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.     

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.     

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.     

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.     

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.     

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.     

Rank order in pairs of communally nursing female mice (Mus musculus domesticus) and Maternal Aggression Towards Conspecific Intruders of Differing Sex

This study examined social behavior between pairs of unfamiliar lactating females, with litters of the same age, at different periods after parturition (3, 7, and 17 days). Tests were generally followed by the formation of communal rearing nests, and subsequent maternal attack on intruders of differing sex was assessed. In all three intervals lactating females showed ritualized attack with formation of clear dominance-subordination relationships before combining litters into communal nests. The dominant females in 90% of cases started to retrieve alien pups into their nests. Agonistic behavior and communal nest formation were most rapid when pups were around 3 days old. Maternal attack on conspecific intruders was mainly displayed by the dominant lactating females. Male and female intruders were equally attacked (in terms of frequency and intensity of attack), but there was less such aggression when pups were around 17 days of age. Nevertheless the topography of biting attack employed against female and male conspecific intruders was different. Females were attacked using a strategy avoiding bites to the head and ventral surface (indicative of “offensive” behavior) whereas males were severely bitten on vulnerable body regions (indicative of “defensive” behavior).     

The introduction of a group of alien mice (Mus musculus L.) into hierarchically organized groups of five male mice

Groups of 3 male or female Mus musculus were introduced into hierarchically organized colonies of 5 male mice for a period of 8 days. The colonies were of 2 kinds; high-level aggressive (HLA), which had been set up 3 days prior to the introduction of the aliens, and low-level aggressive (LLA), which had been established for 21 days before strangers were introduced. Both males and anestrous females were attacked, but males were attacked 5 times more frequently than females. In HLA colonies most of the attacks on the aliens were by the dominant; in LLA colonies there was no difference in the behavior of dominant and subordinate mice toward strangers. Both aggression toward aliens and intracolony aggression declined over the 8 day experimental period. In HLA colonies the dominant mouse mounted females 5 times more frequently than did either his subordinates or male mice in the LLA colonies. In HLA colonies aliens huddled with subordinates to form a single colony with 1 dominant and 7 subordinates. In LLA colonies alien males remained as a discrete group spatially separated in the cage. Female aliens were incorporated into the main colony. In all cases dominant male mice made more attacks on aliens as compared with familiar mice.     

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: 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.     

Selectivity in paternal and infanticidal responses by male mice: effects of relatedness, location, and previous sexual partners.

Male mice tend to be infanticidal to unrelated infants but parental to their own offspring. The present study examines three hypotheses that might explain this apparent discrimination. There was no evidence of selective infanticide toward infants encountered for the first time on the basis of kinship, location, or cues associated with previous sexual partners. However, males tended to direct more paternal responses toward their own unfamiliar infants than toward unrelated infants, infants encountered in the male's home cage than those in the cage of another male, and when cues associated with a previous sexual partner were present. Data suggested that the responses of females to male intruders might influence the responses of those males. It was concluded that the infanticidal responses of male mice are mediated by a particular state of the male but that males in a noninfanticidal state may vary their paternal responsiveness on the basis of direct and indirect cues concerning relatedness.     

Variation in aggressive behavior and anatomo-physiological correlates generated by crowding without physical contact in the house mouse

Behavioral, physiological (i.e., endocrine), and anatomical consequences of crowding in mice were studied in a situation where animals were in auditory, visual, olfactory, and tactile contact but restrained from full physical interactions, to prevent overt aggression. Males that cohabited with females undisturbed by neighboring conspecifics showed greater propensity to attack same-sex intruders and had higher plasma testosterone levels than did their “crowded” counterparts, that is, males cohabiting with females and housed adjacent to other male/female pairs. In this respect, the latter animals resembled submissive males. However, a significant increase in weight of androgen-dependent target organs (i.e., seminal vesicles and preputial glands) was found in crowded males. These data indicate that despite the observed inhibition of social aggression these males are not physiologically comparable (homologous) to male mice that experienced defeat and the stress of submission during fighting. The intriguing possibility that different conversion pathway of testosterone are accelerated, as a result of social communication, in males living in these two environments and the behavioral implications of these possibilities are discussed. Finally, the parental behavior of crowded animals, although not freely interacting with each other, was disrupted, causing a marked decrease in reproductive success. In this situation a high incidence of infanticide of their offspring by both parents was observed, whereas this behavior was virtually absent in non-crowded male/female pairs.     

Social and hormonal factors influencing infanticide and its suppression in adult male Long-Evans rats (Rattus norvegicus)

In a series of six experiments, the experiential and hormonal factors influencing infanticide in Long-Evans hooded rats were examined. Males, but not females, purchased from a breeder as adults exhibited infanticide at high rates, whereas males reared in the laboratory until adulthood were less likely to be infanticidal. Sexual experience reduced the rate of infanticide in laboratory-reared males, and cohabitation with a female through pregnancy and lactation (including exposure to pups) inhibited infanticide in previously infanticidal males. Fourteen days of cohabitation with a pregnant female following copulation inhibited infanticide in males purchased from a breeder, but copulation without cohabitation and copulation followed by cohabitation with a nonpregnant (ovariectomized) female did not inhibit infanticide. Castration of laboratory-reared males in adulthood did not reduce their rate of infanticide, whereas testosterone implants increased the number of males exhibiting infanticide. The importance of hormonal and experiential factors for controlling infanticide in male rats is discussed.     

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.     

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.     

Response of colony mice to intruders with different fighting experience

Six male mice placed in a large, moderately complex enclosure formed a stable dominance hierarchy in which two mice defended adjacent floor areas and the remaining four mice were subordinate and did not form territories. Intruder mice with winning or losing experience in prior paired encounters, or those with no fighting experience, were introduced individually into the colony for 30 minute periods. These intruders were attacked by the dominant members of the colony, and the fighting outcomes were strongly dependent upon the fighting experience of the intruder. Intruders with losing or no fighting experience engaged in little mutual fighting with residents, were easily defeated, and terminated attacks by engaging in subordinate behaviors. Intruders with winning experience fought vigorously with residents, attacked and, in many cases, defeated residents. These results suggest that relatively little winning experience gained in earlier paired encounters may be sufficient to overcome the various fighting advantages enjoyed by a dominant territorial holding member of a colony.     

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.     

Short-term early exposure to pups alters infanticide in adulthood in male but not in female wild house mice (Mus domesticus)

Male and female wild house mice (Mus domesticus) were allowed to remain in the cage of their parents until 30-35 days of age. When a second litter was delivered, the first litter was exposed to the younger pups for 2-10 days. In adulthood the male and female mice that had been exposed to pups as juveniles and an additional group that had cohabitated with their parents for the same length of time but were not exposed to pups were tested for infanticidal behavior. The frequency of infanticide by the adult female mice was not significantly different (55% vs. 70%, respectively). In contrast, the adult males that were exposed to pups as juveniles were significantly less likely to kill young in adulthood when compared with males that were not similarly exposed (35% vs. 80%, respectively). These data further demonstrate the strong influence of experience on the expression of infanticide by male mice and its relative unimportance to the expression of female infanticide.     

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.     

Role of female aggression in prevention of infanticidal behavior in male common voles,Microtus arvalis (Pallas, 1779)

Infanticidal behavior of male common voles (Microtus arvalis) was investigated in relation to the age of unfamiliar pups. Sires from 18 pairs were removed after parturition of their offspring and replaced by unfamiliar males at different ages of the neonates. In group 1, containing six females with their offspring, the new male was introduced into the females' cages on day 1 after the parturition. In group 2 the new male was introduced on day 5 after parturition and in group 3 on day 9 after parturition. The male was removed after 3 days and the neonates recounted. Male common voles killed up to 100% of the neonates in litters containing neonates younger than 9 days by rapid bites to the head of the neonates (groups 1 and 2, mortality rates of 0.86 and 0.38). However, with older pups, a mortality rate of 0.06 was observed while 33% of the intruder males showed signs of injuries (group 3). These findings show that infanticidal behavior of male common voles represents one factor of pup mortality. The results are discussed in relation to changes in the degree of maternal aggression and in the context of the social system of the common vole for solving the conflict between postpartum estrous mating and infanticidal behavior of male common voles. Aggr. Behav. 23:293–298, 1997. © 1997 Wiley-Liss, Inc.