Aunts and Mothers: Adaptive Implications of Allomaternal Behavior of Nonhuman Primates

Explanations of the function of behavior directed toward young primates by conspecifc females other than the mother have emphasized variow outcomes beneficial to "aunts, I' mothers, infants, or some combination thereof. There is little evidence, however, that allomothering benefits mothers or infants to any signifcant degree; allomothering is selfish behavior with highly variable consequences roughly predzctable on the basis of genealogical ties between participants. Selective consequences of infant kidnapping and aunting-to-death are examined, and a hypothesis is suggested concerning the adaptive significance for mothering of allomothering. [adoption, infant-stealing, behavioral selection]     

Allomothering behaviour of new and old world monkeys

The holding or transferring of newborn infants at less than 1 month old by individuals other than the mothers was studied in 24 species of New and Old World monkeys under captive conditions. The observed monkey species could be divided into two types. Group A included eight species of three families where the mothers were tolerant to ‘infant transfer’ and readily retrieved their infants from other individuals, the frequency of infant transfer being high. The infant transfer of this group was termed allomothering behaviour. Group B included 16 species of two families where infant transfer did not occur at all or its frequency was very low and the mothers were possessive of their infants. Once transfer did occur, the infant could not be reclaimed with ease. The relationships between the two groups and taxonomic status, life forms and social types were evaluated in a total of 45 species from the present study and the literature. Correspondences were found with social type and taxonomic status. That is, species of Group A were seen only in the family or one-male type, except for one species, although none of this group appeared in the Cercopithecinae regardless of social types. The significance of infant transfer is discussed in relation to the participants' responses to it and the correlations between the two groups and social types.     

笼养黑叶猴拟母亲行为的观察

2002 年3～12 月, 采用焦点动物观察法和全事件行为记录法对南宁动物园人工饲养的5 群黑叶猴的拟母亲行为进行了观察。5 群黑叶猴中, 有幼体9 只, 成年个体19 只。观察发现非母雌性黑叶猴的拟母亲行为有怀抱、携带、接近、理毛、吻婴5 种类型; 各种行为类型发生的频次从高到低分别为接近(46.19 %) 、怀抱和携带(24.14 %) 、吻婴(20.36 %) 和理毛(9.31 %) 。通过比较还发现: 1) 幼体出生几个月内(4～8 月龄) , 黑叶猴拟母亲行为经常发生。2) 拟母亲行为的强度与幼体的年龄具有较大的关联性, 与非母雌性的育婴经验有关, 育婴经验缺乏的非母雌性对幼体表现出比有育婴经验的个体更强烈的兴趣。3) 拟母亲行为发生受幼猴母亲的默认程度的影响, 有些母亲不允许其它雌猴接触幼体。4) 拟母亲行为有助于缓解群内雌性个体间的冲突, 调节群内个体间的关系。     

Development in Japanese macaques (Macaca fuscata): Sexually dimorphic behavior during the first year of life

We have documented several sexually dimorphic patterns of behavior that develop during the first year of life in infant Japanese macaques and their mothers. Mothers treated their infants differently by sex—mothers of males broke contact with them and retrieved them more frequently than did mothers of females. And mothers of male infants moved more frequently than did mothers of female infants. Male infants played more, played in larger groups, and mounted more frequently; female infants groomed and spent more time close to other monkeys in larger social groups than did males. Female infants were also punished by other group members more frequently than were male infants. We conclude that male and female Japanese macaque infants receive differential treatment early in life by both their own mothers and other animals, and males and females in turn treat their mothers and other animals differently. There appears to be a reciprocal relationship between the behavior of infants, mothers and other social partners that contributes to the development of sexually dimorphic patterns of behavior.     

Distribution of dorsal carriage among simians

We surveyed the literature and obtained information from primate researchers and zookeepers to study the distribution of dorsal carriage among 77 simian species including New and Old World monkeys and apes in relation to arboreality and terrestriality, birth (litter) weight relative to maternal weight, and presence or absence of distinct natal coat colors. All New World monkeys are arboreal and commonly carry their infants dorsally. Conversely, arboreal Old World monkeys do not use dorsal carriage, and only some predominantly terrestrial Old World monkeys do so. Whereas lesser apes (which are highly arboreal) do not use dorsal carriage, arboreal as well as more terrestrial great apes commonly carry their infants dorsally. These findings indicate that simple arboreality or terrestriality is inadequate to explain dorsal carriage by monkeys. Infants of small- to medium-sized New World monkeys have relatively high birth weight compared with maternal weight, and are most likely to be carried dorsally than ventrally even on the first postnatal day. In contrast, infants of large-bodied New World monkeys are carried ventrally first and then dorsally up to the end of their second year, albeit increasingly infrequently. Among Old World monkeys, no association was found between mode of infant transport and birth weight relative to maternal weight, but some terrestrial Old World monkeys displaying dorsal carriage tend to do so with older infants, indicating that such behavior enables the mother to transport the infant with lower energy expenditure. Among terrestrial Old World monkeys, infants with distinctive natal coat colors are rarely carried dorsally until the natal coat color changes to adult coloration: infants with distinctive coat colors clinging to the backs of carriers could be highly visible and thus vulnerable to predation. Dorsal carriage by mothers may prolong the affiliative mother–infant relationship.     

Primate play vocalizations and their functional significance

It is well known that, among mammals, specific play vocalizations are produced exclusively by certain nonhuman primate species. In order to investigate the functional significance of these calls, we examined their phyletic distribution among New World and Old World monkeys. The results indicate that such calls are produced by species in which allomothering behaviour occurs. We propose a functional explanation of play vocalizations according to which they serve as a possible source of information for maternal retrieval of infants whenever necessary.     

Social structure,infant handling,and mothering styles in group-living old world monkeys

I argue that in Old World monkeys, infant handling by individuals other than the mother is a heterogeneous phenomenon in structural and functional terms; species differences in maternal tolerance of infant handling are related to differences in the relative proportion of abusive to affiliative responses made to infants by adult females other than the mother; and infant handling by adult females is related to the species-typical social structure, with particular reference to social relationships among females and patterns of food competition. I apply the proposed relationship among social structure, infant handling, and mothering style to explain the observed variation in mothering styles between and within the subfamilies Colobinae and Cercopithecinae.     

The occurrence of twins and accompanying behavioural changes in the banded langur,Presbytis melalophos

The occurrence of twins in arboreal Old World monkeys and apes is extremely rare. A wild adult femalePresbytis melalophos, however, gave birth to female twins. This stimulated many patterns of behaviour which were rare or absent when single infants were born. Allomothering increased greatly and maltreatment of twins by allomothers was common, even though this was never observed with single infants. Results indicate that the amount of allomothering inP. melalophos is normally controlled by the mother rather than by potential allomothers. The behaviour of the twins also differed from that of single infants. Except when they were taken by allomothers, the twins moved away from their mother much less than did single infants by their second month of life.     

Allomaternal behavior in a group of free-ranging patas monkeys

A free-ranging group of patas monkeys (Erythrocebus patas) containing 18 individually identifiable adult females was observed for approximately 400 hours, equally distributed over two two-month periods corresponding to the breeding and birth seasons, at the La Parguera facility of the Caribbean Primate Research Center. The large number of infants born in the spring and early summer (n = 14) allowed for detailed observations of alloparental behaviors, with a focus on allomothering by the adult females. Seven types of alloparental behaviors were recorded: contact, nuzzling, grooming, agonism, close visual inspection, attempted kidnapping, and kidnapping. Adult females emitted the vast majority of allomaternal behavior, the patterning and frequency of which closely resembled the patterning and frequency of inter-adult female social grooming. Relative dominance status of the participants did not consistently predict the directionality of allomothering. The most commonly observed allomaternal behaviors were contact and nuzzling, which are primarily affiliative behaviors; agonism was rare. Successful kidnapping occurred eight times. Immature monkeys (n = 22) emitted an additional 32 alloparental acts. A propensity towards allomothering by experienced females would be most beneficial to patas infants due to the patas' tendency towards dispersed foraging and rapid flight in the presence of danger. It is possible that direct competition with groups of rhesus macaques for available resources on the island served as a proximal cause for the allomothering observed in this patas group.     

Brain evolution in Old World monkeys.

Sulcal patterns of 14 genera of Old World monkeys were analyzed from 107 endocasts. Colobines and cercopithecines differ in patterns of cerebral convolutions, and functional and evolutionary hypotheses are here proposed regarding those differences. The cercopithecine pattern seems to be the more derived since it suggests relative expansion of prefrontal, and inferior temporal integration cortices as compared to the colobine pattern.     

Functional assessment of subfamily variation in maxillomandibular morphology among Old World monkeys

Among Old World monkeys, subfamily variation in maxillomandibular form is commonly attributed to divergent dietary and social behaviors. However, our knowledge of any musculoskeletal adaptations for gape in cercopithecines, and folivory in colobines, is incomplete. Such data are requisite to a more informed perspective on the evolutionary morphology of these taxa. Structural analyses of gape and biomechanical efficiency were applied to a representative sample of adult cercopithecids. Factors pertaining to the biomechanical scaling of cranial structures were evaluated with least-squares bivariate regression techniques. To assess subfamily differences in masticatory efficiency, analyses of covariance were made between relevant factors. Cercopithecines achieve increased gape and relative canine size mainly with strong positive allometry of the facial skull, combined with a larger gonial angle. Colobines possess a relatively long masseter lever arm and short facial skull, as well as an enlargened masseter-medial pterygoid complex. Subfamily differences in temporalis lever arm scaling are negligible. Biomechanical comparisons within and between subfamilies suggest that the mechanical advantage of the temporalis is relatively greater than that of the masseter, while the mechanical advantage of both muscles increases with face length. Evidence is presented to stress the need for adequate consideration of the dependent variable in allometric investigations of skull form.     

New World primates,new frontiers: Insights from the woolly spider monkey,or muriqui (Brachyteles arachnoides)

Despite over 25 years of intensive research, much of our knowledge of primate behavior has been limited to a small number of Old World, semiterrestrial species. With the exception of chimpanzees, these species share consistent patterns of behavior, including aggressive competition between males, male dominance over females, male dispersal and female kin groups, that have come to characterize the Order Primates. However, as research has expanded to include a number of newly studied species, such generalizations about primate behavior are no longer appropriate. Data presented on the wooly spider monkey, or muriqui (Brachyteles arachnoides), provide examples of the ways in which traditional views of primate behavior are being reconsidered. In muriquis, and in several other New World monkeys, female kin groups do not occur because females disperse from their natal groups. In addition, aggressive competition between males is virtually absent; and, female muriquis appear to be codominant with males. Constraints on sexual dimorphism may help to explain why muriquis (and other New World primates) differ so fundamentally from the better known semi-terrestrial Old World monkeys.Logo of the 1988 International Primatological Society.     

Development and mother-infant relations among captive patas monkeys

Generalizations about the rate of behavioral development and mother-infant relations in nonhuman primates are often based largely on observations of a few closely related species of macaques. Patas monkeys (Erythrocebus patas)are sufficiently distant phylogenetically and distinct in their social and ecological adaptations from the well-studied macaque species that observations of their patterns of infant development and mother-infant relations may indicate to what extent macaque patterns are typical of Old World monkey species. Eight patas infants living with their mothers in an established captive group were observed for 960 hr over the first year of life. These infants showed a rapid rate of behavioral development and attainment of independence from mothers. Patas also have one of the fastest rates of sexual maturation of any Old World monkey species. This pattern of rapid social and sexual development can be viewed as a response to a highly seasonal savannah environment in which there is a premium on ability to achieve nutritional, locomotor, and social self-sufficiency as quickly as possible and to reproduce as early and as often as developmental constraints will permit. Patterns of infant development and mother-infant relations may be best understood as an integral part of a species’ overall life history pattern.     

The socioecology of infant handling in primates: Is the current model convincing?

A strong interest shown by females towards infants other than their own is one of the most consistent behavioral traits found in primates, including humans. Species differences exist, however, in the extent mothers allow other group members to interact with their offspring. Socioecological theory predicts that in species characterized by relaxed, egalitarian dominance relations mothers should allow extensive interactions between their infants and other individuals from the first weeks of life, while in species characterized by nepotistic and despotic dominance relations maternal tolerance of infant handling should be low. While this model received some support from a comparison between colobines and some cercopithecines, several other species, including the Barbary macaque, do not appear to fit easily into the framework. In fact, only about half of all well-studied species follow the predicted pattern, suggesting that other factors, associated with the costs and benefits of the behavior, must be invoked to explain the variation in mothering styles and infant handling found in primates.     

High‐fiber diet promotes weight loss and affects maternal behavior in vervet monkeys

The dramatic increase in obesity in western societies has shifted the emphasis in nutrition research from the problems of undernutrition to the adverse consequences of being overweight. As with humans, Old World monkeys are at increased risk for type II diabetes and other chronic diseases when they gain excessive weight. To prevent overweight and obesity, promote animal health, and provide a more natural level of fiber in the diet, the standard commercial monkey chow diet at a vervet monkey breeding colony was changed to a higher fiber formulation in 2004. The new diet was also higher in protein and lower in carbohydrate and energy density than the standard diet. Because maternal behavior is known to be sensitive to differences in resource availability, data on weight and mother–infant interactions for 147 mothers with 279 infants born from 2000 through 2006 were assessed for effects of the diet change. The results showed that, even though food was provided ad libitum, the mean body weight of breeding females was 10% lower after the transition to the high‐fiber diet. Behaviorally, mothers on the high‐fiber diet were significantly more rejecting to their infants, and their infants had to play a greater role in maintaining ventral contact in the first few months of their lives. The effects of the diet change on maternal rejection were significantly related to the mother's body weight, with lower‐weight mothers scoring higher in maternal rejection. These results demonstrate that maternal behavior is responsive to changes in maternal condition, and that beneficial changes in the diet may have unintended consequences on behavior. Am. J. Primatol. 72:234–241, 2010. © 2009 Wiley‐Liss, Inc.     

Sex differences and social organization in free-ranging spider monkeys (Ateles geoffroyi)

Several aspects of the social system of spider monkeys remain poorly understood in spite of previous studies of their behavior. Our work investigates sex differences of adultAteles geoffroyi to develop a better understanding of their social organization. A six-month field study of this species in Guatemala showed that adult males were both more aggressive and more socially cohesive than females, as well as more territorial. Adult females were more vocal, more submissive, more nonsocial, and more dispersed than adult males. Males were more likely to associate affinitively with other males than with females, and to direct their aggressive behaviors at females rather than males. Spider monkey society was found to be sex-segregated; males traveling and interacting in all-male subgroups, while females travel alone or with offspring. These findings are used, in conjunction with other evidence, to draw inferences about the dynamics of theAteles social system, and to derive an explanation for the evolution of spider monkey social organization. The frugivorous diet ofAteles is linked to the dispersion females and to the cohesion of related adult males, who form cooperative territorial groups, in which the low level of male-male competition is related to the absence of sexual dimorphism. Spider monkeys provide an illuminating contrast to the general primate model, derived from Old World monkeys, which links sexual dimorphism in size to sex differences in behavior, and ultimately to sexual selection.     

Demography, life history, and social structure in Propithecus diadema edwardsi from 1986-2000 in Ranomafana National Park, Madagascar

Prosimian lemurs differ fundamentally from anthropoid primates in many traits related to social structure. By exploring the demography of Milne-Edwards' sifakas (Propithecus diadema edwardsi), and comparing it to other well-studied primates, we explore the effect of demographic and life-history factors on social structure. Specifically, we compare lemur survivorship and fertility patterns to two published composite models: one created for New World and another created for Old World monkeys. Using longitudinal data collected on individual Propithecus diadema edwardsi from four study groups from 1986-2000 in Ranomafana National Park, Madagascar, we quantify 1) group composition, 2) birth seasonality, 3) interbirth interval, 4) life-table values, and 5) population growth estimates. The mortality, survivorship, and life-expectancy schedules indicate high infant and juvenile mortality. Fertility remains high until death. The intrinsic rate of increase and net reproductive rate indicate a shrinking population. We suggest that high mortality rather than low fertility causes the observed population decline. While sifaka survivorship closely resembles New World patterns, fertility resembles Old World patterns, i.e., like New World monkeys, few sifakas survive to reproductive age, and those that do, reproduce at a slow rate resembling the Old World pattern. This necessarily impacts social structure. An adult sifaka at the end of her lifespan will have one only daughter who survives to reproductive age, compared to 3.4 for New World or 2.7 for Old World monkeys. Demography limits the formation of large kin-based groups for sifakas, and survivorship and fertility patterns do not easily permit sifakas to form large same-sex family groups.     

Model life tables for the larger old world monkeys

Mortality statistics for 25 populations of the larger Old World monkeys (members of the subfamily Cercopithecinae) were evaluated with a competing hazard model of mortality. The best eight of these life tables were combined to generate a standard model life table representative of the mortality patterns of these primates. Two applications of the standard model to smooth, graduate, and compare life tables based on limited and defective data are presented.     

Embraces and Grooming in Captive Spider Monkeys

Relatively little information is available regarding the role of social grooming and embraces in spider monkeys that live in fission-fusion societies in which individuals are usually split into subgroups. We investigated whether embraces and grooming have similar roles in captive spider monkeys by examining their occurrence in two contexts. One context was fusion, i.e. when the monkeys moved into an area of the enclosure where other monkeys were present, in which individuals from different subgroups were expected to exchange greeting behavior. The other context was the access to young infants, in which females were expected increase their friendly behavior toward mothers. We collected data by observing all individuals within a subgroup and via focal animal sampling. We found that overall embraces occurred more frequently than grooming and that their distributions were not correlated. The frequency of embraces was positively associated with the number of fusion events per observation, whereas the frequency of grooming bouts was not. Furthermore, embraces were more frequent following initial approaches after fusion versus subsequent approaches, and the figure was higher than the corresponding one for grooming. Mothers received more embraces after than before the birth of their infants, whereas there was no such effect for grooming. Embraces, but not grooming, play a role in the regulation of social relationships in spider monkeys. Embraces may serve as signals of benign disposition in contexts that are likely to be associated with tension, such as fusion and access to infants.     

Proximal Spacing Between Individuals in a Group of Woolly Monkeys (Lagothrix lagotricha) in Tinigua National Park, Colombia

I studied proximal spacing within a group of woolly monkeys (Lagothrix lagotricha) during 7 months at Parque Nacional Tinigua, Colombia. I collected a total of 1188 instantaneous samples on focal individuals, recording the number and age/sex class of individuals that were in contact with, <2 m from, <5 m from the focal animal. The results indicate that proximate spacing reflects social affinities and is related to mother–infant relationship and social grooming. Subadult females and adult males are the sex/age classes with the lowest number of individuals in proximity. There are low proximity between adult females and between adult males and high frequencies of nearness between mother and offspring. Associations between males and females were usually low, but in some cases males showed preferences for a given female. There was a relatively gradual increase in spacing between mothers and their offspring as they became older. Old juvenile males were associated chiefly with other males—mostly subadults—whereas juvenile females maintained some proximity only to their mothers. There are also differences in spacing behavior according to different activity types.