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.     

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.     

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.     

First direct evidence of infanticide and cannibalism in wild snub-nosed monkeys (Rhinopithecus bieti)

Although infanticide has been witnessed in many species of Colobinae, and a case was observed in a captive group of golden snub-nosed monkeys (Rhinopithecus roxellana), observed cases of infanticide in wild snub-nosed monkeys (Rhinopithecus spp.) have not previously been recorded. Here we describe the killing of a 1-month-old infant by a male in a black-and-white snub-nosed monkey (R. bieti) group at Xiaochangdu in Tibet. The infanticidal attack was witnessed as part of a long-term observational study of ecology and behavior that began in June 2003. The male was observed killing and eating the infant. The literature proposes three main explanations for infanticide: two adaptive hypotheses (sexual selection and resource competition), and one nonadaptive hypothesis (social pathology). Individual cases of infanticide, such as this one, are important for comparative purposes, but when examined on their own they are difficult to interpret in relation to established theoretical frameworks. The cases we describe here show some consistency with the sexual selection hypothesis, but the lack of critical information (i.e., as to paternity) makes it impossible to draw a firm conclusion. This is also the first described case of cannibalism in snub-nosed monkeys.     

Attacks on adult females with infants by non-resident males in the François langur

Infanticide by males is a common phenomenon in mammals, especially primates, as lactation lasts much longer than gestation in many species. Usually, infanticidal episodes occur soon after group takeovers, and are traditionally considered a male reproductive strategy (i.e., support the sexual selection hypothesis, Hrdy, 1974). To verify the validity of this conception, we observed one group of François’ langurs in the Nonggang Nature Reserve, China, between August 2003 and July 2004. During the study period, a François’ langur female with the youngest infant in the group was attacked three times by immigrating males, and later disappeared by the third day after the final attack. We suggest that these attacks on the female-infant dyad represent infanticide attempts by males, and may be the cause of the adult female and her infant’s disappearance. Presumably, that female dispersed with her infant to avoid infanticide and was not killed. Though these observations do not completely verify the sexual selection hypothesis, they are not inconsistent with it.     

Infanticide in <Emphasis Type="Italic">Cercopithecus mitis stuhlmanni</Emphasis> in the Kakamega Forest,Kenya: Variation in the Occurrence of an Adaptive Behavior

Infanticide by males is widespread across mammals and especially prevalent among primates. Considerable research has examined how fitness benefits can explain the occurrence of this behavior; less is known, however, about intrapopulation variation in its occurrence. We evaluated 10 infanticides by males in wild blue monkeys according to the sexual selection hypothesis. To explore intrapopulation variation in occurrence of infanticide, we compared these cases to 38 cases that were contextually similar but in which infanticide did not occur. We examined male reproductive benefit, infant age, maternal parity, postconception estrus, group defense, available mating partners, and context of takeover. We based comparisons on daily or near daily records of male presence in the study groups, infant birth dates, and male-female sexual interactions. Infanticides followed predictions of the sexual selection hypothesis: males were unlikely to kill their own offspring, the period for the mother’s return to conception was reduced by half, and males increased their chance of siring her next offspring. Difference in male reproductive benefit, costs, and motivation did not fully explain the observed variation in infanticide occurrence. Infants were more likely to be spared if they were older when a male first arrived, or if their mother had mated with the male in the second month after conception. The most important determinant of infant fate, however, was male identity, a finding consistent with 2 scenarios: 1) an infanticidal tendency may be influenced by a genetic polymorphism that is not fixed in this population or 2) infanticidal behavior may be a conditional male strategy. Further research on intrapopulation variation in infanticidal behavior should focus especially on characteristics of males.     

Infanticide in Propithecus diadema edwardsi: An Evaluation of the Sexual Selection Hypothesis

Infanticide might be described as a reproductive strategy employed by anthropoid primate males when they immigrate into new groups. But infanticide has rarely been observed in wild prosimian primates. For the Malagasy lemurs this may reflect one or more of the following: strict breeding seasons; relative monomorphism in canine tooth and body size; small group sizes; male–female dominance relations; and male–female dyads within groups. We addressed the following questions: Do prosimian males commit infanticide in circumstances similar to those in which anthropoids do? and Is there any reproductive advantage for a highly seasonal breeder to commit infanticide? To help answer these questions, we describe the death of a 24-hr-old infant male Propithecus diadema edwardsi from wounds received during a fight between his mother, her adult daughter, and a newly immigrant male. Interbirth intervals between surviving offspring are 2 years for Propithecus diadema edwardsi; therefore, a male could dramatically shorten the time between reproductive windows by killing an infant. Whether this tactic would be favored by sexual selection cannot be addressed until more information has been collected on the length of interbirth interval due to infanticide relative to that of infant death by other causes; how social factors such as stability of breeding relationships affect long-term male reproductive success; how effective female counterstrategies are to prevent infanticide and/or whether they choose to mate with males that commit infanticide; and how often males that kill infants subsequently sire infants, particularly in groups that contain a resident male.     

Observed case of infanticide committed by a resident male central American black howler monkey (Alouatta pigra)

Although infanticide has been witnessed in other species of howler monkey, and has been inferred for Alouatta pigra, an observed case of infanticide has not previously been recorded for this species. Here we describe the killing of a 2-week-old infant by the resident male of a small social group in southern Belize. The infanticide was witnessed as part of an intensive observational study that began in January 2003. The male was known to have resided in the group for at least 4 months, but it is not known whether he was the father of the infant. The literature proposes three main explanations for infanticide: two adaptive hypotheses (sexual selection and resource competition), and one nonadaptive hypothesis (social pathology). Individual cases of infanticide such as this one are important for comparative purposes, but when examined on their own they are difficult to interpret in relation to established theoretical frameworks. The data presented here show some consistency with the sexual-selection and resource-competition hypotheses, but the lack of critical information (i.e., as to paternity) makes it impossible to draw firm conclusions.     

The evolution of male infanticide in relation to sexual selection in mammalian carnivores

The evolution of infanticide by males has often been explained by the sexual selection hypothesis, which posits that infanticide improves male reproductive success by shortening the interbirth intervals of the mothers of the killed offspring. In Carnivora, however, the fitness advantages assumed in this hypothesis have been shown in only a few species, and it has been argued that male infanticide may be nonadaptive in pinniped carnivores. According to the sexual selection hypothesis, male infanticide is expected to be more prevalent in species in which males are subjected to stronger sexual selection through intrasexual competition over mates. We examined a phylogenetically corrected relationship between male infanticide and sexual size dimorphism (SSD) as a measure of the intensity of sexual selection in carnivores. Our analyses failed to detect a significant association between the occurrence of male infanticide and SSD across carnivores, although they showed that, among fissipeds (typically terrestrial carnivores), males in species with stronger male-biased SSD are significantly more likely to commit infanticide. This suggests that the evolution of male infanticide is correlated with intense sexual selection in fissipeds. In pinnipeds (Odobenidae, Otariidae, and Phocidae), there was no significant association between male infanticide and SSD. Assuming that SSD represents the intensity of sexual selection on males, this result is consistent with the argument that infanticide by male pinnipeds is not a sexually selected behaviour.     

Impact of Male Takeovers on Infant Deaths,Births and Conceptions in Cebus capucinus at Santa Rosa,Costa Rica

Male takeovers are associated with infant wounding and death in 3 of 4 capuchin species. In this paper, I analyze the effects of male takeovers on infant mortality and the subsequent conceptions and interbirth intervals of their mothers over an 18-yr period and test predictions of the sexual selection model of infanticide for white-faced capuchins, (Cebus capucinus). Major findings are that infants are significantly more likely to die in the 3- and 12-mo periods following a takeover than in times of peace and that a female whose infant dies experiences a significantly shorter interbirth interval before her next infant is born than she would have had the former infant survived. In the vast majority of cases, the invading males become resident in the group and are present during the subsequent conceptions of the females in the group. However, overall conception rates do not rise significantly in the year after a takeover, there is no relationship between the age of the infant at death and the length of the mother's subsequent interbirth interval, and it is not yet clear if male infants are preferentially targeted by invading males. Most takeovers occur during the 6-mo dry season and most conceptions occur in the wet season, 3–6 mo later. My findings support the major predictions of the sexual selection model of infanticide in primates and demonstrate that male takeovers of social groups have substantial effects on infant survival and maternal parturition patterns in Cebus capucinus.     

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]     

Male Demography,Female Mating Behavior,and Infanticide in Wild Patas Monkeys (Erythrocebus patas)

Infanticide by males has been hypothesized to be a naturally selected behavioral strategy that increases the infanticidal male's reproductive success. The sexual selection hypothesis has been challenged via alternative, nonadaptive hypotheses that dispute its empirical and theoretical bases. Two of the most widely recognized alternatives are the social pathology hypothesis, in which infanticide results from overcrowding or recent human disturbance, and the generalized aggression hypothesis, in which infanticide is an epiphenomenon of increased male aggression. We report the first case of infanticide in wild, seasonally breeding patas monkeys (Erythrocebus patas) living at a low population density in a stable habitat, conditions which do not support the social pathology hypothesis. Its exceptional occurrence is consistent with the sexual selection hypothesis: over a 7-year period the infanticidal male was the only one of 13 resident males that was not present during the actual conception season but was present during the following birth season. Also consistent with this hypothesis, mothers were differentially targeted for male aggression, which increased sevenfold during the days surrounding the infanticide and then decreased to baseline levels after the infanticide. Aggression targeted at mothers does not support the generalized aggression hypothesis. As predicted by the sexual selection hypothesis, females began soliciting mating immediately after the infanticide, despite its occurrence in the nonconceptive season.     

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.     

Infant mortality after takeovers in wild Ethiopian hamadryas baboons

In this work we report the first observational evidence of infanticide in wild hamadryas baboons. The study group inhabits the lowlands of the northern Rift Valley in Ethiopia and has been under observation for over 1,200 hr, on and off, since October 1996. Here we report observations from August and September 2002 of the consequences of two takeovers of known females with black infants. After the first takeover, the respective infant disappeared and was presumed dead within 11 days of the takeover. After the second takeover, the infant incurred repeated severe aggression from its mother's new leader male and eventually died 4 days after the takeover. We interpret these findings as support for the sexual selection hypothesis regarding male infanticide. We suggest that hamadryas leader males usually protect infants born into their units, but may withhold this protection-or even directly attack and kill infants-after takeovers.     

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.     

Central males instead of multiple pairs in redfronted lemurs, Eulemur fulvus rufus (Primates, Lemuridae)?

In group-living Malagasy primates (Lemuriformes), certain demographic and morphological traits deviate both from theoretical expectations derived from sexual selection theory and from patterns in better-known anthropoid primates. Lemurs lack sexual dimorphism in body and canine size and live in relatively small multimale-multifemale groups with, on average, even adult sex ratios, despite a polygynous mating system. In addition, the majority of gregarious lemurs are cathemeral, that is, they are regularly active both day and night. The social system of cathemeral lemurs has been considered an adaptation to their activity pattern. If so, groups should consist of multiple pairs that aggregate during diurnal activity and range separately at night in response to predation and infanticide risk, respectively. Moreover, mating privileges should exist between pair partners. We tested this hypothesis with data collected on two groups of wild redfronted lemurs in western Madagascar during 1023 focal animal hours spanning 4 months including the mating season. In addition, data on spatial relations were collected on 12 nights. We found no differences in group cohesion between day and night and no behavioural evidence for multiple male-female pairs. Instead, one male in each group monopolized social interactions with all females. However, females copulated with all resident males, although most often with the central male. Thus, basic predictions of the cathemerality hypothesis are unsupported. Multiple matings and indications of oestrous synchrony can be viewed as female counterstrategies against infanticide, whereas reproductive strategies of redfronted lemur males remain obscure. Copyright 1999 The Association for the Study of Animal Behaviour.     

New cases of inter-community infanticide by male chimpanzees at Ngogo,Kibale National Park,Uganda

Infanticide by males has been recorded in four chimpanzee populations, including that in Kibale National Park, Uganda. Some infanticidal attacks occur during inter-community aggression. The sexual selection hypothesis does not easily explain these attacks because they may not directly increase male mating opportunities. However, females in the attackers’ community may benefit by expanding their foraging ranges and thereby improving their reproductive success; thus infanticide may increase male reproductive success indirectly. We report two new cases of infanticide by male chimpanzees at Ngogo, Kibale National Park. Like two previous cases, these occurred during a boundary patrol and were almost certainly between-community infanticides. The patrolling males attacked despite the proximity of males from the victims’ presumed community. This probably explains why, unlike the earlier cases, they did not completely cannibalize their victims. Such attacks seem to be relatively common at Ngogo and infanticide may be an important source of infant mortality in neighboring communities. Our observations cannot resolve questions about the sexual selection hypothesis. However, they are consistent with the range expansion hypothesis: the infanticides occurred during a period of frequent encounters between communities associated with a mast fruiting event, and Ngogo community members greatly increased their use of areas near the attack site during another mast fruiting event one year later. Our observations contribute to growing evidence that lethal intergroup aggression is a common characteristic of wild chimpanzee populations.     

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.     

Infant loss during and after male replacement in gibbons

According to the sexual selection hypothesis, infanticide during resident male replacement is an adaptive strategy that has evolved because the killing of unweaned offspring sired by previous males shortens the inter‐birth intervals of the mothers whose infants are targeted and thereby increases the reproductive fitness of the perpetrator. To test this hypothesis, we describe previously unreported cases of primary male replacement for two gibbon species (Hylobates lar and Nomascus nasutus), and review all other reported cases of primary male replacement in gibbons. Overall, infants were present in nearly half of all cases (16/33, 48%) and of the 18 infants present during replacement, 50% (N = 9) disappeared within 2 months of the event. In four of the five cases where there was sufficient demographic information to identify the likely sire of the subsequent offspring of females that lost infants, the new male was believed to be the sire. Infants were also less likely to die or disappear if the new male and original resident male were possible kin. However, there was no significant difference in the age of infants between those that died or disappeared following replacement and those that survived to weaning (p = .630). Our review of takeover‐related infant loss in gibbons confirms that periods of male instability are risky for unweaned infants and that replacing males benefit from infant loss. Nevertheless, variability in the context of infant loss and difficulties related to data collection in the field make it difficult to test competing hypotheses concerning the mechanisms and functions of infanticide in the small apes.     

Infanticide by a male spectral tarsier (<Emphasis Type="Italic">Tarsius spectrum</Emphasis>)

As part of a long-term field study on the behavioral ecology and conservation of a population of spectral tarsiers (Tarsius spectrum) in Tangkoko Nature Reserve, Sulawesi, Indonesia, I observed the first known instance of infanticide in this species. A young infant was killed by a neighboring male. Neither the epiphenomenal aggression hypothesis, social pathology hypothesis, nutritive benefits of cannibalism hypothesis, nor sexual selection hypothesis are supported by this observation. The only hypothesis that could not be rejected outright, on the basis of this single observation, was the competition for limited resources hypothesis.