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Behavioral correlates to gonadal state in the lizard, Anolis carolinensis
HORMONIS
AND
BEHAVIOR,
Behavioral
4, 307-313
(1973)
Correlates to Gonadal State in the Lizard, Anolis carolinensis DAVID
CREWS’
Institute of’ Animal Behavior, Rutgers University, I01 Warren Street, Newark, New Jersey 07102
Female Andis carulirwr~sis of unknown reproductive condition were introduced into cages containing a sexually active male and the resulting sexual behavior was noted. Female sexual receptivity was found to be correlated with the stages of follicular maturation. These results suggest that sexual receptivity in female A. carolinrnsis is restricted to a time immcdiatcly prccuiing the ovulation of each follicle and is dependent upon follicular development. Evihormonal conditions normally arising during dence is oftered to suggest that during the breeding season, female sexual receptivity is rhythmical and contingent upon the cyclic ovarian changes peculiar to lizards of this genus.
INTRODUCTION While rhere have heen many experimental investigations relating ovarian clranges to changes in sexual receptivity, the majority of these have been restricted to birds and mammals (Young, 1961, 1964). In one of the few such studies with reptiles, Noble and Greenberg (1941) speculated that there existed a direct correlation between maturation of ovarian follicles and sexual receptivity in the lizard, .4noZis carolinensis. In his summary of this research following Noble’s death, Greenberg concluded that female sexual receptivity is dependent upon ovarian secretions and that “copulation is possible only wvhen ripe ova have developed to the point where the associated follicular or interstitial cells produced sufficient hormone to activate the female mating reflexes (Greenberg and Noble, 1944, p. 434).” However, while they were successful in demonstrating that sexual receptivity was dependent upon the presence of the ovaries and that implants of specific crystalline ovarian hormones could induce female receptivity, they did not attempt to relate changes in receptivity to specific stages of follicular maturation. In the present
California
1 Present address: 94720.
Department
of
Zoology,
307 Copyright 0 1973 by Academic Press, Inc. All rieh 1s of reoroduction in any form renervod
llniversity
of
California,
Berkeley.
308
DAVID
CREWS
experiment, an attempt was made to relate, in greater detail than has been attempted before, changes in sexual receptivity to the follicular changes seen during the normal annual ovarian cycle in A. carulinensis. MATERIALS
AND METHODS
Animals For Groups I and 11 (see below), reproductively
inactive, winter
dormant
A. curolinensis were collected in the field in early January 1972. For Group III, breeding females were collected in April 1972. All animals were captured near New Orleans, LA, and shipped to New Jersey on the day of capture. Upon arrival, all animals were given ad lib water and food (mealworms and crickets), kept at room temperatures (21-23OC), and variable photoperiods. Four days later, the healthiest animals were selected, divided into either ah-female or male-female groups, and placed in environmental chambers. Only sexually mature animals were used (males: > 64 mm Snout-Vent length; females: > 49 mm Snout-Vent length; Hamlett, 1952). During the experiment, water and food were available at all times.
Environmental
Regime
Controlled environment chambers (Sherer-Gilett RI-48-BG-LTP) provided a 14L: IOD photic cycle, a daily thermal cycle of 32°C during the light phase of the photic cycle and 23°C during the dark phase, and a constant relative humidity of 70-80 percent. This environmental regime has been shown in previous experiments to reliably induce ovarian recrudescence (OR) in winter dormant females (Crews et al., in press). Each environmental chamber could accomodate six group or testing cages and had full length glass doors enabling the experimenter to monitor the behavior in each cage without disturbing the animals. Light for each cage was provided by two 24 in. DuroTest Vitalite fluorescent tubes.
Cages Both holding and testing cages measured 18% X 20 X 12 in. and contained plants, twigs, and branches for perching and climbing. Each cage had a 10 X 16 in. Plexiglas front panel to facilitate behavioral observations. All cages were made of % in. wire mesh.
Testing Procedure The method used to determine whether sexual receptivity was correlated with follicular development was as follows: After varying periods of exposure
FEMALE
SLXLJAL
RECEPTIVITY
IN LIZARDS
309
to the stimulatory regime, females were removed from their group cages and introduced into testing cages containing a dominant, sexually active male and two subordinate, sexually inactive males. In behavioral tests lasting a maximum of one hour, the females were categorized as being either sexually unreceptive or sexually receptive depending upon whether they stood for, and copulated with, the courting test male. Mating behavior in laboratory populations of A. carolinensis has been previously described by Evans (1936a, 1938), Greenberg and Noble (1944), and Crews (1973a,b). Briefly, the dominant male approaches the female while performing a species-typical bobbing-dewlap extension display pattern. If the female is sexually unreceptive, she will flee and attempt to hide from the approaching male. If the female is receptive, however, she will stand for the courting male, arching her neck as the male comes alongside, thus facilitating his grasping of her neck skin. The male then mounts, brings his tail beneath the female’s tail and, depending upon which side of the female the male is on, everts one of two hemipenes into the female’s cloaca. There is no pelvic thrusting or any visible indication of ejaculation. The length of copulation varies between males (lasting from 238 to 2927 set) and appears to be determined by sensory feedback from the hemipenis during intromission and/or ejaculation (Crews, 1973b).
Determination
of Ovarian Condition
Following the behavioral test, the females were removed from the test cage and their ovarian condition determined. Ovarian condition was determined in the following manner: First, depending upon the state of the ovarian follicles, females were classified as being reproductively inactive, as indicated by the presence of previtellogenic follicles, or reproductively active, as indicated by the presence of yolking follicles. Females with yolking follicles were in turn placed in one of three arbitrarily chosen categories according to the size of the largest ovarian follicle (i.e., the largest follicle being < 3.5, 3.5-6.0, or > 6.0 mm in diameter). Finally, all reproductively active females were considered to be in their first, second, or third follicular cycles depending upon whether there were 0, 1, or 2 corpora lutea (CL) present, respectively. Using this procedure, therefore, neither the reproductive condition nor the sexual receptivity of the females were known prior to testing.
Experimental
Design
In an attempt to correlate changes in sexual receptivity with morphological changes in follicular development, the following groups of females tested for sexual receptivity using the above testing procedure.
rhtvm
310
CREWS
(i). Group 1 (n = 84): Femalesthat had been isolated from malessince the previous breeding season and had been environmentally induced to unseasonalOR whiIe in all-femalegroups. (ii) Group II (n = 39): Femalesthat had been environmentally induced while in male-femalegroups. The only procedural difference in the testing of these females and Group I females was that Group II femaleswere not tested for sexual receptivity until they had been observed to mate with the dominant male in their group cage. (iii) Group III (n = 59): To determine whether female A. carolinensis undergo cycles of sexual receptivity during the breeding seasonand, secondly, whether the pattern is similar to that exhibited by environmentally-induced females, a third group of normally sexually active females were tested for sexual receptivity and their gonadal state subsequently assessed.
RESULTS The results are summarizedin Fig. 1. Group I None of the females that had been environmentally induced while in all-female groups (Group I) and that were later found to be reproductively inactive, as indicated by the presenceof previtellogenic follicles, were receptive to the courtship of the test male. Similarly, none of Group 1 femaleslater found to be in their first follicular cycle but with small (< 3.5 mm in diameter) yolking follicles were sexually receptive. Unfortunately, only two
sexual
Fig. 1. Relationship receptivity.
between
ovarian
condition
and percentage
of females
showing
FEMALE
SCXUAL
KISCliPTIVITY
IN LlZAliDS
311
females from Group I were later found to be in their first follicular cycle with ovaries containing follicles of between 3.5-6.0 mm in diameter; both of these were also unreceptive to the test male. In contrast, all of the females later found to be in their first cycle with large preovulatory follicles of greater than 6.0 mm stood for the courting males and copulated. Similarly, all females later found to have oviducal eggs (= gravid) allowed the test males to copulate with them. Further analysis of these females showed that all were in the latter stages of their second or third follicular cycles. Croup II None of the females known to have copulated at least with the dominant male of their group cage had inactive ovaries or were in the initial stages of their first follicular cycle. Sexually receptive females were later found, upon autopsy, to be in the latter stages of their second or third follicular cycles. The majority of sexually unreceptive females were later found to be in the initial stage of their second or third follicular cycles.
The same relationships between sexual receptivity and follicular maturation were found in normally breeding females. That is, all nonsexually receptive females were later found to be in the initial stages of their second or third follicular cycles while those females that mated had large preovulatory ovarian follicles.
DISCUSSION Under field conditions, female A. curolinensis lay a single egg every lo-14 days for the duration of the breeding season (Hamlett, 1952; Dessauer, 1955b; Gordon, 1956; King, 1966; Licht, in press; Crews, unpublished data). This pattern of ovarian activity is generated by the development and ovulation of a single ovarian follicle alternately between ovaries (see Fig. 2). It is logical to assume that this regular pattern of follicular development, ovulation, and oviposition during the breeding Season also reflects corresponding cyclic changes in the secretion patterns of gonadotropic and ovarian hormones. The present data demonstrate a close correlation between sexual receptivity and stage of follicular maturation. This is indicated by the fact that all first cycle and gravid females receptive to the test male were later found to have a large preovulatory ovarian follicle while none of the females, whether gravid or not, later found to have small yolking follicles, were ever observed to mate. These data suggest, therefore, that sexual receptivity in female A. carolinensis is
DAVID CREWS
312
DAYS
7
14
21
[SJ Ad-.ICC*;3 “C
20
piw,:,;,,r
35
42
49
56
~“..,pat,..
Fig. 2. Schematic representation of the proposed relationship between follicular maturation and sexual receptivity in female Anolis curolinensis during the breeding season.
related to follicle development and is rhythmical in nature in a way that correspondsto cyclic follicular changes. In every group some of the females later found to have follicles of between 3.5 and 6.0 mm in diameter were receptive to the test male while others were not. The transition from nonreceptivity to receptivity may occur during this phase of follicular development. However, the exact point of the transition seems to vary from female to female, suggesting that these variations are due to either individual differences in the amount of hormone secreted by the developing follicle or to individual differences in neural sensitivity to hormone levels. In Group II females (environmentally-induced while in male-female groups), only five females not receptive to the test male were later found to be in the latter stagesof their first follicular cycle. It is noteworthy that these were the only females that can with certainty be said to have mated with the dominant male of their group cageswhile in the sumc follicular cycle as when tested for sexual receptivity with the test male. The fact that these five females failed to mate with the test male suggestseither that (a) familiarity with the male might influence female sexual receptivity or (b) mating might inhibit further sexual receptivity with each follicular cycle but not subsequent mating during later cycles (Crews, 1973b). That coital stimulation may inhibit subsequentsexual receptivity within a single estrous cycle has been demonstrated in mammals (Goldfoot and Coy, 1970; Carter and Schein, 1971; llardy and DeBold, 1972) and birds (Schein and Hale, 1965). Mating does not, however, appear to inhibit female A. carohensis during later fohicular cycles. This is evident because all nine females known to have copulated previously with the dominant male in their group cage and later observed to mate with the test male were found, upon autopsy, to be in the latter stages of their secondor third follicular cycles.
FEMALE
SEXUAL
RECEPTIVITY
IN LIZARDS
313
I wish to thank Dr. Jay S. Rosenblatt and Dr. Harvey H. Feder for their critical reading of the manuscript. This report constitutes part of a dissertation submitted in partial fulfillment of the requirements of the PhD degree, Rutgers University, 1973. This work was conducted while the author was a USPHS trainee (Grant No. GM-1135, Daniel S. Lehrman, Program Director). Contribution No. 134 of the Institute of Animal Behavior. REFERENCES Carter, C. S., and Schein, M. W. (1971). Sexual receptivity and exhaustion in the female golden hamster. IIorm. Behav. 2, 191-200. Crews, D. P. (1973a). Social factors associated with the male in the control of reproduction in the female lizard Anolis carolinensis: The role of courtship and aggression. Unpublished Ph.D. Thesis. Rutgers University. Crews, D. P. (1973b). Coition-induced inhibition of receptivity in female lizards (nnolis carolinensis). Physiol. Behav., in press. Crews, D. P., Roscnblatt, J. S., and Lehrman, D. S. (1973). Effects of unseasonal environmental regime, group presence, group composition, and males’ physiological state on ovarian recrudescence in the lizard, Rnolis carolinensis. Endocr., in press. Dessauer, II. C. (1955). Seasonal changes in the gross organ composition of the lizard, Anolis carolinensis. J. Exp. Zool. 128, l-12. Evans, I.. T. (1936). Behavior of castrated lizards. J. &wet. Psychol. 48, 217-225. Evans, I... T. (1938). Courtship behavior and sexual selection of Anolis. J. Comp. Psychol. 26, 475497. Goldfoot, D. A., and Gay, R. W. (1970). Abbreviation of behavioral estrus in guinea pigs by coital and vaginocervical stimulation. J. Camp. Physiol. Psychol. 72, 426-434. Gordon, R. E. (1956). The biology and biodemography of Anolis carolinensis. Unpublished Ph.D. Dissertation, Tulane University. Greenberg, B., and Noble, G. K. (1944). Social, behavior of the American chameleon (Anolis carolensis Voigt). Physiol. Zool. 17, 392-439. Hamlett, G. W. D. (1952). Notes on breeding and reproduction in the lizard Anolis carolinensis. Copeia 1952, 183-185. Hardy, I>. I:., and DeBold, J. I:. (1972). Effects of coital stimulation upon behavior of the female rat. J. Camp. Physiol. Psychol. 78, 400-408. King, I:. W. (1966). Competition between two south Florida lizards of the genus Anolis. Unpublished Ph.D. Thesis. University of Miami. Licht, P. (1973). Influence of temperature and photoperiod on the annual ovarian cycle in the lizard, Anolis carolinensis. Cope@ in press. Noble, G. K., and Greenberg, B. (1941). Effects of seasons, castration and crystalline sex hormones upon the urogenital system and sexual behavior of the lizard (Anolis carolinensis). I. The adult female. J. Exp. Zool. 88, 451-479. Schein, M. W., and Hale, E. R. 1965. Stimuli eliciting sexual behavior. In F. A. Beach (Ed.), Sex and Behavior, pp. 440-482. Wiley and Sons, New York. Young, W. C. (1961). The hormones and mating behavior. In W. C. Young (Ed.) Sex and Internal Secrerions, Vol. II, pp. 1173-l 239, Williams and Wilkins Co., Baltimore, MD. Young, W. C. (1964). The hormones and behavior. In M. I’lorkin and H. S. Mason (Eds.) Compararive Biochemistry. A Comprehensive Treatise, Vol. VII, pp. 203-252. Academic Press, New York.
AND
BEHAVIOR,
Behavioral
4, 307-313
(1973)
Correlates to Gonadal State in the Lizard, Anolis carolinensis DAVID
CREWS’
Institute of’ Animal Behavior, Rutgers University, I01 Warren Street, Newark, New Jersey 07102
Female Andis carulirwr~sis of unknown reproductive condition were introduced into cages containing a sexually active male and the resulting sexual behavior was noted. Female sexual receptivity was found to be correlated with the stages of follicular maturation. These results suggest that sexual receptivity in female A. carolinrnsis is restricted to a time immcdiatcly prccuiing the ovulation of each follicle and is dependent upon follicular development. Evihormonal conditions normally arising during dence is oftered to suggest that during the breeding season, female sexual receptivity is rhythmical and contingent upon the cyclic ovarian changes peculiar to lizards of this genus.
INTRODUCTION While rhere have heen many experimental investigations relating ovarian clranges to changes in sexual receptivity, the majority of these have been restricted to birds and mammals (Young, 1961, 1964). In one of the few such studies with reptiles, Noble and Greenberg (1941) speculated that there existed a direct correlation between maturation of ovarian follicles and sexual receptivity in the lizard, .4noZis carolinensis. In his summary of this research following Noble’s death, Greenberg concluded that female sexual receptivity is dependent upon ovarian secretions and that “copulation is possible only wvhen ripe ova have developed to the point where the associated follicular or interstitial cells produced sufficient hormone to activate the female mating reflexes (Greenberg and Noble, 1944, p. 434).” However, while they were successful in demonstrating that sexual receptivity was dependent upon the presence of the ovaries and that implants of specific crystalline ovarian hormones could induce female receptivity, they did not attempt to relate changes in receptivity to specific stages of follicular maturation. In the present
California
1 Present address: 94720.
Department
of
Zoology,
307 Copyright 0 1973 by Academic Press, Inc. All rieh 1s of reoroduction in any form renervod
llniversity
of
California,
Berkeley.
308
DAVID
CREWS
experiment, an attempt was made to relate, in greater detail than has been attempted before, changes in sexual receptivity to the follicular changes seen during the normal annual ovarian cycle in A. carulinensis. MATERIALS
AND METHODS
Animals For Groups I and 11 (see below), reproductively
inactive, winter
dormant
A. curolinensis were collected in the field in early January 1972. For Group III, breeding females were collected in April 1972. All animals were captured near New Orleans, LA, and shipped to New Jersey on the day of capture. Upon arrival, all animals were given ad lib water and food (mealworms and crickets), kept at room temperatures (21-23OC), and variable photoperiods. Four days later, the healthiest animals were selected, divided into either ah-female or male-female groups, and placed in environmental chambers. Only sexually mature animals were used (males: > 64 mm Snout-Vent length; females: > 49 mm Snout-Vent length; Hamlett, 1952). During the experiment, water and food were available at all times.
Environmental
Regime
Controlled environment chambers (Sherer-Gilett RI-48-BG-LTP) provided a 14L: IOD photic cycle, a daily thermal cycle of 32°C during the light phase of the photic cycle and 23°C during the dark phase, and a constant relative humidity of 70-80 percent. This environmental regime has been shown in previous experiments to reliably induce ovarian recrudescence (OR) in winter dormant females (Crews et al., in press). Each environmental chamber could accomodate six group or testing cages and had full length glass doors enabling the experimenter to monitor the behavior in each cage without disturbing the animals. Light for each cage was provided by two 24 in. DuroTest Vitalite fluorescent tubes.
Cages Both holding and testing cages measured 18% X 20 X 12 in. and contained plants, twigs, and branches for perching and climbing. Each cage had a 10 X 16 in. Plexiglas front panel to facilitate behavioral observations. All cages were made of % in. wire mesh.
Testing Procedure The method used to determine whether sexual receptivity was correlated with follicular development was as follows: After varying periods of exposure
FEMALE
SLXLJAL
RECEPTIVITY
IN LIZARDS
309
to the stimulatory regime, females were removed from their group cages and introduced into testing cages containing a dominant, sexually active male and two subordinate, sexually inactive males. In behavioral tests lasting a maximum of one hour, the females were categorized as being either sexually unreceptive or sexually receptive depending upon whether they stood for, and copulated with, the courting test male. Mating behavior in laboratory populations of A. carolinensis has been previously described by Evans (1936a, 1938), Greenberg and Noble (1944), and Crews (1973a,b). Briefly, the dominant male approaches the female while performing a species-typical bobbing-dewlap extension display pattern. If the female is sexually unreceptive, she will flee and attempt to hide from the approaching male. If the female is receptive, however, she will stand for the courting male, arching her neck as the male comes alongside, thus facilitating his grasping of her neck skin. The male then mounts, brings his tail beneath the female’s tail and, depending upon which side of the female the male is on, everts one of two hemipenes into the female’s cloaca. There is no pelvic thrusting or any visible indication of ejaculation. The length of copulation varies between males (lasting from 238 to 2927 set) and appears to be determined by sensory feedback from the hemipenis during intromission and/or ejaculation (Crews, 1973b).
Determination
of Ovarian Condition
Following the behavioral test, the females were removed from the test cage and their ovarian condition determined. Ovarian condition was determined in the following manner: First, depending upon the state of the ovarian follicles, females were classified as being reproductively inactive, as indicated by the presence of previtellogenic follicles, or reproductively active, as indicated by the presence of yolking follicles. Females with yolking follicles were in turn placed in one of three arbitrarily chosen categories according to the size of the largest ovarian follicle (i.e., the largest follicle being < 3.5, 3.5-6.0, or > 6.0 mm in diameter). Finally, all reproductively active females were considered to be in their first, second, or third follicular cycles depending upon whether there were 0, 1, or 2 corpora lutea (CL) present, respectively. Using this procedure, therefore, neither the reproductive condition nor the sexual receptivity of the females were known prior to testing.
Experimental
Design
In an attempt to correlate changes in sexual receptivity with morphological changes in follicular development, the following groups of females tested for sexual receptivity using the above testing procedure.
rhtvm
310
CREWS
(i). Group 1 (n = 84): Femalesthat had been isolated from malessince the previous breeding season and had been environmentally induced to unseasonalOR whiIe in all-femalegroups. (ii) Group II (n = 39): Femalesthat had been environmentally induced while in male-femalegroups. The only procedural difference in the testing of these females and Group I females was that Group II femaleswere not tested for sexual receptivity until they had been observed to mate with the dominant male in their group cage. (iii) Group III (n = 59): To determine whether female A. carolinensis undergo cycles of sexual receptivity during the breeding seasonand, secondly, whether the pattern is similar to that exhibited by environmentally-induced females, a third group of normally sexually active females were tested for sexual receptivity and their gonadal state subsequently assessed.
RESULTS The results are summarizedin Fig. 1. Group I None of the females that had been environmentally induced while in all-female groups (Group I) and that were later found to be reproductively inactive, as indicated by the presenceof previtellogenic follicles, were receptive to the courtship of the test male. Similarly, none of Group 1 femaleslater found to be in their first follicular cycle but with small (< 3.5 mm in diameter) yolking follicles were sexually receptive. Unfortunately, only two
sexual
Fig. 1. Relationship receptivity.
between
ovarian
condition
and percentage
of females
showing
FEMALE
SCXUAL
KISCliPTIVITY
IN LlZAliDS
311
females from Group I were later found to be in their first follicular cycle with ovaries containing follicles of between 3.5-6.0 mm in diameter; both of these were also unreceptive to the test male. In contrast, all of the females later found to be in their first cycle with large preovulatory follicles of greater than 6.0 mm stood for the courting males and copulated. Similarly, all females later found to have oviducal eggs (= gravid) allowed the test males to copulate with them. Further analysis of these females showed that all were in the latter stages of their second or third follicular cycles. Croup II None of the females known to have copulated at least with the dominant male of their group cage had inactive ovaries or were in the initial stages of their first follicular cycle. Sexually receptive females were later found, upon autopsy, to be in the latter stages of their second or third follicular cycles. The majority of sexually unreceptive females were later found to be in the initial stage of their second or third follicular cycles.
The same relationships between sexual receptivity and follicular maturation were found in normally breeding females. That is, all nonsexually receptive females were later found to be in the initial stages of their second or third follicular cycles while those females that mated had large preovulatory ovarian follicles.
DISCUSSION Under field conditions, female A. curolinensis lay a single egg every lo-14 days for the duration of the breeding season (Hamlett, 1952; Dessauer, 1955b; Gordon, 1956; King, 1966; Licht, in press; Crews, unpublished data). This pattern of ovarian activity is generated by the development and ovulation of a single ovarian follicle alternately between ovaries (see Fig. 2). It is logical to assume that this regular pattern of follicular development, ovulation, and oviposition during the breeding Season also reflects corresponding cyclic changes in the secretion patterns of gonadotropic and ovarian hormones. The present data demonstrate a close correlation between sexual receptivity and stage of follicular maturation. This is indicated by the fact that all first cycle and gravid females receptive to the test male were later found to have a large preovulatory ovarian follicle while none of the females, whether gravid or not, later found to have small yolking follicles, were ever observed to mate. These data suggest, therefore, that sexual receptivity in female A. carolinensis is
DAVID CREWS
312
DAYS
7
14
21
[SJ Ad-.ICC*;3 “C
20
piw,:,;,,r
35
42
49
56
~“..,pat,..
Fig. 2. Schematic representation of the proposed relationship between follicular maturation and sexual receptivity in female Anolis curolinensis during the breeding season.
related to follicle development and is rhythmical in nature in a way that correspondsto cyclic follicular changes. In every group some of the females later found to have follicles of between 3.5 and 6.0 mm in diameter were receptive to the test male while others were not. The transition from nonreceptivity to receptivity may occur during this phase of follicular development. However, the exact point of the transition seems to vary from female to female, suggesting that these variations are due to either individual differences in the amount of hormone secreted by the developing follicle or to individual differences in neural sensitivity to hormone levels. In Group II females (environmentally-induced while in male-female groups), only five females not receptive to the test male were later found to be in the latter stagesof their first follicular cycle. It is noteworthy that these were the only females that can with certainty be said to have mated with the dominant male of their group cageswhile in the sumc follicular cycle as when tested for sexual receptivity with the test male. The fact that these five females failed to mate with the test male suggestseither that (a) familiarity with the male might influence female sexual receptivity or (b) mating might inhibit further sexual receptivity with each follicular cycle but not subsequent mating during later cycles (Crews, 1973b). That coital stimulation may inhibit subsequentsexual receptivity within a single estrous cycle has been demonstrated in mammals (Goldfoot and Coy, 1970; Carter and Schein, 1971; llardy and DeBold, 1972) and birds (Schein and Hale, 1965). Mating does not, however, appear to inhibit female A. carohensis during later fohicular cycles. This is evident because all nine females known to have copulated previously with the dominant male in their group cage and later observed to mate with the test male were found, upon autopsy, to be in the latter stages of their secondor third follicular cycles.
FEMALE
SEXUAL
RECEPTIVITY
IN LIZARDS
313
I wish to thank Dr. Jay S. Rosenblatt and Dr. Harvey H. Feder for their critical reading of the manuscript. This report constitutes part of a dissertation submitted in partial fulfillment of the requirements of the PhD degree, Rutgers University, 1973. This work was conducted while the author was a USPHS trainee (Grant No. GM-1135, Daniel S. Lehrman, Program Director). Contribution No. 134 of the Institute of Animal Behavior. REFERENCES Carter, C. S., and Schein, M. W. (1971). Sexual receptivity and exhaustion in the female golden hamster. IIorm. Behav. 2, 191-200. Crews, D. P. (1973a). Social factors associated with the male in the control of reproduction in the female lizard Anolis carolinensis: The role of courtship and aggression. Unpublished Ph.D. Thesis. Rutgers University. Crews, D. P. (1973b). Coition-induced inhibition of receptivity in female lizards (nnolis carolinensis). Physiol. Behav., in press. Crews, D. P., Roscnblatt, J. S., and Lehrman, D. S. (1973). Effects of unseasonal environmental regime, group presence, group composition, and males’ physiological state on ovarian recrudescence in the lizard, Rnolis carolinensis. Endocr., in press. Dessauer, II. C. (1955). Seasonal changes in the gross organ composition of the lizard, Anolis carolinensis. J. Exp. Zool. 128, l-12. Evans, I.. T. (1936). Behavior of castrated lizards. J. &wet. Psychol. 48, 217-225. Evans, I... T. (1938). Courtship behavior and sexual selection of Anolis. J. Comp. Psychol. 26, 475497. Goldfoot, D. A., and Gay, R. W. (1970). Abbreviation of behavioral estrus in guinea pigs by coital and vaginocervical stimulation. J. Camp. Physiol. Psychol. 72, 426-434. Gordon, R. E. (1956). The biology and biodemography of Anolis carolinensis. Unpublished Ph.D. Dissertation, Tulane University. Greenberg, B., and Noble, G. K. (1944). Social, behavior of the American chameleon (Anolis carolensis Voigt). Physiol. Zool. 17, 392-439. Hamlett, G. W. D. (1952). Notes on breeding and reproduction in the lizard Anolis carolinensis. Copeia 1952, 183-185. Hardy, I>. I:., and DeBold, J. I:. (1972). Effects of coital stimulation upon behavior of the female rat. J. Camp. Physiol. Psychol. 78, 400-408. King, I:. W. (1966). Competition between two south Florida lizards of the genus Anolis. Unpublished Ph.D. Thesis. University of Miami. Licht, P. (1973). Influence of temperature and photoperiod on the annual ovarian cycle in the lizard, Anolis carolinensis. Cope@ in press. Noble, G. K., and Greenberg, B. (1941). Effects of seasons, castration and crystalline sex hormones upon the urogenital system and sexual behavior of the lizard (Anolis carolinensis). I. The adult female. J. Exp. Zool. 88, 451-479. Schein, M. W., and Hale, E. R. 1965. Stimuli eliciting sexual behavior. In F. A. Beach (Ed.), Sex and Behavior, pp. 440-482. Wiley and Sons, New York. Young, W. C. (1961). The hormones and mating behavior. In W. C. Young (Ed.) Sex and Internal Secrerions, Vol. II, pp. 1173-l 239, Williams and Wilkins Co., Baltimore, MD. Young, W. C. (1964). The hormones and behavior. In M. I’lorkin and H. S. Mason (Eds.) Compararive Biochemistry. A Comprehensive Treatise, Vol. VII, pp. 203-252. Academic Press, New York.