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).     

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 and defensive behaviors in the albino mouse

Attack by dominant male colony mice on intruders included chasing and lateral attack behaviors, while the corresponding intruder behaviors were flight, boxing, and checking. Both of these are similar to the attack and defensive behaviors of colony rats and intruders. However, mice did not show a significant constraint on bites to ventral areas, and the rat defensive behavior of lying on the back, which is effective because of this constraint, was rare; the corresponding “on-top” behavior of attackers was almost absent in mice. These findings strongly support the view that intraspecific attack and defensive behaviors, and target sites for bites, are interrelated factors facilitating effective but nonlethal agonistic interactions in muroid rodents.     

Factors influencing maternal attack on conspecific intruders by lactating female “TO” strain mice

Factors regulating maternal attack in “TO” strain mice were investigated to determine 1) optimal conditions for inducing this behaviour and 2) the likely utility of this activity. Lactating females were more likely to attack male intruders than female intruders. The mate's presence reduced maternal attack in this strain, or (putting it conversely) aggression was generated in the male's absence. Removal of the mothers from their litters for four to five hours also suppressed maternal attack. Investigation of the bite targets in the maternal attack suggested that it is a defensive, rather than an offensive, response.     

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.     

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.     

Targets of attack and defense in play-fighting of the Djungarian hamster Phodopus campbelli: Links to fighting and sex

Analysis of the body targets attacked and defended during play-fighting by juvenile Djungarian hamsters Phodopus campbelli revealed that about 70% of all attacks were directed at the mouth. If successfully contacted, the mouth was briefly licked and nuzzled. The remaining playful attacks were gentle bites directed at the rump, and to a lesser extent, the top of the head. During serious fighting the top of the head and the rump are targets of attack, whereas the mouth is not. Licking and nuzzling the mouth was found to be a behavior performed by adult males at the beginning of sexual encounters. Therefore, play-fighting in juvenile hamsters cannot be thought of merely as a form of “mock fighting” since the principal target is seemingly sexual, not agonistic. The data also show that of the sexual body targets contacted, adult females are more likely to defend the mouth. In this way it is suggested that targets attacked and defended during juvenile play-fighting are derived from adult contexts in which such targets are defended. This hypothesis accounts for the prevalence of agonistic targets in the play-fighting of many species, and may provide a rationale for classifying those amicable targets that are competed for during play-fighting.     

Female behavior in populations of mice in the presence and absence of male hierarchy

Female aggression may be the regulator of population size in small mammals. Freely growing populations of house mice showed several differences in aggressive female behavior in the presence and the absence of a male hierarchy. Territoriality in females and not in males appeared to maintain social order and regulate population density. Certain females were seen patrolling and guarding the territory and chasing and fighting with both male and female intruders. These females did not fight amongst themselves, suggesting that they were not fighting for rank (as do the males) but for territory. Although these aggressive females produced young, the pups were neglected, and few were weaned. The non-aggressive females were the successful breeders. Aggression by the females only occurred when there was reproduction and increased densities. Assembled females with no males present never show this aggression. The occurrence of “male-type” behavior became most apparent when the males were removed at peak population densities. The removed males were then castrated and injected with testosterone cyprionate. Doses were increased by population cage, and therefore all males returned to each freely growing population were given the same dose. The males given oil placebo injections showed no return of a male hierarchy and the females showed high levels of aggression toward them. Males injected with testosterone cyprionate showed return of male aggression and fighting and mounting of females. But the new “dominant” females continued their patrols and chased males away from their territories and did not permit these males to mount. Male-male fighting consisted primarily of frontal attacks to the face and roll and tumble fights. Female-male aggression consisted primarily of attacks to the posterior region targeted at the base of the tail and the genitals of the male. The males were rarely seen attacking females and then only during mating. Females only attacked each other in defense of their territories.     

Analysis of the targets and tactics of conspecific attack and predatory attack in northern grasshopper mice onychomys leucogaster

Comparisons of tactics of fighting between species are often difficult to make since the body targets attacked may differ. Thus it becomes difficult to assess whether differences in fighting tactics are due to species-specific differences in the tactics themselves or due to the different targets attacked. A solution to this problem is to analyse the tactics of a species that attacks different targets under different circumstances. In this way, differences in tactics can be more readily attributed to differences in targets. In this study, resident male northern grasshopper mice (Onychomys leucogaster) were tested against intruding male conspecifics and against laboratory mice (Mus musculus domesticus). Conspecifics were mainly bitten on the lower dorsum, whereas prey were bitten and killed by bites to the nape of the neck. Therefore, it was possible to analyze the tactics of attack by grasshopper mice when attacking different body targets. For example, in order to defend the lower dorsum and the nape, both intruding conspecifics and prey adopted an upright defensive posture. Resident grasshopper mice used the lateral attack tactic to gain access to the lower flanks but not the nape. This illustrates that the lateral attack tactic is not merely a tactic suitable for overcoming the upright defense tactic, but is used in this context only when the target attacked is on the opponent's posterior dorsum. Such withinpecies comparison enables the identification of the contextual rules which govern the use of fighting tactics. © 1992 Wiley-Liss, Inc.     

Behaviour of Young Growing Pigs in a Resident‐Intruder Test Designed to Measure Aggressiveness

A total of 125 growing pigs (47 days old) were tested for aggressive responses on two occasions using a resident‐intruder (R‐I) design. Our aims were twofold: (1) to attempt to replicate earlier work on pigs showing that resident aggression is a consistent individual characteristic, unaffected by weight or sex of the resident or intruder and (2) to develop behavioural measures to characterise the wide range of aggressive responses in the test. Resident pigs, housed since birth with littermates, were placed individually in a divided‐off portion of their home pen, and a smaller, unfamiliar intruder (approximately 66% of the resident's weight) was introduced. The test ended 5 min after the first investigation of the intruder by the resident or when one of the pigs began to attack the other (by delivering a sudden, rapid series of bites). On days 1 and 2, 33.6% and 43.2% of tests, respectively, ended in an attack by a resident. Intruder attacks were rare. Pigs were consistent in whether they attacked or not over the two tests, although attack latencies for pigs attacking in both tests were not correlated. Females were more likely to attack and attacked more quickly than males on the first test day but not in the second test or overall. Intruder sex had some effect on the test outcome (males were attacked more rapidly in the second test only). Resident and intruder weight had no effect. Aggressive pigs (meaning pigs that attacked vs. pigs that did not and fast‐attacking pigs vs. slow‐attacking pigs) showed a number of differences in behaviour during the R‐I test: (1) they took longer to make initial contact with the intruder in their first test; (2) they showed a higher frequency of aggressive acts (single head knocks, bites, and shoves); (3) they spent a greater proportion of the test engaging in social contact with the intruder rather than non‐social behaviours; (4) their social behaviour involved more postures directed toward the head as opposed to flank‐ or rear‐directed postures or re‐establishing social contact; and (5) they showed closer physical contact with intruders during social encounters, as characterised by their lower head positions. Some of these behavioural measures could be used to improve the measuring power of the test in the future. Improved behavioural measures would enable aggressiveness scoring among pigs that did not attack instead of classifying them all together as “non‐attacking.” Aggr. Behav. 28:401–415, 2002. © 2002 Wiley‐Liss, Inc.     

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.     

Ethological analysis of the male rat's socioagonistic behavior in a resident-intruder paradigm

The object of the present study was to assess the rat's socioagonistic behavior by means of ethological procedures. Two groups of male Wistar rats were used: 33 residents and 66 intruders. To allow reliable characterization of social and agonistic patterns, social interactions were increased by the isolation of residents and, on the other hand, both offense in residents and defense in intruders were increased by differences in weight, agonistic experience, and habituation to the enclosure. Encounters were videotaped, and the animals' behavior was analyzed by a 27-pattern ethogram and a software package made up to this end. Several patterns parameters were quantified, and two ethological mathematical models were employed: sequential analysis of preferential directions and cluster analysis based on similarities between patterns. Following mean latencies of the most frequent elements, the first four pattern sequences appeared to be the same in both groups of animals. From the fifth pattern on, residents displayed mainly dominance and threat, whereas intruders showed defensive and submissive patterns. Attack was also displayed by residents, but less frequently than dominance and threat. The alpha status was established by two sorts of domination, either through dominance and threat or by attack. The mean frequency of the intraindividual transition of patterns was higher in residents than in intruders. Pathway graphs, derived from sequential analysis, showed some common dyads, triads, or quadrads of patterns, but they basically defined different behavior structures in residents and intruders. Dendrograms, obtained by cluster analysis, allowed classification of patterns into behavior categories. The categories in residents were exploration, dominance, threat, and attack, and they encompassed 18 elements; in intruders the categories were exploration, dominance, and defense, and they consisted of nine patterns. A submissive category composed of three patterns could be also deduced considering similarity results. To summarize, six behavior categories were obtained: one “socioindividual” (exploration) and five “agonistic” (dominance, threat, attack, submission, and defense). In conclusion, the present study shows how ethological procedures may help to elucidate the rat's socioagonistic behavior and to classify the observed patterns into behavior categories.     

Intruders of differing reproductive status alter aggression differentially in early and late pregnant mice

Independent groups of early and late pregnant mice, housed individually, were observed with an intruder in their home cage. The intruders were either males, virgin, early, or late pregnant females. Male intruders were sniffed less, but more frequently and more severely attacked, than any type of female intruder, both by early and by late pregnant residents. While early pregnant females behaved similarly with the three types of female intruders, late pregnant animals treated them differently: they showed practically no aggression to late pregnant intruders, more to early pregnant ones and were most aggressive towards virgin female intruders. The possible relation of these findings to reproductive behaviour is discussed.     

Neuropharmacological aspects of adaptive pain inhibition in murine “victims” of aggression

This review outlines recent research on a subset of physiological responses in murine “victims” or aggression. In a typical resident-intruder paradigm, the detailed study of intruders has revealed that exposure to conspecific attack (and related stimuli) is associated with two forms of analgesia which appear to be integral components of the murine defensive repertoire. In response to intense/enduring attack, intruder mice display a profound, long-lasting and opioid-mediated analgesia. This reaction is highly correlated with defensive immobility and may function to reduce involuntary cues to further attack. In contrast, the inhibition of pain reactivity in mice tested immediately upon the display of defeat is less intense, shorter-lasting, non-opioid in nature and may function to facilitate active defenses such as escape. As this form of pain inhibition is also evident in intruders exposed to the scent of an aggressive male conspecific, a possible anticipatory defensive function linked to mechanisms of anxiety has been proposed. This hypothesis is supported by 1) the prevention of defeat analgesia by a range of antianxiety drugs (benzodiazepines, 5-hydroxytryptamine_1A [5-HT_1A] receptor agonists, and 5-HT₃ receptor antagonists) and 2) the effects of social defeat on behavior in the elevated plusmaze model of anxiety. These findings are discussed in relation to coping mechanisms in murine “victims” of aggression. © 1995 Wiley-Liss, Inc.     

Infanticide and maternal aggression: Synchrony of male and female reproductive strategies in mice

Thirty-six percent of male mice from three strains attacked newborn pups sired by another male. No male attacked its own offspring. Females did not show differential aggression toward males likely (strangers) or unlikely (sires) to attack their pups. Both forms of aggression were unaffected by housing in rooms which did or did not contain the aggression targets. The three strains differed in strength of maternal aggression but not in the incidence of infanticide. Females showed more aggression when mated with males of the same, rather than a different, strain but no differences with intruders of the same or a different strain. Infanticide by males is best viewed as a postcopulatory, intermale-competition strategy, and maternal aggression as a counter strategy.     

70-kHz vocalizations by male mice do not inhibit aggression in lactating mice

Two experiments investigated the relationship between adult male 70-kHz vocalizations and aggression by lactating female mice (Mus domesticus). Intact, vocalizing males, surgically devocalized males, and naturally nonvocalizing males were used to assess the effects of high frequency vocalizations on maternal aggression. The emission of high frequency vocalizations promoted aggressive behavior by the females. In both experiments, lactating females attacked the vocalizing males more rapidly and showed a higher incidence of aggressive behaviors toward these males than they did to the nonvocalizing male. We suggest that these vocalizations are only one of many situational cues that the female uses to determine her final behavioral response.     

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.     

Agonistic behaviour and bite wound patterns in wild water voles (Arvicola terrestris L.)

Intra‐specific aggression was investigated in a wild colony of Water voles between 1999 and 2004 in South Wales, UK. The occurrence and location (i.e. on the head, neck, body or tail) of bite wounds were recorded for adult and juvenile male and female voles. The greatest (33%) incidence of bite wounds were recorded on juvenile females and the lowest (18%) in adult females. Seasonal analysis of wound data in adults revealed that females were more likely to be bitten during the breeding season whereas bite patterns in males did not vary seasonally. Analysis of bite pattern topography revealed that most Water voles seemingly attempt to bite vulnerable target areas of the body (namely the head and tail). This is in contrast with studies on rats and mice where competitive forms of attack (particularly involving males) largely avoid these areas of the attacked animal's body. Targeting vulnerable areas is normally a characteristic of defensive modes of attack. Patterns of bite topography and agonistic behaviour in this species seem to reflect competitive interactions between individuals, particularly between territorial females and their female offspring, over access to essential resources. Aggr. Behav. 32:599–603. 2006. © 2006 Wiley‐Liss, Inc.