Journal of Comparative and Physiological Psychology 1978, Vol. 92TNo767lT79-1187
Experiential Determinants of Postpartum Aggression in Mice James A. Green University of North Carolina at Chapel Hill The objective of this research was to explore the experiential determinants and the social controls of postpartum aggression in mice. In Experiment 1, a group of seven lactating females was tested repeatedly from Day 2 to Day 22 postpartum against male mice; attacks by the females continued through Day 18. Two other groups of seven females tested only once showed diminished attacks against males by Day 14 postpartum. In Experiment 2, eight females were paired with a male for a week prior to parturition; they showed reliably fewer attacks on Day 2 postpartum than a group of nine females that were isolated prior to parturition. All of these results were obtained in a standard 3-min test. A 24-hr test on Day 4 of Experiment 2 revealed that in both groups female attacks dropped to near zero after 30 min. After female attacks declined, males initiated social behavior which occasioned vocalizations by the females. Further, males attacked in 65% of the tests and destroyed the litters of the females in 53% of the tests. The behavior of the male exerted important influences on the structure of extended female-male interactions.
That female and male mice differ in their aggressive behavior is well established. Female mice have not shown the "spontaneous" aggression characteristic of male mice (Ginsburg & Allee, 1942; Uhrich, 1938). Further, certain experiential manipulations, especially social isolation, have been shown to increase attacks by male mice but not by females (Fredericson, 1952). Recent work has also pointed to hormonal differences as basic to behavioral differences in aggression. Neonatally masculinized females have displayed increased levels of attacks as adults (Bronson & Desjardins, 1968; Edwards, 1969;
This research was supported by National Institute of Child Health and Human Development Grant 5 R01 HD 08464-02 to Robert B. Cairns and Grant 2 T01HD 00193-06 to the Carolina Population Center. The author was supported during preparation of the manuscript by a National Science Foundation predoctoral fellowship. Assistance during collection of the data was provided by D. J. MacCombie, and R. B. Cairns assisted throughout the research project. An earlier version of this paper was presented at the meeting of the American Psychological Association, Washington, D.C., September 1976. Requests for reprints should be sent to James A. Green, Department of Psychology, Davie Hall, University of North Carolina, Chapel Hill, North Carolina 27514.
Vale, Ray, & Vale, 1972). In addition, the sex-specific changes associated with pregnancy, parturition, and lactation have been related to increased female attacks during those periods (Gandelman, 1972; Gandelman & Svare, 1974; Noirot, Goyens, & Buhot, 1975). Nonetheless, many gaps remain in our understanding of the social events that elicit and maintain aggressive behavior in female mice. Several different kinds of social experience have been shown to be related to male aggression; these remain unexplored in female mice. Specifically, the effects of (a) repeated testing, (b) social isolation, and (c) immediate social feedback on male attacks have been well documented (see Cairns, 1973, for a review). The aim of the present research was to investigate the role of these factors in the aggression of female mice during the postpartum period. The following studies, then, were addressed to these questions: (a) Does repeated testing prolong the time in the postpartum period during which females will attack? (b) Does social isolation facilitate the establishment of attacks in the postpartum period? (c) Do females stop attacking during extended testing? (d) What role does the test partner play in maintaining
Copyright 1978 by the American Psychological Association, Inc. 0021-9940/78/9206-1179$00.75
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the interaction during this extended testing? General Method The subjects in these studies were virgin females obtained from an inbred strain of ICR mice. They were housed from weaning with littermates of the same sex in standard laboratory cages (28 X 18 X 13 cm). Food and water were available ad lib, and a 12:12 hr light/dark cycle was employed. All test sessions began within 2 to 4 hr after the onset of the dark cycle. Male ICR mice reared under the same conditions were used for mating purposes. They were introduced into the group-rearing cages of the 90-120-day-old females and were removed 14 days later, at which time the females were placed in the appropriate test conditions. The male object animals used in testing were groupreared ICR mice between 90 and 120 days of age. Males were naive with respect to female contacts at the time of first testing. Both subjects and objects were marked at weaning with a permanent dye to permit individual identification. All tests were scored with a stopwatch in a continuous time-sampling procedure. Five-second blocks and a 31-item social behavior code were used for all tests; the scoring procedure has been more fully described elsewhere (Cairns & Nakelski, 1971). The behavior of both animals was recorded sequentially, which resulted in a continuous record of social behavior for the test period. The primary measure of interest for these studies was attack—a behavior ranging from a discrete bite to more vigorous chasing and biting. When necessary because of distributional assumptions, nonparametric analyses were employed in the data analysis. Analyses of repeated-measures designs in both experiments employed the multivariate technique suggested by McCall and Appelbaum (1973). This technique can give both a test for trends in the data and an unbiased analysis of the overall effects. Finally, conditional probability statements were used in Experiment 2 to explicate sequential dependencies in the social behavior of the test animals.
Experiment 1 The purpose of Experiment 1 was to assess the effects of repeated testing on postpartum aggression. Repeated testing has been shown to lower the threshold for subsequent aggressive responding in male mice (Cairns & Scholz, 1973; King & Gurney, 1954; Lagerspetz & Lagerspetz, 1971). Gandelman (1972) reported that lactating females tested for the first time late in the postpartum period show relatively little aggression. Further, Svare and Gandelman (1973,1976) and St. John and Corning (1973) tested females repeatedly, showing that the high levels of
attack displayed initially decline during the postpartum period. However, a systematic comparison of cross-sectional and longitudinal groups is necessary to give a more precise statement of the effect of previous encounters with a male mouse on postpartum attacks. Method Subjects. After mating, 21 females were isolated in the standard laboratory cages. Seven subjects were assigned randomly to each of three groups. One longitudinal group was tested once daily on Days 2, 6,10, 14,18, and 22 postpartum. One cross-sectional group was tested only once on Day 6 postpartum; a second cross-sectional group was tested only on Day 14 postpartum. All tests were conducted in the females' home cages. Procedure. Three-minute dyadic tests were administered on the days dictated by group assignment. The tests consisted of moving the female's cage to a standard test area, removing the wire top containing the water bottle and food hopper, placing the male in the cage and putting a flat Plexiglas top on the cage. The social interaction was scored for 3 min, then the male was removed from the cage. The male mice used for all tests on Days 2,6, and 14 had never been tested previously; the tests on Days 10, 18, and 22 employed the same males, previously tested with a different female.
Results Initial behavior patterns. When males were first introduced into the females' cages, one of three things typically occurred. On Day 2, in a small percentage of the tests (14%), only mutual sniffing by the female of the head and anogenital region was evident. In 43% of the Day 2 tests, the initial mutual investigation became more and more vigorous as the female began to lunge with paws extended toward the head and flank regions of the male. Tail rattling was often seen. Actual biting of the males was the end result of the escalating social interactions, although it occurred with a long latency (M = 83 sec). In the remaining 43% of the tests, there was virtually no mutual social investigation; biting occurred upon initial contact. A similar patterning of the percentages and the types of initial social behavior applied to the cross-sectional group tested on Day 6. A different picture emerged when the second test of the longitudinal group was
AGGRESSION IN MICE
examined. On Day 6, all animals attacked the male without behavioral precursors. Mean latency to attack was 9 sec, which differed reliably from the mean latency of 83 sec for this group on Day 2, £(6) = 2.4, p < .05. Attack frequency. The frequency data indicated that attacks do decline in the postpartum period, after seeming to peak sometime between Day 2 and Day 6. Repeated testing, however, prolonged the period in which attacks toward the male were a high probability behavior (see Figure 1). This was shown statistically in two ways. First, a multivariate analysis of variance confirmed that the initial increase and subsequent decrease in the scores of the longitudinal group were reliable, F(2, 5) = 12.7, p < .01; quadratic trend, F(l, 6) = 6.8, p < .04. Second, a comparison of subjects that were tested only once with those tested repeatedly showed reliable differences by Day 14 postpartum. The difference between the longitudinal group on Day 6 and the Day 6 cross-sectional group was not reliable (Mann-Whitney U = 12, p < .13). However, the difference between the longitudinal group on Day 14 and the Day 14 cross-sectional group was reliable (U = 9, p < .05). There was a reliable difference between the animals tested for the first time on Day 2 and those tested initially on Days 6 and 14. The decline shown in Figure 1 across these three groups was reliable (Kruskal-Wallis H = 6.6, p < .05). Only the difference between Day 2 and Day 14 was significant (U = 8, p < .04). Percentage of animals attacking. The percentage data paralleled the frequency data. The percentages of animals in the longitudinal group that attacked on each of the six tests were 86%, 100%, 100%, 71%, 71%, and 43%. In the cross-sectional group tested on Day 6, 71% attacked, and in the crosssectional group tested on Day 14, 14% attacked. The change over days in the percentage of animals attacking in the longitudinal group was of borderline significance (Cochran's Q(5) = 11, p < .10). In the cross-sectional groups, the difference between Day 2 and Day 14 was reliable by Fisher's exact probability test (p < .05). No
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o—o Longitudinal Group ® Cross-sectional Groups
"0
2
6 10 14 18 DAYS POSTPARTUM
22
Figure 1. Mean attacks by females during a 3-min test (Experiment 1).
other differences between cross-sectional groups or between analogous longitudinal and cross-sectional groups were reliable. Supplemental results. An additional group of 16 females, 90-120 days old, was exposed to males only through a wire mesh screen in a sham mating procedure. These females were then isolated and tested in a regimen identical to that of the females in Experiment 1; that is, 1 wk after the sham mating procedure (which lasted for 2 wk), the females were tested in a 3-min dyadic test. They were tested again 4 days later, and so on, for a total of six tests. None of these females attacked. This replicated the reports in the literature—nonlactating females typically do not attack males. Discussion Experiment 1 suggests that postpartum attacks during a 3-min test are controlled by at least two interacting factors: (a) time since parturition and (b) the number of prior aggression tests against males. Females that had previously been tested on Days 2 and 6 postpartum were more likely to attack males, and to attack males more vigorously, on Day
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14 than were females with no previous tests. Experiment 2 Experiment 1 provided one link between postpartum aggression and male aggression: Repeated testing seemed to facilitate attack behaviors in the same setting at subsequent times. Experiment 2 was designed to assess the effects on postpartum aggression of two other variables known to be important in male aggression. These were isolation from conspecifics prior to testing and social feedback effects within the interchange itself (Cairns, 1973; Cairns & Scholz, 1973). One procedure that has been commonly employed in the postpartum literature is the isolation of pregnant females for about 1 wk prior to parturition. Tests of the effects of lactation on aggression have therefore been confounded with social isolation (Gandelman, 1972; Gandelman & Svare, 1974; Svare & Gandelman, 1973). However, it has been shown that limited exposure to a male during the postpartum period decreases aggression toward that particular male (Svare & Gandelman, 1973). One purpose of the present experiment was to discover what role, if any, prepartum isolation has on postpartum attacks against familiar and unfamiliar males by pairing pregnant females with males prior to parturition. A rather puzzling finding of Experiment 1 was the relative complacency of males when tested against lactating females. Since the males had been quickly removed from a familiar home environment to be placed in a female's home cage, one possible explanation of their behavior would be that they were not adapted to the novel social environment provided by the lactating mother and her pups. If a male's responses changed as he adapted to or settled into the situation, these new responses could affect the ongoing behavioral sequences. Such temporal shifts in patterns of interaction can give important clues to the physiological processes accompanying behavior, in addition to explicating the immediate social controls of behavior. A necessary part of a behavioral analysis is relating known patterns of male-female interaction
in other contexts to the sequences of behaviors established in the prolonged postpartum tests. Unpublished data (1976) from this laboratory have indicated, for instance, that one typical pattern of malefemale interaction in a 10-min test is the male sniffing the anogenital region repeatedly and the female kicking and vocalizing or withdrawing. Often, this leads to arousal of the male to the point of vigorous grooming, mating, or attacking. This pattern was also evident in the sham-mated females reported on in Experiment 1. Such sequences might also occur during extended postpartum tests sometime after the initial attacks of the female, thus providing a behavioral link between male-female social interaction during the postpartum period and during nonparturient states of the female. The test length of Experiment 2 was extended to 24 hr, and test cages were modified in the hope of providing more natural surroundings. This permitted an analysis of postpartum attacks as part of a larger period of social adaptation, and it provided a more adequate test of the brood-defense hypothesis (Moyer, 1968; Scott, 1966). It was thought that enlarging the cages provided the male test object with some space, although still limited, to escape from the female and vice versa. Small nest boxes were added to provide a more natural situation (Crowcroft, 1966) and one in which the females could more adequately protect their litters. Method Subjects. Seventeen gravid females were randomly assigned to two groups of subjects; each group was tested on Days 2 and 4 postpartum. One group of subjects was paired with a male ICR mouse immediately after mating and throughout the remainder of the experiment. The other group of subjects was isolated immediately after mating and for the rest of the study. Procedure. After the 2-wk mating interval, each female in Group I (Isolated, n = 9) was isolated in a large Masonboard cage (35 X 30 X 35 cm), with two partitions dividing the cage into three chambers (22 X 13 X 35 cm; 8 X 35 X 35 cm; 22 X 22 X 35 cm). Each subject in Group P (Paired, n = 8) was paired with a male that had not been used as a breeder. Cage bottoms were covered with sawdust litter and provided with scraps of butcher paper to serve as nesting material. In addition, each cage was provided with a small transparent Plexiglas
AGGRESSION IN MICE nest box (13 X 10 X 6 cm) which had one entrance (3 X 6cm). A standard 3-min dyadic test was given on Day 2. For Group I this involved placing the male test object at the point farthest from the female and scoring 3 min of social interaction, after which the male was removed. In Group P, this test consisted of removal of the resident male for 1 min, introduction of the new male, removal of the male after 3 min, and replacement of the resident male after 2 min. Three minutes of resident male/ lactating female interaction was also scored at this time of reentry of the resident. On Day 4, the resident male was removed for 1 min, the new male was introduced, and continuous observations were made for 1 hr. Three minutes of observation were also scored at the end of Hours 2, 3,4, and 24 of the test. No resident male reintroduction was made in Group P, but 3 min of baseline resident male/ lactating female social interaction was scored prior to the beginning of the Day 4 test.
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This difference was reliable by Fisher's exact probability test (p < .05). In comparing the data of Group I with those from Day 2 of Experiment 1, it appeared as if the cage changes had not appreciably altered the characteristics of postpartum aggression in this strain. Behavior during extended testing. On Day 4, Group I again attacked more frequently than Group P, but only for the first 3 min of the test. In both groups female attacks declined rapidly during the first 30 min of the test. Further, 11 males counterattacked their female partners. In nine of the tests, male attacks were directed at the litters also. When individual pups in the litters were killed as a result of attacks by males, the females and the males usually cannibalized those particular pups. Average levels of female attack are shown in Figure 2; average levels of male attack are shown in Figure 3. These figures represent 3-min by 3-min summaries of the first 30 min of the test with 3-min summaries at the end of Hours 1, 2, 3, 4, and 24 of the test. (Three-minute blocks of behavior were used here only because this has been the standard short-test length used throughout this work.) The initial difference between the two groups, based on a 3-min sample of behavior,
Daily checks of the nesting and sleeping arrangements revealed that 6 of the 9 animals in Group I employed the nest boxes as sites for parturition and lactation, and 7 of 8 Group P females did likewise. At no time during the experiment were the females seen to be aggressive toward the resident males. The animals always slept together, and the males were often seen licking, retrieving, and sleeping on top of the pups in a lactating position. This behavior also characterized both the baseline data from the Day 4 test and the reentry data after the Day 2 test. None of those data is therefore presented. Familiarity of males is clearly an important determinant of feo—o Group I (Isolated) male attacks. Group P (Paired) Attack behavior during the Day 2 test. The 3-min test on Day 2 replicated the behavioral analysis of Experiment 1; all three patterns of female response were evident, although immediate attacks were seen only in Group I. The latency, probability, and frequency data all indicated that animals which were isolated prior to parturition differed significantly from those that were paired. The mean latency to attack in Group P was 171 sec, whereas the mean latency to attack in Group I was 57 sec, £(15) = 3.9, p < .001. Mean attacks were .4 and 6 12 18 24 30 120 240 1440 7.9 for Group P and Group I, respectively, TIME IN 3-MINUTE SAMPLES t (15) = 2.8, p < .01. In addition, for Group P, the percentage of animals attacking on Figure 2. Mean attacks by females during successive Day 2 was 25%, and for Group I it was 77%. 3-min samples (Experiment 2).
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o—o Group I (Isolated) •—• Group P (Paired)
0
6
12 18 24 30 120 240 1440 TIME IN 3-MINUTE SAMPLES
Figure 3. Mean attacks by males during successive 3min samples (Experiment 2).
was reliable, £(15) = 2.6, p < .02. However, by the end of 6 min of interaction, the difference was no longer reliable, £(15) = .79, p < .4. In addition, Figure 2 shows that the low level of female attacks remained stable over the 24-hr period. Individual analyses. Did the females stop attacking because of male counterattacks? The low but consistent levels of male attack shown in Figure 3 suggested that these counterattacks served that function. However, the examination of the data did not bear out this interpretation. The protocols from each test were examined individually: In five tests, female attacks declined without males ever counterattacking; in nine tests, male attacks occurred, but not until after female attacks had already declined. Only one test could support a punishment explanation of the decline in female attacks. Another explanation of the decline might be that the females rapidly habituated to the intruder. This would imply, however, that some "calming down" or lowering of general arousal level took place. Examining the initiations of nonattack social behaviors and the vocalizations were important to this question. The results are shown in Figure 4. Multivariate analyses of variance of each 2 (Group) X 2 (Time) design for the four behaviors of male initiate, male vocalize, female initiate, and female vocalize yielded the following reliable results: a main effect of group for male initiate, F(l, 15) = 4.8, p < .04; a main effect of time for male vocalize, F(l, 15) = 21.1, p < .001; and main effects of time for female initiate and vocalize, F(l, 15) = 51.7, p < .001 and F(l, 15) = 9.7, p < .001,
respectively. Thus, with reference to Figure 4, the only group main effect was for male initiate, in which the mean in Group P was 3.9 compared with 1.9 for Group I. There were no Group X Time interactions for any measure, and each time main effect was reliable except for male initiate (p < .08). The decline in male vocalizations indicates simply that as males stopped being attacked, they also stopped vocalizing. By the end of 30 min, male vocalizations and female attacks were seen in only 3 of the 17 test dyads. An analysis of conditional probabilities supported the relation of vocalization to attack. Male vocalizations were closely related to female attacks; the probabilities of male vocalizations, given female attacks, were quite high in the first 3 min of the test. In Group P, the median conditional probability was .4 (range of .0-1.0); in Group I, the median was .5 (range of .0-.9). However, the conditional probability for each dyad during Minutes 28-30 was .0, which reflects both the decrease in female attacks and the coupling of male vocalizations to female attacks. The rise in male initiations and female vocalizations (Figure 4) indicates two things; first, as males stopped vocalizing and females stopped attacking, males began to initiate social behaviors—sniffing, nosing, or grooming the female. Second, the drop in female attacks did not indicate a "calming down" of the female. Rather, females were
12 18 24 30 120 TIME IN 3-MINUTE SAMPLES
Figure 4. Mean rates of male and female vocalizations and nonattack social initiations during successive 3-min samples, collapsed across treatment groups (Experiment 2).
AGGRESSION IN MICE
indicating high arousal by vocalizing. Thirteen of 17 females were still vocalizing at the end of 30 min; however, only 4 were still vocalizing after 24 hr, which indicates that the habituation process took longer to occur than the decline in female attacks would indicate. Again, conditional probabilities supported this interpretation of the relationship between male initiations and female vocalizations. Whereas males stopped vocalizing because they were no longer attacked, females began to vocalize after mild social stimulation. The probability of a female vocalization, given a male initiation (sniff, nose, or groom), was quite high at the end of 30 min of testing. In Group P, the median was .3 (range of .0-1.0); in Group 2, the median was .75 (range of .0-1.0). The same conditional probabilities were .0 for all but one test dyad during Minutes 1-3, despite the fact that 9 of 17 males initiated an average of 2.4 times during that period. Discussion Isolation from male mice for 1 wk prior to parturition significantly increased both the probability and frequency of postpartum attacks on an unfamiliar male during a 3-min test. Females stopped attacking quickly during the extended test on Day 4. In 11 of 17 tests, males counterattacked, and in 9 tests male attacks were also directed at the litters of the females. As females stopped attacking, males began initiating nonattack social behavior, and a consistent pattern of male initiation/female vocalization developed. The drop in female attacks was permanent, and the pattern of reactivity to male social initiations showed evidence of having diminished by the end of 24 hr of testing. General Discussion These studies demonstrate that postpartum aggression in female mice has many features in common with aggression in male mice. These include the sensitivity of aggression to (a) previous test experience (prior tests for aggression during the postpartum period increase the probability, speed, and frequency of later attacks against
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males), (b) the structure of the social environment prior to actual testing (females paired with a male prior to and after parturition do not attack those males, and they are less likely than isolated females to attack an unfamiliar male), and (c) the characteristics of the test experience itself, particularly the length of time the test is permitted to continue (female attacks on males declined rapidly during the first 30 min of a 24-hr test). The value of the behavioral analysis presented here is twofold. First, careful reporting of the dominant patterns of nonattack social behavior in aggressive encounters is essential because descriptive data provide one basis for future hypotheses and studies. Second, a dyadic behavioral analysis provides the first clue in untangling the interaction between endogenous and immediate social controls of social behavior. Social feedback during the ongoing social interaction has been shown to play an important role in the establishment and maintenance of attacks in males (Cairns & Scholz, 1973; MacCombie & Cairns, Note 1). With reference to these data, there were no obvious behaviors of the male which caused the decline in female attacks. That decline, therefore, is most reasonably attributed to a nonbehavioral process—motor fatigue or endocrine change being two possibilities. However, the data on female vocalizations help rule out declining arousal levels as an explanation while also showing that the male plays an active role in the ongoing interaction, keeping the female in a state in which vocalizations are prevalent. It should be added that the highly reactive state of the female also seems to serve the function of keeping the male aroused and interested in her. Cairns and Scholz (1973) explored a similar mutual feedback process that leads to attacks between male mice. Svare and Gandelman (1973) reported that lactating females did not attack males that had been housed in the females' cages and separated by wire mesh; however, those females did attack strange males. The females in Experiment 2 of this report, which were paired with males, did not attack strange males. Since the females in this study had more extensive contact with
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males, including prepartum contact and environmental conditions, and the dynamics unrestricted interaction, the conflicting re- of social interaction itself. sults are reasonably attributed to methodReference Note ological differences, although strain differences could be important in this regard. D. J., & Cairns, R. B. Early experience Obviously, these studies do not exhaust 1. MacCombie, and social plasticity: Reducing aggression in isothe possible determinants of female aggreslation-reared mice. Paper presented at the meeting sion. The roles of stimulation from the litter of the American Psychological Association, Chicago, September 1975. and of certain stimulus properties of the intruder have been demonstrated by Svare and Gandelman (1973). Data reported by Svare References and Gandelman (1976) imply that the experience of repeated testing across lactation Bronson, F. H., & Desjardins, C. Aggression in adult mice: Modification by neonatal injections of gonadal periods increases and decreases intensity of hormones. Science, 1968,161, 705-706. attacks in a quadratic manner. However, Cairns, R. B. Fighting and punishment from a develthe inclusion of only one cross-sectional opmental perspective. In J. K. Cole & D. D. Jensen (Eds.), Nebraska Symposium on Motivation (Vol. group in the design makes this conclusion 20). Lincoln: University of Nebraska Press, 1973. tentative. Gandelman and Svare (1974) also Cairns, R. B., & Nakelski, J. S. On fighting in mice: explored the hormonal basis of posipartum Ontogenetic and experiential determinants. Journal aggression through various pregnancy terof Comparative and Physiological Psychology, 1971, 74, 354-364. mination procedures. Strain differences implicate genetic characteristics (Scudder, Cairns, R. B., & Scholz, S. D. Fighting in mice: Dyadic escalation and what is learned. Journal of ComKarczmar, & Lockett, 1967). Some strains parative and Physiological Psychology, 1973, 85, of mice exhibit aggression against strange 540-550. males during the prepartum period Crowcroft, P. Mice all over. Chester Springs, Pa.: Dufour Editions, 1966. (Crowcroft, 1966; Noirot et al, 1975), and others do not (Svare & Gandelman, 1976); Edwards, D. A. Early androgen stimulation and aggressive behavior in male and female mice. Physihowever, even within one strain the probaology and Behavior, 1969,4, 333-338. bility of female attack can vary between Fredericson, E. Aggressiveness of female mice. Journal studies, as it has in this laboratory. of Comparative and Physiological Psychology, 1952, 45, 254-257. The conclusion here is that social behavior R. Mice: Postpartum aggression elicted should be considered the expression of a Gandelman, by the presence of an intruder. Hormones and Becontinuous interaction of previous and curhavior, 1972,3, 23-28. rent experiential and biological conditions. Gandelman, R., & Svare, B. Mice: Pregnancy termination, lactation and aggression. Hormones and This point has already been demonstrated Behavior, 1974,5, 397-405. in the maternal behavior of many species, B., & Allee, W. C. Some effects of condiincluding rats (Rosenblatt & Lehrman, 1963; Ginsburg, tioning on social dominance and subordination in Roth & Rosenblatt, 1967), cats (Schneirla, inbred strains of mice. Physiological Zoology, 1942, Rosenblatt, & Tobach, 1963), sheep and 15, 485-506. goats (Hersher, Richmond, & Moore, 1963), Hersher, L., Richmond, J. B., & Moore, A. U. Maternal behavior in sheep and goats. In H. L. Rheingold and rhesus monkeys (Rosenblum & Kauf(Ed.), Maternal behavior in mammals. New York: man, 1968). Wiley, 1963. The data from the two studies presented King, J. A., & Gurney, N. L. Effect of early social experience on adult aggressive behavior in C57BL/10 here have introduced several experiential mice. Journal of Comparative and Physiological variables into the network of determinants Pyschology, 1954, 47, 326-330. of postpartum aggression. It may prove Lagerspetz, K. M. J., & Lage^spetz, K. Y. H. Changes useful, then, to view aggression as a summary in the agressiveness of mice resulting from selective label for social behaviors that have multiple breeding, learning and social isolation. Scandanavian Journal of Psychology, 1971,12, 241-248. controls. Some of the important determiR. B., & Appelbaum, M. I. Bias in the analysis nants are common to both sexes; it has now McCall, of repeated-measures designs: Some alternative been shown that these include familiarity of approaches. Child Development, 1973, 44, 401the test partner, previous test history, social 415..
AGGRESSION IN MICE Moyer, K. E. Kinds of aggression and their physiological basis. Communications in Behavioral Biology, 1968,2,65-87. Noirot, E., Goyens, J., & Buhot, M.-C. Aggressive behavior of pregnant mice toward males. Hormones and Behavior, 1975,6,9-17. Rosenblatt, J. S., & Lehrman, D. S. Maternal behavior of the laboratory rat. In H. L. Rheingold (Ed.), Maternal behavior in mammals. New York: Wiley, 1963. Rosenblum, L. A., & Kaufman, I. C. Variations in infant development and response to maternal loss in monkeys. American Journal of Orthopsychiatry, 1968, 38, 418-426. Roth, L. L., & Rosenblatt, J. S. Changes in self-licking during pregnancy in the rat. Journal of Comparative and Physiological Psychology, 1967, 63, 397400. Schneirla, T. C., Rosenblatt, J. S., & Tobach, E. Maternal behavior in the cat. In H. L. Rheingold (Ed.), Maternal behavior in mammals. New York: Wiley, 1963.
Scott, J. P. Agonistic behavior of mice and rats: A review. American Zoologist, 1966,6, 683-701. Scudder, C. L., Karczmar, A. G., & Lockett, L. Behavioural developmental studies of four genera and several strains of mice. Animal Behaviour, 1967,15, 353-363. St. John, R. D., & Corning, P. A. Maternal aggression in mice. Behavioral Biology, 1973, 9, 635-639. Svare, B., & Gandelman, R. Postpartum aggression in mice: Experiential and environmental factors. Hormones and Behavior, 1973,4, 323-334. Svare, B., & Gandelman, R. A longitudinal analysis of maternal aggression in Rockland-Swiss albino mice. Developmental Psychobiology, 1976, 9, 437-466. Uhrich, J. The social hierarchy in albino mice. Journal of Comparative Psychology/1938,25, 373-413. Vale, J. R.,,Ray, D., & Vale, C. A. The interaction of genotype and exogenous neonatal androgen: Agonistic behavior in female mice. Behavioral Biology, 1972, 7, 321-334.
Received February 15,1978 •
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Experiential Determinants of Postpartum Aggression in Mice James A. Green University of North Carolina at Chapel Hill The objective of this research was to explore the experiential determinants and the social controls of postpartum aggression in mice. In Experiment 1, a group of seven lactating females was tested repeatedly from Day 2 to Day 22 postpartum against male mice; attacks by the females continued through Day 18. Two other groups of seven females tested only once showed diminished attacks against males by Day 14 postpartum. In Experiment 2, eight females were paired with a male for a week prior to parturition; they showed reliably fewer attacks on Day 2 postpartum than a group of nine females that were isolated prior to parturition. All of these results were obtained in a standard 3-min test. A 24-hr test on Day 4 of Experiment 2 revealed that in both groups female attacks dropped to near zero after 30 min. After female attacks declined, males initiated social behavior which occasioned vocalizations by the females. Further, males attacked in 65% of the tests and destroyed the litters of the females in 53% of the tests. The behavior of the male exerted important influences on the structure of extended female-male interactions.
That female and male mice differ in their aggressive behavior is well established. Female mice have not shown the "spontaneous" aggression characteristic of male mice (Ginsburg & Allee, 1942; Uhrich, 1938). Further, certain experiential manipulations, especially social isolation, have been shown to increase attacks by male mice but not by females (Fredericson, 1952). Recent work has also pointed to hormonal differences as basic to behavioral differences in aggression. Neonatally masculinized females have displayed increased levels of attacks as adults (Bronson & Desjardins, 1968; Edwards, 1969;
This research was supported by National Institute of Child Health and Human Development Grant 5 R01 HD 08464-02 to Robert B. Cairns and Grant 2 T01HD 00193-06 to the Carolina Population Center. The author was supported during preparation of the manuscript by a National Science Foundation predoctoral fellowship. Assistance during collection of the data was provided by D. J. MacCombie, and R. B. Cairns assisted throughout the research project. An earlier version of this paper was presented at the meeting of the American Psychological Association, Washington, D.C., September 1976. Requests for reprints should be sent to James A. Green, Department of Psychology, Davie Hall, University of North Carolina, Chapel Hill, North Carolina 27514.
Vale, Ray, & Vale, 1972). In addition, the sex-specific changes associated with pregnancy, parturition, and lactation have been related to increased female attacks during those periods (Gandelman, 1972; Gandelman & Svare, 1974; Noirot, Goyens, & Buhot, 1975). Nonetheless, many gaps remain in our understanding of the social events that elicit and maintain aggressive behavior in female mice. Several different kinds of social experience have been shown to be related to male aggression; these remain unexplored in female mice. Specifically, the effects of (a) repeated testing, (b) social isolation, and (c) immediate social feedback on male attacks have been well documented (see Cairns, 1973, for a review). The aim of the present research was to investigate the role of these factors in the aggression of female mice during the postpartum period. The following studies, then, were addressed to these questions: (a) Does repeated testing prolong the time in the postpartum period during which females will attack? (b) Does social isolation facilitate the establishment of attacks in the postpartum period? (c) Do females stop attacking during extended testing? (d) What role does the test partner play in maintaining
Copyright 1978 by the American Psychological Association, Inc. 0021-9940/78/9206-1179$00.75
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the interaction during this extended testing? General Method The subjects in these studies were virgin females obtained from an inbred strain of ICR mice. They were housed from weaning with littermates of the same sex in standard laboratory cages (28 X 18 X 13 cm). Food and water were available ad lib, and a 12:12 hr light/dark cycle was employed. All test sessions began within 2 to 4 hr after the onset of the dark cycle. Male ICR mice reared under the same conditions were used for mating purposes. They were introduced into the group-rearing cages of the 90-120-day-old females and were removed 14 days later, at which time the females were placed in the appropriate test conditions. The male object animals used in testing were groupreared ICR mice between 90 and 120 days of age. Males were naive with respect to female contacts at the time of first testing. Both subjects and objects were marked at weaning with a permanent dye to permit individual identification. All tests were scored with a stopwatch in a continuous time-sampling procedure. Five-second blocks and a 31-item social behavior code were used for all tests; the scoring procedure has been more fully described elsewhere (Cairns & Nakelski, 1971). The behavior of both animals was recorded sequentially, which resulted in a continuous record of social behavior for the test period. The primary measure of interest for these studies was attack—a behavior ranging from a discrete bite to more vigorous chasing and biting. When necessary because of distributional assumptions, nonparametric analyses were employed in the data analysis. Analyses of repeated-measures designs in both experiments employed the multivariate technique suggested by McCall and Appelbaum (1973). This technique can give both a test for trends in the data and an unbiased analysis of the overall effects. Finally, conditional probability statements were used in Experiment 2 to explicate sequential dependencies in the social behavior of the test animals.
Experiment 1 The purpose of Experiment 1 was to assess the effects of repeated testing on postpartum aggression. Repeated testing has been shown to lower the threshold for subsequent aggressive responding in male mice (Cairns & Scholz, 1973; King & Gurney, 1954; Lagerspetz & Lagerspetz, 1971). Gandelman (1972) reported that lactating females tested for the first time late in the postpartum period show relatively little aggression. Further, Svare and Gandelman (1973,1976) and St. John and Corning (1973) tested females repeatedly, showing that the high levels of
attack displayed initially decline during the postpartum period. However, a systematic comparison of cross-sectional and longitudinal groups is necessary to give a more precise statement of the effect of previous encounters with a male mouse on postpartum attacks. Method Subjects. After mating, 21 females were isolated in the standard laboratory cages. Seven subjects were assigned randomly to each of three groups. One longitudinal group was tested once daily on Days 2, 6,10, 14,18, and 22 postpartum. One cross-sectional group was tested only once on Day 6 postpartum; a second cross-sectional group was tested only on Day 14 postpartum. All tests were conducted in the females' home cages. Procedure. Three-minute dyadic tests were administered on the days dictated by group assignment. The tests consisted of moving the female's cage to a standard test area, removing the wire top containing the water bottle and food hopper, placing the male in the cage and putting a flat Plexiglas top on the cage. The social interaction was scored for 3 min, then the male was removed from the cage. The male mice used for all tests on Days 2,6, and 14 had never been tested previously; the tests on Days 10, 18, and 22 employed the same males, previously tested with a different female.
Results Initial behavior patterns. When males were first introduced into the females' cages, one of three things typically occurred. On Day 2, in a small percentage of the tests (14%), only mutual sniffing by the female of the head and anogenital region was evident. In 43% of the Day 2 tests, the initial mutual investigation became more and more vigorous as the female began to lunge with paws extended toward the head and flank regions of the male. Tail rattling was often seen. Actual biting of the males was the end result of the escalating social interactions, although it occurred with a long latency (M = 83 sec). In the remaining 43% of the tests, there was virtually no mutual social investigation; biting occurred upon initial contact. A similar patterning of the percentages and the types of initial social behavior applied to the cross-sectional group tested on Day 6. A different picture emerged when the second test of the longitudinal group was
AGGRESSION IN MICE
examined. On Day 6, all animals attacked the male without behavioral precursors. Mean latency to attack was 9 sec, which differed reliably from the mean latency of 83 sec for this group on Day 2, £(6) = 2.4, p < .05. Attack frequency. The frequency data indicated that attacks do decline in the postpartum period, after seeming to peak sometime between Day 2 and Day 6. Repeated testing, however, prolonged the period in which attacks toward the male were a high probability behavior (see Figure 1). This was shown statistically in two ways. First, a multivariate analysis of variance confirmed that the initial increase and subsequent decrease in the scores of the longitudinal group were reliable, F(2, 5) = 12.7, p < .01; quadratic trend, F(l, 6) = 6.8, p < .04. Second, a comparison of subjects that were tested only once with those tested repeatedly showed reliable differences by Day 14 postpartum. The difference between the longitudinal group on Day 6 and the Day 6 cross-sectional group was not reliable (Mann-Whitney U = 12, p < .13). However, the difference between the longitudinal group on Day 14 and the Day 14 cross-sectional group was reliable (U = 9, p < .05). There was a reliable difference between the animals tested for the first time on Day 2 and those tested initially on Days 6 and 14. The decline shown in Figure 1 across these three groups was reliable (Kruskal-Wallis H = 6.6, p < .05). Only the difference between Day 2 and Day 14 was significant (U = 8, p < .04). Percentage of animals attacking. The percentage data paralleled the frequency data. The percentages of animals in the longitudinal group that attacked on each of the six tests were 86%, 100%, 100%, 71%, 71%, and 43%. In the cross-sectional group tested on Day 6, 71% attacked, and in the crosssectional group tested on Day 14, 14% attacked. The change over days in the percentage of animals attacking in the longitudinal group was of borderline significance (Cochran's Q(5) = 11, p < .10). In the cross-sectional groups, the difference between Day 2 and Day 14 was reliable by Fisher's exact probability test (p < .05). No
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o—o Longitudinal Group ® Cross-sectional Groups
"0
2
6 10 14 18 DAYS POSTPARTUM
22
Figure 1. Mean attacks by females during a 3-min test (Experiment 1).
other differences between cross-sectional groups or between analogous longitudinal and cross-sectional groups were reliable. Supplemental results. An additional group of 16 females, 90-120 days old, was exposed to males only through a wire mesh screen in a sham mating procedure. These females were then isolated and tested in a regimen identical to that of the females in Experiment 1; that is, 1 wk after the sham mating procedure (which lasted for 2 wk), the females were tested in a 3-min dyadic test. They were tested again 4 days later, and so on, for a total of six tests. None of these females attacked. This replicated the reports in the literature—nonlactating females typically do not attack males. Discussion Experiment 1 suggests that postpartum attacks during a 3-min test are controlled by at least two interacting factors: (a) time since parturition and (b) the number of prior aggression tests against males. Females that had previously been tested on Days 2 and 6 postpartum were more likely to attack males, and to attack males more vigorously, on Day
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14 than were females with no previous tests. Experiment 2 Experiment 1 provided one link between postpartum aggression and male aggression: Repeated testing seemed to facilitate attack behaviors in the same setting at subsequent times. Experiment 2 was designed to assess the effects on postpartum aggression of two other variables known to be important in male aggression. These were isolation from conspecifics prior to testing and social feedback effects within the interchange itself (Cairns, 1973; Cairns & Scholz, 1973). One procedure that has been commonly employed in the postpartum literature is the isolation of pregnant females for about 1 wk prior to parturition. Tests of the effects of lactation on aggression have therefore been confounded with social isolation (Gandelman, 1972; Gandelman & Svare, 1974; Svare & Gandelman, 1973). However, it has been shown that limited exposure to a male during the postpartum period decreases aggression toward that particular male (Svare & Gandelman, 1973). One purpose of the present experiment was to discover what role, if any, prepartum isolation has on postpartum attacks against familiar and unfamiliar males by pairing pregnant females with males prior to parturition. A rather puzzling finding of Experiment 1 was the relative complacency of males when tested against lactating females. Since the males had been quickly removed from a familiar home environment to be placed in a female's home cage, one possible explanation of their behavior would be that they were not adapted to the novel social environment provided by the lactating mother and her pups. If a male's responses changed as he adapted to or settled into the situation, these new responses could affect the ongoing behavioral sequences. Such temporal shifts in patterns of interaction can give important clues to the physiological processes accompanying behavior, in addition to explicating the immediate social controls of behavior. A necessary part of a behavioral analysis is relating known patterns of male-female interaction
in other contexts to the sequences of behaviors established in the prolonged postpartum tests. Unpublished data (1976) from this laboratory have indicated, for instance, that one typical pattern of malefemale interaction in a 10-min test is the male sniffing the anogenital region repeatedly and the female kicking and vocalizing or withdrawing. Often, this leads to arousal of the male to the point of vigorous grooming, mating, or attacking. This pattern was also evident in the sham-mated females reported on in Experiment 1. Such sequences might also occur during extended postpartum tests sometime after the initial attacks of the female, thus providing a behavioral link between male-female social interaction during the postpartum period and during nonparturient states of the female. The test length of Experiment 2 was extended to 24 hr, and test cages were modified in the hope of providing more natural surroundings. This permitted an analysis of postpartum attacks as part of a larger period of social adaptation, and it provided a more adequate test of the brood-defense hypothesis (Moyer, 1968; Scott, 1966). It was thought that enlarging the cages provided the male test object with some space, although still limited, to escape from the female and vice versa. Small nest boxes were added to provide a more natural situation (Crowcroft, 1966) and one in which the females could more adequately protect their litters. Method Subjects. Seventeen gravid females were randomly assigned to two groups of subjects; each group was tested on Days 2 and 4 postpartum. One group of subjects was paired with a male ICR mouse immediately after mating and throughout the remainder of the experiment. The other group of subjects was isolated immediately after mating and for the rest of the study. Procedure. After the 2-wk mating interval, each female in Group I (Isolated, n = 9) was isolated in a large Masonboard cage (35 X 30 X 35 cm), with two partitions dividing the cage into three chambers (22 X 13 X 35 cm; 8 X 35 X 35 cm; 22 X 22 X 35 cm). Each subject in Group P (Paired, n = 8) was paired with a male that had not been used as a breeder. Cage bottoms were covered with sawdust litter and provided with scraps of butcher paper to serve as nesting material. In addition, each cage was provided with a small transparent Plexiglas
AGGRESSION IN MICE nest box (13 X 10 X 6 cm) which had one entrance (3 X 6cm). A standard 3-min dyadic test was given on Day 2. For Group I this involved placing the male test object at the point farthest from the female and scoring 3 min of social interaction, after which the male was removed. In Group P, this test consisted of removal of the resident male for 1 min, introduction of the new male, removal of the male after 3 min, and replacement of the resident male after 2 min. Three minutes of resident male/ lactating female interaction was also scored at this time of reentry of the resident. On Day 4, the resident male was removed for 1 min, the new male was introduced, and continuous observations were made for 1 hr. Three minutes of observation were also scored at the end of Hours 2, 3,4, and 24 of the test. No resident male reintroduction was made in Group P, but 3 min of baseline resident male/ lactating female social interaction was scored prior to the beginning of the Day 4 test.
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This difference was reliable by Fisher's exact probability test (p < .05). In comparing the data of Group I with those from Day 2 of Experiment 1, it appeared as if the cage changes had not appreciably altered the characteristics of postpartum aggression in this strain. Behavior during extended testing. On Day 4, Group I again attacked more frequently than Group P, but only for the first 3 min of the test. In both groups female attacks declined rapidly during the first 30 min of the test. Further, 11 males counterattacked their female partners. In nine of the tests, male attacks were directed at the litters also. When individual pups in the litters were killed as a result of attacks by males, the females and the males usually cannibalized those particular pups. Average levels of female attack are shown in Figure 2; average levels of male attack are shown in Figure 3. These figures represent 3-min by 3-min summaries of the first 30 min of the test with 3-min summaries at the end of Hours 1, 2, 3, 4, and 24 of the test. (Three-minute blocks of behavior were used here only because this has been the standard short-test length used throughout this work.) The initial difference between the two groups, based on a 3-min sample of behavior,
Daily checks of the nesting and sleeping arrangements revealed that 6 of the 9 animals in Group I employed the nest boxes as sites for parturition and lactation, and 7 of 8 Group P females did likewise. At no time during the experiment were the females seen to be aggressive toward the resident males. The animals always slept together, and the males were often seen licking, retrieving, and sleeping on top of the pups in a lactating position. This behavior also characterized both the baseline data from the Day 4 test and the reentry data after the Day 2 test. None of those data is therefore presented. Familiarity of males is clearly an important determinant of feo—o Group I (Isolated) male attacks. Group P (Paired) Attack behavior during the Day 2 test. The 3-min test on Day 2 replicated the behavioral analysis of Experiment 1; all three patterns of female response were evident, although immediate attacks were seen only in Group I. The latency, probability, and frequency data all indicated that animals which were isolated prior to parturition differed significantly from those that were paired. The mean latency to attack in Group P was 171 sec, whereas the mean latency to attack in Group I was 57 sec, £(15) = 3.9, p < .001. Mean attacks were .4 and 6 12 18 24 30 120 240 1440 7.9 for Group P and Group I, respectively, TIME IN 3-MINUTE SAMPLES t (15) = 2.8, p < .01. In addition, for Group P, the percentage of animals attacking on Figure 2. Mean attacks by females during successive Day 2 was 25%, and for Group I it was 77%. 3-min samples (Experiment 2).
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o—o Group I (Isolated) •—• Group P (Paired)
0
6
12 18 24 30 120 240 1440 TIME IN 3-MINUTE SAMPLES
Figure 3. Mean attacks by males during successive 3min samples (Experiment 2).
was reliable, £(15) = 2.6, p < .02. However, by the end of 6 min of interaction, the difference was no longer reliable, £(15) = .79, p < .4. In addition, Figure 2 shows that the low level of female attacks remained stable over the 24-hr period. Individual analyses. Did the females stop attacking because of male counterattacks? The low but consistent levels of male attack shown in Figure 3 suggested that these counterattacks served that function. However, the examination of the data did not bear out this interpretation. The protocols from each test were examined individually: In five tests, female attacks declined without males ever counterattacking; in nine tests, male attacks occurred, but not until after female attacks had already declined. Only one test could support a punishment explanation of the decline in female attacks. Another explanation of the decline might be that the females rapidly habituated to the intruder. This would imply, however, that some "calming down" or lowering of general arousal level took place. Examining the initiations of nonattack social behaviors and the vocalizations were important to this question. The results are shown in Figure 4. Multivariate analyses of variance of each 2 (Group) X 2 (Time) design for the four behaviors of male initiate, male vocalize, female initiate, and female vocalize yielded the following reliable results: a main effect of group for male initiate, F(l, 15) = 4.8, p < .04; a main effect of time for male vocalize, F(l, 15) = 21.1, p < .001; and main effects of time for female initiate and vocalize, F(l, 15) = 51.7, p < .001 and F(l, 15) = 9.7, p < .001,
respectively. Thus, with reference to Figure 4, the only group main effect was for male initiate, in which the mean in Group P was 3.9 compared with 1.9 for Group I. There were no Group X Time interactions for any measure, and each time main effect was reliable except for male initiate (p < .08). The decline in male vocalizations indicates simply that as males stopped being attacked, they also stopped vocalizing. By the end of 30 min, male vocalizations and female attacks were seen in only 3 of the 17 test dyads. An analysis of conditional probabilities supported the relation of vocalization to attack. Male vocalizations were closely related to female attacks; the probabilities of male vocalizations, given female attacks, were quite high in the first 3 min of the test. In Group P, the median conditional probability was .4 (range of .0-1.0); in Group I, the median was .5 (range of .0-.9). However, the conditional probability for each dyad during Minutes 28-30 was .0, which reflects both the decrease in female attacks and the coupling of male vocalizations to female attacks. The rise in male initiations and female vocalizations (Figure 4) indicates two things; first, as males stopped vocalizing and females stopped attacking, males began to initiate social behaviors—sniffing, nosing, or grooming the female. Second, the drop in female attacks did not indicate a "calming down" of the female. Rather, females were
12 18 24 30 120 TIME IN 3-MINUTE SAMPLES
Figure 4. Mean rates of male and female vocalizations and nonattack social initiations during successive 3-min samples, collapsed across treatment groups (Experiment 2).
AGGRESSION IN MICE
indicating high arousal by vocalizing. Thirteen of 17 females were still vocalizing at the end of 30 min; however, only 4 were still vocalizing after 24 hr, which indicates that the habituation process took longer to occur than the decline in female attacks would indicate. Again, conditional probabilities supported this interpretation of the relationship between male initiations and female vocalizations. Whereas males stopped vocalizing because they were no longer attacked, females began to vocalize after mild social stimulation. The probability of a female vocalization, given a male initiation (sniff, nose, or groom), was quite high at the end of 30 min of testing. In Group P, the median was .3 (range of .0-1.0); in Group 2, the median was .75 (range of .0-1.0). The same conditional probabilities were .0 for all but one test dyad during Minutes 1-3, despite the fact that 9 of 17 males initiated an average of 2.4 times during that period. Discussion Isolation from male mice for 1 wk prior to parturition significantly increased both the probability and frequency of postpartum attacks on an unfamiliar male during a 3-min test. Females stopped attacking quickly during the extended test on Day 4. In 11 of 17 tests, males counterattacked, and in 9 tests male attacks were also directed at the litters of the females. As females stopped attacking, males began initiating nonattack social behavior, and a consistent pattern of male initiation/female vocalization developed. The drop in female attacks was permanent, and the pattern of reactivity to male social initiations showed evidence of having diminished by the end of 24 hr of testing. General Discussion These studies demonstrate that postpartum aggression in female mice has many features in common with aggression in male mice. These include the sensitivity of aggression to (a) previous test experience (prior tests for aggression during the postpartum period increase the probability, speed, and frequency of later attacks against
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males), (b) the structure of the social environment prior to actual testing (females paired with a male prior to and after parturition do not attack those males, and they are less likely than isolated females to attack an unfamiliar male), and (c) the characteristics of the test experience itself, particularly the length of time the test is permitted to continue (female attacks on males declined rapidly during the first 30 min of a 24-hr test). The value of the behavioral analysis presented here is twofold. First, careful reporting of the dominant patterns of nonattack social behavior in aggressive encounters is essential because descriptive data provide one basis for future hypotheses and studies. Second, a dyadic behavioral analysis provides the first clue in untangling the interaction between endogenous and immediate social controls of social behavior. Social feedback during the ongoing social interaction has been shown to play an important role in the establishment and maintenance of attacks in males (Cairns & Scholz, 1973; MacCombie & Cairns, Note 1). With reference to these data, there were no obvious behaviors of the male which caused the decline in female attacks. That decline, therefore, is most reasonably attributed to a nonbehavioral process—motor fatigue or endocrine change being two possibilities. However, the data on female vocalizations help rule out declining arousal levels as an explanation while also showing that the male plays an active role in the ongoing interaction, keeping the female in a state in which vocalizations are prevalent. It should be added that the highly reactive state of the female also seems to serve the function of keeping the male aroused and interested in her. Cairns and Scholz (1973) explored a similar mutual feedback process that leads to attacks between male mice. Svare and Gandelman (1973) reported that lactating females did not attack males that had been housed in the females' cages and separated by wire mesh; however, those females did attack strange males. The females in Experiment 2 of this report, which were paired with males, did not attack strange males. Since the females in this study had more extensive contact with
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males, including prepartum contact and environmental conditions, and the dynamics unrestricted interaction, the conflicting re- of social interaction itself. sults are reasonably attributed to methodReference Note ological differences, although strain differences could be important in this regard. D. J., & Cairns, R. B. Early experience Obviously, these studies do not exhaust 1. MacCombie, and social plasticity: Reducing aggression in isothe possible determinants of female aggreslation-reared mice. Paper presented at the meeting sion. The roles of stimulation from the litter of the American Psychological Association, Chicago, September 1975. and of certain stimulus properties of the intruder have been demonstrated by Svare and Gandelman (1973). Data reported by Svare References and Gandelman (1976) imply that the experience of repeated testing across lactation Bronson, F. H., & Desjardins, C. Aggression in adult mice: Modification by neonatal injections of gonadal periods increases and decreases intensity of hormones. Science, 1968,161, 705-706. attacks in a quadratic manner. However, Cairns, R. B. Fighting and punishment from a develthe inclusion of only one cross-sectional opmental perspective. In J. K. Cole & D. D. Jensen (Eds.), Nebraska Symposium on Motivation (Vol. group in the design makes this conclusion 20). Lincoln: University of Nebraska Press, 1973. tentative. Gandelman and Svare (1974) also Cairns, R. B., & Nakelski, J. S. On fighting in mice: explored the hormonal basis of posipartum Ontogenetic and experiential determinants. Journal aggression through various pregnancy terof Comparative and Physiological Psychology, 1971, 74, 354-364. mination procedures. Strain differences implicate genetic characteristics (Scudder, Cairns, R. B., & Scholz, S. D. Fighting in mice: Dyadic escalation and what is learned. Journal of ComKarczmar, & Lockett, 1967). Some strains parative and Physiological Psychology, 1973, 85, of mice exhibit aggression against strange 540-550. males during the prepartum period Crowcroft, P. Mice all over. Chester Springs, Pa.: Dufour Editions, 1966. (Crowcroft, 1966; Noirot et al, 1975), and others do not (Svare & Gandelman, 1976); Edwards, D. A. Early androgen stimulation and aggressive behavior in male and female mice. Physihowever, even within one strain the probaology and Behavior, 1969,4, 333-338. bility of female attack can vary between Fredericson, E. Aggressiveness of female mice. Journal studies, as it has in this laboratory. of Comparative and Physiological Psychology, 1952, 45, 254-257. The conclusion here is that social behavior R. Mice: Postpartum aggression elicted should be considered the expression of a Gandelman, by the presence of an intruder. Hormones and Becontinuous interaction of previous and curhavior, 1972,3, 23-28. rent experiential and biological conditions. Gandelman, R., & Svare, B. Mice: Pregnancy termination, lactation and aggression. Hormones and This point has already been demonstrated Behavior, 1974,5, 397-405. in the maternal behavior of many species, B., & Allee, W. C. Some effects of condiincluding rats (Rosenblatt & Lehrman, 1963; Ginsburg, tioning on social dominance and subordination in Roth & Rosenblatt, 1967), cats (Schneirla, inbred strains of mice. Physiological Zoology, 1942, Rosenblatt, & Tobach, 1963), sheep and 15, 485-506. goats (Hersher, Richmond, & Moore, 1963), Hersher, L., Richmond, J. B., & Moore, A. U. Maternal behavior in sheep and goats. In H. L. Rheingold and rhesus monkeys (Rosenblum & Kauf(Ed.), Maternal behavior in mammals. New York: man, 1968). Wiley, 1963. The data from the two studies presented King, J. A., & Gurney, N. L. Effect of early social experience on adult aggressive behavior in C57BL/10 here have introduced several experiential mice. Journal of Comparative and Physiological variables into the network of determinants Pyschology, 1954, 47, 326-330. of postpartum aggression. It may prove Lagerspetz, K. M. J., & Lage^spetz, K. Y. H. Changes useful, then, to view aggression as a summary in the agressiveness of mice resulting from selective label for social behaviors that have multiple breeding, learning and social isolation. Scandanavian Journal of Psychology, 1971,12, 241-248. controls. Some of the important determiR. B., & Appelbaum, M. I. Bias in the analysis nants are common to both sexes; it has now McCall, of repeated-measures designs: Some alternative been shown that these include familiarity of approaches. Child Development, 1973, 44, 401the test partner, previous test history, social 415..
AGGRESSION IN MICE Moyer, K. E. Kinds of aggression and their physiological basis. Communications in Behavioral Biology, 1968,2,65-87. Noirot, E., Goyens, J., & Buhot, M.-C. Aggressive behavior of pregnant mice toward males. Hormones and Behavior, 1975,6,9-17. Rosenblatt, J. S., & Lehrman, D. S. Maternal behavior of the laboratory rat. In H. L. Rheingold (Ed.), Maternal behavior in mammals. New York: Wiley, 1963. Rosenblum, L. A., & Kaufman, I. C. Variations in infant development and response to maternal loss in monkeys. American Journal of Orthopsychiatry, 1968, 38, 418-426. Roth, L. L., & Rosenblatt, J. S. Changes in self-licking during pregnancy in the rat. Journal of Comparative and Physiological Psychology, 1967, 63, 397400. Schneirla, T. C., Rosenblatt, J. S., & Tobach, E. Maternal behavior in the cat. In H. L. Rheingold (Ed.), Maternal behavior in mammals. New York: Wiley, 1963.
Scott, J. P. Agonistic behavior of mice and rats: A review. American Zoologist, 1966,6, 683-701. Scudder, C. L., Karczmar, A. G., & Lockett, L. Behavioural developmental studies of four genera and several strains of mice. Animal Behaviour, 1967,15, 353-363. St. John, R. D., & Corning, P. A. Maternal aggression in mice. Behavioral Biology, 1973, 9, 635-639. Svare, B., & Gandelman, R. Postpartum aggression in mice: Experiential and environmental factors. Hormones and Behavior, 1973,4, 323-334. Svare, B., & Gandelman, R. A longitudinal analysis of maternal aggression in Rockland-Swiss albino mice. Developmental Psychobiology, 1976, 9, 437-466. Uhrich, J. The social hierarchy in albino mice. Journal of Comparative Psychology/1938,25, 373-413. Vale, J. R.,,Ray, D., & Vale, C. A. The interaction of genotype and exogenous neonatal androgen: Agonistic behavior in female mice. Behavioral Biology, 1972, 7, 321-334.
Received February 15,1978 •
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