Replacement female house sparrows regularly commit infanticide: gaining time or signaling status?

Although the killing of unrelated young (usually designed asinfanticide) has been typically considered a male behavior,recent research has shown that females may commit infanticideeven more frequently than do males. In rodents and primates,female infanticide represents a strategy associated to competitionfor resources or infant exploitation, but little is known aboutthe causes and reproductive consequences of the killing of conspecificsby females in other vertebrates. In the present article, I focuson infanticide committed by females that replace mates of territorialmales in a population of the house sparrow. I show that (1)replacement females regularly committed infanticide, (2) experiencedfemales committed infanticide more frequently than did novelfemales and tended to select polygynous males to take over theirnests, and (3) laying date and reproductive success after aterritory takeover did not differ between infanticidal and noninfanticidalfemales. These results seem to indicate that infanticide hasnot evolved in females because of the short-term reproductivebenefits it accrues to the perpetrator. I suggest that the killingof unrelated young by females relates to dominance status amongpotential female breeders and that this behavior benefits theperpetrators in terms of mate selection.     

Changes in incidence of infanticidal and parental responses during the reproductive cycle in male and female wild mice Mus musculus

Most studies of infanticide in rodents have been carried out on laboratory animals. In the present study, pairs of infanticidal male and female wild mice were observed for changes in their responsiveness to alien pups during the reproductive cycle. Females killed pups during pregnancy, adopted alien pups during the lactation period, and killed pups again a month after the weaning of their offspring. In males, the transition from infanticidal to parental responses occurred as early as the first half of their mates' pregnancy, and only half of them resumed infanticide a month after the weaning of their litters. Subsequent experiments showed that two independent factors, the experience of copulation and cues from the pregnant female, accounted for the cessation of infanticide and onset of parental care in the male. The adaptive value of the co-existence of multiple mechanisms underlying the cessation of infanticide in male and female house mice is discussed with respect to the social life of this species.     

Infanticide by male house sparrows: gaining time or manipulating females?

The killing of genetically unrelated young by males has been viewed as a strategy that forces victimized females to advance the onset of their next fertile period, thus infanticidal males gain a time advantage that may be crucial to maximize reproductive success. Among females that may raise several broods in a year, a failure occurring relatively earlier in the time-course of the previous breeding attempt may result in an increased investment in the next breeding attempt. This female strategy may be exploited by males in their own interest, and may strongly select for male infanticidal behaviour. I demonstrate that, in the house sparrow, females mated with infanticidal males re-laid earlier, initiated more breeding attempts and fledged more offspring than females mated with non-infanticidal males. These results suggest that both the time saving and the manipulation of female investment are independent mechanisms conferring advantages that may have selected for male infanticide in the studied population.     

Maternal aggression as a deterrent to infanticide in Peromyscus leucopus and P. maniculatus

Adult male and female white-footed mice (Peromyscus leucopus) and deermice (P. maniculatus) from sympatric populations commit infanticide on neonates of either species. A laboratory experiment was conducted to determine whether aggression in maternal females could effectively deter infanticidal intruders. Females of both species exhibited post-partum aggression and dominated intruders of either sex or species in 83 of 88 trials. In the absence of the mother, neonates were attacked by intruders in 82 out of 84 trials. Maternal females were considerably more aggressive than anoestrous females. The implications for female territorially as a mechanism to prevent infanticide are discussed.     

Infanticide in black capuchin monkeys (Cebus apella nigritus) in Iguazú National Park, Argentina

We report here one observed and two potential cases of infanticide during a brief period of 1 month after a dominant male replacement in one group of black capuchin monkeys in Iguazú National Park, Argentina. We also compile infant disappearances and demographic data in seven groups followed from 1-14 years. Behavioral and molecular data showed that the probability that an infanticidal male would kill his own progeny is very low in this species. Females that lost infants less than 6 months old had shorter interbirth intervals than females whose infants survived (14.12 ± 5.32 months, n=17 vs. 20.42 ± 5.65 months, n=34). Females whose infants die shortly after takeovers mate with the presumed infanticidal male during the most fertile days of their subsequent estrous periods giving this male a high probability of siring the new progeny. We recorded 181 proceptive periods and 52 births from 18 adult females in two groups. Most proceptive periods were concentrated during a conception season, but there was an increase in sexual behavior after male takeovers. Seven females copulated while pregnant after the observed male takeover, an unusual behavior in this species in years of group stability. Of 24 infants born during takeover years, 62.5% did not survive the first year, whereas only 22.5% of 80 infants died in years without male replacements. We found a significant positive association between infant mortality and male takeovers, but not with food provisioning. The main cause of infant mortality in this population is associated with male takeovers. Our results suggest that infanticide can have an important effect on the behavior of this species, selecting for female behaviors that function to reduce infanticide risk.     

Infanticide among free-ranging langurs (Presbytis entellus) at jodhpur (Rajasthan/India): Recent observations and a reconsideration of hypotheses

Considerable disagreement characterizes the debate concerning frequency, causation, and function of infanticide in connection with adult male replacements in bisexual one-male troops of hanuman langurs (Presbytis entellus). Detailed observations are presented about two noninfanticidal and three infanticidal male changes including six eye-witness and five presumed cases of infanticide within three langur troops during a long-term study at Jodhpur, Rajasthan, India. The results do not support any explanatory hypotheses focussing on social crowding, regulation of population density, social stress, sexual frustration, incest avoidance, or social bonding, but are in general though not total agreement with the reproductive advantage hypothesis: mainly unrelated infants were killed (one possible exception), the infanticidal male generally sired the subsequent offspring (one exception), and the mean interbirth interval subsequent to infanticide is by 2.1 months shortened. Likewise, several cases of stress induced abortions occurred. It is demonstrated that postconception estrous behaviour is by no means a female counterstrategy to infanticide in order to confuse males concerning the issue of paternity, since an infanticidal male did not spare the subsequent offspring of mothers who copulated with him during pregnancy and pregnant females did not discriminate between fathers and non-fathers.     

Presence of a conspecific increases superparasitism but not infanticide under self‐ and conspecific superparasitism in a semisolitary parasitoid,Echthrodelphax fairchildii (Hymenoptera: Dryinidae)

Female parasitoids are expected to avoid superparasitism (ovipositing in and/or on parasitized hosts) when unparasitized hosts are available. However, when the supply of unparasitized hosts is restricted, they are expected to self‐ as well as conspecifically superparasitize. One of the cues of a reduced availability of unparasitized hosts is the presence of a conspecific. Moreover, if the focal species can perform infanticide, after encountering a conspecific female, the females are expected to kill eggs existing in and/or on hosts when superparasitizing, because the eggs are more likely to be laid by others. In this study we investigated whether females of an infanticidal semisolitary parasitoid, Echthrodelphax fairchildii, increase their frequencies of superparasitism and infanticide after encountering a conspecific female. Echthrodelphax fairchildii females are capable of discriminating between self‐ and conspecific superparasitism until up to 0.75 h after the first egg was laid (self‐superparasitism frequency < conspecific superparasitism frequency). As expected, the female parasitoids were more likely to perform self‐ and conspecific superparasitism after they had encountered a conspecific. In particular, the self‐superparasitism frequency increased highly within a short period after the first oviposition, so that no difference between the self‐ and conspecific superparasitism frequencies was found. In contrast, the infanticidal‐probing frequency remained extremely low, irrespective of whether or not the female parasitoids had encountered a conspecific. Moreover, when superparasitizing, females usually laid female eggs. Possible causes for the low frequency of infanticidal probing and the female‐biased sex ratio are discussed.     

Is Mating Alone Enough to Inhibit Infanticide in Male Bank Voles?

Infanticide, the killing of conspecific young, is commonly recognized as an adaptive behavioural strategy enhancing the fitness of the perpetrator. Infanticide is supposed to be inhibited in several male rodent species after mating with a time lag to the time when perpetrators own offspring would be born. This is because males with no parental care do not recognize their own offspring. It has been suggested that copulation alone is enough to inhibit infanticidal behaviour in male rodents. Infanticidal behaviour occurs in more than 50% of male bank voles (Myodes glareolus), and offspring loss because of infanticide may have a great effect on breeding success and population recruitment. In a laboratory experiment, we studied whether infanticidal male bank voles after successful mating stop the killing of pups. Infanticidal males were paired with a female until successful copulation. After the young were born, the males’ infanticidal behaviour was studied from the time of expected birth of own pups until their post‐weaning age. We predicted that mated infanticidal males are inhibited from committing infanticide especially during the time period when pups are less than 10 d old. Against our prediction, 67% of the infanticidal males continued the killing of pups in the age of 3 d. Infanticidal behaviour remained stable, and half of the males were infanticidal still at the age of weaning of pups. Our results are contradictory to previous studies, as we observed no inhibition of infanticide during early life of pups nor increase in infanticide again when their own offspring would have reached the ‘safe’ age and size after weaning. We suggest that mating alone is not sufficient to inhibit infanticide. Thus, we suggest that other cues of the female with whom the male mated with or on her territory are needed for inhibition to occur.     

Communal nesting and communal nursing in house mice,Mus musculus domesticus

The functional significance of communal nesting and nursing is poorly understood. Female house mice often communally nest, and within these communal nests females appear to indiscriminately nurse all pups, a rare trait for any mammal. In this study, the hypothesis that communal nesting provides protection from conspecific infanticide was tested and supported in semi-natural populations of house mice. Conspecific infanticide in single-mother nests (69%, N = 412) was twice that in communal nests (33%, N = 508). Because this major benefit of communal nesting does not require communal nursing, direct benefits to communal nursing itself were tested. Most proposed benefits should result in heavier weaning weights, but no differences were found between communal and single nests in the semi-natural populations. If communal nursing is to be avoided in communal nests, dams must recognize their own pups. Retrieval tests conducted in the laboratory produced equivocal results. Dams discriminated between pups that differed in age, but not between their own and other age-matched pups. The major survival advantage of communal nesting, coupled with the failure to find nutritional advantages for communally nursed pups, supports a recent suggestion that communal nursing is an unavoidable consequence of communal nesting. This hypothesis is further strengthened by data indicating that communal nesting partners tend to be kin, thereby providing inclusive fitness benefits to communal nursing. Although costs of communal nursing were proposed and tested, no such costs were found. We also show from 15 observations of infanticide that all classes of adults (territorial and non-territorial males, pregnant and non-pregnant females) are infanticidal. These observations are in conflict with previous laboratory studies.     

Infanticide and effectiveness of pup protection in bank voles: does the mother recognise a killer?

Infanticide, the killing of conspecific young, has been documented in numerous species of mammals, especially rodents. In that infanticide is costly to the victim mother, natural selection should favour counter-strategies by females to protect their pups. We studied the frequency of infanticide by male and female bank voles (Clethrionomys glareolus) and the effectiveness of dams in recognising and deterring infanticide. In trials in which unprotected pups were exposed to voles of both sexes, one third of male and female intruders killed pups. When mothers were present at the nest site, not a single female and only 2 of 25 males were able to commit infanticide. Females acted aggressively towards all intruders and hence did not discern between infanticidal and non-infanticidal males and females. Aggression of dams against any intruder indicates that all strange individuals near the nest site of a territorial species form an equal threat to pups. However, the presence of the aggressive dam is sufficient to deter most intruders from harming offspring by keeping them at a distance from the nest site. Heat run before mating, in a species with postpartum oestrus and vulnerable pups in the nest, also might lure potential infanticidal males away from the nest site and obscure the nest location. Received in revised form: 17 October 2001 Electronic Publication     

Infanticide and Maternal Offspring Defence in European Rabbits under Natural Breeding Conditions

Infanticide is an important source of mortality of dependent offspring in several mammal species, whereas female conspecifics are often the perpetrators. This has led to maternal counter‐strategies, such as the defence of the nests. However, cases of infanticide are hard to detect in the field, and studies on maternal offspring defence behaviour under natural breeding conditions are scarce. We conducted such a study on the European rabbit (Oryctolagus cuniculus), which is usually considered to show low maternal care. The study was carried out over 5 yr on a field enclosure population. We (1) studied infanticide rates and the impact of potential determinants: the group density and age structure of the females’ rank hierarchy within the groups; we used the latter as an estimator of social group stability. We (2) studied if mothers defend their breeding burrow against approaching, potentially infanticidal females. Overall, we recorded infanticide in 5% of all litters; infanticide was the cause in 12% of cases of litter mortality. The proportion of infanticide was 7% higher in groups where same‐age females occupied successive rank positions than in groups where the females’ rank hierarchy had a more heterogeneous and linear age structure. We hypothesize that social instability in the former groups was the reason for the increased infanticide risk. Infanticide rates were not correlated with group density and did not differ among mothers with different social ranks. Infanticide occurred exclusively during the first 10 d after parturition. During this time, mothers stayed closer to their breeding burrows than shortly before parturition or during later lactation. Moreover, mothers were more aggressive against other females in proximity to their breeding burrow than in more distant areas. We suggest that the pattern of spacing behaviour and intrasexual aggression of rabbit mothers are an adaptive response to the occurrence of female infanticidal behaviour.     

Distinct preoptic‐BST nuclei dissociate paternal and infanticidal behavior in mice

Paternal behavior is not innate but arises through social experience. After mating and becoming fathers, male mice change their behavior toward pups from infanticide to paternal care. However, the precise brain areas and circuit mechanisms connecting these social behaviors are largely unknown. Here we demonstrated that the c‐Fos expression pattern in the four nuclei of the preoptic‐bed nuclei of stria terminalis (BST) region could robustly discriminate five kinds of previous social behavior of male mice (parenting, infanticide, mating, inter‐male aggression, solitary control). Specifically, neuronal activation in the central part of the medial preoptic area (cMPOA) and rhomboid nucleus of the BST (BSTrh) retroactively detected paternal and infanticidal motivation with more than 95% accuracy. Moreover, cMPOA lesions switched behavior in fathers from paternal to infanticidal, while BSTrh lesions inhibited infanticide in virgin males. The projections from cMPOA to BSTrh were largely GABAergic. Optogenetic or pharmacogenetic activation of cMPOA attenuated infanticide in virgin males. Taken together, this study identifies the preoptic‐BST nuclei underlying social motivations in male mice and reveals unexpected complexity in the circuit connecting these nuclei.     

Determinants of female dispersal in Thomas langurs

Female dispersal occurs in a number of primate species. It may be related to: avoidance of inbreeding, reduction in food competition, reduction of predation risk, or avoidance of infanticide in combination with mate choice. Female dispersal was studied for a 5-year period in a wild population of Thomas langurs (Presbytis thomasi) that lived in one-male multi-female groups. Juvenile and adult individuals of both sexes were seen to disperse. Females appeared to transfer unhindered between groups, mostly from a larger group to a recently formed smaller one. They transferred without their infants and when not pregnant, and seemed to transfer preferentially during periods when extra-group males were harassing their group. During these inter-group encounters extra-group males seemed to try to commit infanticide. Thus, the timing of female transfer was probably closely linked to infanticide avoidance. Moreover, females seemed to transfer when the resident male of their group was no longer a good protector. The observations in the present study suggest that females transferred to reduce the risk of infanticide. Female dispersal may have another ultimate advantage as well, namely inbreeding avoidance. Due to the dispersal of both females and males the social organization of Thomas langurs was rather fluid. New groups were formed when females joined a male; male takeovers were not observed. Bisexual groups had only a limited life span, because all adult females of a bisexual group could emigrate. This pattern of unhindered female dispersal affects male reproductive strategies, and in particular it might lead to infanticidal behavior during inter-group encounters. Am. J. Primatol. 42:179–198, 1997. © 1997 Wiley-Liss, Inc.     

Face to face with the woolly spider monkey. Review of faces in the forest: The Endangered Muriqui Monkeys of Brazil,by Karen B. Strier. New York,Oxford University Press,Inc., 1992, 138 pp, $49.50

During an intertroop encounter, an infanticide was observed in a population of ringtailed lemurs (Lemur catta) at Berenty Reserve, Madagascar. The killer was a male that had not been previously observed to mate with any females in the infant's troop. This observation, combined with other observations of infanticidal behavior by males at Berenty Reserve and the Duke University Primate Center, is consistent with the hypothesis that infanticide is a reproductive tactic for some male ringtailed lemurs. © 1994 Wiley-Liss, Inc.     

Severe Aggression Among Female Pan troglodytes schweinfurthii at Gombe National Park, Tanzania

Aggression is generally more severe between males than between females because males gain greater payoffs from escalated aggression. Males that successfully defeat rivals may greatly increase their access to fertile females. Because female reproductive success depends on long-term access to resources, competition between females is often sustained but low key because no single interaction leads to a high payoff. Nonetheless, escalated aggression can sometimes immediately improve a female’s reproductive success. Resisting new immigrants can reduce feeding competition, and infanticide of other females’ young can increase a female’s access to resources. East African chimpanzees live in fission-fusion communities in which females occupy overlapping core areas. Growing evidence indicates that reproductive success correlates with core area quality, and that females compete for long-term access to core areas. Here we document 5 new cases of severe female aggression in the context of such competition: 2 attacks by resident females on an immigrant female, a probable intracommunity infanticide, and 2 attacks on a female and her successive newborn infants by females whose core areas overlapped hers. The cases provide further evidence that females are occasionally as aggressive as males. Factors influencing the likelihood and severity of such attacks include rank and size differences and the presence of dependable allies. Counterstrategies to the threat of female aggression include withdrawing from others around the time of parturition and seeking male protection. We also discuss an unusual case of a female taking the newborn infant of another, possibly to protect it from a potentially infanticidal female.     

Role of pregnancy and parturition in induction of maternal behavior in prairie voles (Microtus ochrogaster)

In prairie voles (Microtus ochrogaster), most virgin females are infanticidal. To determine the onset of maternal responsiveness, female prairie voles were tested for maternal behavior as virgins and at different times throughout pregnancy. Female voles that were infanticidal as virgins by and large remained infanticidal throughout pregnancy. In contrast, about 30% of voles that were maternal as virgins became infanticidal during pregnancy. To test whether events associated with parturition facilitate the onset of maternal behavior, females had their litters delivered by Caesarean section within a day of expected delivery or were allowed to give birth naturally with sham surgery occurring shortly before or after birth. Females that gave birth naturally were fully maternal and did not attack unrelated pups, but females subjected to artificial delivery remained infanticidal. This suggests that events closely related to parturition are crucial for full development of maternal behavior in female prairie voles.     

Social suppression of female reproductive maturation and infanticidal behavior in cooperatively breeding Mongolian gerbils

In several cooperatively breeding species, reproductively suppressed, nonbreeding females are attracted to infants and routinely provide alloparental care, while breeding females may attack or kill other females' infants. The mechanisms underlying the transition from alloparental to infanticidal behavior are unknown. In this study, we tested the hypothesis that this transition is associated with cessation of reproductive suppression and onset of ovarian activity in the Mongolian gerbil (Meriones unguiculatus), a cooperatively breeding rodent. Young female gerbils were housed with their natal family (FH), with a female pairmate (PH) or singly (SH). When females were either 11-13 or 16-18 weeks of age, we characterized their behavioral responses to an unfamiliar pup, reproductive development, and plasma progesterone, cortisol, and prolactin concentrations. In both age groups, FH females were significantly less likely to attack pups than PH or SH females and in fact never did so. FH females also had smaller ovaries and uteri, less developed scent glands, and lower progesterone levels, and were more likely to be anovulatory than PH or SH females, especially in the 11- to 13-week-old age group. Prolactin concentrations did not differ with reproductive status but were significantly higher in females that did not attack pups than in those that did. We found no other significant associations, however, between reproductive or endocrine measures and behavioral responses to pups. These results suggest that cohabitation with the natal family inhibits both infanticidal behavior and reproductive maturation in young female gerbils but that these two effects may not be causally related.     

Infanticide and social flexibility in the genus <Emphasis Type="Italic">Gorilla</Emphasis>

Based on the cases of infanticide by male mountain gorillas reported from the Virunga volcanic region, the socioecological and life history features of gorillas satisfy the conditions for which infanticide may be expected. However, there are considerable variations in the occurrence of infanticide between habitats. We analyze the recent reports of infanticides that were directly observed or are suspected based on field evidence in two populations of eastern and western lowland gorillas (Kahuzi and Mbeli Bai, respectively) along with previous reports on mountain gorillas, and consider which social features are linked with and which factors influence the occurrence of infanticide in the gorilla populations. All victims were suckling infants and most of them were killed by males who seemed unrelated to them. Dependent infants are most vulnerable to infanticide when the protector male (its putative father in most cases) is absent, and so male protection ability seems to be important in determining female transfer decisions. Two cases observed in Kahuzi suggest that the infanticidal male may discriminate between infants to accept and those to kill according to his previous interactions with their mothers. Mating for a prolonged period prior to parturition is necessary for immigrant females to avoid infanticide by the new male of the group that they join. Infanticide was usually associated with female transfer, and the patterns of female association at transfer may shape variations in social structure between populations. Female mountain gorillas prefer large groups with multiple males and tend to transfer alone in order to seek more protection against infanticide in Virunga. By contrast, female eastern and western lowland gorillas tend to transfer with other females to small groups or solitary males, and maturing silverbacks take females to establish new groups through group fission in Kahuzi and Mbeli Bai. These differences may result in more multi-male and larger groups in the Virungas than in Kahuzi and Mbeli Bai. Rapid changes in density of gorilla social units and their relations following drastic environmental changes caused by recent human disturbances may also increase the probability of infanticide.     

Infanticide by Male Lions Hypothesis: A Fallacy Influencing Research into Human Behavior

Recently, familial abuse and killing of children have been correlated with infanticidal behavior by nonhuman male animals which is postulated to be genetic. However, infanticide by males as an evolutionary mechanism is unlikely to occur in primates, and is equally unlikely in lions. To investigate the sexual selection hypothesis of infanticide for lions, four questions should be considered: (1) because they all mate freely with lionesses, are male pride lions closely related? (often they are not), (2) do males kill the young cubs when they join a pride? (few such cases have been observed), (3) do the females then mate with the new males to produce offspring? (yes), and (4) do the males remain with the pride for over two years to protect this new generation? (often not). Field data indicate that in NO instance do we know that male lions killed cubs in a new pride, mated with their mother, and then remained with the pride to protect their own young. Rather, female lions may kill more cubs than males and certainly cause many more cub deaths by allowing them to starve, [ infanticide by male lions, infanticide hypothesis, faulty science]     

Polyandry enhances offspring survival in an infanticidal species

The adaptive significance of polyandry is an intensely debated subject in sexual selection. For species with male infanticidal behaviour, it has been hypothesized that polyandry evolved as female counterstrategy to offspring loss: by mating with multiple males, females may conceal paternity and so prevent males from killing putative offspring. Here we present, to our knowledge, the first empirical test of this hypothesis in a combined laboratory and field study, and show that multiple mating seems to reduce the risk of infanticide in female bank voles Myodes glareolus. Our findings thus indicate that females of species with non-resource based mating systems, in which males provide nothing but sperm, but commit infanticide, can gain non-genetic fitness benefits from polyandry.