Male Influx, Infanticide, and Female Transfer in Macaca radiata radiata

In bonnet macaques, males usually disperse between groups and females remain philopatric, but researchers have reported female transfer. We report a rare case of male influx during the mating season in our bonnet macaque study group in the Anaimalai Hills. The density of bonnet macaques in the study region was unusually high. The study group had a single, crippled adult male with a long tenure and 5 adult females. During the mating season, adult females approached and mated with outgroup males, and then several males entered the group. The adult male left the group without any resistance. The incoming males mated with 3 receptive females, forcibly mated with 2 lactating females, and attacked and killed 2 infants. During the influx, 2 outgroup females joined the group. The data suggest that male influxes provide an opportunity for infanticide and female transfer, which can have important fitness consequences even in species in which they rarely occur.     

Within-group cannibalism by adult male chimpanzees

In the Mahale Mountains National Park, Tanzania, a young adult male chimpanzee was observed to feed on a 3-month-old male infant of the same unit-group. Four other adult males and an adult female shared the carcass. The mother of the victim had immigrated from a neighboring unit-group four years previously. Circumstantial evidence strongly suggests that the first-observed cannibal male also killed the infant. The adult male and the mother of the victim had been familiar socially and sexually with each other since the female immigrated. Since the mother of the victim had usually been ranging in the peripheral part of the unit-group's range, i.e., the overlapping area of the two unit-group's ranges during pregnancy and soon after birth, the infanticidal male might have had reason to suspect the paternity of her infant. Four such cases of within-group cannibalism by adult males suggest that the female range and association pattern before and after parturition are key factors allowing an infant to survive. The possibility of male-biased infanticide is also discussed.     

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.     

Observed infanticides following a male immigration event in black howler monkeys, Alouatta pigra, at Palenque National Park, Mexico

This study describes two cases of directly observed and one case of nearly observed infanticide after an adult male immigrated into a multimale–multifemale group of black howler monkeys (Alouatta pigra) at Palenque National Park, Mexico. The immigrant male entered the group alone, injured the central adult male, presumably evicted the noncentral adult male, and killed all three young infants present over the course of three consecutive days in February 2010. Three weeks after the infanticide events, the three adult females who lost their infants were observed to sexually solicit and copulate with both the infanticidal male and the injured central male. Multimale mating is an effective reproductive strategy that females employ to confuse paternity and reduce the risk of infanticide, but the extent to which promiscuous mating after infanticide events is part of a counterstrategy in this species is still unknown. More cases of infanticide will need to be observed to assess the degree to which infanticide avoidance shapes the social system of the black howler monkey.     

DNA analyses support the hypothesis that infanticide is adaptive in langur monkeys.

Although the killing of dependent infants by adult males is a widespread phenomenon among primates, its causes and consequences still remain hotly debated. According to the sexual selection hypothesis, infanticidal males will gain a reproductive advantage provided that only unrelated infants are killed and that the males increase their chances of siring the next infants. Alternatively, the social pathology hypothesis interprets infanticide as a result of crowded living conditions and, thus, as not providing any advantage. Based on DNA analyses of wild Hanuman langurs (Presbytis entellus) we present the first evidence that male attackers were not related to their infant victims. Furthermore, in all cases the presumed killers were the likely fathers of the subsequent infants. Our data, therefore, strongly support the sexual selection hypothesis interpreting infanticide as an evolved, adaptive male reproductive tactic.     

Mating Strategies in Relation to Sexually Selected Infanticide in a Non-Social Carnivore: the Brown Bear

Based on the sexually selected infanticide (SSI) hypothesis, infanticide can be an adaptive mating strategy for males, but this is has rarely been documented in non‐social mammals. This phenomenon should not benefit females, so one would expect females to evolve mating counter strategies in order to protect their infants from infanticidal males. Cases of SSI are extremely difficult to document in the field, especially for non‐social species. Using field observations and genetic methods, we describe mating strategies employed by both sexes of brown bears (Ursus arctos) in relation to SSI. We present evidence for the first time suggesting that infanticide is an adaptive male mating strategy in this non‐social carnivore, as all requirements for SSI are fulfilled (1) infanticide shortens the time to the mother's next estrus, (2) the perpetrator is not the father of the killed infants, and (3) putative perpetrators sire the next litter. Moreover, all infanticide cases occurred during the mating season. We expected that primarily immigrant males were infanticidal, as in social species. However, we found that resident adult males commonly committed infanticide. Perhaps they recognize females they have mated with previously. Moreover, we used DNA‐based parentage testing to demonstrate a minimum of 14.5% of multiple paternities (up to 28% for litters with at least three young). Female promiscuity to confuse paternity may be an adaptive counter strategy to avoid infanticide.     

Infanticide and cannibalism by male chimpanzees at Ngogo, Kibale National Park, Uganda

Researchers have documented infanticide by adult males in four wild chimpanzee populations. Males in three of these have killed infants from outside of their own communities, but most infanticides, including one from Kanyawara, in Kibale National Park, Uganda, took place within communities. Here we report two new cases of infanticide by male chimpanzees at a second Kibale site, Ngogo, where the recently habituated chimpanzee community is the largest yet known. Both infanticides happended during boundary patrols, which occur at a high frequency there. Patrolling males attacked solitary females who were unable to defend their infants successfully. The victims were almost certainly not members of the Ngogo community. Males cannibalized both infants and completely consumed their carcasses. These observations show that infanticide by males is widespread in the Kibale population and that between-community infanticide also happens there. We discuss our observations in the context of the sexual selection hypothesis and other proposed explanations for infanticide by male chimpanzees. The observations support the arguments that infanticide has been an important selective force in chimpanzee social evolution and that females with dependent infants can be at great risk near range boundaries, but why male chimpanzees kill infants is still uncertain.     

Infanticide risk and infant defence in multi-male free-ranging sooty mangabeys, Cercocebus atys

For years, infanticide by males was thought to be unlikely in multi-male primate species. Recent studies have, however, presented evidence of infanticide in such species and a recent model by Broom and colleagues predicts that males’ age and rank influence the occurrence of infanticide: youngest and highest-ranking immigrant males are more likely to commit infanticide than their older and lower-ranking counterparts if putative fathers fail to protect infants. I collected data on adult free-ranging sooty mangabey females in the Taï National Park, Ivory Coast, over 11 months including a birth and a mating season. Infanticide had been previously reported in captivity for this species, but not in the wild. Several males entered the group prior to and during the mating season. As predicted by the model, only the more dominant immigrant ones attacked mother-infant pairs significantly more often than did other males. Mothers often reacted with counter-attacks. Potential fathers guarded and supported infants and mothers throughout the period of infant vulnerability. Furthermore, as only one of seven infants died despite 136 observed attacks on mother-infant pairs and unattended infants by immigrant males, we conclude that cooperation between putative fathers and mothers represents an effective protection against infanticide.     

Tail raising by baboon mothers toward immigrant males

Behavioral responses of adult females to recently immigrated adult males were examined in two groups of chacma baboons in the Moremi Wildlife Reserve, Botswana. Mothers carrying infants respond negatively by raising their tails, avoiding, and screaming when in proximity to immigrant males. These responses are not given by mothers when their infants are away from them or by females who do not have infants. Also, the negative responses by mothers carrying infants are given only to immigrant males and not to long-term resident males. These observations are in concordance with the growing evidence of infanticide in savanna baboon societies: mothers would be expected to show negative responses to potentially aggressive males, particularly immigrants. There was evidence to suggest that mothers respond negatively to immigrants only insofar as these males could not have sired their infants. If confirmed by subsequent observations, this result would lend support to the sexual selection model of infanticide.     

Spatial relationships between recent mothers and other troop members in red howler monkeys (Alouatta seniculus)

Data on spatial relationships between eight mothers with young infants and other troop members collected during a study of free-ranging red howlers are used to examine two predictions: (a) that among immature and adult females, individuals showing the greatest interest in young infants are those who would incur the greatest benefit and lowest costs in doing so, and, (b) that since red howler infants may be killed by males, the male who spends most time near an infant is its likely father. Results indicate that females with infants spent less time near the new mother than did immature females and adult females without infants. Those dominant males who were the infant's likely father spent significantly more time near the new mother than did the subordinate males.     

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.     

Sexual selection in the monogamous barn swallow (Hirundo rustica). II. Mechanisms of sexual selection

Mechanisms of sexual selection in the monogamous, sexually dimorphic barn swallow (Hirundo rustica) were studied during a seven-year period. First, the sex ratio of reproducing adults was male-biased, and mated males had significantly longer tail ornaments than unmated males. Secondly, some of the unmated individuals later committed infanticide and became mated with the mother of the killed brood. Fathers of killed broods had significantly shorter tails than other males, and there was a tendency for infanticidal males to have longer tail ornaments than other unmated males. Thirdly, long-tailed male barn swallows were more successful in acquiring extra-pair copulations than other males, and females involved in extra-pair copulations, as compared to females not involved in such copulations, had mates with shorter tail ornaments. Fourthly, male barn swallows having long tails as compared to short-tailed males acquired mates in better body condition. Females mated to long-tailed males reproduced earlier, laid more eggs and were more likely to have two clutches than were females mated to short-tailed males. Finally, females mated to long-tailed males put more effort into reproduction than did other females, as evidenced by their relatively larger contribution to feeding of offspring. Thus, at least five different components of sexual selection affected male reproductive success. Selection arising from differential success during extra-pair copulations, differential reproductive success and differential male reproductive effort thus accounted for most of the selection on tail ornaments in male barn swallows.     

Attacks on neonates by a male mangabey (Cercocebus atys)

Aggressive behavior by an adult male toward selected infants and their mothers was observed during a long-term study of reproduction in a captive social group of sooty mangabeys (Cercocebus atys). The highest-ranking adult male in this group was observed to attack and bite three neonates out of a total of 13 infants born in 1982. All three attacks were directed attacks in which infants were grabbed from their mothers and bitten in the head. The first infant was fatally injured; the other two probably would have sustained fatal wounds had the male's canines not been blunted beforehand and had observers not intervened. The attacks were preceded by a pattern in which the male persistently stalked or chased the mother-infant pairs, a behavior first observed in the hours immediately following parturition. Unlike attacks in wild baboon groups following male immigration, these attacks on infants occurred in a stable social group in which the male attacker had been a lifelong resident. This male, however, had gained alpha rank only 3 months before attacking the first infant. These attacks, in the context of other evidence of aggression and wounding, are discussed relative to current models of infanticide in primates.     

A case study of mother-son transfer in mountain gorillas

In mountain gorillas (Gorilla g. beringei), male immigration in bi-sexual units is rare. This paper presents the case of a nearly weaned male infant gorilla who followed his mother in her transfer. This case was recorded in the study population at the Kariske Research Center in 1988. The data come from observation in Group B (on 12 days just prior to the transfer and on 54 days after the transfer over a period of 6 months). The situation of the infant did match the conditions in which infanticide occurs in gorillas, but he was not killed, despite receiving male aggression and being wounded twice. In fact, both the mother and the infant received male aggression more frequently than the long term residents in the group. The aggression received by the mother decreased after she mated with the males and after she weaned the infant. The aggression received by the infant, however, did not decrease after his mother mated with the males, and increased in intensity. The infant reacted fearfully to male aggression, in marked contrast to his mother, who reacted either with indifference, or by simply avoiding the males. The aggression eventually stopped, and the infant became a blackback in Group B. Evolutionarily, the death of the infant would not have markedly accelerated the mother's return to estrus, but the death of the infant could still have benefitted the males, by decreasing the reproductive output of a competitor. Adult male gorillas are also presumably selected to resist male immigration. Proximately, the aggression directed towards the infant was not related to mating access to the mother. The sex of the infant may contribute to explain the post-transfer male aggression, but data on the integration of old female infants in a new group is needed to test whether the sex of the infant has an effect on their vulnerability to infanticide. Also, the intense fear displayed by the infant may have played a role in prompting male aggression.     

An attempted within-group infanticide in wild chimpanzees

Two high-ranking adult male chimpanzees (Pan troglodytes) of M group in the Mahale Mountains National Park, Tanzania, tried to get a newborn female infant of an adult female who was born in M group. The mother was not seen to mate with these adult males during the probable conception cycle of the infant, but she disappeared from the group during the later cycle, when she may have been inseminated by a male of one of the neighboring unit groups. The adult males failed to get the infant because the grandmother of the newborn and her female friend cooperated to protect the mother and infant from attacks by the males. The sexual selection hypothesis for infanticide by adult male chimpanzees holds for this observed case. The sudden disappearance of another infant, a healthy female, strongly suggests the killing of female infants too. Therefore, the asserted male-biased infanticide in chimpanzees appears to be less tenable.     

Mother-infant cannibalism in thick-tailed bushbabies (Galago crassicaudatus umbrosus)

Mother-infant cannibalism in species of galagos as in several other species of non-human primates is a common phenomenon. In non-human primates kept in laboratory conditions many of the observed cases of cannibalism were not associated with starvation and with infanticide. Cannibalism in galagos was observed in at least five different species. In several laboratories, like the Duke University Primate Center, the frequencies of cannibalism in galagos species in captivity have been reduced by the isolation of pregnant female before the parturition from her companions, especially adult males. At the Primate Behaviour Research Group (University of Witwatersrand, Johannesburg, South Africa) three cases of cannibalism were observed in twoGalago crassicaudatus umbrosus' mothers before the end of the third day after birth. To understand the reasons why the mothers cannibalize their own infants, it was decided to analyze the mother-infant interaction which preceded the death of the infants. InGalago crassicaudatus twin and triplet births are very common. In one of our two observed mothers who cannibalized their infants, there was one triplet birth. In this study the two pregnant females were isolated in two separated cages ten days before giving birth. One of the two observed mothers gave birth to triplets, the other had a single birth. At the end all four infants were cannibalized. In all cases the cannibalization started after the infant's death. The infants' deaths were caused by lack of maternal care which caused them to starve. The results show that the triplet's mother differed in some of her behaviour towards her infants. In one of the cannibalized infants behaviours such asNipple andMother Passive Prevent were never seen before death. In our cases it seems that cannibalism was probably due to the laboratory condition that for generation to generation caused stress to the mothers and changed their maternal behaviours, which lead to the death of the offspring which after death became a consumable resource.     

Male Infanticide in the Golden Snub-Nosed Monkey (<Emphasis Type="Italic">Rhinopithecus roxellana</Emphasis>), a Seasonally Breeding Primate

In nonhuman primates, infanticide by adult males can occur when the leader male is ousted from a one-male, multifemale group, or when male dominance rank changes within a multimale, multifemale group. According to the sexual selection hypothesis, this behavior may be adaptive if perpetrators increase their reproductive success by killing unrelated, unweaned infants, thus shortening the interbirth interval of the mother, and then siring her next infant. Under an alternative hypothesis, infanticide is a byproduct of aggressive male–male competition and these predictions do not hold. Direct observations of the context surrounding infanticide in free-ranging primate populations that allow a test of these predictions are rare. Here, we document four cases of male infanticide and report paternity data for a group of golden snub-nosed monkeys (Rhinopithecus roxellana) at Shennongjia, China. Three cases of infanticide by new leader males supported the predictions of the sexual selection hypothesis, while another provides partial support for the sexual selection hypothesis, but can also be explained via a nonadaptive hypothesis. In this latter case, a male from an all-male group killed an infant during an aggressive episode that appeared to be accidental, as it took place 7 mo before a male takeover happened, and the perpetrator did not obtain any reproductive advantage. We conclude that most male infanticide events in golden snub-nosed monkeys are consistent with the adaptive selection sexual hypothesis.     

Infant Mortality Risk and Paternity Certainty Are Associated with Postnatal Maternal Behavior toward Adult Male Mountain Gorillas (Gorilla beringei beringei)

Sexually selected infanticide is an important source of infant mortality in many mammalian species. In species with long-term male-female associations, females may benefit from male protection against infanticidal outsiders. We tested whether mountain gorilla (Gorilla beringei beringei) mothers in single and multi-male groups monitored by the Dian Fossey Gorilla Fund’s Karisoke Research Center actively facilitated interactions between their infants and a potentially protective male. We also evaluated the criteria mothers in multi-male groups used to choose a preferred male social partner. In single male groups, where infanticide risk and paternity certainty are high, females with infants <1 year old spent more time near and affiliated more with males than females without young infants. In multi-male groups, where infanticide rates and paternity certainty are lower, mothers with new infants exhibited few behavioral changes toward males. The sole notable change was that females with young infants proportionally increased their time near males they previously spent little time near when compared to males they had previously preferred, perhaps to encourage paternity uncertainty and deter aggression. Rank was a much better predictor of females’ social partner choice than paternity. Older infants (2–3 years) in multi-male groups mirrored their mothers’ preferences for individual male social partners; 89% spent the most time in close proximity to the male their mother had spent the most time near when they were <1 year old. Observed discrepancies between female behavior in single and multi-male groups likely reflect different levels of postpartum intersexual conflict; in groups where paternity certainty and infanticide risk are both high, male-female interests align and females behave accordingly. This highlights the importance of considering individual and group-level variation when evaluating intersexual conflict across the reproductive cycle.     

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]     

Infant mortality following male takeovers in wild geladas

Since Sugiyama's [1965] first observations of infanticide, empirical evidence from a multitude of primate species has supported the sexual selection hypothesis-the idea that males enhance their reproductive success by killing nonrelated, unweaned infants to hasten the mothers' return to fertility. Like other primates that live in social groups where paternity certainty is high, the social structure of geladas [Theropithecus gelada] suggests that infanticide by males could enhance their reproductive success. Nevertheless, empirical evidence for infanticide in this species is limited to anecdotal accounts. Using the timing of infant mortality and female reproductive and behavioral data collected across 26 months from a population of geladas living in the Simien Mountains National Park, Ethiopia, we test whether sexually selected infanticide occurs in this species. We also examine two additional hypotheses [noninfanticide hypothesis and generalized aggression hypothesis] for this population. Results suggest that sexually selected infanticide in geladas may, indeed, be a threat to females with dependent infants. First, male takeovers-the most likely time for infanticide-were associated with subsequently elevated rates of infant death [a 32-fold increase] comprising nearly 60% of all infant mortality. Second, females who lost infants during this period returned to fertility more quickly than if infants had lived [IBIs were 50% shorter], and third, all of these females were observed to mate with the new male. We found little to no support for other hypotheses. Finally, these results raise the possibility that anecdotal reports [from previous studies and this study] of pregnancy termination, accelerated weaning, and deceptive sexual swellings may represent female counterstrategies to male infanticide in geladas.