Effect of Mother's Dominance Rank on Offspring Temperament in Infant Rhesus Monkeys (Macaca mulatta)

In humans, temperament plays an important role in socialization and personality. Some temperaments, such as behavioral inhibition are associated with an increased risk for psychopathology. Nonhuman primates can serve as a model for neurobiological and developmental contributions to emotional development and several recent studies have begun to investigate temperament in nonhuman primates. In rhesus monkeys, dominance rank is inherited from the mother and is associated with social and emotional tendencies that resemble differences in temperament. The current study assessed differences in temperament in infant rhesus monkeys as a function of maternal dominance rank. Temperament was assessed in 26 infants (13 males) from birth until 6 months of age with a battery that included Brazelton test, human intruder test, human intruder‐startle, cortisol stress reactivity, and home cage observations of interactions with peers and the mother. Throughout testing, infants lived with their mothers and a small group of other monkeys in indoor/outdoor runs. Dominance rank of the mothers within each run was rated as either low/middle (N = 18, 9 male) or high/alpha (N = 8, 4 female). Infants of high‐ranking mothers displayed more intruder‐directed aggression and reduced startle potentiation in the human intruder tests. Dominant offspring also had reduced levels cortisol and startle across development and spent more time away from mothers in the interaction tests. These results suggest that dominance of the mother may be reflected in behavioral reactivity of infants early in life. These findings set up future studies, which may focus on contributing factors to both dominance and temperament such as genetics, rearing, and socialization. Such factors are likely to interact across development in meaningful ways. These results also suggest future human‐based studies of a similar relationship may be warranted, although social dominance is clearly more complex in human than macaque societies. Am. J. Primatol. 75:65‐73, 2013. Published 2012 by Wiley Periodicals, Inc.?     

Estimates of milk constituents from lactating bonnet macaque (Macaca radiata) mothers between two and seven months post‐partum

Background The literature regarding milk composition in non‐human primates collected across offspring development is limited. We assayed milk samples from bonnet macaque (Macaca radiata) mothers as part of studies characterizing development of this species. Methods Milk was obtained when possible longitudinally from seven lactating bonnet macaque mothers. Samples were frozen until analysis. Individual samples were analyzed to determine the concentrations of electrolytes including sodium, potassium, calcium, chloride, and magnesium, as well as urea, protein, lipids, glucose, and lactose. Results A trend for increased lipids as well as protein percentage was noted with increasing infant age. Chloride and calcium showed an increase with age, whereas other electrolytes remained relatively stable across development. Conclusions The composition of the milk of this particular macaque species was similar to other Old World primates as well as humans. These data add to the limited information available on milk constituents among mammals.     

Regressive periods in primate behavioral development with reference to other mammals

Studies on behavioral development in 12 species of monkeys indicate normal fluctuations of high frequency of nipple contact. These periods decrease in intensity as the infant develops and occur at similar times in development in the 12 species. Literature on 11 species of primates and three species of non-primates indicates similar regressions in mother-infant contact, which implies a common genetic basis for the phenomenon.     

Grooming,kinship, and co‐feeding in captive spider monkeys (Ateles geoffroyi)

Allo‐grooming is perhaps the most powerful affiliative behavior observed in non‐human primates. However, the functional significance of grooming in New World monkeys has not yet been fully understood, perhaps because grooming is less frequently observed in platyrrhines. To differentiate the potential role of affiliative investment and/or kinship on sharing access to food (co‐feeding) in spider monkeys, behavioral data on grooming, embracing, and feeding were collected from two different groups of captive study subjects: a familiar/kin group and a non‐familiar/non‐kin group. The results of this study suggest that family‐related spider monkeys that engage in grooming tend to share access to food resources more than unfamiliar conspecifics that do not groom. One explanation for this difference is that the unfamiliar study subjects had not yet invested in the affiliative social network, were not reciprocating their affiliative investments and hence, had a higher tendency toward single animal monopolizing resources. Degree of relatedness alone was not found to be a determinant for sharing the access to food, suggesting that familiarity in spider monkeys is based on the extent to which animals invest in affiliative relationships. In this study, only animals that had engaged in long‐term grooming and recognized each other as familiar shared the access to food. Therefore, it might be likely that in spider monkeys, long‐term grooming of high intensity has to be developed for co‐feeding to occur. Zoo Biol 20:293–303, 2001. © 2001 Wiley‐Liss, Inc.     

Fire and home range expansion: A behavioral response to burning among savanna dwelling vervet monkeys (Chlorocebus aethiops)

The behavioral adaptations of primates to fire‐modified landscapes are of considerable interest to anthropologists because fire is fundamental to life in the African savanna—the setting in which genus Homo evolved. Here we report the behavioral responses of a savanna‐dwelling primate, vervet monkeys (Chlorocebus aethiops), to fire‐induced ecological change. Using behavioral and spatial data to characterize ranging patterns prior to and postburn and between burn and nonburn years, we show that these primates inhabiting small, spatially bound, riverine habitats take advantage of newly burned savanna landscapes. When subjects encountered controlled fires, they did not flee but instead avoided the path of the fire seemingly unbothered by its approach. After fire, the primates' home range expanded into newly burned but previously unused areas. These results contribute to understanding the response of non‐human primates to fire‐modified landscapes and can shed light on the nature and scope of opportunities and constraints posed by the emergence of fire‐affected landscapes in the past. Results also expose deficiencies in our knowledge of fire‐related behavioral responses in the primate lineage and highlight the need for further investigation of these responses as they relate to foraging opportunities, migration, resource use, and especially fire‐centric adaptations in our own genus. Am J Phys Anthropol 154:554–560, 2014. © 2014 Wiley Periodicals, Inc.     

Arm movements in monkeys: behavior and neurophysiology

Reaching to objects of interest is very common in the behavioral repertoire of primates. Monkeys possess keen binocular vision and make graceful and accurate arm movements. This review focuses on behavioral and neurophysiological aspects of eye-hand coordination in behaving monkeys, including neural coding mechanisms at the single cell level and in neuronal populations. The results of these studies have converged to a common behavioral-neurophysiological ground and provided a springboard for studies of brain mechanisms underlying motor cognitive function.     

Increased inherent intestinal granzyme B expression may be associated with SIV pathogenesis in Asian non-human primates

Background Unlike Asian non‐human primates, chronically SIV‐infected African non‐human primates (NHP) display a non‐pathogenic disease course. The different outcomes may be related to the development of an SIV‐mediated breach of the intestinal mucosa in the Asian species that is absent in the African animals. Methods To examine possible mechanisms that could lead to the gut breach, we determined whether the colonic lamina propria (LP) of SIV‐naïve Asian monkeys contained more granzyme B (GrB) producing CD4 T cells than did that of the African species. GrB is a serine protease that may disrupt mucosal integrity by damaging tight junction proteins. Results We found that the colonic LP of Asian NHP contain more CD4⁺/GrB⁺ cells than African NHP. We also observed reduced CD4 expression on LP T cells in African green monkeys. Conclusion Both phenotypic differences could protect against SIV‐mediated damage to the intestinal mucosa and could lead to future therapies in HIV⁺ humans.     

Comparison of rectal and tympanic core body temperature measurement in adult Guyanese squirrel monkeys (Saimiri sciureus sciureus)

Background Measuring core body temperature in a manner that is safe for animals and veterinary personnel is an important part of a physical examination. For nonhuman primates, this can involve increased restraint, additional stress, as well as the use of anesthetics and their deleterious effects on body temperature measurements. The purpose of this study was to compare two non‐invasive methods of infrared tympanic thermometry to standard rectal thermometry in adult squirrel monkeys. Methods Tympanic temperatures were collected from 37 squirrel monkeys and compared to rectal temperatures using a human and veterinary infrared tympanic thermometer. Results Compared with rectal temperature measurements, the human tympanic thermometer readings were not significantly different, while the veterinary tympanic thermometer measurements were significantly higher (P < 0.05). There were no differences between sexes. Conclusions The tympanic thermometer designed for use in humans can be used in adult squirrel monkeys as an alternative to rectal thermometry for assessing core body temperature.     

A longitudinal assessment of behavioral development in wild capuchins: Personality is not established in the first 3 years

Animal personality is defined as consistent individual differences across time and situations, but little is known about how or when those differences are established during development. Likewise, several studies described the personality structure of adult capuchin monkeys, without assessing the ontogeny of these personality traits. We analyzed the behavioral repertoire of 12 wild infants (9 males, 3 females) yellow-breasted capuchin monkeys (Sapajus xanthosternos), in Una Biological Reserve (Bahia, Brazil). Each infant was observed and filmed weekly from birth until 36 months, through daily focal sampling. We analyzed the behavior of each individual in 10 developmental points. By means of component reduction (principal component analysis), we obtained four behavioral traits: Sociability, Anxiety, Openness, and Activity. We investigated whether there were developmental effects on those traits by fitting regression models for the effect of time on behavioral traits, controlling for monkey identity, sex, and cohort. Sociability (decreasing) and Anxiety (increasing) changed significantly along development. By means of repeatability analysis, we did not find intra-individual consistency across time in those traits, so we cannot discriminate stable personality traits in early ontogeny. Our results show that the personality structure of capuchin monkeys is not established during early development, in agreement with the literature on human personality.     

Cynomolgus monkeys (Macaca fascicularis) may not become infected with equine herpesvirus 9

Background It was suggested that Equine herpesvirus 9 (EHV‐9) could be transmitted to higher non‐human primates. Methods Four cynomolgus monkeys (Macaca fascicularis) were inoculated with EHV‐9 by the nasal route. Results No abnormalities were observed pathologically, immunohistochemically, and genetically. Conclusions These findings indicate that cynomolgus monkeys are not susceptible to EHV‐9.     

A neurophysiologically-based mathematical model of flash visual evoked potentials

Evidence is presented that a neurophysiologically-inspired mathematical model, originally developed for the generation of spontaneous EEG (electroencephalogram) activity, can produce VEP (visual evoked potential)-like waveforms when pulse-like signals serve as input. It was found that the simulated VEP activity was mainly due to intracortical excitatory connections rather than direct thalamic input. Also, the model-generated VEPs exhibited similar relationships between prestimulus EEG characteristics and subsequent VEP morphology, as seen in human data. Specifically, the large correlation between the N1 amplitude and the prestimulus alpha phase angle, and the insensitivity of P2 to the latter feature, as observed in actual VEPs to low intensity flashes, was also found in the model-generated data. These findings provide support for the hypothesis that the spontaneous EEG and the VEP are generated by some of the same neural structures and that the VEP is due to distributed activity, rather than dipolar sources.     

Learning to control a brain-machine interface for reaching and grasping by primates

Reaching and grasping in primates depend on the coordination of neural activity in large frontoparietal ensembles. Here we demonstrate that primates can learn to reach and grasp virtual objects by controlling a robot arm through a closed-loop brain–machine interface (BMIc) that uses multiple mathematical models to extract several motor parameters (i.e., hand position, velocity, gripping force, and the EMGs of multiple arm muscles) from the electrical activity of frontoparietal neuronal ensembles. As single neurons typically contribute to the encoding of several motor parameters, we observed that high BMIc accuracy required recording from large neuronal ensembles. Continuous BMIc operation by monkeys led to significant improvements in both model predictions and behavioral performance. Using visual feedback, monkeys succeeded in producing robot reach-and-grasp movements even when their arms did not move. Learning to operate the BMIc was paralleled by functional reorganization in multiple cortical areas, suggesting that the dynamic properties of the BMIc were incorporated into motor and sensory cortical representations.     

Ecological constraints on the development of infant independence in rhesus

Mother-infant dyads were observed among three populations of rhesus monkeys (Macaca mulatta) in India and Nepal. This research had three purposes: 1) to examine the influences of maternal activities (ie, feeding, locomotion, and rest) and arboreality on the early development of infant independence; 2) to determine whether interpopulation differences in the development of infant independence can be accounted for by correlated differences in maternal time budgets and the amount of time infants spent on the ground; and 3) to explore how patterns of maternal care may or may not mitigate increased risk of infant mortality resulting from human harassment. Despite significant interpopulation differences in maternal time budgets, the amount of time infants spent on the ground, and the degree of harassment the animals experienced, few interpopulation differences in infant development could be found. The application of a multiple regression/ correlation analysis revealed that the development of infant independence was affected by the above factors but that those factors were acting in complementary ways to constrain development and to minimize the differences across populations.     

Learning to Control a Brain–Machine Interface for Reaching and Grasping by Primates

Reaching and grasping in primates depend on the coordination of neural activity in large frontoparietal ensembles. Here we demonstrate that primates can learn to reach and grasp virtual objects by controlling a robot arm through a closed-loop brain–machine interface (BMIc) that uses multiple mathematical models to extract several motor parameters (i.e., hand position, velocity, gripping force, and the EMGs of multiple arm muscles) from the electrical activity of frontoparietal neuronal ensembles. As single neurons typically contribute to the encoding of several motor parameters, we observed that high BMIc accuracy required recording from large neuronal ensembles. Continuous BMIc operation by monkeys led to significant improvements in both model predictions and behavioral performance. Using visual feedback, monkeys succeeded in producing robot reach-and-grasp movements even when their arms did not move. Learning to operate the BMIc was paralleled by functional reorganization in multiple cortical areas, suggesting that the dynamic properties of the BMIc were incorporated into motor and sensory cortical representations.     

Consistent inter‐individual differences in common marmosets (Callithrix jacchus) in Boldness‐Shyness,Stress‐Activity,and Exploration‐Avoidance

The study of animal personality, defined as consistent inter‐individual differences in correlated behavioral traits stable throughout time and/or contexts, has recently become one of the fastest growing areas in animal biology, with study species ranging from insects to non‐human primates. The latter have, however, only occasionally been tested with standardized experiments. Instead their personality has usually been assessed using questionnaires. Therefore, this study aimed to test 21 common marmosets (Callithrix jacchus) living in three family groups, in five different experiments, and their corresponding controls. We found that behavioral differences between our animals were not only consistent over time, but also across different contexts. Moreover, the consistent behaviors formed a construct of four major non‐social personality components: Boldness‐Shyness in Foraging, Boldness‐Shyness in Predation, Stress‐Activity, and Exploration‐Avoidance. We found no sex or age differences in these components, but our results did reveal differences in Exploration‐Avoidance between the three family groups. As social environment can have a large influence on behavior of individuals, our results may suggest group‐level similarity in personality (i.e., “group personality”) in common marmosets, a species living in highly cohesive social groups. Am. J. Primatol. 78:961–973, 2016. © 2016 The Authors. American Journal of Primatology published by Wiley Periodicals, Inc.     

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.     

Species diversity and relative abundance of lactic acid bacteria in the milk of rhesus monkeys (Macaca mulatta)

Background Mother’s milk is a source of bacteria that influences the development of the infant commensal gut microbiota. To date, the species diversity and relative abundance of lactic acid bacteria in the milk of non‐human primates have not been described. Methods Milk samples were aseptically obtained from 54 female rhesus monkeys (Macaca mulatta) at peak lactation. Following GM17 and MRS agar plating, single bacterial colonies were isolated based on difference in morphotypes, then grouped based on whole‐cell protein profiles on SDS–PAGE. Bacterial DNA was isolated and the sequence the 16S rRNA gene was analyzed. Results A total of 106 strains of 19 distinct bacterial species, belonging to five genera, Bacillus, Enterococcus, Lactobacillus, Pediococcus, and Streptococcus, were identified. Conclusions Maternal gut and oral commensal bacteria may be translocated to the mammary gland during lactation and present in milk. This pathway can be an important source of commensal bacteria to the infant gut and oral cavity.     

Monomorphic Region of the Serotonin Transporter Promoter Gene in New World Monkeys

Genetic variation in the human serotonin system has long been studied because of its functional consequences and links to various neuropsychiatric and behavior‐related disorders. Among non‐human primates, the common marmosets (Callithrix jacchus) and tufted capuchins monkeys (Cebus apella) are becoming increasingly used as models to study the effects of genes, environments, and their interaction on physiology and complex behavior. In order to investigate the independent functions of and potential interactions between serotonin‐related genes, anxiety and neuropsychiatric disorders, we analyzed the presence and variability of the serotonin transporter gene‐linked polymorphic region (5‐HTTLPR) in marmoset and capuchin monkeys. By PCR and using heterologous primers from the human sequence, we amplified and then sequenced the corresponding 5‐HTT region in marmosets and capuchins. The resulting data revealed the presence of a tandem repeat sequence similar to that described in humans, but unlike humans and other Old World primates, no variable length alleles were detected in these New World monkeys, suggesting that if serotonin transporter is involved in modulating behavior in these animals it does so through different molecular mechanisms. Am. J. Primatol. 74:1028‐1034, 2012. © 2012 Wiley Periodicals, Inc.     

Links between the discovery of primates and anatomical comparisons with humans,the chain of being,our place in nature,and racism

I focus on the crucial links between the discovery of nonhuman primates by Westerners, discussions on our place in nature, the chain of being, racism, and the history of primate comparative anatomy and of so‐called “anatomical human racial studies.” Strikingly, for more than a millennium humans knew more about the internal anatomy of a single monkey species than about that of their own bodies. This is because Galen used monkeys to infer human anatomy, in line with the human‐animal continuity implied by the Greek notion of scala naturae. With the rise of Christianity, nonhuman primates were increasingly seen in a negative way. A more positive view emerged in the 14th century when nonhuman primates were directly studied/seen by Europeans, culminating in Tyson's 1699 work showing that chimps share more gross anatomical similarities with humans than with monkeys. However, the discomfort caused by this human‐chimp similarity then led to a new idea of animal‐human discontinuity, now related not to anatomy but to “civilization”: between Europeans vs. non‐Europeans + other primates. Moreover, Linnaeus' Systema Naturae and the emergence of “anatomical racial studies” influenced by Camper's craniology then led to even more extreme ideas, such as the notion that Europeans were both mentally and morphologically “ideal.” Unfortunately the biased and often incorrect “results” of such studies, combined with ideas based on Darwin's “struggle for survival”, became crucial in propaganda that lead to the rise of eugenics in the end of the 19th/first half of 20th centuries and that culminated in Nazism. Since the 1950s there has been an emphasis on the continuity/unity between all human groups and other primates, in great part influenced by what happened during World War 2. Reviews such as this one are, therefore, particularly necessary to illuminate and guard against attitudes against “the Other” and racist ideologies that are re‐emerging in modern political discourse across the globe.     

Interleukin-1 induces sleep-like behavior and alters call structure in juvenile rhesus macaques

To date, there have been no investigations of the behavioral effects of interleukin-1 (IL-1) in nonhuman primates. In this study the locomotor behavior and vocalizations of juvenile rhesus monkeys were monitored for 45 minutes following intravenous injections of recombinant human IL-1 alpha. In addition, their reaction to a broadcasted recording of infant monkey distress calls was determined 20 minutes after the beginning of each test session. IL-1 induced sleep-like inactivity and significantly diminished the monkey's behavioral and vocal responses to the broadcasted calls. The coo calls uttered by the monkeys following IL-1 treatment also had a longer duration and lower fundamental frequency than calls during the control condition. As several studies have indicated that behavioral effects of IL-1 may be mediated by corticotropin-releasing hormone (CRH), a second group of rhesus monkeys was given injections of CRH. CRH did not alter behavior or call structure at the dose administered. These results extend previous research on the behavioral effects of IL-1 to include the nonhuman primate and provide the first evidence that cytokines can affect vocal communication in rhesus monkeys. © 1995 Wiley-Liss, Inc.