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.     

Effect of chronic ethanol administration on intermale aggression in rats

An experiment was performed to study the effect of chronic ethanol administration on intermale aggression in rats using a 24-hour resident-intruder test. During the resident-intruder test residents displayed virtually all of the agonistic behaviors, and intruders displayed virtually all of the defensive behaviors. Intruders treated with ethanol displayed more defensive behavior and elicited more agonistic behavior than control intruders. Twenty minutes into the resident-intruder test intruders showed the greatest increase in corticosterone (338% vs. 129%), while residents showed the greatest increase in testosterone (103% vs. 18%). On the 2nd day of the resident-intruder test intruders lost more weight than residents (21.5 g vs. 10.2 g). Plasma corticosterone levels remained elevated for the intruders, and in particular for those intruders displaying defensive behaviors regardless of the resident's behavior. Plasma testosterone levels remained elevated for those residents that were paired with intruders that displayed defensive behaviors regardless of the resident's behavior. The frequency and severity of biting attacks by ethanol residents was significantly greater than that of control residents. In addition, the locus of biting attack shifted from the upper back of intruders paired with control residents to the flanks, tail, lower feet, and ventral surface on intruders paired with ethanol residents.     

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).     

A pinch or a lesion: a reconceptualization of biting consequences in mice

Intruder and resident male colony mice exhibit an array of distinct defensive and offensive behaviors. Intruders typically show more boxing, flight, defensive sideways position, on the back position and general locomotion, while residents exhibit higher levels of attack, olfactory investigation, aggressive grooming, and biting, with a preference for dorsal bite locations. Here, analysis of bite locations on the body of the intruder mice showed that the majority of bites produced few lesions (i.e. actual puncturing of the skin) when compared to scrapes or no markings. Most bites were directed to the back of the opponent animal with very few bites directed towards the opponents' vulnerable ventrum. In particular, bites directed at the relatively hairless ventrum produced no lesions. These findings, along with previous work on mice and rats, suggest that intraspecific offense with preferred target sites for biting, facilitates an effective but largely nonwounding interaction between resident and intruder mice. Furthermore, bruise and wound analyses suggest an association between bite targets and tissue damage. The preference for specific bite locations may be complimented by a differential intensity of attack, with the back attracting the strongest bites and the ventrum the weakest. This apparent nonwounding fighting pattern contradicts the current evaluation of rodent wounding severity in this paradigm and can therefore refine the usage of this model and of the protocols associated with it.     

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.     

The role of body weight in resident-intruder aggression

The behavior of male NIH Swiss mice of various body weights in the resident-intruder test of aggression was investigated. Mice were housed individually for 10 days prior to the test, and allocated to six groups. In the first three groups body weights of residents and group-housed intruders were matched, and the animals were divided into light, average, or heavy groups. In the last three groups weights of the intruder mice were either matched with the residents, or intruders were lighter or heavier than the residents. We found that light residents spent significantly less time in aggressive behaviors and longer time in defensive behaviors than the other two groups. The heavy mice showed most social investigation. The body weights of intruders were also shown to affect the behavior in the test: those residents which had light opponents spent a longer time in aggressive behavior than those which had matched or heavy opponents. The resident mice with heavy opponents showed most defensive behaviors. To study whether pharmacological manipulation may have different effects on behavior in the resident-intruder test in mice having different weights, animals of light, average, and heavy body weight received a low dose (0.8 g/kg) of ethanol 30 min prior to the test. We did not note any effect of ethanol on aggressive behavior in the three groups. The results suggest that body weight plays a significant role in determining the level of aggression and defensive behaviors in the resident-intruder test.     

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.     

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.     

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.     

Functions of the vibrissae in the defensive and aggressive behavior of the rat

Removal of mystacial vibrissae for strange rats placed in an established rat colony produced reliable decrements in defensive boxing for these animals, and corresponding increases in freezing. In a subsequent experiment, removal of the vibrissae of the attacking colony males did not change the attack behavior of the vibrissectomized animals. These results indicate that the vibrissae are involved in defensive boxing behavior, but play no essential role in the elicitation or maintenance of conspecific attack in the rat.     

Relationship between mousekilling and conspecific aggression in the male rat

In order to investigate the relationships between mousekilling and conspecific aggression, behavioral variables of killer and nonkiller rats were compared in a “resident-intruder” paradigm, in resident as well as in intruder animals. The occurrence of offensive items (offensive sideways, attack) was significantly higher in killer rats when they were residents; their corresponding opponents displayed more defensive behaviors. No significant difference in aggressive behaviors was noted when the comparison was done in the intruders. These results and those of previous studies suggest that there is a correlation between mousekilling and intraspecific offensive behaviors. Some similarities in the situations where both behaviors are elicited–eg, introduction of an unfamiliar intruder into a familiar environment–may contribute to the existence of such a correlation and the possibility of common mechanisms underlying both behaviors is discussed.     

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.     

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.     

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.     

Habituation of aggressive behavior in mice: A parametric study

The decline of aggression as a result of repeated episodes of fighting may represent a habituation phenomenon. The frequency of biting and sideways threat by male mice toward conspecific intruders declined over ten 5-min confrontations. Aggression returned to about 50% of original levels when a new intruder was introduced. Variations in length or frequency of confrontation indicated that the rate of decline of attack bites and sideways threats depended on these confrontation parameters. The condition that provided the fewest opportunities to fight provided the least decline in the frequency of attack and threat. The frequency of attack bites and sideways threats elicited by the presentation of a new intruder after repeated confrontations was greater than the frequency of attack bite and sideways threat in the last confrontation with the original intruder, when the resident and intruder were relatively inexperienced. Spontaneous recovery of attack and threat occurred but rate of recovery did not depend on confrontation parameters. The results indicate that the decrement of aggression in mice in repeated confrontations may be the result of habituation but fatigue is an important cofactor.     

Attack and defense in conspecific fighting in tree shrews (Tupaia belangeri)

Principles of conspecific defense have been analyzed for rodents, in which specific target sites for biting by attackers on defenders serve as an important determinant of the actions involved in both attacker and defender behavior. In an effort to determine the generality of these principles, attack and defensive behaviors and target sites for biting attack were evaluated in a nonrodent species, the tree shrew (Tupaia belangeri). Brief daily and repeated conspecific dyadic encounters between adult, socially experienced males (dominants, attackers), and adult, socially naive males (subordinates, defenders) that had been transferred into the territory of the dominants, produced a polarization of attack and defense. The dominant males showed chase, chase attack, jump attack, and biting behaviors, while the subordinates displayed flight and freezing. The vast majority of bites, as well as wounds and bruises, were on the subordinates’ backs. These patterns are very similar to those previously found in rats and mice and suggest that the organization of fighting, with targets of biting (or other painful) attack serving as an important determinant of both attacker (dominant) and defender (subordinate) behavior, may show considerable generality across nonrodent as well as rodent species. Although relatively few wounds were found after 28 days of repeated and daily encounters, the subordinate tree shrews show a variety of behavioral, neuroendocrine, and central nervous changes, indicating that they are stressed by these encounters per se. Aggr. Behav. 27:139–148, 2001. © 2001 Wiley‐Liss, Inc.     

Effects of reactivity to dorsal stimulation and social role on aggressive behavior in laboratory rats

Rats were selected on the basis of reactivity to dorsal tactile stimulation and then tested in a resident-intruder paradigm. While reactivity of residents did not influence the occurrence of agonistic behaviors or wounding of residents and intruders, reactivity of intruders did affect offensive and defensive patterns of interactions and the wounds sustained by residents and intruders. Subsequent to resident-intruder testing, rats were tested for shock-induced aggression. The pattern of the results and the results of additional experiments demonstrated that resident-intruder experience could affect subsequent shock-induced aggressive behavior.     

Reflexive fighting in the albino rat: Aggressive or defensive behavior?

Specific agonistic responses of albino rats were compared for dominant colony rats and intruders, and for rats in a “reflexive fighting” task. The “reflexive fighters” showed high levels of defensive responses such as boxing and freezing, and very low levels of aggressive behaviors such as piloerection, biting, and the lateral display. This pattern clearly suggests that the behaviors measured in the reflexive fighting task reflect conspecific defensive reactions, rather than “shockelicited aggression.” Moreover, striking responses seen in the reflexive fighting task also occur at a high rate when footshock is given to a solitary rat held in a boxing posture. Thus it appears that “reflexive fighting” primarily involves defensive rather than aggressive responses.     

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.