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.     

Dental caries prevalence as evidence for agriculture and subsistence variation during the Yayoi period in prehistoric Japan: biocultural interpretations of an economy in transition

The Yayoi period represents the earliest point of agricultural dependence in Japan, dating from approximately 2500 BP to AD 300. Yayoi period people consumed wet-rice as a primary subsistence base. This article uses dental caries prevalence to interpret the biocultural implications of agriculture among these people by testing the following hypotheses: 1) Yayoi period agriculturalists had greater frequencies of carious teeth than Jomon period foragers, 2) regional variation in carious tooth frequencies will be observed among Yayoi period agriculturalists, while 3) variation in carious tooth frequencies will be observed between male and female agriculturalists. Statistically significant differences in carious teeth were observed between the agriculturalists from Southern Honshu and all other samples. These differences suggest greater reliance on cariogenic plants among farmers from Southern Honshu and are consistent with an agricultural economy. The people of the Yayoi period from Tanegashima Island and Northern Kyushu did not have significantly different carious tooth frequencies compared to Jomon period foragers. This suggests that rice alone was not a more cariogenic dietary substance than those consumed by Jomon period foragers but a cariogenic food nonetheless. Dietary heterogeneity between the prehistoric people of the Yayoi period from Southern Honshu and those from Northern Kyushu and Tanegashima Island is also inferred from these differences. Significantly greater frequencies of carious teeth among older aged Yayoi period females compared with males suggest dietary differences between the sexes.     

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.     

A fatal attack on an unweaned infant by a non-resident male in a free-ranging group of Japanese macaques (Macaca fuscata) at Katsuyama

A non-resident male attacked a 4-month-old unweaned infant in a free-ranging group of Japanese macaques (Macaca fuscata) and it died 2 days later from a severe wound. When the infant was alone at the feeding site, the non-resident male rushed at it. The infant ran away as soon as it became aware of the male, but was captured. The male bit the infant on its hand, foot, and arm, while continuously scanning his surroundings. He did not kill the infant immediately and, after the infant escaped, he did not chase or attack it at all. Although the infants right arm was bleeding heavily, it survived until the following day. The infanticide occurred a few weeks before the mating season began, so the victims mother soon resumed estrus and the subsequent inter-birth interval was shortened. The first-, second-, and fourth-ranking adult males had died or disappeared a few months before this infanticide, and there were no other group members near the infant when the infanticidal male appeared. The infanticidal male had not been observed before this incident. Compared to one-male groups, the occurrence of infanticide in multi-male groups of Japanese macaques is extremely infrequent. However, in other reports of infanticide in Japanese macaques as well as in this case, it has been noted that infanticide is likely to occur in the pre- or early-mating season, when there are no resident males to defend the infant against attacks, and when a threatening male is least likely to be the infants father.Electronic Supplementary Material Supplementary material is available for this article at     

Behavioral and endocrine dynamics associated with infanticide in a black and white colobus monkey (Colobus guereza)

Infanticide has been observed in several colobines, but only one infanticide has previously been documented for black and white colobus monkeys (Colobus guereza). This report describes an infanticide observed in Kibale National Park, Uganda, in the summer of 2001. An adult male from a neighboring group attacked and killed a young infant whose mother subsequently remained in her own group and was observed mating 10 days later. She engaged in two mating periods of several days each, separated by approximately 1 month, during which she copulated frequently with the dominant male within her group. Urinary estrogen (EC) and progesterone metabolite (PdG) excretion patterns demonstrated that the female resumed ovarian cycling soon after the infanticide. Because the infanticidal male did not attempt to mate with the victim's mother, his actions were not consistent with the predictions of the sexual-selection hypothesis. We speculate that infanticide associated with intergroup aggression may help secure access to high-quality resources for the infanticidal male's group.     

Infant Killing in Primates: A Review of Observed Cases with Specific Reference to the Sexual Selection Hypothesis

Discussion of infant killing in free-ranging primates has focused on the sexual selection hypothesis developed by Hrdy during the mid-1970s. This hypothesis suggests that infant killing is a form of sexual competition whereby an infanticidal male gains a reproductive advantage by selectively killing the offspring of his male rivals. Despite criticisms that the evidence in support of the hypothesis is distorted by misinterpretation of data and observer bias, the sexual selection hypothesis, bolstered in part by additional reports of infanticide in a variety of specks, has become entrenched as the primary explanatory hypothesis for primate infanticide. However, the majority of reliably documented instances of infanticide in primates come from a very small number of species, and a careful examination of the specific context of each of these episodes fails to support the interpretation of infanticide as a primatewide adaptive complex. Most importantly, the atmosphere of generalized inter- and intrasexual aggression that surrounds the majority of infant killings obscures the evolutionary significance of this behavior.     

Dietary variation and stress among prehistoric Jomon foragers from Japan

Current archaeological evidence indicates that greater dietary reliance on marine resources is recorded among the eastern Jomon, while plant dependence prevailed in western/inland Japan. The hypothesis that the dietary choices of the western/inland Jomon will be associated with greater systemic stress is tested by comparing carious tooth and enamel hypoplasia frequencies between the eastern and western/inland Jomon. Demographic collapse coincides with climate change during the Middle to Late Jomon period, suggesting dwindling resource availability. It is hypothesized that this change was associated with greater systemic stress and/or dietary change among the Middle to Late Jomon. This hypothesis is tested by comparing enamel hypoplasia and carious tooth frequencies between Middle to Late and Late to Final Jomon foragers. Enamel hypoplasia was significantly more prevalent among the western/inland Jomon. Such findings are consistent with archaeological studies that argue for greater plant consumption and stresses associated with seasonal resource depletion among the western/inland Jomon. Approximately equivalent enamel hypoplasia frequencies between Middle to Late and Late to Final Jomon foragers argues against a demographic collapse in association with diminished nutritional returns. Significant differences in carious tooth frequencies are, however, observed between Middle to Late and Late to Final Jomon foragers. These results suggest a subsistence shift during the Middle to Late Jomon period, perhaps in response to a changed climate. The overall patterns of stress documented by this study indicate wide-spread environmentally directed biological variation among the prehistoric Jomon.     

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.     

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.     

Hunter-gatherer energetics and human obesity

Western lifestyles differ markedly from those of our hunter-gatherer ancestors, and these differences in diet and activity level are often implicated in the global obesity pandemic. However, few physiological data for hunter-gatherer populations are available to test these models of obesity. In this study, we used the doubly-labeled water method to measure total daily energy expenditure (kCal/day) in Hadza hunter-gatherers to test whether foragers expend more energy each day than their Western counterparts. As expected, physical activity level, PAL, was greater among Hadza foragers than among Westerners. Nonetheless, average daily energy expenditure of traditional Hadza foragers was no different than that of Westerners after controlling for body size. The metabolic cost of walking (kcal kg(-1) m(-1)) and resting (kcal kg(-1) s(-1)) were also similar among Hadza and Western groups. The similarity in metabolic rates across a broad range of cultures challenges current models of obesity suggesting that Western lifestyles lead to decreased energy expenditure. We hypothesize that human daily energy expenditure may be an evolved physiological trait largely independent of cultural differences.     

A case of infanticide in a recently found gelada population in Arsi, Ethiopia

There have been no reports of infanticide in wild gelada baboons and it has been argued that infanticide is not necessary in geladas, since the birth interval of female gelada can be shortened after takeover of a unit by a new leader male without infanticide. However, we observed an instance of infanticide in a newly-found wild gelada population in the Arsi Region of Ethiopia. After a leader male of the unit was severely wounded by a leopard attack, he was quite weakened. The second male of the unit, a young adult male, became the leader of the unit three weeks later, but the former leader continued to stay in the unit as a second male. After a week, two other adult males joined the unit which, therefore, came to include four adult males. The infanticide took place nine days later. The perpetrator was one of the immigrant males and he showed great interest in the mother of the unweaned victim infant. Although the perpetrator copulated with her after the infanticide, the usurper was found to own all three adult females after two weeks following the infanticide; i.e. the perpetrator could not own any female. The wounded former leader showed conspicuous protective behavior towards the victim's mother and the dead infant. One possible explanation for the occurrence of infanticide in this population of geladas is as follows. Gelada males in this area may be able to join units more easily to form multi-male units but then have shorter tenure in the units. Facing the unstable condition of units, they may sometimes engage in infanticide to increase their breeding opportunities, even before becoming a leader.     

Preliminary assessment of natal attraction and infant handling in wild Colobus vellerosus

This study describes natal attraction and infant handling in wild ursine colobus (Colobus vellerosus). Focal animal samples were collected from five infants of 1-16 weeks of age (mean: 14.5 focal hours per infant). Group members may be attracted to an infant, but unable to handle it because of resistance from the mother. We thus measured natal attraction independently from infant handling by the number of interactive approaches received. The youngest infants were most attractive. Immature females were attracted to and handled infants more than other group members. Mothers were tolerant of most handling attempts and infant-directed aggression was rare. A sixth infant was attacked by members of an all-male band, which allowed us to record the expression of natal attraction and infant handling in the context of an acute threat of infanticide. This infant was carried by non-mothers less frequently than the other infants, and its mother resisted handling attempts more often.     

Intra- and interspecific dominance hierarchies and variation in foraging tactics of two species of stream-dwelling chars

Aggressive interactions, foraging behavior, habitat use and diet were studied in sympatric populations of white-sported char,Salvelinus leucomaenis, and Dolly Varden,Salvelinus malma, in a Japanese mountain stream. Underwater observations on individuals of both species revealed two distinct behavioral regimes: aggressive drift foragers and non-aggressive benthos foragers. Aggressive drift foragers defended partial territories around focal points from which they made forays to capture invertebrates drifting in the water column. Non-aggressive benthos foragers cruised around and beneath cobble in large foraging ranges that overlapped each other. Intra- and interspecific, size-dependent dominance hierarchies were recognized among aggressive drift foragers, whereas non-aggressive benthos foragers showed no such relationships. Terrestrial invertebrates were the most abundant prey in the diets of drift foragers, whereas a very small proportion of the diet of benthos foragers was made up of these taxa. Benthos foragers showed more complex diet composition than drift foragers. These results suggest that non-aggressive benthos foragers may avoid not only interference but also exploitative competition by using alternative foraging tactics. The proportion of drift foragers to benthos foragers among white-spotted char was more than 35 times that among Dolly Varden. The significant difference in the proportion of each species using the two types of foraging strategy results in interspecific food segregation in sympatric populations.     

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.     

Reduced dietary conservatism in a wild bird in the presence of intraspecific competition

The presence of intraspecific competitors can increase foraging costs through exploitation of resources. Optimal foraging theory suggests that when the cost of pursuing one food type increases, alternative resources should be accepted. Accepting novel foods readily might put a competitor at an advantage over its more conservative rivals in the race for sufficient sustenance, but also opens it to the danger of poisoning by chemically protected food. Dietary conservatism is a foraging behaviour characterised by a prolonged avoidance of novel foods, long after neophobia (initial fear of novel objects) has been overcome, and so might be seen as a disadvantage to foragers in a competitive situation. There are two stable foraging strategies found within forager populations: 1) adventurous consumers (AC) which rapidly accept novel foods and 2) foragers showing dietary conservatism (DC). The expression of these two strategies may also vary with environmental conditions. The aim of this study was to investigate the effect of intraspecific competition on the levels of dietary conservatism displayed among wild caught blue tits Cyanistes caeruleus. Blue tits were offered items of both novel and familiar foods under two conditions: with a competitor and without. Our results showed that individuals who experienced competition incorporated the novel items into their diet faster than those who did not experience competition. This study demonstrates, for the first time, the degree of plasticity in the expression of the DC trait using wild birds in laboratory conditions. This plasticity represents a significant adaptation to reduce the costs of foraging conservatively when novel alternative resources should be accepted.     

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 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.     

Neandertal energetics and foraging efficiency

Mechanical interpretations of Neandertal skeletal robusticity suggest extremely high activity levels compared to modern humans. Such activity patterns imply high energy requirements; yet it has been argued that Neandertals were also inefficient foragers. The present study addresses this apparent conflict by estimating energy needs in Neandertals and then evaluating those estimates in the context of energetic and foraging data compiled for contemporary human foragers and nonhuman primates. Energy demands for Neandertals were determined by first predicting basal metabolic rates (BMR) from body weight estimates using human standards developed by the World Health Organization [FAO/WHO/UNU (1985) Energy and Protein Requirements. Report of the Joint FAO/WHO/UNU Export Committee, Geneva: WHO]. Total daily energy expenditure (kcal/day) was then estimated assuming high levels of physical activity (i.e., 2--3 x BMR), comparable to those observed among subsistence-level populations today. These estimates of energy requirements (ranging from 3000--5500 kcal/day) were then used to determine Neandertal foraging efficiency assuming (1) minimal survival-level foraging returns, and (2) daily foraging times longer than those observed among any contemporary foraging group and comparable to a nonhuman primate. Even with these extremely conservative parameters, estimates of Neandertal foraging efficiency (approximately 800--1150 kcal/h foraged) were comparable to those observed among living hunter-gatherers. These results indicate that if Neandertals did have heavy activity levels, as implied by their skeletal robusticity, they would have required foraging efficiencies within the range observed among modern groups. Thus, Neandertals could have been either highly active or poor foragers, but they could not have been both.     

Male strategies and Plio-Pleistocene archaeology

Archaeological data are frequently cited in support of the idea that big game hunting drove the evolution of early Homo, mainly through its role in offspring provisioning. This argument has been disputed on two grounds: (1) ethnographic observations on modern foragers show that although hunting may contribute a large fraction of the overall diet, it is an unreliable day-to-day food source, pursued more for status than subsistence; (2) archaeological evidence from the Plio-Pleistocene, coincident with the emergence of Homo can be read to reflect low-yield scavenging, not hunting. Our review of the archaeology yields results consistent with these critiques: (1) early humans acquired large-bodied ungulates primarily by aggressive scavenging, not hunting; (2) meat was consumed at or near the point of acquisition, not at home bases, as the hunting hypothesis requires; (3) carcasses were taken at highly variable rates and in varying degrees of completeness, making meat from big game an even less reliable food source than it is among modern foragers. Collectively, Plio-Pleistocene site location and assemblage composition are consistent with the hypothesis that large carcasses were taken not for purposes of provisioning, but in the context of competitive male displays. Even if meat were acquired more reliably than the archaeology indicates, its consumption cannot account for the significant changes in life history now seen to distinguish early humans from ancestral australopiths. The coincidence between the earliest dates for Homo ergaster and an increase in the archaeological visibility of meat eating that many find so provocative instead reflects: (1) changes in the structure of the environment that concentrated scavenging opportunities in space, making evidence of their pursuit more obvious to archaeologists; (2) H. ergaster's larger body size (itself a consequence of other factors), which improved its ability at interference competition.