Maternal aggression in mice and rats towards male and female conspecifics

Although postpartum aggression is primarily studied in laboratory mice and rats, it is unclear how the two species compare in terms of the factors associated with peak levels of aggressive behavior. Using the same experimental protocol, we assessed the relative effect of intruder sex and time since parturition on the frequency of maternal aggression in Long-Evans rats and CFW mice. Females were studied for 2 consecutive cycles of pregnancy and lactation. During the first lactation, aggression was tested 2 times per week for 3 weeks in order to select animals that attacked at least once. During the second lactation, both pup care and aggressive behavior were assessed in detail. Testing occurred twice in each lactation week, with postpartum days 1–7, 8–14, and 15–21 considered weeks 1, 2, and 3, respectively. Maternal behavior towards 3 pups was observed for 5 minutes, followed by a confrontation with an intruder. Lactating females encountered female intruders once per week, and male intruders in the alternate weekly test. The same behaviors were measured in the 2 species, except for the tail rattle exhibited by mice and the aggressive posture shown by rats. Lactating rats and mice show similar decreases in pup care behavior as lactation progresses in time; yet the factors associated with peak levels of aggression differ between species. In Long-Evans rats, female intruders receive more attacks, threats, and aggressive postures than males. Frequency of attack bite and sideways threat declines in each passing week of lactation. Lactating mice are more aggressive toward male intruders throughout the lactation period. Mice still attack and threaten during the third week of lactation, but less often in comparison to the first week. Therefore, peak levels of aggression vary in mice and rats both as a function of intruder sex and lactation week.     

Offensive and defensive bite-target topographies in attacks by lactating rats

The attacks by resident lactating Wistar rats on sexually naive conspecifics of both sexes were examined. Male and female intruders were equally attacked in terms of frequency and number of bites, but the topographies of biting seen in these encounters were different. Similarly to male-male agonistic interactions, females were attacked in a fashion which avoided bites to the head and snout (“offensive” attack), whereas males were frequently bitten on such vulnerable regions (“defensive” attack). This dichotomy in bite pattern suggests that different motivations and functions underlay maternal aggression in these situations. The defensive attack on males may be a deterrent to infanticide since only male intruders counterattack lactating females and kill their pups. The attack on females may be concerned with resource competition.     

Rank order in pairs of communally nursing female mice (Mus musculus domesticus) and Maternal Aggression Towards Conspecific Intruders of Differing Sex

This study examined social behavior between pairs of unfamiliar lactating females, with litters of the same age, at different periods after parturition (3, 7, and 17 days). Tests were generally followed by the formation of communal rearing nests, and subsequent maternal attack on intruders of differing sex was assessed. In all three intervals lactating females showed ritualized attack with formation of clear dominance-subordination relationships before combining litters into communal nests. The dominant females in 90% of cases started to retrieve alien pups into their nests. Agonistic behavior and communal nest formation were most rapid when pups were around 3 days old. Maternal attack on conspecific intruders was mainly displayed by the dominant lactating females. Male and female intruders were equally attacked (in terms of frequency and intensity of attack), but there was less such aggression when pups were around 17 days of age. Nevertheless the topography of biting attack employed against female and male conspecific intruders was different. Females were attacked using a strategy avoiding bites to the head and ventral surface (indicative of “offensive” behavior) whereas males were severely bitten on vulnerable body regions (indicative of “defensive” behavior).     

Different patterns of biting attack employed by lactating female mice (Mus domesticus) in encounters with male and female conspecific intruders

Attacks by resident lactating female mice were examined in a variety of situations. Relatively few attack bites to vulnerable body regions were seen when pairs of unfamiliar lactating females fought, establishing social status prior to communal nesting. Sexually naive male and female intruders were equally prone to attack by lactating females, but patterns of bite attack generated by them were very different; males received the more damaging attacks. More signs of "fear" were seen in the lactating females' responses to male rather than female intruders. Varied motivations may underlie attacks by lactating females directed to conspecific intruders. Defensive patterns of biting by lactating females are more consistently directed towards males, intruders that are more likely to harm or destroy the litter. Although attacks by females rarely thwarted infanticide by male intruders, the behavior may acutely protect parental investment.     

The decline of aggressiveness in male mice during group caging as determined by punishment delivered by the cage mates

Group-housed rodents are generally less aggressive than isolated counterparts. The present study examined the role of defeat by cage mates as a reason for this decline in aggressiveness. In Experiment I, highly aggressive isolated male mice were introduced into aggressive or nonaggressive resident groups. The intruder's level of aggressiveness directed toward a group-housed standard opponent declined more rapidly after daily exposure to the aggressive than to the nonaggressive groups. Intruders in the aggressive groups received more attacks from their cage mates, and delivered fewer attacks to them than did the intruders in the nonaggressive groups. In Experiment II, the intruders lived for seven days in small wire net cages in the middle of the group cages. Their level of aggressiveness toward standard opponents decreased little during the preexposure but after being put freely into the groups, their aggressiveness declined to a minimal level within a day. Experiment III showed that when the wire net protection in the middle of the cage was installed after the group caging experience, the aggressiveness of the intruders did not return to the isolation level as effectively as it did in isolation. This is explained by the aggression-inhibiting content that the cues from the cage mates have acquired during group caging. The decline of aggressiveness in male mice during group caging is determined by punishment delivered by the cage mates.     

Does fear modulate defensive and offensive types of maternal attack in mice?

Swiss CD‐1 lactating mice show a different pattern of attack toward intruders of differing sex, displaying defensive attack against the male (bites on the head and ventrum associated with fear) and offensive attack against the female (bites on the back and flanks with no elicitation of fear). This dichotomy may reflect diverse functions of maternal aggression: the attack toward males (the more infanticidal gender in laboratory strains) has been interpreted as a counterstrategy to infanticide, whereas the attack toward females may serve to establish a social hierarchy or to space rivals of the same sex. In terms of proximal mechanisms, fear may be a key factor involved in the modulation of the different patterns of attack. In Experiment 1 we compared the pattern of attack of lactating females in Swiss CD‐1 and Wild mice toward male and female intruders in relation to fear components of behavior of the attacking dams. Results showed that in Swiss mice, male intruders were attacked with a defensive type of attack accompanied by high levels of fear, whereas female intruders did not elicit fear in the attacking animal but were attacked with an offensive pattern. In Wild mice, both types of intruders were attacked with a defensive pattern; notwithstanding, fear was evident only toward male intruders. This suggests that fear is not totally responsible for the expression of the defensive type of attack. To test the hypothesis that defensive attack toward male and female intruders may be related to the infanticidal potential of the intruder, Experiment 2 examined levels of infanticide in both male and female Swiss CD‐1 and Wild mice. Swiss female mice showed virtually no infanticidal behavior, whereas Swiss males and both sexes of Wild mice showed similarly high levels of infanticide (55%–75%). From a game theory perspective, the defensive pattern of maternal attack toward female intruders in Wild mice is discussed as “extreme” defense of a high value resource and thus, functionally, a competitive form of aggression. Aggr. Behav. 26:193–203, 2000. © 2000 Wiley‐Liss, Inc.     

Responses of dominant and subordinate male rats to the odors of male and female conspecifics

The resident-intruder paradigm was used to examine the effects of social dominance and individual recognition on odor preferences and urine-marking in male rats. Resident males were significantly more aggressive than intruders and spent more time investigating the odors of familiar intruders. Resident males urine-marked most over the odors of females and familiar intruders while intruders marked least over the odor of the familiar resident. Intruders did not avoid investigating nor marking over the odors of familiar resident males or other conspecifics. These results suggest that individual odors of male rats may be more salient than a general odor of dominance, and that the dominant males increase their investigation and marking over the odors of familiar subordinates but not unfamiliar subordinates. The importance of olfactory learning during aggressive interactions is discussed.     

Sex differences in aggressive behaviour in various strains of mice

Two nonalbino inbred (C57 BL/6 and C3H/He) and one albino strain (Swiss) of mice were compared for female aggression toward intruders: 1 in period of lactation, 2 in nonlactating state and (3) in nonlactating state but previously rubbed with urine of lactating females; and for male aggression toward familiar or unfamiliar opponents. The results showed that resident females of the C57 and Swiss strain vigorously attack lactating intruders introduced into their cages. This effect was mediated by urinary cues emitted by the latter mice. It was also shown that Swiss residents displayed aggression towards nonlactating females, irrespective of their strain. Groups of C57 residents reacted most aggressively towards Swiss females, less aggressively towards C3H intruders, but did not show any aggression towards their own nonlactating conspecifics. In contrast, none of the C3H resident female groups displayed aggression towards intruding females of any category or strain. The results also showed that the males of the three strains displayed little (Swiss and C3H) or no aggression (C57) towards familiar opponents, whereas they directed increased aggressive responses towards unfamiliar ones. Comparisons among the three strains of mice revealed that Swiss males were the most aggressive in either situation. On the other hand, the finding that C3H males showed aggressive responses suggested that male and female aggression are, in this strain, under separate genetic or hormonal control.     

Naloxone differentially alters parental aggression by female mice towards conspecific intruders of differing sex

Lactating mice respond differently to male and female conspecific intruders, displaying defensive attack towards the former and offensive attack towards the latter. Two studies are reported in which the effects of naloxone on this differential response pattern were assessed. In the first study, lactating residents were pretreated with saline or naloxone (0.5, 2.5 mg/kg) and consecutively confronted with intruders of differing sex. Results suggested that attack (offensive) against female conspecifics is more sensitive to the inhibitory effects of opiate-receptor blockade than attack (defensive) on males. This conclusion was strengthened in a follow-up study, in which independent groups of lactating residents were used to further examine the effects of naloxone (0.5 mg/kg) on response to male and female intrusion. Analysis indicated that this low dose of naloxone significantly inhibited attack on female, but not on male, intruders. Indeed, in response to male, but not to female, intrusion, naloxone-treated residents showed a significant increase in fear-related behaviour. Findings are discussed in relation to the motivational differences in the response of lactating mice to intruders of differing sex and to possible mechanisms underlying the reported differential effects of opiate-receptor blockade.     

Analysis of ultrasonic vocalizations emitted by residents during aggressive encounters among rats (Rattus norvegicus)

This investigation was concerned with the extent to which aggressive resident rats emit 40-70-kHz vocalizations and the effect of these signals on intruders. In Experiment 1, deafened and intact intruder males were given two encounters with resident animals. Deafened intruders engaged in a higher duration of immobile or freezing postures than intact animals. Experiment 2 indicated that the augmentation of freezing found among deafened intruders was not due to an inability to detect ultrasounds made by residents since intruders encountering devocalized resident males showed no reliable differences in specific motor patterns from intruders paired with intact residents. The results further demonstrated that 40-70-kHz vocalizations are produced almost entirely by intruding animals since there were no significant changes in occurrence of these calls when resident males were devocalized. Under the constraints of the testing procedures employed, the role of ultrasonic communication during the initial formation of agonistic relations could not be determined experimentally.     

Maternal aggression in rats: Changes over pregnancy and lactation in a sprague-dawley strain

Maternal aggression in a Sprague-Dawley strain of laboratory rat (Charles River CD) was explored from Day 1 after mating on Day 0 through Day 24 of lactation (L0-L24). Aggression toward unfamiliar male “intruders” during 10-min tests was low among nonpregnant, nonlactating females and during the first 10 days of gestation. Frequency of attack on intruders increased moderately but significantly by Gestation Day 16 (G16; Experiment 1) or G21 (Experiment 2), a prepartum phenomenon not previously reported in laboratory rats. Levels of aggression were highest, however, during the first 9 days of lactation, when attacks averaged more than 6 per 10-min session. Attacks declined sharply in frequency after L14 and by L24 did not exceed levels observed among nonpregnant females. Experiment 3 examined the importance of the test site (home cage with nest and pups, if any, vs unfamiliar cage without nest or pups) to agonistic behavior associated with pregnancy and lactation. Late pregnant females tested in a novel cage were not aggressive; however, females tested shortly after delivering their pups were highly aggressive, averaging over four attacks per 5-min session. In novel cage tests frequency of attack remained high through L4 but declined significantly by L7. These data are consistent with the hypothesis that maternal aggression at its onset is primarily under hormonal control, but becomes increasingly dependent upon external factors, presumably pup stimulation, during the postpartum period.     

The effects of urine on aggressive responses by male golden hamsters

Twenty adult male golden hamsters were isolated into individual cages for a period of six weeks, at the end of which time they had introduced into their home cages, on three occasions, a castrated male intruder. On each occasion the castrated intruder was daubed on the anogenital region with urine from one of three sources: (1) intact females, (2) other castrated males, and (3) intact males. Urine from a different source was applied to the castrated intruder on each of the three tests. Resident males consistently showed more aggression, sniffing, and following and less defensive behavior than the intruders. However, aggression by the resident males showed a significant variance over the three urine treatments given to the intruder. It is concluded that like male mouse urine, male hamster urine contains attack-provoking cues, but that unlike that of the mouse, female urine does not appear to be attack-inhibiting in this species.     

Genotype and environment in the social interactions of wild and domestic “Norway” rats

Wild rats, Rattus norvegicus, (a) trapped as adults or (b) of the second generation in captivity (lab-wild), and domestic rats of two strains, were studied for 28 days in artificial colonies in large cages with attached nest boxes. Controls were kept in mated pairs in small cages. Each colony consisted of six males and six females. The interactions of the males in six colonies of trapped rats were highly “stressful;” 61% died; and most of the survivors lost weight and had greatly enlarged adrenals. In each colony, however, there was a male (an alpha) that gained in weight and spent much time, during the dark hours, in the open on the floor of the cage; and in three colonies there were also other males (“betas”) that gained in weight. The adrenals of alphas and betas weighed about the same as those of the controls. In one of the 12 colonies of domestic rats one male behaved like a wild male; but in the other colonies the males gained in body weight and their adrenal weights resembled those of the controls. In three colonies of lab-wild rats 22% of the males died, but there was no evidence of males of different status. The findings confirm that the “agonistic” behavior of domestic rats is usually much attenuated in comparison with that of the wild type; a number of methodologic implications are discussed.     

Social dominance and individual aggressiveness

Male rats exhibiting high, moderate, or low levels of offensive aggressive behavior in interactions with intruders in their home cage were grouped in mixed-sex colonies with 1 male of each aggression-level group in each colony. Agonistic interactions measured 1, 2, 3, 7, 14, 21, and 22 days after colony formation indicated that highly aggressive males on pretests continued to be more aggressive, becoming the dominant colony male in five of seven colonies and attacking intruders more often than less aggressive males. In the two remaining colonies the moderately aggressive male became dominant. This relationship, which was consistent over a number of indices, including offensive and defensive behaviors, and wound counts and wound sites, was seen even when a substantial weight differential favored the less aggressive animal. Dominance relationships were rapidly established and within-group fighting declined significantly over the 21-day test period. Pretest offensive levels also influenced the behavior of subordinates, with high or moderately aggressive subordinates showing more defense in interactions with dominants and receiving more wounds than did low-aggression subordinates. Dominant males also showed more defense in interacting with those subordinates which had been more aggressive during pretests. This pattern of results suggests that aggression level of the subordinate as well as the dominant may be an important factor determining the intensity of agonistic interactions in male rats.     

Effects of novel odors on intermale attack behavior in mice

Offensive, defensive, and nonagonistic social behaviors of resident male mice toward unfamiliar intruders were examined during exposure to the novel odors of chocolate or sheep's wool. Both novel odors reduced lateral attacks and boxing when compared to familiar sawdust odor. Chocolate, but not sheep's wool, also reliably increased flight behavior by residents. Neither social behaviors nor self-grooming were affected by these odors. The novel odors had no effect upon, or actually decreased, the defensive responses of intruders towards residents. The equivalent effectiveness of both predator and nonpredator odors in elevating risk assessment and suppressing attack during firsttime exposure, and the decreased potency of cat odors following repeated exposure, suggests that novelty contributes to the enhanced defensiveness seen among subjects during initial exposure to predator odors. © 1995 Wiley-Liss, Inc.     

Maternal aggression in mice: Protection of young is a by-product of attacks at the home site

Lactating female mice attacked male intruders in their home cages but showed little attack behavior either in novel cages or in cages with which they had been familiarized. Presence or absence of young did not determine the occurrence of maternal aggression, whereas attacks on the young by the intruder decreased maternal aggression and increased cannibalism of pups by the dams. Apparently, if the function of maternal aggression in mice is protection of the young, such protection occurs because the pups are in a place where attacks are likely to occur and not because the dam “defends” the young.     

Ultrasounds produced by rats accompany decreases in intraspecific fighting

Male intruder rats were placed individually into the cage of an established resident on 2 occasions separated by a 7–8 day interval. Residents readily attacked intruders and both animals lost weight during the first encounter. In contrast, no serious fighting occurred on the second encounter, and both intruders and residents maintained their body weight during the 24-hr test. Observation of the intruder's behavior during the first 30 min of each encounter indicated that defensive-submissive postures represent a response to an attack that only temporarily inhibits aggression whereas the emission of 22 kHz calls by the intruder is associated with a relatively permanent decrease in the resident animal's aggressive response.     

On the dual nature of maternal aggression in rats

Presentation of a natural predator, a cat, was used to differentiate elements of maternal attack by female rats on a male intruder. Following exposure (without direct physical contact) of post-partum females to a cat or to a toy stuffed cat (control group), the females were replaced in their home cages and presented with a male intruder rat. Cat exposure reliably decreased lateral attack to the intruder, as well as locomotion, but had no effect on either jump attack or an upright defensive posture (boxing). Since predator exposure produces a somewhat durable increase in defense, along with inhibition of nondefensive behavior, these results suggest that maternal aggression represents a mixture of offensive, usually related to competition, and defensive (protective) behaviors. The results indicate that maternal aggression, as a parental care behavior, appears to be at least partially resistant to fear. © 1996 Wiley-Liss, Inc.     

Maternal aggression toward infanticidal males of different social status in wild house mice (Mus musculus domesticus)

Maternal aggression was examined in wild female mice (Mus musculus domesticus) derived from animals trapped in Alberta, Canada. Lactating females were tested for their behavior toward intruder males during the time of postpartum estrus while housed in a two-cage apparatus containing a defensible nest area. Prior to being used as intruders, sexually naive males were screened for their behavior toward a newborn pup (83% exhibited infanticide). Only infanticidal males were then housed in pairs and allowed to establish a dominance hierarchy. Dominance status was further verified by a urine marking test. The dominant and subordinate infanticidal males were then placed into a lactating female's cage and observed for 1 hr. The test was terminated immediately when a male began to attack the pups. Lactating females attacked the males in both groups, but subordinate males received more intense attacks than dominant males. Dominant males elicited significantly more fear/defense behavior than subordinate intruders. All of the dominant males and only one submissive male attacked the pups. Females were thus successful in blocking infanticide only by infanticidal subordinate males. Since females do not persist in attacking males with high fighting ability, one function of maternal aggression could be to assess the fighting, and resource holding, potential of a future mate. © 1994 Wiley-Liss, Inc.     

Aggression in domesticated rats reared in a burrow-digging environment

Male and female rats were raised individually in either large boxes filled with soil (burrow environment) or laboratory cages of comparable size (cage environment). In a test of intruder-elicited aggression, intruders exposed to burrow-environment residents lost more body weight, were more likely to have empty stomachs, and received more wounds during a 24 hour aggression test. The results indicate that the physical environment during the period from weaning to maturity is an important determinant of aggression intensity in adult rats.