GENERAL

AND

COMPARATIVE

ENDOCRINOLOGY

(1990)

77,2462.55

Endocrine and Behavioral Responses to Aggression and Social Dominance in the Green Anole Lizard, Anolis carolinensis NEIL

GREENBERG*

AND DAVID

CREWS?

*Department of Zoology and Life Sciences Graduate Program in Ethology, Knoxville, Tennessee 37996, and tlnstitute of Reproductive Biology, Department Texas, Austin, Texas 78712

University of Tennessee, of Zoology, University

of

Accepted April 18, 1989 Adult males of the small arboreal iguanid lizard, Anolis carolinensis, will fight and form social dominance hierarchies when placed in habitats with limited resources. The relationships between time since initial aggressive interaction, relative social dominance, reproductive activity, and corticosterone and androgen levels were determined for 34 pairs of lizards. A discriminant analysis established a “dominance index” which indicated that over 90% of the difference between individuals who had won or lost aggressive interactions (putative social dominants and subordinates) was attributable to a single discriminant function reflecting altered body color, perch site selection, and circulating androgen. Animals that had darker body color also selected lower perch sites and had depressed rates of courtship relative to winners of tights and were thus designated as social subordinates. These animals also had levels of circulating androgen significantly lower than that of dominants, but circulating corticosterone was not significantly affected. Winners of tights showed a dramatic surge in circulating androgen at 1 hr but returned to near control values by 1 week; losers, however, showed depressed circulating androgen levels at 1 week. o 1990AcademicPW, IK.

Aggressive behavior, social dominance, and reproductive activity have been associated with adrenal and other physiological responses to environmental stressors in many vertebrates, including several reptiles (Greenberg and Wingfield, 1987). The interactions between these responsive systems and behavior indicate that their underlying physiological substrate involves hormones that have multiple effects. For example, hormones associated with activation of the adrenal axis can also enhance acquisition and delay extinction of active avoidance behavior (Bohus and de Wied, 1980) and hormones associated with gonadal activation can directly affect sensory-perceptual functions (Beach, 1974; Gandelman, 1983) as well as affecting attention either directly (Andrew, 1972) or by means of interactions with adrenocortical hormones (Oades, 1979). One of the primary ambitions of experimental behavioral endocrinology is to

determine the manner in which such multiple effects are integrated and coordinated with each other and the environment. The green anole lizard, Anolis carolinensis, is uniquely suited to the investigation of the manner in which environmental stimuli and physiological variables are integrated in the control of agonistic behavior. The dermal chromatophores of this species have no direct sympathetic innervation (Kleinholz, 1938), but are responsive to circulating hormones associated with physiological stress such as melanotropin (Greenberg et al., 1986) and epinphrine, thus permitting body color to be utilized as a relatively direct indication of an endocrine response to environmental stressors (Greenberg and Crews, 1983). Studies on A. carolinensis have documented body color changes in both agonistic interactions and long-term relationships (Greenberg et al., 1984). For example, the males that ini246

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tiate almost all sexual activity are characteristically completely green while subordinate, sexually inactive males are typically brown. This study was undertaken to determine the association between the outcome of an agonistic interaction, subsequent social dominance, reproductive behavior, and androgen and corticosterone levels in the lizard, Anolis carolinensis, at different points in time after an initial interaction. METHODS Adult A. carolinensis were commercially supplied by the Snake Farm, LaPlace, Louisiana. When received, animals were placed in habitats under conditions known to initiate and maintain gonadal recrudescence throughout the year (Crews and Garrick, 1970; Crews et al., 1974; Licht, 1967, 1971). The stimulatory regimen had a photic cycle of 14 hr light:10 hr dark, and provided corresponding daily temperature fluctuations of 32:22”. Temperature is known to be a significant variable in the responses of lizard adrenal to ACTH (Licht and Bradshaw, 1969), on spermatogenesis (Licht, 1971), and in the production and action of androgens (Pearson er al., 1976). Humidity varied inversely with temperature ranging from 70 (day) to 90% (night) RH. Behavioral techniques. Prior to behavioral experimentation, 68 adult males (minimum size, 61 mm snout-to-vent) were individually housed for a minimum of 3 weeks in glass vivaria (25 x 25 x 30 cm) provided with 20-cm diagonal wooden perches and a substrate of sphagnum moss. Food consisted of commercially supplied l-cm crickets which maintained alertness in the lizards when provided on alternate days and allowed to hide in the moss. Handling was strictly minimized to eliminate this potential stressor (Meier et al., 1973). Each lizard was briefly exposed to individual receptive females and intruding males to determine disposition to court or to manifest territorial aggression; tests were halted in 5 min or if copulation or a tight seemed imminent. Each was also characterized along two dimensions associated with physiological stress or social status: body color and perch-site selection (Greenberg et al., 1984). The range of variability manifest for each of these dimensions was divided into several clearly delineated units and was represented on an ordinal scale based upon their sequence of expression in an agonistic situation (Table 1). Because the expression of body color is also sensitive to ambient light reflectance and temperature, habitats were provided with uniform illumination levels, background color, and

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temperature in order to minimize direct, nonsocial sources of variability in the responses of chromatophores to circulating hormones. Pairs of individuals randomly selected to be subjects were introduced to each other by removing the opaque divider separating two connecting vivaria. The distinctive displays exchanged between subjects (Greenberg, 1977), including body color changes indicative of adrenal activation (Greenberg, 1983), were documented; the pairs were left together in the enclosure and body color and perch-site selection were recorded twice daily for up to 1 week. The terms “winner” or “loser” designate subjects that (1) engaged in an agonistic encounter and manifested a postorbital “eyespot,” indicating adrenal epinephrine release (Greenberg, 1983), and (2) performed displays that included sagittal expansion of the body profile, a posture unique to conspecific aggression (Greenberg, 1977). Losers were identified by (1) their cessation of display and (2) exclusion from higher perch sites, the adoption of a head-down or cryptic posture, or attempts at flight. The terms “dominant” and “subordinate” are used to designate subjects during the period of cohabitation subsequent to the initial agonistic encounter. Relative social dominance was determined by daily observations of staged feeding or female introduction episodes in which subjects manifested priority of access to food or females in at least 75% of observations. Further, submissiveness was indicated by observations of supplantation from perch site, or withdrawal from an arena of activity when the other lizard displays or approaches. Subordinate behavior was manifest in all instances of exposure to a display and approximately 25% of the observed instances of the other lizard’s approach. Dominant individuals, unlike subordinates, will not withdraw or be supplanted from a perch site when approached. In the conditions provided, winners of tights invariably become social dominants. Daily observations of body color and perch-site selection were recorded on a hand-held Hewlett-Packard 51B computer. Staged agonistic and courtship episodes were documented with an electromechanical event recorder (Esterline Angus 20-channel recorder); observations of feeding and social dominance interactions were recorded by pen. Data were then transferred or transcribed onto an IBM 5 150 computer and subjected to analysis using SAS. Sexual behavior after the introduction of a receptive female was characterized by rapid nodding (Table 1), a key element of courtship behavior (Crews, 1975; Greenberg, 1977). Observer effects on subjects were minimized by means of closed-circuit color television surveillance. Hormone assays. Blood samples were taken by rapid decapitation at 1 hr, 1 day, or 1 week following the agonistic interaction. The procedure was performed between 1400 and 1600, times at which corti-

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AND

TABLE SCORING

PROTOCOL

FOR BODY

COLOR,

CREWS

1

SITE SELECTION, AND SOCIAL LIZARDS, ANOLIS CAROLINENSM

DISPLAY

BEHAVIOR

IN GREEN

ANOLE

Color index: An ordinal scale of body colors progressively observed during agonistic encounters or manifested in experimentally stressed lizards. 1. 2. 3. 4. 5. 6. 7.

(G) all visible pigmented body surfaces a light to moderate green. (GB) part green/part brown. (B) all visible pigmented body surfaces a light to moderate brown. (DB) more than 50% of the body surface is dark brown. (DB/ES) dark brown with an eyespot (ES), a black spot near the posterior margin of the orbit. (G/ES) all visible pigmented body surfaces moderate to dark green with eyespot. (G/B/ES) body color is blotchy, irregularly pigmented dark green and dark brown, with eyespot.

Sire selection: An ordinal scale of perching sites, ranging from optimal predatory surveillance sites through degree of displacement in response to aggression or social dominance behavior by another male. 1. 2. 3. 4. 5. 6.

top of perch, favored predatory/social surveillance site. upper half of perch. lower half of perch. on substrate; sustained presence, not foraging for prey. covert perching; hiding; squirreled around perch, in crevice, or out of line of sight of other lizard. burrowed into substrate; frequently with head only above surface.

Display behavior: Units of male behavior observed in contexts of nonspecific disturbance, intrusion or activity of a conspecific males, or intrusion or activity of a female.

AD ET SE RN

pushup/dewlap only (vertical movements of anterior body with brief extension of red dewlap; constitutes the 2- to 4-set “assertion” display, response to a broad spectrum of perturbations) extended throat (unique element of “threat” display, sustained expansion of the throat profile, response to possible conspecific intrusion) sagittal expansion (unique element of “challenge” display, sustained posture incorporating ET and displaying expanded lateral profile, response to active conspecific intruder) rapid nod of head (unique feature of “courtship” response to female; typically followed by approach and attempt at copulation)

D Instantaneous scan or 30-set indent sampling of three 4-hr time bins during photoperiod not counted); dyad tests conducted for a minimum of 5 min. costerone levels are known to be relatively high (Green and Greenberg, unpublished data). Total time betwen the initial disturbance and decapitation was less than 20 sec. Total androgen (ANDR) and corticosterone (CS) were chromatographically separated and their circulating levels were then determined by radioimmunoassay using established procedures (Moore et al., 1985; Whittier et al., 1987). The intraassay coefftcient of variation (CV) and the interassay CV were 6.0 and 7.0%, respectively, for total androgens, and 3.3 and 13.0% for corticosterone. Accuracy values averaged 95.9% for androgens and 86.2% for corticosterone. Statistical procedures. Analyses of the contribution of the variables documented to the differences between groups (“winners/dominants” and “losers/ subordinates”) employed multiple discriminant analysis (Pimental and Frey, 1978). Discriminant scores were used as a continuous measure of dominance, the

(first and last hours

rationale being that those characters most effective in distinguishing between or characterizing behaviors of animals in two conditions will be most heavily weighted by the multiple analysis. This procedure effectively maximizes the distances between two populations (winner/loser or dominant/subordinate) for the variables documented. A dominance index (DI) was derived by multiplying each variable documented by its respective canonical coefftcient (color-dif, + 0.17; site-dif, + 1.04; log CS, -0.09; log ANDR, -0.58). The behavioral variables, body color and perch-site selection, were represented as the difference between the average pre- and postencounter values to minimize the variability between individuals. The signitlcances of hormonal differences attributable to outcomes of encounters and social dominance were inferred by contrasting the sampled hormone levels manifest in each group with that of a control group randomly selected from the same pool of subjects prior to experi-

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mentation. The endocrine variables, nanograms per milliliter of plasma ANDR and CS, were log transformed for statistical analysis. The significance of differences between color and site changes and the hormone levels of the winners and losers at the three sampling intervals was analyzed by Welch’s modified t test. The significance of hormone changes following the initial interaction was determined by MANOVA; courtship data was analyzed by Fisher’s exact probability test.

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h-l

0 -

Dominant Subordinate

LIGHTER

0.0 -0.2 -0 4 -0 6

DARKER

I . I

ONEHOUR

RESULTS Body color and perch-site selection were immediately and obviously affected by fighting; circulating levels of ANDR, but not of CS, were also affected as revealed by the hormone assays. Dominance index. A multiple discriminant analysis indicated that 91% of the difference between groups could be accounted for by a single discriminant function (canonical variable). This represents an index of relative social dominance (DI) and reflects the confidence with which the constituent variables of the index could be used to distinguish a dominant from a subordinate individual. The significance of the index (Z’ < 0.0001, Roy’s greatest root) is attributable primarily to the contributions of three of the four variables: perch height change, body color change, and circulating ANDR levels; CS levels did not contribute significantly to the index. Color differences. Lizards that won fights showed little or no change in color from that seen before the encounter. Losers, on the other hand, showed some variability in the first hour following a fight, but generally were darker in body color than in their preencounter period (Fig. 1). Because of their initial variability, the body color scores of losers were significantly lower (indicating darker) than their prefight scores only at 1 day and 1 week. The difference in body color between winners and losers, however, was significant at all times (1 hr, F = 6.21, prob > F = 0.022; 1 day, F = 10.21, prob > F = 0.007; 1 week, F = 10.61, prob > F = 0.0035). The correlation

ONE DAY

ONE WEEK

1. Changes in body color scores (see Table 1) following aggressive interaction in cohabiting green anole lizards A. cnrolinensis sampled at 1 hr (n = 12 pairs), 1 day (n = 10 pairs), and 1 week (n = 15 pairs) following an aggressive interaction. Positive changes indicate lighter color, negative changes indicate darker. FIG.

between the extent of color change and the dominance index (the first discriminant function) was 0.62. Site differences. Following fights, changes in site-selection scores (site-dif) were evident as winners adopted higher perch sites and losers adopted lower ones (Fig. 2). The difference in perch-site scores between winners and losers was significant at all sampling intervals (1 hr, F = 20.18, prob > F = 0.0002; 1 day, F = 8.30, prob > F = 0.0129; 1 week, F = 35.07, prob > F = 0.0001); however, the change from prefight levels was significant for winners only at 1 hr and 1 day. The postfight perch.” L-

I

0.5

HffiHER

0.0 -0 5 -1 .o -1.5

LOWER

I

-2.0 ! ONE HOUR

ONE DAY

ONEWEEK

2. Changes in perch-site selection scores (see Table 1) following aggressive interaction in cohabiting green anole lizards A. carolinensis sampled at 1 hr (n = 12 pairs), 1 day (n = 10 pairs), and 1 week (n = 15 pairs) following an aggressive interaction. Positive changes indicate higher perch selected, negative changes indicate lower. FIG.

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site scores of losers indicated that the adoption of perch sites was significantly lower than their prefight sites at 1 day and 1 week. The correlation between the extent of site change and the dominance index was 0.93, indicating a large contribution of this variable to the distinction between losers and winners following a fight. Reproductive activity. Both winners and losers recovered some courtship activity after fighting as indicated by the number of displays incorporating rapid nods, but winners had higher levels than losers at all times tested, attaining sexual activity levels comparable to their prefight levels by 1 week (Fig. 3). This was significantly higher than the activity of losers (Fisher’s exact test, P = 0.026). At 1 hr postfight, winners displayed 66% of their prefight level of courtship activity while none of the losers courted. One day following a fight, winners and losers courted at 77 and 15% of that group’s pretight levels, respectively. One week following a fight, winners manifested 100% of their pretight levels of courtship head nods, while only 12 of the losers performed this display at prefight levels in response to introduced females. Androgen levels. The mean level of circulating total ANDR in winners was higher than that found in control subjects at all sampling times, but the elevation was significant only 1 hr (P = 0.003 Roy’s greatest

100

ii 2

*O 60

B g

40

SUBORDINATE

20

ONE WR

ONE DAY

ONEWEEK

3. Percentage of control values of courtship behavior shown by subjects in each group during the hour (n = 9 pairs), day (n = 10 pairs), or week (n = 15 pairs) following an aggressive interaction. FIG.

AND CREWS

root). The mean levels of circulating androgen in losers, while slightly depressed, were not significantly lower at any sampling time from that of control subjects. However, because of this slight depression in losers, the difference in mean hormone levels between winners and losers was significantly different at 1 hr and 1 week after combat, but not at 1 day (Table 2). The overall correlation between ANDR levels and the dominance index was -0.66. Corticosterone levels. The mean levels of circulating CS in either winning or losing subjects were not significantly different from those of control subjects at any of the sampling times. Further, there were no significant differences between winners and losers at different times (Table 2). The overall correlation between CS and the dominance index was -0.12. DISCUSSION

Following an initial aggressive interaction, winning and losing green anole lizards manifested significant differences in body color, perch-site selection, and circulating levels of androgen, but not in the circulating concentrations of CS. These differences were generally sustained through the subsequent period of cohabitation and were associated with the relative social dominance of individual lizards. Behavior. The agonistic interactions between adult male green anole lizards involve characteristic exchanges of mutual stalking, display, and body color change (Greenberg, 1977). The changes in color are relatively rapid and indicate fluctuating levels or availability of several chromatotrophic hormones, all of which are also associated with effects on behavior as well as physiological response to environmental stressors (Greenberg and Crews, 1983). Lizards that lost agonistic interactions manifested body color darkening, frequently several seconds before any obvious action indicated the outcome (Sigmund,

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TABLE

AND

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2

RELATIVE HORMONE LEVELS OF CORTICOSTERONE(CS) AND ANDROGEN (ANDR) IN WINNERS AND LOSERS OF AGONISTIC ENCOUNTERS Winners/dominants Variable Corticosterone (% of control level)* 1 hr 1 day 1 week Androgen (% of control levels)’ 1 hr 1 day 1 week

Losers/subordinates

Levels (n)

Levels (n)

F”

124% (11) 172% (8) 107% (13)

149% (11) 131% (8) 109% (12)

0.02 0.33 0.49

0.89 0.57 0.49

81% (10) 94% (9) 60% (12)

8.78 0.13 8.46

0.008 0.73 0.008

470%

(12)

127% (8) 104% (14)

F’rob > F

’ rig/ml log transformed before F statistic calculated. b Mean control level of CS = 6.82 r&ml (SEM = 1.45) (n = 9). c Mean control level of ANDR = 1.64 r&ml (SEM = 0.55) (n = 9).

1978). Compared to their prelight behavior, ordinates. There was no indication that felosers were also found at lower perch sites, males discriminated males on the basis of an indication of reduced social dominance body color or were differentially responsive (Greenberg et al., 1984). to dominants and subordinates, but they The darker body color manifest by sub- did appear more responsive to more active ordinate A. carolinensis was associated in males, typically the dominant. earlier studies (Greenberg et al., 1984) with Androgen levels. The most dramatic difa physiological stress response. This dark- ference between groups was the high circuening is probably attributable to increased lating androgen levels in winners sampled availability of the pituitary peptide, melan- at 1 hr. The levels of circulating androgen otropin (MSH), closely related to ACTH were also significantly greater in winners and known to parallel its release in re- than in losers at 1 week postencounter. sponse to CRF (Proulx-Ferland et al., This finding recalls the short-term fluctua1982). Recently, the level of circulating tions in the ANDR levels associated with MSH in A. carolinensis has been found to changes in behavior following the aggresbe sensitive to social and environmental sive encounters of male songbirds (Wingstressors (Greenberg and Chen, 1987). It is field and Ramenofsky, 1987; Wingfield and reduced in response to the acute stress as- Moore, 1987), which are most apparent sociated with aggression, possibly because during the period in which social relationof catecholamine suppression of its release ships are being established (Wingfield et from the pituitary, but significantly ele- al., 1987). In male mountain spiny lizards, vated in long-term social subordination Sceloporus jarrovi, on the other hand, although behavior following agonistic inter(Greenberg et al., 1986). actions is altered, Moore (1988) found no Courtship behavior was also markedly reduced in losers at all sampling intervals detectable changes in circulating levels of following an interaction; winners showed a testosterone. The studies of S. jarrovi, slight decrease following a fight but at- however, were different from those of A. tained prefight levels of activity within 1 carolinensis in several significant details apart from the species difference. For exweek. Females were receptive, as indicated by their expression of slow head nods ample, in the study of S. jarrovi, territorial (Greenberg, 1977), even in response to sub- aggression was elicited from free-living

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males in the field by tethered intruders that were removed immediately after the interaction. It appears that at least in some contexts, physiological stress and a depressed hypothalamic-pituitary-gonadal axis are not invariably linked. In song sparrows, CS treatment does not affect plasma levels of LH, and gonads are maintained in a nearfunctional state, enabling a rapid resumption of reproductive activity as soon as the adrenal stress response abates (Wingfield and Silverin, 1986). Such a response might be of considerable utility to social subordinates in a community where mortality of dominants is high, possibly due to their more conspicuous body color and perch site selection. Interestingly, there is an apparent correspondence between androgen and perch heights at which lizards are found. At the time androgen is highest, winners are found at significantly higher perches. Subordinates, on the other hand, show the lowest perch height selection scores at 1 week, the time at which androgen is most depressed. This observation is consistent with others on this species: isolated castrated males, females, and juveniles will spontaneously perch at lower heights than isolated intact males (Greenberg and Hake, 1990; Greenberg, unpublished data) as will castrated males when they win aggressive interactions (Greenberg et al., 1984). Such observations indicate that endocrine factors may be as significant a variable in microhabitat selection as is social experience. Previous workers found that increased testis weight and elevated plasma testosterone levels were associated with dominance behavior in three of six green anoles (Pearson et al., 1976). In long-term (4 month) undisturbed hierarchies, however, the androgen levels of dominants were not higher than those of subordinates (cited in Pearson et al., 1976). In the present study, ANDR levels of dominants at 1 week were similar to levels seen in the control group, but at

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this time the subordinates showed a level of circulating ANDR well below that of controls. The control value of ANDR (mean, 1.64; SEM, 0.55) is lower than that seen in another study of captive Anolis (Crews et al., 1974), but in the earlier study, the males were long-term experimental animals subjected to daily tests of courtship and aggression. While the results indicate that social experience affects levels of circulating ANDR, we cannot discount the possibility that ANDR was highly elevated in future winners of fights. The control values of ANDR, however, were determined in individuals randomly selected from the same pool of subjects as those that interacted socially. Subordinate green anoles were also reproductively inactive, perhaps corresponding to reduced ANDR levels, although there is no direct evidence on how low androgen levels must be before reproductive dysfunctions are manifest. An elevated circulating androgen level is often positively correlated with reproductive activity (Crews and Silver, 1980) and its depression is associated with physological stress (Greenberg and Wingfield, 1987). This could be due to a cross-system feedback inhibition of gonadotropin attributable to adrenal androgen (Kime et al., 1980; and see Christian, 1980) secondary to increased adrenal activity, a classic indicator of the physiological stress response. Alternatively, there could be an altered sensitivity of the testes to gonadotropin. Corticosterone levels. There was a slight but comparable elevation in CS levels in both winners and losers. This is in contrast to an earlier study (Greenberg et al., 1986) in which CS levels were significantly elevated in subordinate males cohabiting with a dominant following an initial aggressive encounter. There are several possible reasons for the present finding of relative “stability” of CS levels within and between the groups at varying times and in previous research: First, in the present study, no

RESPONSES

TO AGGRESSION

more than 1 week had passed before blood sampling, while the subordinates in the earlier study were sampled after at least 3 weeks. In a study of rats, the response of CS to chronic environmental stressors was constant for the first 2 weeks but increased markedly in subsequent weeks (Vogel and Jensch, 1988). Second, short-term CS fluctuations might be masked by already mildly elevated levels in both groups as a function of captivity (Grassman and Crews, 1987). In baboons, comparable elevations in the levels of glucocorticoids are shown by both dominants and subordinates in response to stress, although dominants have lower basal concentrations (Sapolsky, 1986). Third, in the present study, lizards were subject to the perturbation of courtship tests during the period of cohabitation; in the earlier study in which a CS increase in subordinates was observed, individuals were undisturbed for the entire period of cohabitation. An inhibitory effect of CS on male aggressive behavior and testicular function was observed by Tokarz (1987) in a congener, A. sagrei. The effective subordination of A. carolinensis in the absence of a distinct CS change in the present study, however, indicates that the CS-related inhibition of aggression seen by Tokarz is part of a more complex ensemble of adaptive responses to a specific form of acute stress. The CS response of A. carolinensis, while slight, might have been sufficient to activate a mechanism similar to that described in squirrel monkeys. When monkeys were allowed to establish social relations, plasma cortisol levels rose in all subjects, but at 24 hr (but not 3 hr or 1 week), only dominant males showed increases in testosterone (Coe et al., 1982). In the first hour following the acute stress of rapid capture and immobilization, high-ranking male baboons showed an increase in ANDR levels while subordinate males responded by declines (Sapolsky, 1986). In both cases, luteinizing hormone concentrations were

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similarly suppressed, indicating a peripheral mechanism for the effect of acute stress on dominants. This was attributed in part to reduced sensitivity of tastes of testes of high-ranking males to glucocorticoid suppression. However, Sapolsky’s (1986) findings of attenuated transient ANDR rise in dominants following stress-induced catecholamine blockade indicate that sympathetic epinephrine and norepinephrine are acting peripherally to increase ANDR concentrations, possibly by means of altered blood circulation through the testes and/or direct stimulation of ANDR release. In pigs, exogenous ACTH can stimulate a significant and relatively rapid but transient elevation in testicular testosterone secretion by means of a mechanism that does not involve pituitary gonadotropins (Fenske et al., 1981). ACKNOWLEDGMENTS We gratefully acknowledge the expert technical help of Yuki Morris with RIA procedures, the advice on statistics of Dr. Ralph O’Brien, and the laboratory assistance of Donna Layne. This work was made possible by NSF Grant BNS-8406028 and a University of Tennessee Faculty Research Award to N. Greenberg and MH41770 and RSA MH00135 to D. Crews.

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Coe, C. L., Frankhn, D., Smith, E. R., and Levine, S. (1982). Hormonal responses accompanying fear and agitation in the squirrel monkey. Physiol. Behav. 29, 1051-1057. Coe, C. L. , Mendoza, S. P., and Levine S. (1979). Social status constrains the stress response in the squirrel monkey. Physiol. Behav. 23, 633-638. Crews, D. (1975). Inter- and intraindividual variation in display patterns in the lizard, Anolis carolinensis. Herpetologica

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Crews, D., and Garrick, L. D. (1970). Methods of inducing reproduction in captive reptiles. In “Reproductive Biology and Diseases of Captive Reptiles” (J. B. Murphy and J. T. Collins, Eds.), pp. 4%70. Sot. Stud. Amphib. Rept., Miami University, Oxford, Ohio. Crews, D., Rosenblatt, D. S., and Lehrman, D. S. (1974). Effects of unseasonal environmental regimen, group presence, group composition, and male’s physiological state on ovarian recrudescence in the lizard, Anolis carolinesis. Endocrinology 94, 541-547. Crews, D., and Silver, R. (1980). Reproductive physiology-behavior interactions in nonmammalian vertebrates. In “Handbook for Behavioral Neurobiology” (R. W. Coy and D. W. Pfaff, Eds.). Plenum, New York. Fenske, M., Holtz, W., Pitzel, L., and Konig, A. (1981). Effects of ACTH-induced testosterone release on the secretion of pituitary gonadotrophin and prolactin release in male pigs. In “Gonadal Steroids and Brain Function, Exp. Brain Res. Suppl. 3” (W. Wuttke and R. Harowski, Eds.), pp. 342-343. Springer-Verlag, New York. Gandelman, R. (1983). Gonadal hormones and sensory function. Neurosci. Biobehav. Rev. 7, l-17. Grassman, M., and Crews, D. (1987). Dominance and reproduction in an all-female lizard species. Behav. Ecol. Sociobiol. 21, 141-147. Greenberg, N. (1977). A neuroethological study of display behavior in the lizard Anolis carolinensis (Reptilian, Lacertilia, Iquanidae). Amer. Zool. 17, 191-201. Greenberg, N. (1983). Central and autonomic aspects of aggression and dominance in reptiles. In “Advances in Vertebrate Neuroethology” (J.-P. Ewert, R. R. Capranica, and D. J. Ingle, Eds.), pp. 1135-l 144. Plenum, New York. Greenberg, N., and Chen, T. (1987). Aggression and social submissiveness alter melanotropin (MSH) in the lizard. Amer. Zool. 27(4), 49A. [Abstract] Greenberg, N., and Crews, D. (1983). Physiological ethology of aggression in amphibians and reptiles. In “Hormones and Aggressive Behavior” (B. Svare, Ed.), pp. 46%506. Plenum, New York. Greenberg, N., and Hake, L. (1990). Hatching and

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