenge intrudersfor at least two weeks following castrationif returned to their home cage (Crews etal., 1978). If placed in a new environment,agonistic behavior declines sharply. Famil-iarity with the environment also modulatesthe agonistic behavior of sexually-activemales. An intact or castrated, androgen-treated male will not immediately defenda new cage, especially if it is larger than hisprevious home cage (Crews, unpublished).

There is evidence also to suggest thatcourtship and aggression have differentneural thresholds in responsiveness to an-drogen. For example, the pattern of rein-statement of first aggression followed bycourtship is seen in winter dormant malesupon environmental stimulation (Crews,1974a), in castrates given subcutaneous an-drogen replacement therapy (Crews,

19746; Crews et al., 1978), and in long-term castrates upon intracranial implan-tation of hormones (Crews and Morgen-taler, unpublished) (Fig. 6).

Sexual receptivity in female A. carolinen-sis is also controlled by a complex sequenceof hormonal and neural events. In all ano-line lizards, a single follicle matures and isovulated; in A. carolinensis, this occursevery 2 wk in the breeding season (Crews,1973a; Hamlett, 1952; Licht, 1973). Dur-ing this time, Anolis females will stand fora courting male (estrus) only during thelatter half of the follicular cycle (Crews,1973a; Stamps, 1977) and, unless mated,will remain receptive for about 24 hr afterovulation. Plasma estrogen levels are lowduring the early stages of follicular growthbut increase three-fold immediately beforeovulation (Tokarz and Crews, unpub-lished). Progesterone levels are highestduring the breeding season, but it is as yetnot known if they vary with follicular con-dition.

Female sexual behavior is estrogen-de-pendent in A. carolinensis. Ovariectomyabolishes sexual receptivity while treat-ment with exogenous estrogen reinstatesestrus in a dose-related manner (Crews,1979a, b). As in many mammals, progester-one plays a central role in A. carolinensis incoordinating the physiological and behav-ioral events during the breeding season. Inoviparous lizards, luteal progesterone in-fluences ovarian activity directly. The du-ration of egg retention is reduced follow-ing lutectomy, thereby decreasing theinterval between follicular cycles in both S.undulatus (Roth etal., 1973) and C. unipar-ens (Cuellar, 1979), while administration ofexogenous progesterone prevents gonad-otropin-induced ovarian growth in S. cyan-ogenys (Callard et al., 1972; see also Yaronand Widzner, 1978). Recent studies withA. carolinensis show that estrogen acts atthe neural level to increase progesteronereceptor in the diencephalon (McEwen,Tokarz, and Crews, unpublished); estro-gen and progesterone synergize to facili-tate the onset of female sexual receptivity(McNicol and Crews, 1979). It is significantthat about half of the females tested and

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later found to be in the middle of theirsecond or third follicular cycles are sex-ually receptive versus none of the femalesat the same ovarian stage of their first fol-licular cycle (Crews, 1973a). Finally, thereis some evidence that progesterone canalso have an inhibitory effect on femalesexual receptivity in A. carolinensis as inmany mammalian species (Valenstein andCrews, 1977; McNicol and Crews, 1979).

While the expression of sexual receptiv-ity depends upon ovarian hormones, itsmaintenance is liable to exteroceptive stim-uli. If a preovulatory female mates, she willnot be receptive again until the next follic-ular cycle. Since intact, estrogen-primedfemales are rendered unreceptive to malecourtship whereas ovariectomized, estro-gen-primed females are once again recep-tive within 24 hr of mating (Valenstein andCrews, 1977), the presence of the ovaries(or, more likely, some change in ovarianhormone production) is critical for thislong-term inhibition of female sexual re-ceptivity.

Intromission by the male is the criticalstimulus initiating mating-induced inhibi-tion of estrous behavior in A. carolinensis(Crews, 19736). In rodents, vagino-cervicalstimulation during mating initiates a neu-roendocrine reflex involving an initial re-lease of prolactin and maintained eleva-tions of progesterone that effectivelysuppresses lordosis behavior (Adler, 1974;Carter et al., 1976). Our evidence, al-though still incomplete, suggests the exis-tence in A. carolinensis of a similar neu-roendocrine reflex whereby female sexualreceptivity, induced by ovarian hormones,is terminated by sensory stimuli. Thesestimuli also alter the female's hormonalstate, maintaining nonreceptivity until thefollicle is ovulated and another follicle be-gins to develop.

As mentioned previously, seasonallybreeding vertebrates exhibit circannualrhythms in sensitivity to environmentaland physiological stimuli. For example, inA. carolinensis there is a sharp decrease insensitivity to temperature, social stimuli,and exogenous gonadotropin in the latesummer and early fall, the reproductiverefractory period (Crews and Licht, 1974;

Crews and Garrick, 1980; Licht, 1971).Whether this refractoriness is controlled atthe level of the gonads or the brain or bothis still unclear (cf., Crews and Licht, 1974;Crews and Garrick, 1980; Cuellar andCuellar, 1977). The time of year is a po-^tentially important variable in behavioralstudies as well. We have documented re-cently that ovariectomized A. carolinensisare behaviorally less sensitive to estrogenreplacement therapy in the refractory pe-riod than in the breeding season (Fig. 7),suggesting a circannual rhythm in neuralsensitivity to ovarian hormones.

Adrenal hormones and social organization.There are several related ways in whichinterrenal/adrenal function might be sig-nificant in the social behavior of lizards:social stress, reproductive condition, andskin color.

Social stress. Stimuli provided by conspe-cifics can be stressful and require physio-logical compensation on the part of the re-sponding animal if homeostasis is to bepreserved. To a considerable extent thecompensation can be anticipatory, prepar-ing an animal for imminent stress.

Acute stress elicits an "emergency" or"fight or flight" response by means of hy-pothalamic activation of the sympatheticnervous system and stimulation of adrenalchromaffin cell secretion of the catechol-amines E and NE. Sustained stress resultsin increased pituitary ACTH secretionwhich, in turn, stimulates release of inter-renal steroids. If an animal cannot adaptto the chronic activation of physiologicaldefenses, a potentially-lethal "hypersym-pathetic" (Wehle et al., 1978) or "generaladaptation syndrome" (Selye, 1956) devel-ops. The specific relationship of socialstress to adrenal function requires furtherstudy, but at least two lines of evidence in-dicate this to be a fruitful area. Crowdingof the iguanid lizard Dipsosaurus results insignificantly enlarged interrenal/adrenalglands (Callard et al, 1973). In the teiidlizard Cnemidophorus, reduced social statusis correlated with enlarged interrenal/ad-renal glands (Brackin, 1978). The stress ofreproductive activity may also be reflectedin interrenal activity. In Dipsosaurus, fe-males have larger glands, especially during

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the active reproductive phase (Callard etal., 1973), an effect probably attributableto elevated estrogen levels in the lizard, asin mammals (Kitay, 1969).

Reproductive condition. Conditions which^engender stress also frequently affect re-

productive functions (e.g., Bliss et al.,1972; Ramaley, 1974; Archer, 1979) al-though it is not clear the extent to whichthese are correlated rather than causallyrelated phenomena. Subordinate lizardsare chronically stressed and have reducedreproductive function (Crews, unpub-lished; Greenberg, unpublished) as well asenlarged adrenal/interrenal glands (Brack-in, 1978).

Skin color. Morphological color changesinvolve absolute amounts of pigment,while physiological color change refers tothe relative visibility of color as affected bychromatophore pigment granule disper-sion or aggregation (see above). Social con-trol of the physiology underlying colorchange is an excellent example of howboth internal and external environmentsmay combine to regulate social signals.Both sympathetic activation and melanocytestimulating hormone (MSH) can affectbody color. However, A. carolinensis, inspecific social situations, exhibits chromato-phore responses controlled by E and NE(Hadley and Goldman, 1969), while MSHmay not have a significant influence (Had-ley and Bagnara, 1975). Unlike most liz-ards, the chromatophores of A. carolinensishave no sympathetic innervation (Klein-holtz, 1938), and thus this species providesus with a natural experiment in which ac-tivation of adrenal catecholamines arereadily obvious. In most instances, bodycolor is a balance between the effects of Eand NE on and adrenergic receptors(Hadley and Goldman, 1969) or betweenthe density of the receptors themselves.This balance, however, appears to betipped one way for dominants (character-istically green) and the other way for sub-ordinates (characteristically brown). Thus,by using color, the status of males and cer-tain of its physiological correlates can be as-sociated (Greenberg, unpublished). Thereare two other ways in which the E/NEbalance is altered: by the emergency re-

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FIG. 6. Seasonal differences in behavioral sensitivityto estrogen in the green anole, Anolis carolinensis.Adult females obtained in June (•) and September(O) were ovariectomized within two weeks of arrivalin the laboratory. Two weeks following ovariectomy,females were pretested for sexual receptivity (•). Im-mediately following the pretest, females were treatedwith estradiol benzoate (1.4 ftg, s.c.) and tested dailyfor sexual receptivity. Mean and standard error andsample sizes are shown. (Tokarz and Crews, unpub-lished.)

sponse in acutely stressful situations andby an increase in corticosterone facilitatedmethylation of NE to E (Wurtman et al.,1967) under the influence of chronicstress.

Color as an external indication of phys-iological condition and status has been ex-ploited as a social signal in several lizardspecies (Harris, 1964). In A. agama, terri-torial dominants have a bright red head,the sight of which elicits defensive re-sponses in subordinates and aggression inother dominants. Harris (1964) asserts thatthe sight of the red head acts as a "sup-pressor" of dominance behavior in subor-dinate males. A dominant S. cyanogenys hasonly to lift its head, revealing its blue chin,to suppress activity in subordinates observ-ing him (Greenberg, 19776). In A. caroli-nensis, subordinate animals, while display-

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ing some indications of physiological stress(brown skin color) do not suffer autonomiccollapse. However, when long-term domi-nants are displaced, they often die after arelatively brief period of behavioraldepression (Greenberg, unpublished dataon A. carolinensis and A. agama).

CONCLUDING REMARKS

The work reviewed here demonstrateshow the environmental and physiologicalmilieus are integrated in the regulation ofsocial displays and thus social organization.These adaptations have evolved to syn-chronize reproductive activities and maxi-mize fitness in the environment in whichthe animals evolved. Because of the wealthof information available on their ecologyand anatomy, many reptiles are uniquelysuited to the investigation of specific prob-lems in behavior. The research with thegreen anole lizard, Anolis carolinensis, inparticular, illustrates how the methodolog-ical perspective of ethology and compara-tive psychology and different levels ofanalysis can be combined to give us a betterunderstanding of how internal and exter-nal stimuli interact.

ACKNOWLEDGMENTS

We wish to thank Richard Tokarz forreading the manuscript. Unpublished re-search supported in part by NSF BNS-13796, NINCDS 15305, NICHHD 12709,and NIMH Research Scientist Develop-ment Award MH00135 to DC, and by NIHBiomedical Support Grant RR-07088 to theUniversity of Tennessee and a SchweppeResearch and Education Fund Award toNG.

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