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.     

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.     

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.     

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.     

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

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

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.     

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.     

Effect of conspecific sex on aggression during pregnancy and lactation in golden hamsters

The effect of conspecific sex on maternal aggression in hamsters was determined by comparing the frequency of aggressive responses by dams continuously housed with either a virgin male or female cagemate during pregnancy and lactation. Dams easily established aggressive dominance over male cagemates soon after pairing, and their aggression was low thereafter for the duration of pregnancy and lactation. The aggression of dams with females, on the other hand, tended to fluctuate with highs during mid pregnancy and mid lactation and lows around birth. When dam aggression was low around birth, female cagemates frequently became aggressively dominant, and several dams lost their litters. The higher aggression of dams toward females than males is probably a reflection of greater intrasexual competition for environmental resources that includes pups.     

Decline of maternal behavior in the virgin and lactating rat.

Sensitized virgins and postpartum lactating mothers, both exhibiting maternal behavior, were given donor litters that increased in age by 1 day, for 28 days, starting at the onset of maternal behavior. Each day females were tested for maternal behavior with pups 4-8 days old: Maternal care (i.e., nursing/crouching, retrieving, nest building and licking) and maternal withdrawal, rejection, and prevention of nursing were recorded. After the ninth day, females were also tested with the progressively older pups from 10 to 28 days of age with which they were living. Virgins and lactating mothers showed generally similar patterns of maternal care although some differences were found, and they declined in maternal behavior toward the older pups in a similar manner. Maternal behavior did not decline in tests with younger pups. The results are interpreted as supporting the hypothesis that the decline as well as the maintenance of maternal behavior postpartum is nonhormonally mediated.     

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.     

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

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

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.     

Dexamethasone can prevent stress-related litter deficits in the golden hamster

This study was designed to examine the effects of social subordination during early pregnancy in the golden hamster (Mesocricetus auratus). Primiparous females were mated to proven breeders and stressed during early pregnancy. Females were housed singly throughout gestation except for Days 4, 5, and 6 when they were paired for 10-min intervals three times each day with another female matched for age, weight, and day of pregnancy. Within each of the pairs, one female was consistently dominant to the other. Controls were exposed to a novel area instead of a conspecific. At parturition, all pups were counted, sexed, and weighed. There were no significant differences between control and dominant females' litter sizes and sex ratios. Subordinate females produced significantly smaller litters than control or dominant dams and significantly lower sex ratios than control dams. Subordinates produced fewer males than control or dominant dams, but there were no differences in the number of females produced. The entire experiment was repeated exactly except that females received a small dosage of dexamethasone in their drinking water on Days 3-7 of pregnancy. In this second group, there were no significant reductions in mean litter size, sex ratio, or pup weights among litters born to subordinate dams. These results suggest that subordinate dams produce smaller litters via selective resorption of males in utero and that the typical adrenal response to stress mediates this response.     

Prepartum changes in maternal responsiveness and nest defense in Rattus norvegicus

Changes in maternal responsiveness during late pregnancy were traced by exposing females to foster pups (15-30-min tests) under conditions favoring the rapid initiation of maternal behavior. Groups were tested when nonpregnant or on Days 17, 20, 21, or 22 of pregnancy (Day 22 = parturition). Nulliparous females were compared with primiparous and with "experienced breeders." Nest defense was observed by introducing unfamiliar males (2-min tests) on Day 22. Results focused attention on three periods: (a) Days 17-20, when maternal responsiveness was lower than in the nonpregnant condition, (b) Day 21, when maternal responsiveness returned to or rose above nonpregnant levels, and (c) on Day 22, the 3.5 hr prior to delivery, during which 90% of females almost immediately retrieved, gathered, and tended foster pups and during which 92% attacked the unfamiliar intruders. (Attacks were rare earlier.) Maternally experienced females were more responsive to pups than nulliparous females when nonpregnant and throughout late pregnancy, but both groups were equally likely to show prepartum aggression.     

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.     

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.     

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.     

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.     

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.