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.     

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.     

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).     

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.     

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.     

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.     

Rare male aggression directed toward females in a female‐dominated society: Baiting behavior in the spotted hyena

Spotted hyenas (Crocuta crocuta) are gregarious carnivores. The females are socially dominant to males, and adult males rarely direct aggression toward adult females. This study analyzed all cases in which adult immigrant males behaved aggressively toward adult females in a large population of free‐living hyenas in Kenya, observed for 11 years. Our goals were to describe the conditions under which male attacks on females occur, and address possible adaptive functions. Most aggression directed by adult immigrant males against females occurred when coalitions of two or more males attacked a single adult female, who typically responded by defending herself and fighting back. Male aggression against females frequently occurred at sites of ungulate kills, but males never behaved aggressively toward females over food, and all male attacks on females were unprovoked. Although no mounting or other copulatory behaviors ever occurred during or immediately after an attack, the number of male attacks on females peaked around the time of conception. Daily rates at which males attacked females did not vary with female social rank. However, daily attack rates did vary significantly with female reproductive state, and the highest rates of male attack on females were observed during the two stages of the reproductive cycle during which females were most likely to conceive litters. The adaptive significance of male aggression against females in this species remains unknown, but a tight association between male attacks on females and a female's time of conception provides strong evidence of some role for male aggression in hyena sexual behavior. In particular, our data are consistent with hypotheses suggesting that male aggression toward females in this species either serves to inform females about male fitness or represents sexual harassment. Aggr. Behav. 29:457–474, 2003. © 2003 Wiley‐Liss, Inc.     

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.     

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.     

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.     

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.     

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.     

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.     

Effects of female presence on intrasexual aggression in male lizards,Podarcis hispanicus

Resource value and expected gain in reproduction may affect motivation to fight and the likelihood of winning. Previous experiments have showed that males increase their fighting effort when defending a territory that contains females. However, we hypothesized that for an intruding lizard, the value of a new territory may be lower if he already has a female in his own territory, and consequently, aggressivity should be lesser than if he has no access to any female. We staged encounters between males of the lizard Podarcis hispanicus in outdoor terraria to analyze the outcome and detailed behaviors involved in agonistic interactions in the presence or absence of a female in the terraria of resident and intruders. Our results showed that when a female was present, the level of aggressivity of the resident male was higher; the probability of winning the contest also increased, but only if the intruding male had no females in his own terraria. In contrast, when the intruding male was also the owner of another territory containing a female, residents were less aggressive. We suggest that the lack of information on the reproductive state of an unfamiliar female may be enough to decrease fighting motivation of an intruding male, if he has more expectations of success with his own familiar female. We conclude that differences in expected reproductive success with different females may help to decide the outcome of conflicts between males quicker and cheaper. Aggr. Behav. 28:491–498, 2002. © 2002 Wiley‐Liss, Inc.     

Aggressive behavior of adult bank voles (Clethrionomys glareolus) towards conspecifics

Male and female bank voles reared in different conditions were investigated for their aggressiveness in order to show how social factors modify intermale and interfemale behavior. Singly reared males or females were paired with a tested animal for 10 min. The number of attacks and the accumulative attack times of singly reared males were higher than for females reared in similar conditions. The differences were not, however, statistically significant due to the variation among tested animals. There were significant differences in aggressiveness of females reared in various conditions before the test. Most attacks were observed in females reared with intact males. In this group, the accumulative attack time was significantly higher than that of singly reared, grouped females, or females kept with castrated or castrated-testosterone-treated males. Also, the aggression of males was affected by breeding. Both the number of attacks and the accumulative attack times were elevated in intact males kept with females. Housing of males in groups and castration significantly decreased the number of attacks of these animals. Injection of testosterone increased aggression in castrated males. It is suggested that olfactory signals in bank voles released by males increase aggression in females and the female's signals stimulate male behavior.     

Role of female behavior in controlling population growth in mice

Sex ratio does not appear to be a factor in generating the characteristic population growth curve. Freely growing populations of house mice, consisting of all females and one male, stopped their growth at approximately the same densities as normal sexratio populations used as references. The mechanism(s) of female control of population dynamics may be related to female aggressive behavior. As the all-female/one-male populations approached their maximum size, the females began to show wounding patterns and social hierarchies in much the same manner as males in populations with normal sex ratios. The male in each of the populations was severely wounded in the posterior region, and each lost its tail as a result of injuries which could have been inflicted only by the females. The female social hierarchy can be seen only when there has been reproduction and population growth. Assembled populations of all females rarely exhibit aggressive behavior. Female aggression becomes apparent only when the population approaches its maximum size and thereafter. These data are consistent with the hypothesis that males are competitive among themselves for territory and social rank, and ultimately to mate with the females. Other investigators have indicated that females respond to population size, which may reflect increased competition between the females with the establishment of territories. Thus female agression may control population growth, a role previously ascribed to male aggression.     

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.     

Response of male and female Siberian hamsters towards pups

The influence of sex, reproductive maturity, and parental experience on the behavior of Siberian hamsters (Phodopus sungorus sungorus) toward strange pups was examined in this study. Immature, mature, or parentally experienced male and female Siberian hamsters were presented with 3- to 8-day-old pups. We recorded pup carrying during the initial 10 min, nesting with pups after 8 or 14 h, and attacking pups during the test period. Among inexperienced animals, more mature males attacked pups than did immature males or mature females. Parental experience significantly decreased pup attacks by males and increased nesting with pups by both males and females. Repeated testing did not modify the responses to pups. We conclude that in Siberian hamsters both caretaking and aggressive responses to pups may be shown by immature and mature animals of both sexes. Parental experience resulted in increased caretaking by males and females and decreased aggressive responses by males.     

Sensory cues that elicit ultrasonic vocalizations in female rats (Rattus norvegicus)

Female rats emit ultrasonic vocalizations during copulation. Female vocalizations are associated with darting and other proceptive behavior. In addition, females frequently call while approaching the male. A series of experiments was undertaken to determine whether female rats emit ultrasonic vocalizations in response to other rats or to their odors. Females were exposed either to bedding soiled by males or females or to devocalized conspecifics separated from the subject by a barrier. Females vocalized more to male cues than to female cues, regardless of whether the odor cues were from soiled bedding or from a devocalized conspecific. In addition, subjects vocalized more when presented with a devocalized female rather than a neutral stimulus. Furthermore, devocalized adult males, separated by a barrier, were more effective than either devocalized castrated or juvenile males in eliciting vocalizations; in turn, castrates and juveniles were more effective than neutral stimuli. Female calling was likely induced by odors from the male. In one experiment, the female subject was positioned in such a way that she could neither see or touch the stimulus male. Presentation of tape-recorded male vocalizations did not affect calling by the female. Vocalizations emitted by females in response to male odors may attract males or may facilitate subsequent copulatory behavior by the male.     

Gonadal hormones and intrasexual aggressive behavior in female bank voles (Clethrionomys glareolus)

The effects of gonadal hormones on aggressive behavior in the female bank vole was investigated in 10 min home cage tests. Ovariectomized (ovx) or intact females injected with oil, with progesterone (P), with a mixture of progesterone and estrogen (P+E), or with testosterone (T) alone were confronted in a resident-intruder test with unfamiliar, nonoperated females as intruders. Intact females showed aggressive behavior more frequently than ovx females. Ovx females injected with P, with P+E, or with T made significantly more attacks, and these attacks lasted longer than those observed for oil-treated voles. The results indicate that P, the typical female hormone, is responsible for aggressive behavior in female bank voles; however, only T increased the duration of interfemale aggression. Aggr. Behav. 24:63–70, 1998. © 1998 Wiley-Liss, Inc.