Physiology&Behavior,Vol.52, pp. 1043-1046, 1992
0031-9384/92$5.00 + .00 Copyright© 1992PergamonPressLtd.
Printedin the USA.
Ovariectomy Does Not Attenuate Aggression by Primiparous Lactating Female Rats D. J. ALBERT, .1 R. H. J O N I K * A N D M. L. WALSH~-
*Psychology Department, University of British Columbia, Vancouver, British Columbia, Canada V6T 1Z4 and tSchool of Kinesiology, Simon Fraser University, Burnaby, British Columbia, Canada VSA 1S6 Received 27 April 1992 ALBERT, D. J., R. H. JONIK AND M. L. WALSH. Ovariectomydoesnot attenuateaggressionbyprimiparouslactatingfemale rats. PHYSIOL BEHAV 52(6) 1043-1046, 1992--Nulliparous female hooded rats were allowed to cohabit with a sexuallyactive male in a large living cage. Aggressiontoward an unfamiliar female was assessed during the second and third week of pregnancy. Within 12 to 24 h followingparturition females were ovariectomized(n = 7) or sham-ovariectomized(n = 6) in a manner that balanced previousaggressionscores. Aggressionwas assessed at 48 h followingovariectomyand at three weeklyintervalsthereafter. Ovariectomized and sham-ovariectomizedfemales did not differ in the number of attacks, number of bites, duration of on-top, or frequency of piloerection on any test day followingparturition. These results indicate that circulating levelsof ovarian steroids do not influence the level of aggression by a primiparous lactating female toward an unfamiliar female conspecific. Aggression
Maternal aggression
Maternal behavior
A primiparous lactating female, a primiparous pregnant female, or a nulliparous female cohabiting with a sterile male are each aggressive toward an unfamiliar conspecific ( 1,3,12-18,21). The aggression is behaviorally similar in each of these states. It includes the display of piloerection and the use of lateral attack ( l, 12,13,15). The aggression is directed toward an unfamiliar male or female rat (1), but is only used in the nest area (1,21). Although the aggressive behavior toward an unfamiliar conspecific is similar in different reproductive states, the hormonal foundation of the aggression seems to vary. The aggression of a primiparous pregnant female disappears within 48 h following ovariectomy and can be at least partially maintained by an injection of estradiol benzoate (19). The aggression of a female cohabiting with a sterile male disappears within 27 h following ovariectomy and can be maintained over a 3-week period by combined estradiol plus testosterone replacement [Silastic implants, (4)]. In contrast, the aggression of a primiparous lactating female apparently does not decline following removal of gonadal and pituitary hormones [hypophysectomy, (13)]. However, only one series of observations has been made, and in this experiment, hypophysectomy was done at 4 days postpartum and aggression was assessed only at 9 days postpartum. This leaves the possibility that the aggressiveness would be seen to be attenuated postoperatively if ovarian hormones were removed sooner following parturition or if aggression was assessed on several occasions during lactation. The present experiment reexamined the influence of gonadal hormones on the aggressiveness of lactating females. The aggression of pregnant females was assessed twice during the course
Requests for reprints should be addressed to D. J. Albert.
1043
of pregnancy. Between 12 and 24 h following parturtion, half of the females were ovariectomized and the other half shamovariectomized. The aggression of all animals was assessed at 48 h postoperatively and at three weekly intervals thereafter. METHOD The subjects were female (250 to 300 g) and male (275 to 325 g) hooded rats derived from stock obtained from Charles River, Canada. They had been reared in same-sex cages since weaning. Colony lighting was a 12/12 h light/dark cycle with all testing done in the last third of the light cycle.
Housing Females to be tested for aggression were housed in wood cages (50 × 60 × 20 cm high) with a Plexiglas front, a hardware cloth top, and dried corn cob chips on the floor. During the first 2 weeks in this living situation, each female subject was housed with a female slightly smaller than itself. This permitted adaptation to the living area. At the end of 2 weeks, the female cagemate was exchanged for a sexually active male. The male had been observed to be sexually active when exposed to an estradiol/ progesterone-primed female. The male cagemate cohabited with the female for 20 days. At the end of this time, it was removed, leaving the pregnant female as the sole cage occupant. Following parturition, pups remained with the mother except during aggression tests.
1044
ALBERI. JONIK ANI) WAt..%tt
Behavioral l'esting
R E S t rl I S
Aggression tests were given during the second and third weeks of cohabitation with a male. Fifteen min prior to each aggression test, the male cagemate was removed from the cage and placed in a clean bin with corn cob chips. At the same time, an unfamiliar female (200 to 220 g) to be used as the target of the aggression was injected with 0.25 mg diazepam (Hoffman-LaRoche). The unfamiliar female intruder was left in the cage for a 10-rain period. At the end of that time, the intruder was removed and the male cagemate returned. One group of female intruders was used in the tests prior to parturition and a second group in the postpartum tests. The same intruder was never used more than once with the same resident female. Small female intruders were used to encourage aggression by the resident female; diazepam was routinely used in these tests to decrease defensiveness and produce more uniform intruder behavior (1,2,7,8). Attacks, bites, on-top, and piloerection were recorded during the aggression tests. Lateral attacks were scored when the resident female rose up on its toes, arched its back, approached the target animal laterally, and pushed against it. A lunge attack was recorded when the resident female jumped at the target animal and bumped or bit it. On-top was registered when the resident attacked and then stood over the target animal. Piloerection was scored when the hair on the sides and back was erect. A composite aggression score was calculated for each test using the following formula: Composite aggression = (number of attacks) + 0.2 [attack duration (s)] + (number of bites) + 0.2 [on-top duration (s)] + piloerection. Piloerection was scored as 4 if complete and present for the entire session, 2 if partial or if present for only part of the test session, and 0 if absent. The composite aggression score has been empirically formulated to give approximately equal weight to each measure of active aggression (8). It is more stable than any single measure of aggression (1,8) and was used to divide animals into groups having a comparable level of aggressiveness.
b,:rperimental Manipulation Fifteen of 16 females gave birth in the fourth week following pairing with a male. Fourteen of these females were subject to surgery between 12 and 24 h following parturition. Eight females were ovariectomized and six were given sham ovariectomies (ether anesthesia). Each female was kept in an individual bin for 1 to 2 h and then returned to its living cage and pups. Seven ovariectomized females and all six sham ovariectomized females resumed maternal behavior when returned to their litter. One ovariectomized female ignored its pups. One postpartum female was not subjected to surgery because it did not behave maternally toward its litter. Both of these females were dropped from the experiment. An aggression test was given to each female at 48 h postoperatively (72 h following parturition). Additional tests were given at 10, 17, and 24 days postpartum. The postpartum aggression tests were carried out in a manner identical to those given prepartum. Pups were removed 15 rain prior to each test. At the end of the sixth aggression test, the females were killed and the surgical manipulations confirmed.
Statistical Analysis The aggression scores were subjected to a two-way analysis of variance (BMDP) followed by paired comparisons (NewmanKeuls tests). Piloerection scores were subjected to a M a n n Whitney U-test for each test day.
('omposite Aggression ,S'corc,~ Comparable levels of aggression were emitted toward an unfamiliar female by ovariectomized (N = 7) and sham-ovariectomized (N = 6) resident female rats at all tests postoperatively [Fig. 1; Group: F(1, 11) = 0.1, p > 0.80; paired comparisons, all p > 0.10, Newman-Keuls test]. Composite aggression scores tended to increase during pregnancy for both groups. The level of aggression was highest at the first test postpartum (72 h) and declined over the course of lactation [test day: F(5, 55) = 36, p < 0.01" test day × group: F(5, 55) = 0.4, p > 0.80].
Individual Measures of Aggression Ovariectomized and sham-ovariectomized females did not differ in attack frequency, attack duration, number of bites, or on-top duration [group: all F(I, 1 l) < 1.1, all p > 0.30; paired comparisons, all p > 0.10, Newman-Keuls test]. As with the composite aggression scores, each individual measure of aggression increased during pregnancy, reached its highest level at the first test following parturition, and declined during the course of lactation [test day: all F(5, 55) > 11, all p < 0.01, group × test: all F(5, 55) < 1.2, all p > 0.30]. Piloerection scores did not differ between groups on any day pre- or postoperatively (Fig. I ; all p > 0.25). DISCUSSION Erskine, Barfield, and Goldman (13) decreased circulating levels of gonadal hormones in primiparous females by means of hypophysectomy at 5 days following parturition and observed no decrement in the display of aggression on day 9 of lactation. This observation is confirmed and extended by the present failure to observe an attenuation of aggression over the entire course of lactation with females ovariectomized between 12 and 24 h postpartum. Both of these results contrast with the demonstrated importance of these hormones in maintaining aggression during pregnancy and pseudopregnancy. Mayer and Rosenblatt (19) have shown that ovariectomized/pregnancy-terminated primiparous females decline in aggressiveness when tested 48 h postoperatively. Estradiol benzoate (20 #g/kg), administered at the time of ovariectomy, at least partially maintains aggression at the 48-h test. Parallel results have been obtained with pseudopregnant females. Aggression toward an unfamiliar conspecific declines within 27 h following ovariectomy and can be maintained by a combination of exogenous estradiol and testosterone (2,4,7). The influence of gonadal hormones on aggression toward an unfamiliar conspeeific depends on a female rat's reproductive state and past experience. Initial activation of the aggression appears to require both gonadal hormones and sexual activity, because the aggression can be activated by cohabitation with a sexually active intact or sterile male (1,19) but not by cohabitation with a female (1) or with a sexually inactive male (6). During pregnancy or pseudopregnaney, aggression appears to be maintained by gonadal hormones and greatly attenuated by ovariectomy (2,4,7,19). At parturition, there is a surge in aggressiveness that appears due, at least in part, to a high level of estradiol and testosterone in conjunction with a precipitous decline in progesterone (5). During lactation, aggression toward an unfamiliar conspecific becomes independent of the level of circulating gonadal hormones and dependent on experiential events. Thus, removal of gonadal hormones is without effect, whereas removal of sensory stimulation associated with the pups substantially re-
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1046
ALBERT, J O N I K A N D WALStt
duces aggression (12-14). However, the independence of aggressiveness on gonadal h o r m o n e s during lactation may not be complete. The level of aggression clearly declines over the course of lactation in spite of the c o n t i n u o u s presence of pups
(Fig. 1). The basis for this decline is unexplored. Finally, Jn multiparous females, initial observations suggest that aggression may b e c o m e i n d e p e n d e n t of both circulating gonadal h o r m o n e s and the presence of pups ( 1O, 11 ).
REFERENCES 1. Albert, D. J.; Dyson, E. M.; Petrovic, D. M.; Walsh, M. L. Activation of aggression in female rats by normal males and by castrated males with testosterone implants. Physiol. Behav. 44:9-13; 1988. 2. Albert, D. J.; Jonik, R. H.; Walsh, M. L. Hormone-dependent aggression in female rats: Testosterone plus estradiol prevents the decline in aggression following ovariectomy. Physiol. Behav. 49:673677; 1991. 3. Albert, D. J.; Jonik, R. J.; Walsh, M. L. Hormone-dependent aggression in male and female rats: Experiential, hormonal, and neural foundations. Neurosci. Biobehav. Rev. 16:177-192; 1992. 4. Albert, D. J.; Jonik, R. H.; Walsh, M. L. Aggression by a female rat cohabiting with a sterile male declines within 27 hours following ovariectomy. Physiol. Behav. (in press). 5. Albert, D. J.; Jonik, R. H.; Walsh, M. L. Interaction of estradiol, testosterone, and progesterone in the modulation of hormonedependent aggression in the female rat. Physiol. Behav. 52:773779; 1992. 6. Albert, D. J.; Jonik, R. H.; Watson, N. V.; Moe, 1. V.; Walsh, M. L. Aggression by a female rat cohabiting with a sterile male: Termination ofpseudopregnancy does not abolish aggression. Physiol. Behav. 50:519-523; 1991. 7. Albert, D. J.; Petrovic, D. M.; Walsh, M. L. Ovariectomy attenuates aggression by female rats cohabiting with sexually active sterile males. Physiol. Behav. 45:225-228; 1989. 8. Albert, D. J.; Walsh, M. L.; Gorzalka, B. B.; Siemens, Y.; Louie, H. Testosterone removal in rats results in a decrease in social aggression and a loss of social dominance. Physiol. Behav. 36:401-407; 1986. 9. Albert, D. J.; Walsh, M. L.; Zalys, C.; Dyson, E. M. Maternal aggression and intermale social aggression: A behavioral comparison. Behav. Proc. 14:267-275; 1987. 10. Blanchard, D. C.; Fukunaga-Stinson, C.; Takahashi, L.; Flannelly,
11. 12. 13. 14. 15. 16. 17. 18. 19. 20. 21.
K. J.; Blanchard, R. J. Dominance and aggression in social groups of male and female rats. Behav. Proc. 9:31-48; 1984. DeBold, J. F.; Miczek, K. A. Aggression persists after ovariectomy in female rats. Horm. Behav. 8:177-190; 1984. Erskine, M. S.; Barfield, R. J.; Goldman, B. D. Intraspecific fighting during late pregnancy and lactation in rats and effects of litter removal. Behav. Biol. 23:206-218; 1978. Erskine, M. S.; Barfield, R. J.; Goldman, B. D. Postpartum aggression in rats: I. Effects of hypophysectomy. J. Comp. Physiol. Psychol. 94:484-494; 1980. Ferriera, A.; Hansen, S. Sensory control of maternal aggression in Rattus norvegicus. J. Comp. Psychol. 100:173-177; 1986. Flannelly, K. J.; Flannelly, L. Opponents' size influences maternal aggression. Psychol. Rep. 57:883-886; 1985. Flannelly, K. J.; Flannelly, L. Time course of postpartum aggression in rats (Ratus norvegicus). J. Comp. Physiol. Psychol. 101 : 101 - 103; 1987. Flannelly, K. J.; Flannelly, L.; Lore, R. Postpartum aggression against intruding male conspecifics in Sprague-Dawley rats. Behav. Proc. 13:279-286; 1986. Gandelman, R.; Simon, N. G. Postpartum fighting in the rat: Nipple development and the presence of young. Behav. Neural Biol. 28: 350-360; 1980. Mayer, A. D.; Rosenblatt, J. S. Prepartum changes in maternal responsiveness and nest defense in Rattus norvegicus. J. Comp. Psychol. 98:177-188; 1984. Mayer, A. D.; Rosenblatt, J. S. Hormonal factors influence the onset of maternal aggression in laboratory rats. Horm. Behav. 21:253267; 1987. Paul, L.; Gronek, J.; Politch, J. Maternal aggression: Protection of young is a by-product of attacks on the home site. Aggress. Behav. 6:19-29; 1980.
0031-9384/92$5.00 + .00 Copyright© 1992PergamonPressLtd.
Printedin the USA.
Ovariectomy Does Not Attenuate Aggression by Primiparous Lactating Female Rats D. J. ALBERT, .1 R. H. J O N I K * A N D M. L. WALSH~-
*Psychology Department, University of British Columbia, Vancouver, British Columbia, Canada V6T 1Z4 and tSchool of Kinesiology, Simon Fraser University, Burnaby, British Columbia, Canada VSA 1S6 Received 27 April 1992 ALBERT, D. J., R. H. JONIK AND M. L. WALSH. Ovariectomydoesnot attenuateaggressionbyprimiparouslactatingfemale rats. PHYSIOL BEHAV 52(6) 1043-1046, 1992--Nulliparous female hooded rats were allowed to cohabit with a sexuallyactive male in a large living cage. Aggressiontoward an unfamiliar female was assessed during the second and third week of pregnancy. Within 12 to 24 h followingparturition females were ovariectomized(n = 7) or sham-ovariectomized(n = 6) in a manner that balanced previousaggressionscores. Aggressionwas assessed at 48 h followingovariectomyand at three weeklyintervalsthereafter. Ovariectomized and sham-ovariectomizedfemales did not differ in the number of attacks, number of bites, duration of on-top, or frequency of piloerection on any test day followingparturition. These results indicate that circulating levelsof ovarian steroids do not influence the level of aggression by a primiparous lactating female toward an unfamiliar female conspecific. Aggression
Maternal aggression
Maternal behavior
A primiparous lactating female, a primiparous pregnant female, or a nulliparous female cohabiting with a sterile male are each aggressive toward an unfamiliar conspecific ( 1,3,12-18,21). The aggression is behaviorally similar in each of these states. It includes the display of piloerection and the use of lateral attack ( l, 12,13,15). The aggression is directed toward an unfamiliar male or female rat (1), but is only used in the nest area (1,21). Although the aggressive behavior toward an unfamiliar conspecific is similar in different reproductive states, the hormonal foundation of the aggression seems to vary. The aggression of a primiparous pregnant female disappears within 48 h following ovariectomy and can be at least partially maintained by an injection of estradiol benzoate (19). The aggression of a female cohabiting with a sterile male disappears within 27 h following ovariectomy and can be maintained over a 3-week period by combined estradiol plus testosterone replacement [Silastic implants, (4)]. In contrast, the aggression of a primiparous lactating female apparently does not decline following removal of gonadal and pituitary hormones [hypophysectomy, (13)]. However, only one series of observations has been made, and in this experiment, hypophysectomy was done at 4 days postpartum and aggression was assessed only at 9 days postpartum. This leaves the possibility that the aggressiveness would be seen to be attenuated postoperatively if ovarian hormones were removed sooner following parturition or if aggression was assessed on several occasions during lactation. The present experiment reexamined the influence of gonadal hormones on the aggressiveness of lactating females. The aggression of pregnant females was assessed twice during the course
Requests for reprints should be addressed to D. J. Albert.
1043
of pregnancy. Between 12 and 24 h following parturtion, half of the females were ovariectomized and the other half shamovariectomized. The aggression of all animals was assessed at 48 h postoperatively and at three weekly intervals thereafter. METHOD The subjects were female (250 to 300 g) and male (275 to 325 g) hooded rats derived from stock obtained from Charles River, Canada. They had been reared in same-sex cages since weaning. Colony lighting was a 12/12 h light/dark cycle with all testing done in the last third of the light cycle.
Housing Females to be tested for aggression were housed in wood cages (50 × 60 × 20 cm high) with a Plexiglas front, a hardware cloth top, and dried corn cob chips on the floor. During the first 2 weeks in this living situation, each female subject was housed with a female slightly smaller than itself. This permitted adaptation to the living area. At the end of 2 weeks, the female cagemate was exchanged for a sexually active male. The male had been observed to be sexually active when exposed to an estradiol/ progesterone-primed female. The male cagemate cohabited with the female for 20 days. At the end of this time, it was removed, leaving the pregnant female as the sole cage occupant. Following parturition, pups remained with the mother except during aggression tests.
1044
ALBERI. JONIK ANI) WAt..%tt
Behavioral l'esting
R E S t rl I S
Aggression tests were given during the second and third weeks of cohabitation with a male. Fifteen min prior to each aggression test, the male cagemate was removed from the cage and placed in a clean bin with corn cob chips. At the same time, an unfamiliar female (200 to 220 g) to be used as the target of the aggression was injected with 0.25 mg diazepam (Hoffman-LaRoche). The unfamiliar female intruder was left in the cage for a 10-rain period. At the end of that time, the intruder was removed and the male cagemate returned. One group of female intruders was used in the tests prior to parturition and a second group in the postpartum tests. The same intruder was never used more than once with the same resident female. Small female intruders were used to encourage aggression by the resident female; diazepam was routinely used in these tests to decrease defensiveness and produce more uniform intruder behavior (1,2,7,8). Attacks, bites, on-top, and piloerection were recorded during the aggression tests. Lateral attacks were scored when the resident female rose up on its toes, arched its back, approached the target animal laterally, and pushed against it. A lunge attack was recorded when the resident female jumped at the target animal and bumped or bit it. On-top was registered when the resident attacked and then stood over the target animal. Piloerection was scored when the hair on the sides and back was erect. A composite aggression score was calculated for each test using the following formula: Composite aggression = (number of attacks) + 0.2 [attack duration (s)] + (number of bites) + 0.2 [on-top duration (s)] + piloerection. Piloerection was scored as 4 if complete and present for the entire session, 2 if partial or if present for only part of the test session, and 0 if absent. The composite aggression score has been empirically formulated to give approximately equal weight to each measure of active aggression (8). It is more stable than any single measure of aggression (1,8) and was used to divide animals into groups having a comparable level of aggressiveness.
b,:rperimental Manipulation Fifteen of 16 females gave birth in the fourth week following pairing with a male. Fourteen of these females were subject to surgery between 12 and 24 h following parturition. Eight females were ovariectomized and six were given sham ovariectomies (ether anesthesia). Each female was kept in an individual bin for 1 to 2 h and then returned to its living cage and pups. Seven ovariectomized females and all six sham ovariectomized females resumed maternal behavior when returned to their litter. One ovariectomized female ignored its pups. One postpartum female was not subjected to surgery because it did not behave maternally toward its litter. Both of these females were dropped from the experiment. An aggression test was given to each female at 48 h postoperatively (72 h following parturition). Additional tests were given at 10, 17, and 24 days postpartum. The postpartum aggression tests were carried out in a manner identical to those given prepartum. Pups were removed 15 rain prior to each test. At the end of the sixth aggression test, the females were killed and the surgical manipulations confirmed.
Statistical Analysis The aggression scores were subjected to a two-way analysis of variance (BMDP) followed by paired comparisons (NewmanKeuls tests). Piloerection scores were subjected to a M a n n Whitney U-test for each test day.
('omposite Aggression ,S'corc,~ Comparable levels of aggression were emitted toward an unfamiliar female by ovariectomized (N = 7) and sham-ovariectomized (N = 6) resident female rats at all tests postoperatively [Fig. 1; Group: F(1, 11) = 0.1, p > 0.80; paired comparisons, all p > 0.10, Newman-Keuls test]. Composite aggression scores tended to increase during pregnancy for both groups. The level of aggression was highest at the first test postpartum (72 h) and declined over the course of lactation [test day: F(5, 55) = 36, p < 0.01" test day × group: F(5, 55) = 0.4, p > 0.80].
Individual Measures of Aggression Ovariectomized and sham-ovariectomized females did not differ in attack frequency, attack duration, number of bites, or on-top duration [group: all F(I, 1 l) < 1.1, all p > 0.30; paired comparisons, all p > 0.10, Newman-Keuls test]. As with the composite aggression scores, each individual measure of aggression increased during pregnancy, reached its highest level at the first test following parturition, and declined during the course of lactation [test day: all F(5, 55) > 11, all p < 0.01, group × test: all F(5, 55) < 1.2, all p > 0.30]. Piloerection scores did not differ between groups on any day pre- or postoperatively (Fig. I ; all p > 0.25). DISCUSSION Erskine, Barfield, and Goldman (13) decreased circulating levels of gonadal hormones in primiparous females by means of hypophysectomy at 5 days following parturition and observed no decrement in the display of aggression on day 9 of lactation. This observation is confirmed and extended by the present failure to observe an attenuation of aggression over the entire course of lactation with females ovariectomized between 12 and 24 h postpartum. Both of these results contrast with the demonstrated importance of these hormones in maintaining aggression during pregnancy and pseudopregnancy. Mayer and Rosenblatt (19) have shown that ovariectomized/pregnancy-terminated primiparous females decline in aggressiveness when tested 48 h postoperatively. Estradiol benzoate (20 #g/kg), administered at the time of ovariectomy, at least partially maintains aggression at the 48-h test. Parallel results have been obtained with pseudopregnant females. Aggression toward an unfamiliar conspecific declines within 27 h following ovariectomy and can be maintained by a combination of exogenous estradiol and testosterone (2,4,7). The influence of gonadal hormones on aggression toward an unfamiliar conspeeific depends on a female rat's reproductive state and past experience. Initial activation of the aggression appears to require both gonadal hormones and sexual activity, because the aggression can be activated by cohabitation with a sexually active intact or sterile male (1,19) but not by cohabitation with a female (1) or with a sexually inactive male (6). During pregnancy or pseudopregnaney, aggression appears to be maintained by gonadal hormones and greatly attenuated by ovariectomy (2,4,7,19). At parturition, there is a surge in aggressiveness that appears due, at least in part, to a high level of estradiol and testosterone in conjunction with a precipitous decline in progesterone (5). During lactation, aggression toward an unfamiliar conspecific becomes independent of the level of circulating gonadal hormones and dependent on experiential events. Thus, removal of gonadal hormones is without effect, whereas removal of sensory stimulation associated with the pups substantially re-
COMPOSITE A ~ O N
NUMBER OF Bill:.5
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1046
ALBERT, J O N I K A N D WALStt
duces aggression (12-14). However, the independence of aggressiveness on gonadal h o r m o n e s during lactation may not be complete. The level of aggression clearly declines over the course of lactation in spite of the c o n t i n u o u s presence of pups
(Fig. 1). The basis for this decline is unexplored. Finally, Jn multiparous females, initial observations suggest that aggression may b e c o m e i n d e p e n d e n t of both circulating gonadal h o r m o n e s and the presence of pups ( 1O, 11 ).
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