High-risk pregnancy in rhesus monkeys (Macaca mulatta): a case of ectopic, abdominal pregnancy with birth of a live, term infant, and a case of gestational diabetes complicated by pre-eclampsia

Background  Cases of abdominal pregnancy, in the form of intra-abdominal mummified fetuses, have been described in nonhuman primates. Gestational diabetes and pre-eclampsia are common pregnancy complications in women.
Methods  Two timed-bred rhesus monkeys had high-risk pregnancies, an abdominal pregnancy with delivery of a live term infant, and a case of gestational diabetes that later developed pre-eclampsia.
Results  The monkey that had abdominal pregnancy later died from septic peritonitis. The monkey had a colonic adenocarcinoma that may have allowed leakage of intestinal contents into the abdomen. Her infant was fostered to another female and survived. The monkey with gestational diabetes and pre-eclampsia was treated with a regimen similar to that used in women, and a live infant was delivered at day 157 of gestation by Caesarian section.
Conclusion  These cases underscore the value of timed-breeding and the similarities between pregnancy complications in women and in nonhuman primates.     

Ontogeny of limb mass distribution in infant baboons (Papio cynocephalus)

Primates have more distally distributed limb muscle mass compared to most nonprimate mammals. The heavy distal limbs of primates are likely related to their strong manual and pedal grasping abilities, and interspecific differences in limb mass distributions among primates are correlated with the amount of time spent on arboreal supports. Within primate species, individuals at different developmental stages appear to differ in limb mass distribution patterns. For example infant macaques have more distally distributed limb mass at young ages. A shift from distal to proximal limb mass concentrations coincides with a shift from dependent travel (grasping their mother's hair) to independent locomotion. Because the functional demands placed on limbs may differ between taxa, understanding the ontogeny of limb mass distribution patterns is likely an essential element in interpreting the diversity of limb mass distribution patterns present in adult primates. This study examines changes in limb inertial properties during ontogeny in a longitudinal sample of infant baboons (Papio cynocephalus). The results of this study show that infant baboons undergo a transition from distal to proximal limb mass distribution patterns. This transition in limb mass distribution coincides with the transition from dependent to independent locomotion during infant development. Compared to more arboreal macaques, infant baboons undergo a faster transition to more proximal limb mass distribution patterns. These results suggest that functional demands placed on the limbs during ontogeny have a strong impact on the development of limb mass distribution patterns.     

Hand preferences for coordinated bimanual actions in 777 great apes: implications for the evolution of handedness in hominins

Whether or not nonhuman primates exhibit population-level handedness remains a topic of considerable scientific debate. Here, we examined handedness for coordinated bimanual actions in a sample of 777 great apes including chimpanzees, bonobos, gorillas, and orangutans. We found population-level right-handedness in chimpanzees, bonobos and gorillas, but left-handedness in orangutans. Directional biases in handedness were consistent across independent samples of apes within each genus. We suggest that, contrary to previous claims, population-level handedness is evident in great apes but differs among species as a result of ecological adaptations associated with posture and locomotion. We further suggest that historical views of nonhuman primate handedness have been too anthropocentric, and we advocate for a larger evolutionary framework for the consideration of handedness and other aspects of hemispheric specialization among primates.     

New records of within-group infanticide and cannibalism in wild chimpanzees

Two cases of within-group infanticide and cannibalism were observed among the M Group chimpanzees of the Mahale Mountains, Tanzania. In both cases, victimized infants were male, 5 – 6 months of age, and in good health when killed. Four to five years have passed since the mothers of the victims immigrated into M Group as nulliparous immigrants. In one case the 2nd-ranking male was observed to detach the infant from the mother's belly. Both infants were finally killed by the alpha male after several adult males scrambled for the bodies. There was no evidence that the mothers had mated with males other than those of M Group. Nor was there evidence that the mothers had restrictive mating relationships with some of the M Group adult males. What little evidence is available shows that the mothers had mated mostly with adolescent and other immature males during their conception cycles. However, at least in one case, the mother began to mate more with adult males rather than with immature males after the infanticide. It is proposed that the function of within-group male infanticide can be explained by the male-male competition hypothesis developed for hanuman langurs and other nonhuman primates.     

Maternal Anxiety in Rhesus Macaques (Macaca mulatta)

Visual monitoring and scratching were used as behavioral indicators of maternal and social anxiety in small captive groups of rhesus macaques. Young infants were especially at risk from other group members during the first weeks of locomotion away from their mothers. Mothers received aggression from other individuals irrespective of their infants' presence or absence. The rate at which mothers scratched themselves increased significantly when their infants moved away from them and when the infants approached or were approached by individuals who frequently harassed them. The rate of maternal scratching and the rate of glancing at the infant and at other individuals when the infant was away decreased as infants grew older and became less vulnerable to harassment. In contrast, the rate of maternal scratching and visual monitoring of other individuals when the infant was in contact remained stable across the first 12 wk of lactation. The rate of maternal scratching increased when the mother-infant pair was in spatial proximity to the adult male or higher ranking adult females. Although visual monitoring and scratching showed a similar sensitivity to social variables, it is speculated that they might reflect different components of anxiety, namely, anticipation of danger and uncertainty due to motivational conflict. The results of this investigation indicate that a macaque mother's emotional reactivity to a perceived danger for herself and her infant can be measured quite accurately using the rates of visual monitoring and scratching and that the latter represent reliable tools to investigate the emotional correlates of maternal behavior in nonhuman primates.     

Empty Nest: A Case Study of Maternal Response to Separation From a Juvenile Offspring in a Captive Sumatran Orangutan (Pongo pygmaeus abelii)

Improving the welfare of captive nonhuman primates requires evaluating the stressors created by the captive environment and reducing their negative effects. Social separation, although sometimes necessary for managing the genetic diversity of captive populations of animals, causes both psychological and physiological stress in human and primate monkey infants. Few studies have examined the maternal response of great ape mothers to separation from their offspring. This article describes the behavioral changes of a mother orangutan (Pongo pygmaeus abelii) after separation from her juvenile daughter. We collected data on measures of proximity and social behavior before the separation of the mother-infant dyad and of locomotion, arboreality, abnormal behavior, solitary behavior, and vocalization both before and after separation. We observed no behavioral indications of protest but observed some indications of despair after separation: decreased locomotion, increased inactivity, and increased self-directed behavior. In addition, we observed increases in arboreality and object-oriented behavior during morning sessions. These findings suggest that mother-juvenile separation in orangutans might be less stressful for mothers than might be expected. Such research has implications for the welfare and management of captive animals.     

Empty Nest: A Case Study of Maternal Response to Separation From a Juvenile Offspring in a Captive Sumatran Orangutan (Pongo pygmaeus abelii)

Improving the welfare of captive nonhuman primates requires evaluating the stressors created by the captive environment and reducing their negative effects. Social separation, although sometimes necessary for managing the genetic diversity of captive populations of animals, causes both psychological and physiological stress in human and primate monkey infants. Few studies have examined the maternal response of great ape mothers to separation from their offspring. This article describes the behavioral changes of a mother orangutan (Pongo pygmaeus abelii) after separation from her juvenile daughter. We collected data on measures of proximity and social behavior before the separation of the mother-infant dyad and of locomotion, arboreality, abnormal behavior, solitary behavior, and vocalization both before and after separation. We observed no behavioral indications of protest but observed some indications of despair after separation: decreased locomotion, increased inactivity, and increased self-directed behavior. In addition, we observed increases in arboreality and object-oriented behavior during morning sessions. These findings suggest that mother-juvenile separation in orangutans might be less stressful for mothers than might be expected. Such research has implications for the welfare and management of captive animals.     

Nighttime Wakefulness Associated with Infant Rearing in Callithrix kuhlii

Parent-infant cosleeping occurs in human and nonhuman primates, yet studies on the impact of cosleeping on parental sleep patterns have been limited to human mothers. We examined the effects of cosleeping on the nighttime wakefulness of a biparental New World primate, Wied's black tufted-ear marmoset (Callithrix kuhlii). We compared the sleep patterns of marmoset parents caring for young infants to those without infants, using an 8 mm videocamera and timelapse VCR under infrared illumination. The presence of young infants significantly impacted the sleep of mothers but not fathers. In fact, mothers rearing young infants were awake >3 times as often as mothers without infants. We also examined the nighttime wakefulness of marmoset parents across the first 9 weeks of infant life (birth through weaning). Although callitrichid mothers tend to reduce their daytime investment in offspring very early in infant life by relinquishing the care of infants to fathers and alloparents, increased nighttime wakefulness was not limited to the early postpartum period for the mothers. Instead, mothers exhibited more nighttime wakefulness than fathers did across the first 9 weeks of infant life. Our results indicate that the presence of infants has a greater impact on the sleep patterns of Callithrix kuhlii mothers than fathers, suggesting that mothers are more involved in infant care than previously realized and that fathers are not nearly as involved in nighttime care as their behavior during the day would suggest.     

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.     

Generation of transgenic monkeys with human inherited genetic disease

Modeling human diseases using nonhuman primates including chimpanzee, rhesus, cynomolgus, marmoset and squirrel monkeys has been reported in the past decades. Due to the high similarity between nonhuman primates and humans, including genome constitution, cognitive behavioral functions, anatomical structure, metabolic, reproductive, and brain functions; nonhuman primates have played an important role in understanding physiological functions of the human body, clarifying the underlying mechanism of human diseases, and the development of novel treatments for human diseases. However, nonhuman primate research has been restricted to cognitive, behavioral, biochemical and pharmacological approaches of human diseases due to the limitation of gene transfer technology in nonhuman primates. The recent advancement in transgenic technology that has led to the generation of the first transgenic monkey in 2001 and a transgenic monkey model of Huntington’s disease (HD) in 2008 has changed that focus. The creation of transgenic HD monkeys that replicate key pathological features of human HD patients further suggests the crucial role of nonhuman primates in the future development of biomedicine. These successes have opened the door to genetic manipulation in nonhuman primates and a new era in modeling human inherited genetic disorders. We focused on the procedures in creating transgenic Huntington’s disease monkeys, but our work can be applied to transgenesis in other nonhuman primate species.     

Historical perspective of genetic research with nonhuman primates

Genetics became firmly established as a scientific discipline early in the twentieth century, but major genetic research programs that involve nonhuman primates have been initiated only in the last two decades. Considerable activity in this area has been stimulated by the concurrent development of powerful techniques for detecting variability in chromosomes, proteins, and DNA; the establishment of pedigreed breeding colonies; and the recognition that nonhuman primates are ideally suited as models of human disease and social structure. The subdisciplines of cytogenetics, immunogenetics, and biochemical genetics have established a firm basis for biomedical and evolutionary research with nonhuman primates, and they will contribute greatly to future research initiatives. More recently, the advent of molecular genetics has enhanced the opportunities for research; and the exploration of nonhuman primates as potential models for genetically mediated diseases has been richly rewarded.We stand at the threshold of a new and exciting era in genetic research with nonhuman primates. The results of research programs already underway not only will provide more definitive answers about the origin of man, but also will play a critical role in solving the health-related problems of the present and of the future.     

Death among geladas (Theropithecus gelada): a broader perspective on mummified infants and primate thanatology

Despite intensive study in humans, responses to dying and death have been a neglected area of research in other social mammals, including nonhuman primates. Two recent reports [Anderson JR, Gillies A, Lock LC. 2010. Pan thanatology. Current Biology 20:R349–R351; Biro D, Humle T, Koops K, Souse C, Hayashi M, Matsuzawa T. 2010. Chimpanzee mothers at Bossou, Guinea carry the mummified remains of their dead infants. Current Biology 20:R351–R352] offered exciting new insights into behavior toward dying and dead conspecifics in our closest living relatives—chimpanzees. Here, we provide a comparative perspective on primate thanatology using observations from a more distant human relative—gelada monkeys (Theropithecus gelada)—and discuss how gelada reactions to dead and dying groupmates differ from those recently reported for chimpanzees. Over a 3.75‐year study period, we observed 14 female geladas at Guassa, Ethiopia carrying dead infants from 1 hr to ≥48 days after death. Dead infants were carried by their mothers, other females in their group, and even by females belonging to other groups. Like other primate populations in which extended (>10 days) infant carrying after death has been reported, geladas at Guassa experience an extreme climate for primates, creating conditions which may favor slower rates of decomposition of dead individuals. We also witnessed the events leading up to the deaths of two individuals and the responses by groupmates to these dying individuals. Our results suggest that while chimpanzee mothers are not unique among primates in carrying their dead infants for long periods, seemingly “compassionate” caretaking behavior toward dying groupmates may be unique to chimpanzees among nonhuman primates (though it remains unknown whether such “compassionate” behavior occurs outside captivity). Am. J. Primatol. 73:405–409, 2011. © 2010 Wiley‐Liss, Inc.     

Adoption in Anthropoid primates

Reports of adoption in nonhuman primates are reviewed, including spontaneous adoptions of orphans or infants whose mothers have been removed from the group, temporary adoptions of offspring of sick mothers, adoptions arising out of kidnapping, and adoptions resulting from manipulations involving presenting infants to adults. Adoptive behavioral patterns resemble nonadoptive alloparental patterns. The literature indicates certain trends: adult females, especially if lactating or in the late stages of pregnancy, are most likely to adopt neonates. Older infants are more likely to be adopted by juveniles or by adult males. Weaned or weanable orphans that get adopted have reasonable chances of survival, while orphans still reliant on milk are unlikely to survive. An infant adopted by an adult female will develop socially as a member of the female’s matriline. Adoptions involving closely related individuals are consistent with kin-selection theory. Others appear to reflect “reproductive error” arising out of an attraction to young infants. Yet other cases might reflect reciprocal altruism. Continued documentation of cases of adoption will yield more data on costs and benefits and on whether rates and forms of adoption, such as alloparental behavior, vary systematically with social systems.     

Uniqueness of primate forelimb posture during quadrupedal locomotion

Among the characteristics that are thought to set primate quadrupedal locomotion apart from that of nonprimate mammals are a more protracted limb posture and larger limb angular excursion. However, kinematic aspects of primate or nonprimate quadrupedal locomotion have been documented in only a handful of species, and more widely for the hind than the forelimb. This study presents data on arm (humerus) and forelimb posture during walking for 102 species of mammals, including 53 nonhuman primates and 49 nonprimate mammals. The results demonstrate that primates uniformly display a more protracted arm and forelimb at hand touchdown of a step than nearly all other mammals. Although primates tend to end a step with a less retracted humerus, their total humeral or forelimb angular excursion exceeds that of other mammals. It is suggested that these features are components of functional adaptations to locomotion in an arboreal habitat, using clawless, grasping extremities.     

The ontogeny and phylogeny of children’s object and fantasy play

We examine the ontogeny and phylogeny of object and fantasy play from a functional perspective. Each form of play is described from an evolutionary perspective in terms of its place in the total time and energy budgets of human and nonhuman juveniles. As part of discussion of functions of play, we examine sex differences, particularly as they relate to life in the environment of evolutionary adaptedness and economic activities of human and nonhuman primates. Object play may relate to foraging activities. Although fantasy play has been viewed as limited to humans, we speculate that certain types of fantasy play may be present in some nonhuman primates. Fantasy play may enable juveniles to see situations from different perspectives. We conclude that fantasy play may have immediate effects and object play may have deferred effects.     

Development of schematic face preference in macaque monkeys

This study investigated schematic face preferences in infant macaque monkeys. We also examined the roles of whole and partial features in facial recognition and related developmental change. Sixteen infant monkeys, all less than two months old, were presented with two stimulus pairs. Pair A consisted of "face" and "parts," with the components representing facial parts (i.e. eyes, mouth, and nose). Pair B consisted of "configuration" and "linear," each including three black squares. In each pair, one of two stimuli represented a facial configuration, namely "face" and "configuration." Visual following responses toward each stimulus were analyzed. The results revealed an early preference for schematic faces in these nonhuman primates. Infants less than one month of age showed a preference only for a stimulus that contained only whole facial configuration (i.e. "configuration" in Pair B). One-month-old macaque infants showed a preference only for "face" but not for "configuration." This result means that their preference at that age was affected by both the shape of the components and the overall configuration. As the developmental change and the contribution of both facial features are similar to those in human infants, it may suggest that primates share common cognitive processes in early schematic face recognition.     

Diversity and temporal dynamics of primate milk microbiomes

Milk is inhabited by a community of bacteria and is one of the first postnatal sources of microbial exposure for mammalian young. Bacteria in breast milk may enhance immune development, improve intestinal health, and stimulate the gut‐brain axis for infants. Variation in milk microbiome structure (e.g., operational taxonomic unit [OTU] diversity, community composition) may lead to different infant developmental outcomes. Milk microbiome structure may depend on evolutionary processes acting at the host species level and ecological processes occurring over lactation time, among others. We quantified milk microbiomes using 16S rRNA high‐throughput sequencing for nine primate species and for six primate mothers sampled over lactation. Our data set included humans (Homo sapiens, Philippines and USA) and eight nonhuman primate species living in captivity (bonobo [Pan paniscus], chimpanzee [Pan troglodytes], western lowland gorilla [Gorilla gorilla gorilla], Bornean orangutan [Pongo pygmaeus], Sumatran orangutan [Pongo abelii], rhesus macaque [Macaca mulatta], owl monkey [Aotus nancymaae]) and in the wild (mantled howler monkey [Alouatta palliata]). For a subset of the data, we paired microbiome data with nutrient and hormone assay results to quantify the effect of milk chemistry on milk microbiomes. We detected a core primate milk microbiome of seven bacterial OTUs indicating a robust relationship between these bacteria and primate species. Milk microbiomes differed among primate species with rhesus macaques, humans and mantled howler monkeys having notably distinct milk microbiomes. Gross energy in milk from protein and fat explained some of the variations in microbiome composition among species. Microbiome composition changed in a predictable manner for three primate mothers over lactation time, suggesting that different bacterial communities may be selected for as the infant ages. Our results contribute to understanding ecological and evolutionary relationships between bacteria and primate hosts, which can have applied benefits for humans and endangered primates in our care.     

Birth intervention and non-maternal infant-handling during parturition in a nonhuman primate

Direct intervention in infant delivery by non-parturient individuals is a rare phenomenon in nonhuman primates. In contrast, birth assistance by other individuals, or the practice of midwifery, is universal among human societies and generally believed to be a behavior unique to our species. It has been proposed that the enlarged head of the human fetus and the relatively narrow birth canal constrained by bipedalism has made human parturition more difficult than in nonhuman primates, and these anatomic challenges have led to the rotation of the fetus in the birth canal and an occiput anterior (i.e., backward-facing) orientation of emergence. These characteristics have hindered the mother’s ability to self-assist the delivery of the infant, therefore necessitating assistance by other individuals or midwives for successful birth. Here we report the first high-definition video recordings of birth intervention behavior in a wild nonhuman primate, the white-headed langur (Trachypithecus leucocephalus). We observed that while a primiparous female gave birth to an infant in an occiput posterior (i.e., forward-facing) orientation, a multiparous female intervened in the delivery by manually pulling the infant out of the birth canal and cared for it in the following hours. Our finding shows extensive social interactions throughout parturition, and presents an unequivocal case of non-maternal intervention with infant birth in a nonhuman primate.     

The evolution of human speech: The role of enhanced breathing control

Many cognitive and physical features must have undergone change for the evolution of fully modern human language. One neglected aspect is the evolution of increased breathing control. Evidence presented herein shows that modern humans and Neanderthals have an expanded thoracic vertebral canal compared with australopithecines and Homo ergaster, who had canals of the same relative size as extant nonhuman primates. Based on previously published analyses, these results demonstrate that there was an increase in thoracic innervation during human evolution. Possible explanations for this increase include postural control for bipedalism, increased difficulty of parturition, respiration for endurance running, an aquatic phase, and choking avoidance. These can all be ruled out, either because of their evolutionary timing, or because they are insufficiently demanding neurologically. The remaining possible functional cause is increased control of breathing for speech. The main muscles involved in the fine control of human speech breathing are the intercostals and a set of abdominal muscles which are all thoracically innervated. Modifications to quiet breathing are essential for modern human speech, enabling the production of long phrases on single expirations punctuated with quick inspirations at meaningful linguistic breaks. Other linguistically important features affected by variation in subglottal air pressure include emphasis of particular sound units, and control of pitch and intonation. Subtle, complex muscle movements, integrated with cognitive factors, are involved. The vocalizations of nonhuman primates involve markedly less respiratory control. Without sophisticated breath control, early hominids would only have been capable of short, unmodulated utterances, like those of extant nonhuman primates. Fine respiratory control, a necessary component for fully modern language, evolved sometime between 1.6 Mya and 100,000 ya. Am J Phys Anthropol 109:341–363, 1999. © 1999 Wiley-Liss, Inc.     

A comparative psychophysical approach to visual perception in primates

Studies on the visual processing of primates, which have well developed visual systems, provide essential information about the perceptual bases of their higher-order cognitive abilities. Although the mechanisms underlying visual processing are largely shared between human and nonhuman primates, differences have also been reported. In this article, we review psychophysical investigations comparing the basic visual processing that operates in human and nonhuman species, and discuss the future contributions potentially deriving from such comparative psychophysical approaches to primate minds.