Positional behavior of free-ranging Japanese macaques (<Emphasis Type="Italic">Macaca fuscata</Emphasis>)

Positional behavior was quantitatively studied in identified free-ranging Japanese macaques (Macaca fuscata). Five male and 11 female adults were observed in a forested mountain habitat. Data were analyzed for proportion of bout distance, number and time of each locomotion and postural type. Japanese macaques are semiterrestrial, and mainly walk and run quadrupedally. This supports the notion that Macaca are generally quadrupeds. Sex differences in positional behavior were found in the preference of substrate and types of positional behavior. Males and females tend to be terrestrial and arboreal, respectively. Males leap more frequently and longer in distance than do females when they are feeding in trees. These sex differences are considered to be related to differences in morphology, food choice, social activity, and the nursing of infants. Frequencies of leaping and the distance covered by leaping in Japanese macaques are more than those of long-tailed macaques which are arboreal quadrupeds. However, Japanese macaques leap shorter distances at a time than do long-tailed macaques, which indicates that body size may be related to leaping distance more than the frequency of leaping and the distance covered by leaping. Japanese macaques are not as specialized for terrestrial locomotion as pig-tailed macaques. They use both terrestrial and arboreal supports, and are considered to be semi-terrestrial quadrupeds, somewhere between the arboreal long-tailed macaque and the terrestrial pig-tailed macaque. Electronic Publication     

Functions of an unreported “rocking-embrace” gesture between female Japanese Macaques (Macaca fuscata) in Kinkazan Island,Japan

Recently, research has focused on the effects of the concurrence of multimodal signals and their efficacy and meaning. We observed an unreported behaviour, a ventro-ventral “rocking-embrace” gesture that is always accompanied by lip smacking as the facial expression and sometimes by a girney call, in wild Japanese macaques (Macaca fuscata) living in Kinkazan Island, northern Japan. This study examined the form and contexts of the occurrence of such multimodal signals in order to elucidate its functions. Eighty-eight cases of rocking embrace were recorded during 183 h of observation over 22 days. Adult females were involved in all of the cases. Of the 71 cases between adult females in which behaviours prior to the rocking embrace could be identified, 13 cases were allogrooming interruptions, 11 were aggression, and 42 were approaches, most of which occurred between non-kin grooming partners. The rocking embrace was often followed by allogrooming. This suggests that rocking embraces occur under stressful conditions and may function to reduce tensions. This conclusion is consistent with the contexts and functions of lip smacking and girneys shown in previous studies. In contrast with lip smacking and girneys, neither a rocking embrace nor a ventro-ventral embrace (without rocking) between anoestrous adult females has been previously shown in Japanese macaques. In other macaque species, however, the latter gesture is often observed as an affiliative behaviour that immediately follows conflict; it functions to reconcile or as a greeting when it occurs immediately after an approach. Rocking embraces among the Kinkazan macaques occur in contexts similar to, and have a similar function to, the ancestral gesture of ventro-ventral embracing (which is hidden in Japanese macaques) and the ancestral display of lip smacking (which is still observed in Japanese macaques). The ventro-ventral embrace as a tactile signal might have been hidden since it was made redundant by the visual signal of lip smacking in ancestral macaques.     

Highly Polymorphic Microsatellite Markers for the Assessment of Male Reproductive Skew and Genetic Variation in Critically Endangered Crested Macaques (<Emphasis Type="Italic">Macaca nigra</Emphasis>)

Genetic analyses based on noninvasively collected samples have become an important tool for evolutionary biology and conservation. Crested macaques (Macaca nigra), endemic to Sulawesi, Indonesia, are important for our understanding of primate evolution as Sulawesi macaques represent an exceptional example of primate adaptive radiation. Crested macaques are also Critically Endangered. However, to date we know very little about their genetics. The aim of our study was to find and validate microsatellite markers useful for evolutionary, conservation, and other genetic studies on wild crested macaques. Using fecal samples of 176 wild macaques living in the Tangkoko Reserve, Sulawesi, we identified 12 polymorphic microsatellite loci through cross-species polymerase chain reaction amplification with later modification of some of these primers. We tested their suitability by investigating and exploring patterns of paternity, observed heterozygosity, and evidence for inbreeding. We assigned paternity to 63 of 65 infants with high confidence. Among cases with solved paternity, we found no evidence of extragroup paternity and natal breeding. We found a relatively steep male reproductive skew B index of 0.330 ± 0.267; mean ± SD) and mean alpha paternity of 65% per year with large variation across groups and years (29–100%). Finally, we detected an excess in observed heterozygosity and no evidence of inbreeding across our three study groups, with an observed heterozygosity of 0.766 ± 0.059 and expected heterozygosity of 0.708 ± 0.059, and an inbreeding coefficient of ?0.082 ± 0.035. Our results indicate that the selected markers are useful for genetic studies on wild crested macaques, and possibly also on other Sulawesi and closely related macaques. They further suggest that the Tangkoko population of crested macaques is still genetically variable despite its small size, isolation, and the species’ reproductive patterns. This gives us hope that other endangered primate species living in small, isolated populations may also retain a healthy gene pool, at least in the short term.     

Development of quadrupedal locomotion on level surfaces in Japanese macaques

Longitudinal comparisons of high-speed quadrupedal locomotion on level surfaces were made on 4 infant Japanese macaques (Macaca fuscata) with normal mother-infant relationships. Compared to adults, infants exhibited considerable variation in each step of locomotion. Braking components of foot force tended to be larger in the forelimb than in the hindlimb during the infant stage of development. Conversely, accelerating components were larger in the hindlimb than in the forelimb. In 1- and 2-month-old infants, vertical components in the hindlimb were not significantly larger than those of the forelimb. Fore- and hindlimb differentiation in infant Japanese macaques resembles that of adult macaques even at this early stage of development.     

Genes,social transmission,but not maternal effects influence responses of wild Japanese macaques (<Emphasis Type="Italic">Macaca fuscata</Emphasis>) to novel-object and novel-food tests

Using long-term maternal pedigree data, microsatellite analysis, and behavioral tests, we examined whether personality differences in wild Japanese macaques (Macaca fuscata) are associated with additive genetic effects, maternal influences, or belonging to a particular social group. Behaviors elicited by novel-object tests were defined by a component related to caution around novel-objects (Ob-PC1) and behaviors elicited by novel food-tests were defined by correlated components related to consummatory responses (Fo-PC1) and caution around novel foods (Fo-PC2). The repeatability of Ob-PC1 was modest and not significant; the repeatabilities of Fo-PC1 and Fo-PC2 were moderate and significant. Linear mixed effects models found that sex, age, sex × age, provisioning, trial number, date, time of day, season, and distance to the closest monkey were not related to personality. Linear mixed effects models of females older than 2 years found that high rank was associated with greater caution around novel objects. Linear models were used to determine whether sex, age, group membership, maternal kinship, or relatedness had independent effects on the personality similarity of dyads. These analyses found that pairs of macaques that lived in the same group were less similar in their caution around novel objects, more closely related pairs of macaques were more similar in their tendency to eat novel food, and that pairs of macaques in the same group were more similar in how cautious they were around novel foods. Together, these findings suggest that personality in this population of wild monkeys was driven by rank, genetic effects, and group effects, the latter possibly including the need to exploit different niches in the environment.     

Human Faces Are Slower than Chimpanzee Faces

Background

While humans (like other primates) communicate with facial expressions, the evolution of speech added a new function to the facial muscles (facial expression muscles). The evolution of speech required the development of a coordinated action between visual (movement of the lips) and auditory signals in a rhythmic fashion to produce “visemes” (visual movements of the lips that correspond to specific sounds). Visemes depend upon facial muscles to regulate shape of the lips, which themselves act as speech articulators. This movement necessitates a more controlled, sustained muscle contraction than that produced during spontaneous facial expressions which occur rapidly and last only a short period of time. Recently, it was found that human tongue musculature contains a higher proportion of slow-twitch myosin fibers than in rhesus macaques, which is related to the slower, more controlled movements of the human tongue in the production of speech. Are there similar unique, evolutionary physiologic biases found in human facial musculature related to the evolution of speech?

Methodology/Prinicipal Findings

Using myosin immunohistochemistry, we tested the hypothesis that human facial musculature has a higher percentage of slow-twitch myosin fibers relative to chimpanzees (Pan troglodytes) and rhesus macaques (Macaca mulatta). We sampled the orbicularis oris and zygomaticus major muscles from three cadavers of each species and compared proportions of fiber-types. Results confirmed our hypothesis: humans had the highest proportion of slow-twitch myosin fibers while chimpanzees had the highest proportion of fast-twitch fibers.

Conclusions/significance

These findings demonstrate that the human face is slower than that of rhesus macaques and our closest living relative, the chimpanzee. They also support the assertion that human facial musculature and speech co-evolved. Further, these results suggest a unique set of evolutionary selective pressures on human facial musculature to slow down while the function of this muscle group diverged from that of other primates.     

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.     

Responses to Vocalizations and Auditory Controls in the Human Newborn Brain

In the adult brain, speech can recruit a brain network that is overlapping with, but not identical to, that involved in perceiving non-linguistic vocalizations. Using the same stimuli that had been presented to human 4-month-olds and adults, as well as adult macaques, we sought to shed light on the cortical networks engaged when human newborns process diverse vocalization types. Near infrared spectroscopy was used to register the response of 40 newborns'' perisylvian regions when stimulated with speech, human and macaque emotional vocalizations, as well as auditory controls where the formant structure was destroyed but the long-term spectrum was retained. Left fronto-temporal and parietal regions were significantly activated in the comparison of stimulation versus rest, with unclear selectivity in cortical activation. These results for the newborn brain are qualitatively and quantitatively compared with previous work on newborns, older human infants, adult humans, and adult macaques reported in previous work.     

Seroprevalence of Japanese encephalitis virus infection in captive Japanese macaques (Macaca fuscata)

Japanese encephalitis virus (JEV), which is transmitted by mosquitoes, infects many animal species and causes serious acute encephalitis in humans and horses. In this study, a serosurvey of JEV in Japanese macaques (Macaca fuscata) reared in Aichi Prefecture was conducted using purified JEV as an antigen for ELISA. The results revealed that 146 of 332 monkeys (44 %) were seropositive for JEV. In addition, 35 of 131 monkeys (27 %) born in the facility were seropositive, and the annual infection rate in the facility was estimated as 13 %. Our results provide evidence of the frequent exposure of many Japanese macaques to JEV, suggesting that there is a risk of JEV transmission to humans by mosquitoes.     

The Number of Louse Eggs on Wild Japanese Macaques (<Emphasis Type="Italic">Macaca fuscata</Emphasis>) Varies with Age,but Not with Sex or Season

During grooming, primates remove harmful ectoparasites, such as ticks and lice, and there is direct evidence for a health benefit of tick removal. Grooming behaviors differ among primates with respect to age and sex. Moreover, the number of ectoparasite may exhibit seasonal variation. Therefore the number of ectoparasites on a host may vary with effects, host age and sex, and season. However, these effects have not been a focus of louse infestation studies of primates. Grooming in Japanese macaques is related to sex and age, with developmental changes in behavior corresponding to the timing of tooth eruption. Moreover, behavioral data for Japanese macaques suggest that lice load may differ with the season. Thus, we examined whether the number of louse eggs varies according to host macaque sex, age, and season, and whether it changes in response to tooth eruption. We counted unhatched and hatched eggs attached to the hair on six 1-cm² areas on the left wrist skin of culled macaques, using a stereoscopic microscope. We sampled five winter coats and three summer coats for each age class: infant, juvenile, adolescent, and adult. The number of unhatched and hatched eggs was related to age, but not to sex and season. There were significant differences in the number of unhatched eggs between infants and adults, juveniles and adults, and adolescents and adults. There were also significant differences in the number of hatched eggs between infants and adults, juveniles and adults, adolescents and adults. Tooth eruption did not influence the number of louse eggs. These results suggest that researchers should consider the age of host animals when assessing the relationship between grooming and ectoparasites.     

Highly polymorphic STR marker amplified with human DYS389 primers in Japanese macaques (Macaca fuscata)

Amplification products from male and female Japanese macaques were obtained by PCR with human Y-chromosomal DYS389 primers. These products were examined by electrophoresis and sequence analysis. The PCR products from the 12 Japanese macaques tested had different band patterns on an electrophoretogram. Sequence analysis of the products revealed that the high polymorphism originated from variable numbers of repeats of two separate CTAT sequences. The sequences of the Japanese macaque products were similar to those of the reference human DYS389 sequence. However, variable CTGT repeats and a difference in the second forward primer binding site yielded two products in human males, DYS389I and DYS389II, which do not exist in Japanese macaques. Our results suggest that the human DYS389 primers may be a potential tool not only for distinguishing between human and Japanese macaque DNA samples, but also for identifying individual macaques, because of the highly polymorphic alleles.     

CBC and serum chemistry differences between Indian-derived and Chinese–Indian hybrid rhesus monkey infants

Hematological and clinical biochemistry measures are commonly utilized as indicators of the health status of nonhuman primates. Among individuals in a population of a given species, there may be considerable variation in these parameters. Still wider variation may be found among different strains or subspecies of some orders. To date, few studies have addressed this phenomenon among strains of nonhuman primates of a given species. Blood samples for hematological and serum biochemical analyses were obtained from 29 Indian-derived and 13 Chinese-Indian hybrid nursery-reared rhesus macaque infants. Total protein, mean corpuscular hemoglobin concentration, mean corpuscular hemoglobin, erythrocyte count, hemoglobin, and hematocrit were all higher in the hybrid infants. These results indicate that the origin or strain of the animal should be considered when designing studies using rhesus macaques. © 1996 Wiley-Liss, Inc.     

Pulling the covers in electronic health records for an association study with self-reported sleep behaviors

ABSTRACT

The electronic health record (EHR) contains rich histories of clinical care, but has not traditionally been mined for information related to sleep habits. Here, we performed a retrospective EHR study based on a cohort of 3,652 individuals with self-reported sleep behaviors documented from visits to the sleep clinic. These individuals were obese (mean body mass index 33.6 kg/m²) and had a high prevalence of sleep apnea (60.5%), however we found sleep behaviors largely concordant with prior prospective cohort studies. In our cohort, average wake time was 1 hour later and average sleep duration was 40 minutes longer on weekends than on weekdays (p < 10^?12). Sleep duration varied considerably as a function of age and tended to be longer in females and in whites. Additionally, through phenome-wide association analyses, we found an association of long weekend sleep with depression, and an unexpectedly large number of associations of long weekday sleep with mental health and neurological disorders (q < 0.05). We then sought to replicate previously published genetic associations with morning/evening preference on a subset of our cohort with extant genotyping data (n = 555). While those findings did not replicate in our cohort, a polymorphism (rs3754214) in high linkage disequilibrium with a previously published polymorphism near TARS2 was associated with long sleep duration (p < 0.01). Collectively, our results highlight the potential of the EHR for uncovering the correlates of human sleep in real-world populations.     

Viral factors determine progression to AIDS in simian immunodeficiency virus-infected newborn rhesus macaques.

To evaluate how viral variants may affect disease progression in human pediatric AIDS, we studied the potential of three simian immunodeficiency virus (SIV) isolates to induce simian AIDS in newborn rhesus macaques. The three virus isolates were previously shown to range from pathogenic (SIVmac251 and SIVmac239) to nonpathogenic (SIVmac1A11) when inoculated intravenously into juvenile and adult rhesus macaques. Six newborn macaques inoculated with pathogenic, uncloned SIVmac251 developed persistent, high levels of cell-associated and cell-free viremia, had no detectable antiviral antibodies, and had poor weight gain; these animals all exhibited severe clinical disease and pathologic lesions diagnostic for simian AIDS and were euthanatized 10 to 26 weeks after inoculation. Two newborns inoculated with pathogenic, molecularly cloned SIVmac239 developed persistent high virus load in peripheral blood, but both animals had normal weight gain and developed antiviral antibodies. One of the SIVmac239-infected neonates exhibited pathologic lesions diagnostic for SAIDS and was euthanatized at 34 weeks after inoculation; the other SIVmac239-infected neonate remained alive and exhibited no significant clinical disease for more than 1 year after inoculation. In contrast, three newborn rhesus macaques inoculated with the nonpathogenic molecular clone, SIVmac1A11, had transient, low-level viremia, seroconverted by 10 weeks after inoculation, had normal weight gain, and remained healthy for over 1 year. These results indicate that (i) newborn rhesus macaques infected with an uncloned, virulent SIVmac isolate have a more rapid, fulminant disease course than do adults inoculated with the same virus, (ii) the most rapid disease progression is associated with lack of a detectable humoral immune response in SIV-infected infant macaques, (iii) a molecularly cloned, attenuated SIV isolate is nonpathogenic in neonatal macaques, and (iv) SIV-infected neonatal macaques exhibit patterns of infection, virus load, and disease progression similar to those observed in human immunodeficiency virus-infected children. This SIV/neonatal rhesus model of pediatric AIDS provides a rapid, sensitive model with which to compare the virulence of SIV isolates and to study the mechanisms underlying the differences in disease progression in human immunodeficiency virus-infected infants.     

Darwin’s Duchenne: Eye Constriction during Infant Joy and Distress

Darwin proposed that smiles with eye constriction (Duchenne smiles) index strong positive emotion in infants, while cry-faces with eye constriction index strong negative emotion. Research has supported Darwin’s proposal with respect to smiling, but there has been little parallel research on cry-faces (open-mouth expressions with lateral lip stretching). To investigate the possibility that eye constriction indexes the affective intensity of positive and negative emotions, we first conducted the Face-to-Face/Still-Face (FFSF) procedure at 6 months. In the FFSF, three minutes of naturalistic infant-parent play interaction (which elicits more smiles than cry-faces) are followed by two minutes in which the parent holds an unresponsive still-face (which elicits more cry-faces than smiles). Consistent with Darwin’s proposal, eye constriction was associated with stronger smiling and with stronger cry-faces. In addition, the proportion of smiles with eye constriction was higher during the positive-emotion eliciting play episode than during the still-face. In parallel, the proportion of cry-faces with eye constriction was higher during the negative-emotion eliciting still-face than during play. These results are consonant with the hypothesis that eye constriction indexes the affective intensity of both positive and negative facial configurations. A preponderance of eye constriction during cry-faces was observed in a second elicitor of intense negative emotion, vaccination injections, at both 6 and 12 months of age. The results support the existence of a Duchenne distress expression that parallels the more well-known Duchenne smile. This suggests that eye constriction–the Duchenne marker–has a systematic association with early facial expressions of intense negative and positive emotion.     

Probability of paternity exclusion and the number of loci needed to determine the fathers in a troop of macaques

We calculated the probability of paternity exclusion (P) in 6 troops of rhesus and Japanese macaques housed in open enclosures and 68 wild troops of Japanese, crab-eating, and toque macaques using 33 genetic loci which encoded the blood protein variations detected by electrophoretic techniques. In the open enclosures, especially of rhesus troops, we obtained a fairly high probability of paternity exclusion and succeeded in determining the fathers of offspring. However, we found significant differences between the observed and calculated probabilities in most of the troops. These differences were ascribed to a situation whereby the Hardy-Weinberg equilibrium had not been attained in the troops and/or the numbers of variable loci were too small. In the wild troops of Japanese, crab-eating, and toque macaques, the means ofP were 0.2274 (0.0192–0.5017), 0.4635 (0.1676–0.7151), and 0.7382 (0.6266–0.7954), respectively. We also estimated the number of loci needed to determine the fathers of offspring with a probability of 0.8 assuming that ten males were present in the troop. The estimated number was about 13.5 times, 5 times and 1.8 times the number of loci examined on average in the troops of Japanese, crab-eating and toque macaques, respectively. This means that determination of most of the fathers of offspring in wild troops of these macaques, even of toque macaques which have a rather high probability of paternity exclusion, is difficult so long as we employ only electrophoretic techniques.     

Environmental and Social Factors Associated with the Occurrence of Stone-Handling Behavior in a Captive Troop of <Emphasis Type="Italic">Macaca fuscata</Emphasis>

Stone-handling, a documented behavioral tradition in Japanese macaques (Macaca fuscata), occurs in both captive and provisioned free-ranging troops. We utilize data systematically collected as part of a broader investigation of stone-handling behavior in a captive troop to elucidate the environmental and social factors responsible for its occurrence. We analyzed contexts of stone-handling over 18 mo to determine under what conditions individuals most often perform it. There is clear seasonal variation in the occurrence of stone-handling. The lowest number and shortest duration of stone-handling bouts were in winter, gradually increasing to a peak in summer, and again decreasing toward autumn. Monkeys stone-handled more on clear sunny days than on cloudy or rainy ones. They displayed the behavior less under stressful conditions caused by human intervention or by aggression among troop members. Such stressful social conditions appeared to decrease individual motivation for stone-handling. In other words, individuals most frequently performed stone-handling under more relaxed environmental and social conditions. The findings are consistent with the hypothesis that stone-handling is a form of solitary object play behavior in macaques.     

Telomere dynamics in monkeys: Increased cell turnover in macaques infected with chimeric simian-human immunodeficiency viruses

Abstract: To address the question of how cell turnover is affected by retroviral infections, we used the telomeric terminal restriction fragments (TRFs) as markers of cell replicative history and measured their length in macaques infected with chimeric simian-human immunodeficiency viruses (SHIVs). The TRF lengths of mononuclear cells in 104 samples, including longitudinal samples from nine cynomolgus and ten pig-tailed macaques infected with SHIV, and in samples from 26 uninfected macaques, were quantitated by an improved method, based on two-dimensional calibration of DNA sizes, pulsed field electrophoresis, and high-resolution Southern blot images. The average TRF lengths of peripheral blood mononuclear cells (PBMCs) from uninfected pig-tailed (14.9 ± 1.6 kbp) and cynomolgus (14.1 ± 1.8 kbp) macaques were about 3 and 5 kbp longer than those of human infants and 30-year-old adults, respectively. The rate of TRF length shortening in infected pig-tailed macaques was significantly (P = 0.035) higher (2.2-fold) than in uninfected monkeys. The TRFs in SHIV-infected cynomolgus monkeys, which, in general, had lower viral loads than pig-tailed macaques, shortened on average more rapidly (1.6-fold) than in uninfected animals, but the difference was not statistically significant. The TRFs of mononuclear cells from the lymph nodes of two rapidly progressing SHIV-infected macaques that developed AIDS and died also shortened in parallel but somewhat more rapidly than in the PBMCs. These results suggest that the rate of PBMC turnover in macaques could be increased several-fold during infections by immunodeficiency viruses, likely due to immune activation by SHIV antigens.