Effects of cohabitation with another female on aggressive behaviour in pregnant mice

Pregnant, nonpregnant (but mated) and virgin females were individually housed or lived with a pregnant or nonpregnant cagemate. They were subjected to a series of successive daily encounters with a male intruder, the cagemate being excluded. The most aggressive subjects were pregnant females living with a pregnant cagemate. Isolated pregnant females were as aggressive as pregnant females with a nonpregnant cagemate. Nonpregnant and virgin females were the least aggressive. Nevertheless nonpregnant subjects living with a pregnant cagemate generated higher aggressive scores than nonpregnant females living alone. The way in which a pregnant cagemate influences the aggressive behaviour of another pregnant or nonpregnant female is discussed.     

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.     

Anxiety and maternal aggression in house mice (Mus musculus): a look at interindividual variability

The hypotheses were tested that mouse motherhood is accompanied by decreased reactivity to aversive stimuli and that female anxiety is inversely related to the probability of displaying intense forms of postpartum aggression. Outbred Swiss female mice were tested for anxiety in a light/dark choice test when virgin, pregnant, or lactating, and then tested for maternal aggression (5-min exposure to a male intruder) on postpartum Day 7. Anxiety declined in pregnant and lactating females when compared with virgin animals. Furthermore, females who displayed higher scores of postpartum fighting were less anxious in the previous test regardless of reproductive stage. Part of interindividual variability in postpartum aggression might thus be related to differences in the extent to which individuals perceive and react to anxiogenic situations. In addition, the higher emotionality characterizing the C57BL/6 and DBA/2 inbred strains may be responsible for the lack of a clear-cut exhibition of maternal aggression in these two strains.     

The potential effects of protected nests and cage complexity on maternal aggression in house mice

I studied the behavior of nursing house mice (Mus musculus) in captivity and used a two-by-two factorial design to test the hypothesis that the combination of a protected nest along with a chance for the intruders to retreat would improve the ability of resident females to defend their litters from infanticidal males. A chance for the intruder to retreat was manipulated by testing the resident females in either a single- or a two-compartment cage. The effect of a protected nest was examined by providing females with a nest box having a narrow entrance. During each test, an infanticidal adult male was introduced into the cage of a resident female and her pups. I observed that neither the presence of a protected nest nor the chance for the intruders to retreat to a different compartment, or a combination of the two, increased the ability of a female to defend her litter against an intruder male. Moreover, neither of these two factors influenced the overall behavior of the resident females. I obtained similar results after using data from previous studies to examine the influence of both of these factors on the efficiency of maternal aggression. Overall, these two approaches showed that females are often unable to prevent intruders from committing infanticide. I discuss the validity of the hypothesis that maternal aggression evolved as a mechanism to protect offspring from infanticide. Aggr. Behav. 24:385–396, 1998. © 1998 Wiley-Liss, Inc.     

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.     

Attack by female mice on “Strangers”

In this study the aggressive responses directed by small groups of female mice towards virgin, pregnant, and lactating female strangers, which were individually introduced into their cages, were compared. The results obtained show that, except when lactating, pregnant females are neither attacked much more often nor any more severely than virgin mice. It is suggested that only the state of lactation favors the production of stimuli (olfactory) which release attack by female mice.     

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.     

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.     

Attack priming and satiation in female golden hamsters: Tests of some alternatives to the aggression arousal interpretation

“Priming” a female hamster by allowing it a single attack on an intruder placed into its home cage transiently decreases the latency and increases the probability of attack on a second trial. Although we have previously argued that this priming effect reflects an increase in aggressive arousal, an alternative interpretation is that the fear elicited by placing a foreign object into the subject's home cage is reduced when it happens again on the second trial. Another interpretation is that priming is an effect of intruder novelty, i.e., the subject perceives a difference between the first and second intruders which causes it to attack the second more quickly. Experiment 1 compared the standard two trial paradigm with different intruders to trials in which (1) the first intruder was withdrawn and used again in the second trial, and (2) the intruder remained in the cage following the first attack. All intruders were pretreated with the analgesic-sedative methotrimeprazine to reduce the variability of their behavior. Neither hypothesis tested in Experiment 1 was supported, strengthening the interpretation of attack priming as a manipulation that affects primarily internal motivational mechanisms specific to aggression. Allowing a hamster to carry out a protracted series of attacks produces a “satiation” effect that is the reverse of priming, i.e., the latency of a subsequent attack is increased and its probability reduced. It is possible that the attack satiation observed in our earlier studies was not the result of processes internal to the subject, but could have been due to habituation to a particular intruder or to certain stimuli emitted by it during the protracted interaction. In Experiment 2 subjects were given three sessions of 10 successive trials using either 1 intruder presented repeatedly, 2 intruders presented alternately, or 10 different intruders presented once each. No difference among conditions was found in this study either suggesting that subject's aggressive behavior is insensitive to whatever changes may occur in intruders' behavior or other stimulus characteristics when they have been treated with methotrimeprazine. The lack of differences among test conditions in both experiments is most likely due to the efficacy of the drug in “standardizing” intruder behavior. Experiment 2 also revealed an interesting difference in two measures of attack latency. The time elapsing between intruder presentation and attack, i.e., the standard measure of latency, decreased from the first to the fourth trail; it then increased steadily over the remaining trials. The cumulative time that the subject remained in contact with the intruder prior to attack, a measure more indicative of attention to the intruder, dropped to an asymptotic value by the second trial. This difference suggests that the satiation effect may be accounted for by subjects' increasing avoidance of the intruders over trails, perhaps as a way of regualting their level of aggressive arousal.     

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.     

Intruding male red swamp crayfish,Procambarus clarkii,immediately dominate members of established communities of smaller,mixed-sex conspecifics

The effects of competing asymmetries (intruder size advantage vs. prior residence) on dominance relationships were investigated in a laboratory setting. Sexually mature (Form I) male red swamp crayfish, 25%-27% larger than the average member of several mixedsex communities of 20-25 sexually mature conspecifics, individually intruded upon these communities on successive days. Each community was invaded once a day, with each of these large intruders invading every community once during the experiment. Five days after the last large intruder invasion, novel intruder group males, approximately the same size as the average community member, individually invaded the same communities, all communities being invaded once during a single day of testing. These novel intruders were used to differentiate the effects of intruder size from those effects of being put into a novel environment. During each intrusion, the frequencies of dominance, submission, aggressive standoffs, and nonaggressive interactions between the intruder and members of the community were recorded. The large intruders on each day immediately and virtually completely dominated all encountered community members, and the large intruders were significantly more dominant than the novel, smaller-sized intruders. The size advantage of the large intruders overwhelmed prior residence in influencing dominance outcomes, even in these well established communities. © 1995 Wiley-Liss, Inc.     

Mice: the initiation and maintenance of pregnancy-induced aggression following thelectomy

Two experiments were conducted in order to assess the effects of thelectomy (i.e., nipple removal) on the display of pregnancy-induced aggression in Rockland-Swiss (R-S) albino mice. Pregnant animals, thelectomized on Gestation Day (GD) 12, exhibit a high incidence and intensity of aggression toward adult R-S male intruders during tests conducted on GDs 14, 16, and 18 (i.e., during the last third of gestation in this species). Since thelectomized dams display levels of aggression (i.e., 63% incidence) equivalent to those of sham-operated and nonoperated animals (53 and 67% incidence, respectively), it would appear that nipple presence is not a critical factor for the maintenance of pregnancy-induced aggression in mice (Experiment 1). To examine the effects of nipple deprivation on the initiation of pregnancy-induced aggression, virgin animals were thelectomized prior to mating, then repeatedly tested for aggression at 2-day intervals of gestation. Unlike nipple-intact dams, pregnant mice, deprived of nipples prior to conception, rarely exhibit (less than 17% incidence) agonistic behaviors toward intruder males (Experiment 2). These findings suggest that the development and self-stimulation of nipples early in pregnancy may be important conditions for the display of heightened aggression with advancing pregnancy in mice.     

Effect of residence and size asymmetries upon the agonistic interactions between juvenile white‐seabream (Diplodus sargus cadenati de la Paz,Bauchot and Daget, 1974)

The behavioural patterns of juvenile white‐seabream suggest that asymmetry in residence is an important factor governing the outcome of contest between individuals of this species. Asymmetries due to resident status had strong effects on agonistic behaviour, with asymmetries in body sizes producing weaker effects. Resident fish won all the combats against intruders of lower or similar length. However, when the intruder was larger than the residents (higher than 5% in length and 20% in weight), the percentage of combats won by the residents decreased to 85.7%. There was a significant correlation between fight intensity and size asymmetry in favour of the resident fish. The resident fish was more aggressive and persistent in attacks, and contests were more intense when the size of the intruder was greater. During agonistic interactions, the frontal attacks and lateral displays were more frequent when the intruders were similar or larger than residents. Attacks to the flanks and chases were more frequent in pairs where the intruders were smaller. Aggr. Behav. 25:297–303, 1999. © 1999 Wiley‐Liss, Inc.     

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

This investigation was concerned with the identification of the ultrasonic vocalizations produced by intruders during aggressive interactions and the role of these signals in agonistic behavior of rats. In the first experiment, experienced resident males were paired with both devocalized and intact vocalizing naive intruder males. Devocalization of the intruder males resulted in a drastic decrease in 50-kHz vocalizations and the elimination of all 22-kHz vocalizations. This almost total absence of ultrasonic vocalizations was not accompanied by any change in resident aggressive behavior or intruder defensive and submissive behavior. In a second experiment, naive intruders were tested with either deafened or intact resident males. Similarly, preventing residents from hearing intruder ultrasounds had no detectable effect on any aggressive behavior. These experiments are not consistent with the correlative evidence that intruder-produced 22-kHz vocalizations inhibit the aggressive behavior of the resident. The results also show that most of the ultrasonic vocalizations emitted during aggressive encounters are probably produced by the intruder.     

Failure of strange females to cause pregnancy block in collared lemmings, Dicrostonyx groenlandicus

The effects of exposure to unfamiliar females on pregnancy success of recently mated females were examined in collared lemmings (Dicrostonyx groenlandicus). Four days after mating, females in their home cage were exposed to strange, female intruders that were either nonpregnant or 16 days pregnant. Other recently mated females were introduced to the home cage of 16-day-pregnant females. Pregnancy success of the recently mated females was not reduced in any of these treatments. In the paired encounters, there was no relationship between dominance status and pregnancy status, nor between dominance and pregnancy success. These results do not support the hypothesis that in species in which females are aggressive and readily commit infanticide, unfamiliar females should cause other females to terminate early-stage pregnancies.     

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).     

The effects of negative reinforcement for irritable aggression on resident-intruder behavior

This experiment demonstrated that rats trained to display elevated levels of shock-induced aggression in a negative reinforcement paradigm displayed more boxing behavior than yoked control groups in a later test in which intruder rats were placed in the home cage of resident rats. Resident or intruder status did not affect the influence of the negative reinforcement procedure on the observed resident-intruder behavior of trained animals; however, naive intruders paired with trained residents displayed increased defensive behavior, suggesting that negative reinforcement for shock-induced aggression affected the behavior of these residents.     

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.     

Aggressive behavior in inbred strains of mice during pregnancy

Female aggressive behavior toward adult male ICR/JCl mice was compared for virgin and pregnant mice of five inbred strains (BALB/c, C3H/He, C57BL/6, DBA/2J, and AKR/J). Pregnant females from four strains except BALB exhibited intense aggressive behavior, whereas only virgin AKR females were aggressive. Aggressive behavior began in early pregnancy, was highest in midpregnancy, and declined slightly thereafter until the day of parturition. The level of aggressive behavior showed significant strain differences. The topography of aggressive behavior was also different among the four strains. DBA females showed marked contrast with the other three strains in the temporal changes of aggression in the first phase of encounter. Furthermore, strain specific behavioral pattern of aggression was demonstrated based on six behavioral acts ( Darting , Chasing, Attack, Biting, Wrestling, and Boxing). Virgin and pregnant AKR females showed the identical behavioral pattern of aggression.     

Pheromone‐mediated intrasexual aggression in male lizards,Podarcis hispanicus

Sex recognition is based on color signals in many species of lizards. However, olfactory stimuli are also clearly involved, and many species might rely primarily on chemoreception. We aimed to examine whether color pattern or odors, or a combination of both factors, induce the aggressive response of males of the lizard P. hispanicus. We experimentally manipulated the coloration and odor of male P. hispanicus, thereby creating groups with all combinations between coloration and odor of males or females. Using data from staged encounters, we compared the responses of resident males to the experimental groups of manipulated males and their response to unmanipulated individuals (males and females). Responding males reacted significantly more aggressively to intruders with male odors independent of their coloration, whereas intruders with female odors did not elicit aggressive responses but were preferentially courted, irrespective of their actual sex and body coloration. In addition, intruders with female odors elicited a higher number of tongue‐flick explorations than male odor ones. Comparisons with unmanipulated male and female intruders agreed with these expectations. Therefore, at least at close range, odoriferous cues seem to be more important than color patterns in sex recognition and intrasexual aggression by male P. hispanicus. We suggest that this might be a pattern commoner than expected in many species of reptiles.Aggr. Behav. 28:154–163, 2002. © 2002 Wiley‐Liss, Inc.