Lipsmacking Imitation Skill in Newborn Macaques Is Predictive of Social Partner Discrimination

Newborn rhesus macaques imitate facial gestures even after a delay, revealing the flexible nature of their early communicative exchanges. In the present study we examined whether newborn macaques are also sensitive to the identities of the social partners with whom they are interacting. We measured infant monkeys'' (n = 90) lipsmacking and tongue protrusion gestures in a face-to-face interaction task with a human experimenter in the first week of life. After a one-minute delay, the same person who previously presented gestures or a different person returned and presented a still face to infants. We had two primary predictions: (1) infants would demonstrate higher rates of overall gesturing, and especially lipsmacking—an affiliative gesture—to a familiar person, compared to a novel person, and (2) infants'' imitative skills would positively correlate with gestures to familiar, but not unfamiliar, social partners, as both abilities may reflect a strong general social interest. We found that overall infants did not produce more gestures or more lipsmacking when approached by a familiar person compared to a novel person; however, we did find individual differences in infants'' social responsiveness: lipsmacking imitation was positively correlated with lipsmacking during the return period when the person was the same (p = .025), but not when the person was novel (p = .44). These findings are consistent with the notion that imitative skill is reflective of infants'' more general interest in social interactions.     

Is lipsmacking an indicator of social status in baboons?

Lipsmacking is performed by many Old World monkey species, and some studies of baboons and macaques suggest that lipsmacking may be associated with social status. We studied 60 adult anubis baboons (Papio cynocephalus anubis) for 18 months, measured social status and the rate of lipsmacking, and used these data to test the hypothesis that lipsmacking is related to social status. Our results indicate that social status and lipsmacking were not significantly correlated for either males or females. Analysis of lipsmacking in relation to social class (high vs. low) showed no significant difference between status classes for either sex. Lipsmacking was, however, found to be positively associated with affinitive behaviors. These results suggest that baboon lipsmacking provides positive social communication independently of social status.     

A comparative study of neonatal skeletal development in Cebus and other primates

Comparisons of hand/wrist radiographs of neonatal Cebus albifrons (n = 14) and Cebus apella (n = 4) with those of Saimiri sciureus boliviensis (n = 9) and Macaca mulatta (n = 63) reveal that the cebid monkeys show much less skeletal ossification at birth than macaques. Differences in gestation time alone cannot account for the differences in skeletal maturity at birth in the two groups of monkeys. The skeletal precocity of the newborn macaques indicates that their ossification either begins earlier in gestation or proceeds at a more rapid rate, or both. This, in turn, raises questions about the timing of organogenesis and gestational comparability in cebid and cercopithecid monkeys. The advanced state of ossification seen in macaques at birth is not typical of other groups of anthropoid primates, including Cebus, Saimiri, Pan and Homo, and may represent an ontogenetic specialization.     

Immunization of newborn rhesus macaques with simian immunodeficiency virus (SIV) vaccines prolongs survival after oral challenge with virulent SIVmac251

There is an urgent need for active immunization strategies that, if administered shortly after birth, could protect infants in developing countries from acquiring human immunodeficiency virus (HIV) infection through breast-feeding. Better knowledge of the immunogenic properties of vaccine candidates in infants and of the effect of maternal antibodies on vaccine efficacy will aid in the development of such a neonatal HIV vaccine. Simian immunodeficiency virus (SIV) infection of infant macaques is a useful animal model of pediatric HIV infection with which to address these questions. Groups of infant macaques were immunized at birth and 3 weeks of age with either modified vaccinia virus Ankara (MVA) expressing SIV Gag, Pol, and Env (MVA-SIVgpe) or live-attenuated SIVmac1A11. One MVA-SIVgpe-immunized group had maternally derived anti-SIV antibodies prior to immunization. Animals were challenged orally at 4 weeks of age with a genetically heterogeneous stock of virulent SIVmac251. Although all animals became infected, the immunized animals mounted better antiviral antibody responses, controlled virus levels more effectively, and had a longer disease-free survival than the unvaccinated infected monkeys. Maternal antibodies did not significantly reduce the efficacy of the MVA-SIVgpe vaccine. In conclusion, although the tested vaccines delayed the onset of AIDS, further studies are warranted to determine whether a vaccine that elicits stronger early immune responses at the time of virus exposure may be able to prevent viral infection or AIDS in infants.     

人工投食行为对非人灵长类社会生态的影响

近年来,国内开展了对几种非人灵长类投食群的研究。借鉴日本猴(Macaca fuscata)、恒河猴(M.mulatta)和黑猩猩(Pan troglodytes)长期积累的研究经验,有利于我们减少人工投食对非人灵长类带来的不利影响,也有利于推动国内非人灵长类社会生态学的深入研究。本文通过比较这三种灵长类野生群和投食群之间的差异,量化地分析了人工投食对灵长类动物社会生态学方面的影响。结果表明在社会行为方面,人工投食会导致灵长类动物的聚集、增加争斗频率、改变个体间等级关系、延缓分群现象、影响活动域和增加新兴行为。在种群数量方面,人工投食会缩短雌性性成熟时间、增加出生率和婴猴存活率、减少成年猴死亡率。而人工投食对雄性性成熟、出生间隔等方面的影响仍需要进一步考证。最后我们讨论了人工投食行为的利弊,并建议应谨慎和妥善地实施人工投食,和对非人灵长类投食群进行合理的监管。     

The question of animal culture

In this paper I consider whether traditional behaviors of animals, like traditions of humans, are transmitted by imitation learning. Review of the literature on problem solving by captive primates, and detailed consideration of two widely cited instances of purported learning by imitation and of culture in free-living primates (sweet-potato washing by Japanese macaques and termite fishing by chimpanzees), suggests that nonhuman primates do not learn to solve problems by imitation. It may, therefore, be misleading to treat animal traditions and human culture as homologous (rather than analogous) and to refer to animal traditions as cultural.     

Interannual variability in fruit abundance and the reproductive seasonality in Sumatran Long-tailed macaques (Macaca fascicularis)

In an environment with a seasonal food supply, most primate species show birth peaks which precede the peak food period by some two to five months. Sumatran Long-tailed macaques (Macaca fascicularis), however, showed birth peaks during or after the fruit peak. Years of high birth rates and early birth peaks alternated with years of low birth rates and late peaks. The timing of births was strongly influenced by a female's condition, which depends on food supply and her previous reproductive history. Pregnant females were more active than other females, whereas females with young infants were less active.
The unusual timing of births is ascribed to the unpredictability of the height of the annual fruit peak. This hypothesis is supported by the reproductive patterns of other South-east Asian primates and by a model comparing the two types of reproductive timing. Further differences between the two strategies of reproductive timing are predicted.     

Imitation,objects, tools,and the rudiments of language in human ontogeny

Human beings are imitative generalists. We can immediately imitate a wide range of behaviors with great facility, whether they be vocal maneuvers, body postures, or actions on objects. The ontogeny of this skill has been an enduring question in developmental psychology. Classical theory holds that the ability to imitate facial gestures is a milestone that is passed at about one year. Before this time infants are thought to lack the perceptual-cognitive sophistication necessary to match a gesture they can see with one they cannot see themselves perform. A second developmental milestone is the capacity for deferred imitation, i.e. imitation of an absent model. This is said to emerge at about 18 months, in close synchrony with other higher-order activities such as object permanence and tool use, as part of a general cognitive shift from a purely sensory-motor level of functioning to one that allows language. Research suggests that the imitative capacity of young infants has been underestimated. Human infants are capable of imitating facial gestures at birth, with infants less than one day old manifesting this skill. Moreover recent experiments have established deferred imitation well before the predicted age of 18 months. Studies discussed here show that 9-month-olds can duplicate acts after a delay of 24 hours, and that 14-month-olds can retain and duplicate as many as five actions over a 1-week delay. These new findings re-raise questions about the relation between nonverbal cognitive development and language development: What aspects, if any, of these two domains are linked? A hypothesis is delineated that predicts certain very specific relations between particular cognitive and semantic achievements during the one-word stage, and data are reported supporting this hypothesis. Specifically, relations are reported between: (a) the development of object permanence and the use of words encoding disappearance, (b) means-ends understanding (as manifest in tool use) and words encoding success and failure, and (c) categorization behavior and the onset of the naming explosion. This research on human ontogeny suggests close and highly specific links between aspects of early language and thought.     

Infant‐Directed Communication in Lowland Gorillas (Gorilla gorilla): Do Older Animals Scaffold Communicative Competence in Infants?

Infant-directed speech is a linguistic phenomenon in which adults adapt their language when addressing infants in order to provide them with more salient linguistic information and aid them in language acquisition. Adult-directed language differs from infant-directed language in various aspects, including speech acoustics, syntax, and semantics. The existence of a "gestural motherese" in interaction with infants, demonstrates that not only spoken language but also nonvocal modes of communication can become adapted when infants are recipients. Rhesus macaques are so far the only nonhuman primates where a similar phenomenon to "motherese" has been discovered: the acoustic spectrum of a particular vocalization of adult females may be altered when the addressees are infants. The present paper describes how gorillas adjust their communicative strategies when directing intentional, nonvocal play signals at infants in the sense of a "nonvocal motherese." Animals of ages above infancy use a higher rate of repetitions and sequences of the tactile sensory modality when negotiating play with infants. This indicates that gorillas employ a strategy of infant-specific communication.     

Social behaviour of stump-tailed macaques in captivity

Facial expressions and gestures seen in eight wild caught adult and three laboratory born stump-tailed macaques are described. Systematic observations, designed to show the association of these with attack, fleeing, grooming, or copulating are reported. The behaviour is in general very similar to that of other macaques.However, we find that Presenting and Lipsmacking are given by animals who are likely to win or lose fights and are shown to babies. These are clearly not just appeasing in function (reducing attack) but also reassuring (reducing fleeing). Two forms of non-sexual Presenting were found to follow and lead to different behaviour. Copulation appears to be different from that described in rhesus, ejaculation occuring on each mounting, which last for around one minute. In our animals the males bit the females during the later stages of copulation, but seldom showed any signs of aggression when not mounting.Grin-lipsmacking (lipsmacking with lips retracted exposing the teeth) is associated with fleeing, with changing from fighting to grooming and with copulation. A link between these situations may be provided earlier in development by the observation that mothers comfort frightened, Grin-lipsmacking babies by manipulating the external genitalia.     

Neonatal abandonment in Japanese macaques

This study analyzed long-term demographic data relative to a captive colony of Japanese macaques (Macaca fuscata) in order to evaluate factors predicting increased probability of infant neonatal abandonment. Overall, 7.7% of liveborn infants were abandoned at birth. Probability of abandonment was significantly increased in primiparous and, to a lesser extent, low-ranking mothers. Primiparous mothers abandoned about 40% of their infants at birth. Mother age and infant sex had no independent effects on the probability of neonatal abandonment. Primiparous mothers that did not abandon their infants suffered increased infant mortality and showed longer interbirth intervals compared to same-age multiparous mothers. These results are partially consistent with adaptive hypotheses predicting maternal divestment under unfavorable conditions, and with proximate explanations linking abandonment to inexperience and stress.     

Human infants and baboons show the same pattern of handedness for a communicative gesture

To test the role of gestures in the origin of language, we studied hand preferences for grasping or pointing to objects at several spatial positions in human infants and adult baboons. If the roots of language are indeed in gestural communication, we expect that human infants and baboons will present a comparable difference in their pattern of laterality according to task: both should be more right-hand/left-hemisphere specialized when communicating by pointing than when simply grasping objects. Our study is the first to test both human infants and baboons on the same communicative task. Our results show remarkable convergence in the distribution of the two species' hand biases on the two kinds of tasks: In both human infants and baboons, right-hand preference was significantly stronger for the communicative task than for grasping objects. Our findings support the hypothesis that left-lateralized language may be derived from a gestural communication system that was present in the common ancestor of baboons and humans.     

Maternal Responsiveness Increases during Pregnancy and after Estrogen Treatment in Macaques

Maternal responsiveness in primates has long been considered emancipated from endocrine factors and entirely dependent on experience and cognition. Here we report that group-living pigtail macaque females increased their rate of interaction with infants in the last weeks of pregnancy in correspondence with an increase in plasma levels of estradiol and progesterone. Estrogen treatment increased the rate at which ovariectomized rhesus females interacted with infants. This is the first evidence that steroid hormones influence maternal responsiveness in anthropoid primates. All untreated ovariectomized females and nonpregnant females interacted with infants, indicating that although estrogen can enhance responsiveness to infants, ovarian or pregnancy hormones are not necessary for the expression of infant-directed behavior in female macaques. The findings of this study suggest fundamental similarities, rather than differences, in the endocrine modulation of maternal responsiveness in primates and other mammals.     

Grandmothers care for orphans in a provisioned troop of Japanese macaques (<Emphasis Type="Italic">Macaca fuscata</Emphasis>)

This study reports cases in which grandmothers and other closely related adult females cared for orphans in the Arashiyama E-troop, a provisioned troop of Japanese macaques (Macaca fuscata). I observed the behavioral patterns of three orphans (aged 1, 2, and 3 years, respectively). The grandmothers cared for two orphans, while three other closely related adult females cared for the rest of the orphans whose grandmothers were absent. These observations differ from those of previous studies that reported that grandmothers were indifferent towards orphans. This intraspecific variation may be attributed to the demographic conditions of the troop in this study, which had only a few related nulliparous adult females, as a result of artificial birth control. In this group, adult females showed decreased fecundity and an increased interbirth interval as they received birth control treatment; thus, in the absence of their own dependent infants, these females may have invested time in the care of related orphans. Although caregiving by grandmothers is believed to be rare or insignificant in primates, this study suggests that grandmothers and other closely related adult females play an important role for orphans in troops with few related adult females.     

Recombinant vesicular stomatitis virus vector mediates postexposure protection against Sudan Ebola hemorrhagic fever in nonhuman primates

Recombinant vesicular stomatitis virus (VSV) vectors expressing homologous filoviral glycoproteins can completely protect rhesus monkeys against Marburg virus when administered after exposure and can partially protect macaques after challenge with Zaire ebolavirus. Here, we administered a VSV vector expressing the Sudan ebolavirus (SEBOV) glycoprotein to four rhesus macaques shortly after exposure to SEBOV. All four animals survived SEBOV challenge, while a control animal that received a nonspecific vector developed fulminant SEBOV hemorrhagic fever and succumbed. This is the first demonstration of complete postexposure protection against an Ebola virus in nonhuman primates and provides further evidence that postexposure vaccination may have utility in treating exposures to filoviruses.     

Language beyond action.

The discovery of mirror neurons in macaques and of a similar system in humans has provided a new and fertile neurobiological ground for rooting a variety of cognitive faculties. Automatic sensorimotor resonance has been invoked as the key elementary process accounting for disparate (dys)functions, like imitation, ideomotor apraxia, autism, and schizophrenia. In this paper, we provide a critical appraisal of three of these claims that deal with the relationship between language and the motor system. Does language comprehension require the motor system? Was there an evolutionary switch from manual gestures to speech as the primary mode of language? Is human communication explained by automatic sensorimotor resonances? A positive answer to these questions would open the tantalizing possibility of bringing language and human communication within the fold of the motor system. We argue that the available empirical evidence does not appear to support these claims, and their theoretical scope fails to account for some crucial features of the phenomena they are supposed to explain. Without denying the enormous importance of the discovery of mirror neurons, we highlight the limits of their explanatory power for understanding language and communication.     

Growth and developmental outcomes of three high-risk infant rhesus macaques (Macaca mulatta)

Infants classified as "high risk" are born with a greater chance of developing medical complications at birth, and may have cognitive and other developmental complications later in life. Very few reports exist regarding the survival and outcome of such infants in primate colonies. Here we present early growth and developmental data on three high-risk infant rhesus macaques (one female and two males) that were born either with intrauterine growth restriction (IUGR; born below the 1st birth weight percentile for gestational age) or extremely prematurely (at gestational days 128 and 140; mean full-term gestation=164 days). We compared the outcome of these infants with that of healthy controls born at term and found no gross developmental delays in these infants with respect to growth, neonatal reflex and motor skill development, early cognitive development, or social behavior. Neurological and cognitive assessments were compared in terms of both postnatal and gestational age. The survival of these infants was dependent on a 24-hr staffed nursery and a fluid protocol that catered to each high-risk infant's individual needs. When such measures are implemented, infants such as these have a good chance of survival and can serve as excellent models for high-risk human babies and their subsequent development.     

The Hand That Feeds the Monkey: Mutual Influence of Humans and Rhesus Macaques (<Emphasis Type="Italic">Macaca mulatta</Emphasis>) in the Context of Provisioning

Historically, humans and other primates (primates henceforth) have coexisted across cultures and contexts, and many primate populations use anthropogenic food sources as their main or supplementary food. While primates may actively forage for such food, they are also directly provisioned by humans in many regions. Ethnoprimatology views humans and primates as cohabitants of integrated socioecological spaces who mutually influence each other’s ecologies and social lives. We contextualized provisioning of primates by humans within an ethnoprimatological framework and examined if the availability of anthropogenic food affected primate diets or the amount of time primates spent in anthropogenic habitats and whether primates influenced the human act of provisioning. To this end, we used scan sampling on a group of rhesus macaques across a year, and conducted interviews with 86 people who paused at a nearby tea shop for refreshments. We found that the macaques’ consumption of natural resources and dietary diversity decreased, and they spent more time in human-modified habitats when provisioned food was available. We also found that particular behaviors of the provisioned macaques stimulated provisioning by humans. Our findings show that provisioning influences macaque feeding ecology and habitat use, and that the behavior of the macaques themselves drives people to provide them with food subsidies, illustrating a complex web of interactions between the sympatric species.     

Growth, weaning and maternal investment from a comparative perspective

The process of weaning is related to a critical or threshold body weight attained by offspring among large-bodied mammals; the anthropoid primates, ungulates and pinnipeds. While weaning weight was allometrically related to maternal weight in interspecific comparisons, it was isometrically related to neonatal weight. When a neonate had grown to four times its birth weight, it was weaned. Differences between taxonomic groups were found only among the fasting phocids, where weanlings attained a lower, but proportional, weight. The duration of lactation was only weakly allometrically related to maternal or neonatal weight, and varied between individuals intraspecifically as a function of maternal condition. The time to weaning appears to be ecologically sensitive rather than to reflect interspecific life-history variation, in that, irrespective of the time to weaning, similar proportional weights appear to be attained. Interspecific similarities in threshold weaning weights are suggested to result from constraints on maternal abilities to meet energetic requirements of offspring through lactation after infants attain a threshold weight.