Age changes in plasma IGF-1 concentration in free-ranging Japanese macaques (Macaca fuscata)

To obtain fundamental data on the endocrine background for the wild Japanese macaque (Macaca fuscata) growth profiles, we have measured plasma insulin-like growth factor 1 (IGF-1) concentrations of free-ranging and open-enclosed Japanese macaques from five different regions in their habitat. General features of the IGF-1 levels in those troops were: 1) an age-dependent increase in the young macaques and 2) distinctively higher values among several adult females. The age changes in IGF-1 levels during the adolescent period in the free-ranging Japanese macaques were similar to those in the caged Japanese macaques.     

Plasma cholesterol levels in free-ranging macaques compared with captive macaques and humans

Plasma total cholesterol in free-ranging Japanese macaques (Macaca fuscata) on Koshima islet and in free-ranging long-tailed macaques (Macaca fascicularis) at Pangandaran in Indonesia was found to occur at very low levels compared with captive macaques and humans. Although total cholesterol levels in captive macaques were lower than humans, differences in HDL cholesterol levels were only small. In both sexes of wild and captive Japanese macaques, total cholesterol levels decreased from birth through to young adulthood but then increased in adult females of the captive group. In contrast, the value for adult females of the wild troop remained at a low level. Low TCH levels in adult females of the wild Japanese macaque troop may be due to a low energy intake and may have caused a delay in the onset of sexual maturation. Plasma TCH levels increased with the addition of 0.1% dietary cholesterol over six weeks in captive long-tailed macaques. That the cholesterol value after six weeks was dependent on cholesterol levels prior to supplementation indicates that captive macaques are slightly saturated with cholesterol.     

Optimization of a Novel Non-invasive Oral Sampling Technique for Zoonotic Pathogen Surveillance in Nonhuman Primates

Free-ranging nonhuman primates are frequent sources of zoonotic pathogens due to their physiologic similarity and in many tropical regions, close contact with humans. Many high-risk disease transmission interfaces have not been monitored for zoonotic pathogens due to difficulties inherent to invasive sampling of free-ranging wildlife. Non-invasive surveillance of nonhuman primates for pathogens with high potential for spillover into humans is therefore critical for understanding disease ecology of existing zoonotic pathogen burdens and identifying communities where zoonotic diseases are likely to emerge in the future. We developed a non-invasive oral sampling technique using ropes distributed to nonhuman primates to target viruses shed in the oral cavity, which through bite wounds and discarded food, could be transmitted to people. Optimization was performed by testing paired rope and oral swabs from laboratory colony rhesus macaques for rhesus cytomegalovirus (RhCMV) and simian foamy virus (SFV) and implementing the technique with free-ranging terrestrial and arboreal nonhuman primate species in Uganda and Nepal. Both ubiquitous DNA and RNA viruses, RhCMV and SFV, were detected in oral samples collected from ropes distributed to laboratory colony macaques and SFV was detected in free-ranging macaques and olive baboons. Our study describes a technique that can be used for disease surveillance in free-ranging nonhuman primates and, potentially, other wildlife species when invasive sampling techniques may not be feasible.     

Prevalence of glucose intolerance in free-ranging Macaca fascicularis of Mauritius

Oral glucose tolerance tests (OGTTs) were carried out on 30 free-ranging long-tailed macaques (Macaca fascicularis) on the island of Mauritius, following the suggestion that severe glucose intolerance and diabetes mellitus might be prevalent in this macaque population. OGTTs revealed no evidence of frank diabetes mellitus in the sample. However, 13% of individuals showed impaired glucose tolerance, with preserved insulin secretion, suggesting the presence of the target tissue resistance to insulin characteristic of human noninsulin-dependent diabetes mellitus (NIDDM). The macaques with impaired glucose tolerance were neither obese nor aged. Glucose levels at all time points of the OGTT in normal macaques in our free-ranging sample were lower than reported in captive populations, perhaps due to greater physical activity. Our observations demonstrate that a genetic predisposition to glucose intolerance does exist in M. fascicularis, and that this condition, well documented in laboratory macaques, is not simply an artifact of captivity.     

Semi-free breeding of tropical Celebes macaques (Macaca tonkeana) in a continental European climate.

Celebes macaques have been successfully bred for four years in a free-ranging colony in French pre-Alps where they are exposed to continental European climate and temperature variation of 65 centigrades.     

猕猴觅食策略的地域性差异

本文通过1年连续野外观察（2015年12月至2016月11月）,对比研究了广东省内伶仃—福田国家级自然保护区野生群和台山上川岛猕猴省级自然保护区内半野生投食群的猕猴觅食策略异同,分析了食物数量和食物营养对猕猴觅食行为的影响,探讨了猕猴对生境变化的应对策略及其适应机制。研究结果表明,野生群和半野生群猕猴均偏好取食低灰分果实。另外,比起取食较少的果实,半野生群猕猴主要取食的果实具有低含水量和低蛋白等特点。全年来看,野生群猕猴偏好取食分布数量多的果实;半野生群猕猴食果频率月间波动受环境果实量影响,符合能量最大化理论。野生群和半野生群猕猴采食乔木树叶的行为均不受乔木数量的影响;而且两者采食所有生活型植被的叶的行为不受叶营养的影响。本研究表明猕猴会根据环境的食物资源数量和质量调整其觅食策略,具有对不同生活环境灵活适应的能力。     

Differential distribution of antibodies to different viruses in young animals in the free-ranging rhesus macaques of Cayo Santiago

BACKGROUND: The breeding colony of free-ranging rhesus macaques was established in 1938 in Cayo Santiago (CS) with animals collected in northern India. The seroprevalence to cercopithecine herpesvirus type 1 (B virus) and simian retroviruses has been studied previously. RESULTS: This is the first report on the seropositivity to different viruses using samples collected shortly after removing animals (n = 245) from CS. All samples were negative for measles, simian immunodeficiency virus and simian type D retroviruses. The overall prevalence of antibodies was around 50% for simian T-lymphotropic virus I (STLV-I). For B virus, the prevalence was 38%. CONCLUSIONS: Data obtained showed marked differences in the antibody distribution to B virus and STLV-I within the free-ranging colony of rhesus macaques. Implication of these data for the Specific Pathogen Free program at the Caribbean Primate Research Center are also discussed.     

Body Size and Proportions and Pelage Color of Free-Ranging Macaca mulatta from a Zone of Hybridization in Northeastern Thailand

Rhesus (Macaca mulatta) and long-tailed (M. fascicularis) macaques belong to the same species, and are parapatric within a zone that lies between 15° and 20° N on the Indochinese peninsula. Researchers have reported probable hybrids between the 2 species from that zone, but have not studied the extent of introgression. To test for phenotypic evidence of hybridization, we collected body mass, morphometrics (body size and proportions), and pelage color readings from free-ranging rhesus living close to the zonal boundary at Wat Tham Pa Mak Ho (WTPMH), Wang Saphun district, Loei province, northeastern Thailand (17°14′N, 101°47′E). Female WTPMH rhesus macaques (n =12) were 10–20% smaller, but with a greater relative tail length than the captive Chinese or Indian female rhesus. Female WTPMH were larger than the free-ranging long-tailed macaques, but with similar limb proportions and a shorter relative tail length. The WTPMH rhesus macaques also displayed the bipartite pelage color pattern typical of Macaca mulatta . The evidence suggests slight contribution of long-tailed macaques to the gene pool of the WTPMH population. Further sampling of other macaque populations within the zone and genetic analysis are essential to address better the question of hybridization. Determination of the distribution and range of biobehavioral variation of macaques within the zone is urgently needed, because their habitat is being rapidly destroyed by deforestation, and their demography and social structure are threatened by artificial disturbance.     

Blood Characteristics of the Crab-Eating Monkeys (Macaca fascicularis) in Bali Island,Indonesia: Implication of Water Deficiency in West Bali

Environmental effects on blood characteristics of macaques were examined by comparing serveral blood indices of the free-ranging crab-eating monkeys (Macaca fascicularis) in two distinct regions of Bali Island, Indonesia. The total plasma protein level and concentrations of' creatinine and sodium ion were higher with macaques of Teluk Terima in the west part of Bali Island (dry area) than those in the central Bali (wet area). Results indicated that water deficiency in the dry area significantly affects the blood characteristics of macaques.     

Vomiting in Wild Bonnet Macaques

Researchers have not studied vomiting that is not associated with pathological behavior in nonhuman primates. Scientists generally assume that vomiting provides protection by ejecting toxins from the body, but the explanation is not fully supported by the literature. We report on 163 instances of vomiting from 2 groups of free-ranging bonnet macaques in southern India. The macaques routinely reingested their vomit. The reingestion was unlike that in abnormal behavior of both humans and nonhuman primates. We suggest that the tendency to hoard food in their cheek pouches explains why they reingested the vomit.     

Seroprevalence of SV40-like polyomavirus infections in captive and free-ranging macaque species

BACKGROUND AND METHODS: To investigate the seroprevalence of polyomavirus infections in macaques, we analyzed 1579 sera from nine different species for antibodies cross-reactive with simian virus 40 (SV40) in an enzyme-linked immunosorbent assay. Most samples were collected from captive animals, but we also investigated a colony of free-ranging Barbary macaques (Macaca sylvanus). RESULTS: High seropositive rates were found in rhesus macaques (Macaca mulatta; 74.7%), cynomolgus macaques (Macaca fascicularis; 44.8%) and Tonkean macaques (Macaca tonkeana; 41.7%), especially in animals imported from China. Low rates were measured in cynomolgus macaques from Mauritius (8.8%), and in Barbary macaques (1.4%). Seropositivity was age-dependent increasing to >70% in animals of 5 years and older. CONCLUSIONS: High seroprevalence rates were found in different species of macaques, dependent on their origin. Very low infection rates found in Barbary macaques and cynomolgus macaques from Mauritius suggest that these animals in the wild are not commonly infected by SV40-like viruses.     

Reproductive failure in macaques

Reproductive failure among captive and free-ranging macaques is common. Many females experience amenorrhea or anovular cycles. Females who successfully conceive often lose the conceptus before implantation. After implantation, fetuses are aborted because of maternal, paternal, fetal, or placental abnormalities. Death postpartum is likely if infants are premature or if animals are subject to social stress, especially trauma. Based on published reports, reproductive failure among macaques includes an average of 16.3% abortions, 9.9% stillbirths, 21.9% neonatal deaths, and 15.2% infant deaths.     

Aggression in adult male primates: A comparison of confined Japanese macaques and free-ranging olive baboons

The frequencies and types of adult male aggressive behavior of confined Japanese macaques (Macaca fuscata)and free-ranging olive baboons (Papio anubis)were compared. The baboons, which do not have a mating season, were more aggressive to conspecific males than were the macaques during their nonmating season. The baboons also solicited aid during aggressive encounters more frequently than the macaques. However, during their mating season, the macaques were more aggressive to conspecific females than were the baboons. The macaques were also involved in more triadic sequences of aggression, and the frequency of occurrence of these patterns supported Chase’s theory of dominance hierarchy formation and maintenance. The differences in aggressive behavior appeared to be related to the seasonal reproductive cycle of the macaques.     

Reproductive biology of rhesus and Japanese macaques

This paper offers a comparison of the reproductive biology of the Japanese macaques of Arashiyama, Japan and the free-ranging rhesus macaques of Silver Springs, Florida, U.S.A. The data indicate that rhesus macaques of Silver Springs have a higher reproductive rate than the Japanese macaques of Arashiyama. The reproducive rate of the rhesus monkeys over three birth seasons is 82% and that for the Japanese macaque is 53%. The higher reproductive rate of rhesus monkeys is accomplished through an earlier onset of sexual maturation (4 and 5 years for the rhesus and 5 and 6 years for the Japanese monkeys) and a shorter interbirth interval (14.27±5.54 months for rhesus and 18.00±6.57 months for Japanese monkeys). It is suggested that, because of the relatively harsh winters experienced by Japanese macaques, the slower reproductive rate of the Japanese monkeys has been selected for in order to enable females to lengthen the time in which maternal care is extended to their offspring.     

Testing for links between face color and age,dominance status,parity, weight,and intestinal nematode infection in a sample of female Japanese macaques

Studies of the role of secondary sexual ornaments in mate choice tend to focus on colorful traits in males, but females of many animal species express colorful ornamentation too. Among non-human primates, investigations into the role of female secondary sexual traits as indicators of life history characteristics, reproductive success, and health status have mostly focused on sexual swellings, whereas only few studies have been conducted on the role of facial color. Recent studies on rhesus macaques and mandrills suggested that female ornamentation might provide information about female life history characteristics, but not on disease resistance factors and parasite infection, which have been shown to affect male ornamentation in some non-primate species. In Japanese macaques (Macaca fuscata), females have brightly colored faces that are indicative of their reproductive status. Here, we aimed to determine whether female facial color might also convey information about age, dominance rank, parity, weight, and intestinal nematode infection in free-ranging individuals. We analyzed whether female facial parameters (luminance and redness) were linked to these individual characteristics, using digital photography and data on intestinal parasite infection collected systematically during 1 month for each of seven free-ranging females. We found no evidence to suggest that female facial color is an indicator of any of these measures in Japanese macaques. Considering our small data set, it is still preliminary to draft any clear conclusions. Future studies combining digital, hormonal, parasitological and behavioral data are needed to assess the possible role of female face color on male preferences and mating choice in Japanese macaques.     

Suspensory behavior and its role in positional activities of Japanese macaques

Suspensory behavior of free-ranging Japanese macaques was classified based on the kinematics and situations, and incidence of the behavior recorded with the continuous focal animal sampling method was compared between different age groups. Of all age groups, infants used the various types of suspension most frequently, and the frequency declined rapidly with age. Suspension was used as 1) a safety device by infants, to prevent falling down from supports when losing balance, 2) a feeding posture and 3) a supplement for shortage of the reaching length composed of limbs and trunk lengths in young macaques. The roles of suspensory behavior in the development of positional activities in Japanese macaques are briefly discussed.     

Considering human-primate transmission of measles virus through the prism of risk analysis

Measles is a respiratory virus that is endemic to humans. Human-nonhuman primate (NHP) transmission of the measles virus has been shown to cause significant morbidity and mortality in NHP populations. We investigated serological evidence of exposure to measles virus in two free-ranging populations of macaques at the Bukit Timah (BTNR) and Central Catchment Nature (CCNR) reserves in Singapore and the Swoyambhu Temple in Katmandu, Nepal. At BTNR/CCNR none of the 38 macaques (Macaca fascicularis) sampled were seropositive for antibodies to measles virus. In contrast, at Swoyambhu 100% (n = 39) of the macaques (M. mulatta) sampled were seropositive for antibodies to the measles virus. Here the contrasting seroprevalences of the two sites are analyzed using risk analysis. These case studies show how risk analysis can be used to approach the phenomenon of cross-species pathogen transmission.     

Flexibility in Food Extraction Techniques in Urban Free-Ranging Bonnet Macaques,Macaca radiata

Non-human primate populations, other than responding appropriately to naturally occurring challenges, also need to cope with anthropogenic factors such as environmental pollution, resource depletion, and habitat destruction. Populations and individuals are likely to show considerable variations in food extraction abilities, with some populations and individuals more efficient than others at exploiting a set of resources. In this study, we examined among urban free-ranging bonnet macaques, Macaca radiata (a) local differences in food extraction abilities, (b) between-individual variation and within-individual consistency in problem-solving success and the underlying problem-solving characteristics, and (c) behavioral patterns associated with higher efficiency in food extraction. When presented with novel food extraction tasks, the urban macaques having more frequent exposure to novel physical objects in their surroundings, extracted food material from PET bottles and also solved another food extraction task (i.e., extracting an orange from a wire mesh box), more often than those living under more natural conditions. Adults solved the tasks more frequently than juveniles, and females more frequently than males. Both solution-technique and problem-solving characteristics varied across individuals but remained consistent within each individual across the successive presentations of PET bottles. The macaques that solved the tasks showed lesser within-individual variation in their food extraction behavior as compared to those that failed to solve the tasks. A few macaques appropriately modified their problem-solving behavior in accordance with the task requirements and solved the modified versions of the tasks without trial-and-error learning. These observations are ecologically relevant – they demonstrate considerable local differences in food extraction abilities, between-individual variation and within-individual consistency in food extraction techniques among free-ranging bonnet macaques, possibly affecting the species’ local adaptability and resilience to environmental changes.     

Unregelmässig aufgebaute Zellgemeinschaften des Samenepithels beim free-ranging japanischen Makak (Macaca fuscata) in der Paarungszeit

Testicular biopsies were obtained from 11 adult males of free-ranging Japanese macaques trapped from Takasakiyama troops at the height of the breeding season. The spermatogenesis was observed on Bouin fixed and hematoxylin-eosin stained sections, especially from the viewpoint of seminiferous epithelial cycle. One cycle may be classified into seven stages. The classification, however, is not very easily carried out, because the seminiferous epithelium is, in most cases, very irregularly constructed, and typical germ cell associations which are easily identified, are infrequently observed. On the basis of the classification, various types of irregularities in the arrangement of the cellular associations were investigated and classified. In an unexpectedly large number of seminiferous tubular cross-sections, the lumina are obscured or obliterated owing to disarrangement of germ cells. As a consequence of this, the tubular sections with clearly discernible lumina are very rarely found (38 in a total of 1,215 observed cross-sections). Furthermore, the presence of several different stages in a singular cross-section is rather a common phenomenon (404 in a total of 1,215). It remains unanswered, whether these findings would be obtained in all other free-ranging Japanese macaques.     

Sensitive assays for simian foamy viruses reveal a high prevalence of infection in commensal, free-ranging Asian monkeys

Foamy viruses (FV) are retroviruses that naturally infect many hosts, including most nonhuman primates (NHPs). Zoonotic infection by primate FV has been documented in people in Asia who reported contact with free-ranging macaques. FV transmission in Asia is a concern, given abundant human-NHP contact, particularly at monkey temples and in urban settings. We have developed three assays capable of detecting the presence of FV in Asian NHP species that are commensal with humans: enzyme-linked immunosorbent assay (ELISA), Western blot assays using recombinant viral Gag protein, and an indicator cell line that can detect macaque FV. The recombinant ELISA correlates very well with the presence of FV sequences detected by PCR. We have used these assays to demonstrate both that FV is highly prevalent among free-ranging NHPs and that seroconversion occurs at a young age in these animals. These assays should also prove useful for large-scale analysis of the prevalence of FV infections in human populations in Asia that are commensal with free-ranging NHPs.