Extra-large cluster formation by Japanese macaques (Macaca fuscata) on Shodoshima Island, central Japan, and related factors

Japanese macaques on Shodoshima Island habitually form very large rest clusters, in which 50+ or even 100+ individuals huddle together. This behavior is not seen in any other populations of the species. Mean cluster sizes of two groups of Shodoshima monkeys are three and four in summer and 17 and 16 in winter, respectively. A maximum of 137 individuals have been seen to huddle in one cluster. It is difficult to explain the extra large clusters on Shodoshima only as an adaptive behavior against cold, since Shodoshima is relatively warm in the range of habitats for Japanese macaques. Compared with other groups of Japanese macaques, Shodoshima monkeys show: more frequent affinitive interactions, shorter inter-individual distance, more frequent ignoring of exclusion, more frequent aggression, less intense aggression, and more frequent counter-aggression. These characteristics suggest that the Japanese macaques on Shodoshima have relaxed dominant relations. The specific social organization of Shodoshima monkeys may sustain the formation of extra large clusters. Inter-group comparisons suggest that the social structure of Japanese macaques might be highly plastic, and that Shodoshima monkeys have less despotic, more tolerant social relations than typically reported for this species.     

Grooming site preferences determined by lice infection among Japanese macaques in Arashiyama

I investigated the effect of the density of louse eggs (Pedicinus obtusus andP. eurygaster) on grooming site preferences in Japanese macaques (Macaca fuscata). Louse eggs were more often found on the outer side of the body (upper back, lower back, outer arms, and outer legs) than on the inner side of the body (chest, belly, inner arms, and inner legs). Japanese macaques were more likely to be groomed on the outer side than the inner side of the body by allogrooming and autogrooming. Such grooming site preferences correlated with the distribution of louse eggs but not with the areas of body parts. Thus, the ecology of lice might affect grooming behavior of Japanese macaques. Five hundred and fifty louse eggs were estimated to parasitize an adult female Japanese macaque. Considering the intrinsic rate of natural increase of lice, monkeys need to be groomed almost every day. This suggests that Japanese macaques need grooming partners and form social bonds with others for everyday grooming.     

Population genetical study of Japanese macaques,Macaca fuscata,in the shimokita A1 troop,with special reference to genetic variability and relationships to Japanese macaques in other troops

The genetic variations of 35 individuals of the Shimokita A1 troop of mainland Japanese macaques,Macaca fuscata fuscata, which live at the northern end of the habitat of the species, were investigated using 33 electrophoretically detectable blood protein loci. Among the loci examined, six were polymorphic. The average heterozygosity per individual was calculated as 0.0442. This was the highest value among all troops of Japanese macaques so far investigated. The mainland macaques of the Shimokita A1 troop were more differentiated genetically from other mainland macaque troops than were Yaku macaques, the subspeciesM. f. yakui.     

Role of some physical characteristics in species recognition by pigtail monkeys

Three adult pigtail monkeys pressed a lever to see pictures of pigtail and Japanese monkeys with a variety of physical features being removed. The features included head, tail, body, background, and color. The duration and the interval of exposure of these visual stimuli were dependent upon subjects' responding. Preferences for those pictures were evaluated by the ratio of lever-pressing duration to interval of lever-pressing. Two of the subjects showed a consistent preference to see pictures of pigtail monkeys over those of Japanese monkeys. Though this preference tended to maintain when these physical features were removed, it became relatively weak when head and head + tail were removed. These results suggest that pigtail macaques may discriminate species based not on a single characteristics but on some combination of features, and that head may be relatively important than the other features.     

Detection of a unique genotype of monkey B virus (Cercopithecine herpesvirus 1) indigenous to native Japanese macaques (Macaca fuscata)

The Japanese macaque or snow monkey (Macaca fuscata) is an autochthonous monkey in Japan. It has long been assumed that the monkey population was not infected with Cercopithecine herpesvirus 1 (monkey B virus [BV]) since cases of human BV infection have never been reported in Japan. Although serologic testing of captive snow monkeys in Japan revealed antibodies to BV, it was thought that native Japanese macaques had either been infected with herpes simplex virus from humans or with BV from other imported macaque species. To clarify this issue, we performed polymerase chain reaction (PCR) analysis to amplify BV sequences from trigeminal ganglia of 30 Japanese macaque monkeys that were seropositive for BV. Sequences from two BV genes, UL27 (360 bp) and UL19 (1.0 Kbp), from 3 of 30 monkeys were amplified. Results of restriction fragment length polymorphism analysis and DNA sequencing of the fragments provided evidence that native Japanese macaques are infected with BV. Phylogenetic analysis indicated that these monkeys harbor their own genotype of BV that is different from other known BV genotypes, and provided additional evidence supporting the co-evolution of BV and macaques.     

Japanese macaques form a cross-modal representation of their own species in their first year of life

We tested whether infant Japanese macaques (Macaca fuscata) have a cross-modal representation of their own species. We presented monkeys with a photograph of either a monkey or a human face on an LCD monitor after playing back a vocalization of one of those two species. The subjects looked at the monitor longer when a human face was presented after the monkey vocalization than when the same face was presented after human vocalization. This suggests that monkeys recall and expect a monkey’s face upon hearing a monkey’s voice.     

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.     

Frog- and lizard-eating behaviour of wild Japanese macaques in Yakushima,Japan

Frog- and lizard-eating and related behaviours were observed on eight occasions in two troops of wild Japanese macaques (Macaca fuscata yakui) in Yakushima, between March 1984 and April 1989. In each case, the first animal seen handling the prey was an adult. Juveniles showed interest in the prey, sniffed or mouthed it in three cases, and ate discarded parts of it in another. In the three cases where capture was observed, detection of the prey appeared to be fortuitous. Four monkeys ate leaves after eating meat. Those leaves identified were of species not commonly eaten. Though invertebrate-eating is common and widespread among Japanese macaques, the consumption of vertebrates is rare. The possibility that these behaviours represent a local tradition among the Yakushima macaques is discussed.     

Differences in hair density of Japanese monkeys (Macaca fuscata fuscata) with locality and age

The hair density of free-ranging Japanese monkeys (Macaca fuscata fuscata) living in three different areas was investigated. The Japanese monkeys had thicker hair than other macaques. The hair density in the Japanese monkeys varied with locality: the northern monkeys had thicker hair than the southern ones. The density did not vary markedly with age up to 3 years of age, but then decreased gradually up to adult age (≧7 years old). The remarkable growth of the trunk suggested that the total number of hairs increased with age, especially during the period as a juvenile.     

Phylogenetic relationships among Japanese, rhesus, Formosan, and crab- eating monkeys, inferred from restriction-enzyme analysis of mitochondrial DNAs [published erratum appears in Mol Biol Evol 1988 Sep;5(5):601]

Mitochondrial DNA (mtDNA) polymorphisms in four species of macaques, i.e., Japanese monkey (Macaca fuscata), rhesus monkey (M. mulatta), Formosan monkey (M. cyclopis), and crab-eating monkey (M. fascicularis), were analyzed to study phylogenetic relationships. When 17 restriction enzymes of 6-bp recognition were used, 42-49 sites were observed in the samples. The estimated number of nucleotide substitutions per site among Japanese, rhesus, and Formosan monkeys ranges from 0.0318 to 0.0396, and that between the crab-eating monkey and the other monkeys from 0.0577 to 0.0653. These findings suggest that the crab-eating monkey diverged from the other three approximately 1.5-3.0 Myr before the present (Mybp) and that the Japanese, rhesus, and Formosan monkeys diverged approximately 0.9-1.8 Mybp, although the branching order cannot be determined conclusively.      

Species discrimination and concept formation by rhesus monkeys (Macaca mulatta)

There are 19 species in genusMacaca and some of them are living in sympatry (Fooden, 1980). Although inter-specific hybrids are relatively easy to produce under artificial conditions, hybridization does not occur naturally. What is preventing that among the species of genusMacaca? Three rhesus monkeys acquired a discrimination between pictures with rhesus monkeys and without rhesus monkeys. All subjects showed positive transfer of this discrimination to new pictures with rhesus monkeys and without rhesus monkeys. A further test showed that these monkeys could discriminate between pictures of rhesus monkeys and pictures of Japanese monkeys. The results suggest that rhesus monkeys recognize rhesus monkeys as a class, independent of the actual stimuli such as a picture or an individual monkey. The ability to recognize members of their own species and the opportunities for such learning may be an important factor preventing hybridization among the species of genusMacaca.     

A Markerless 3D Computerized Motion Capture System Incorporating a Skeleton Model for Monkeys

In this study, we propose a novel markerless motion capture system (MCS) for monkeys, in which 3D surface images of monkeys were reconstructed by integrating data from four depth cameras, and a skeleton model of the monkey was fitted onto 3D images of monkeys in each frame of the video. To validate the MCS, first, estimated 3D positions of body parts were compared between the 3D MCS-assisted estimation and manual estimation based on visual inspection when a monkey performed a shuttling behavior in which it had to avoid obstacles in various positions. The mean estimation error of the positions of body parts (3–14 cm) and of head rotation (35–43°) between the 3D MCS-assisted and manual estimation were comparable to the errors between two different experimenters performing manual estimation. Furthermore, the MCS could identify specific monkey actions, and there was no false positive nor false negative detection of actions compared with those in manual estimation. Second, to check the reproducibility of MCS-assisted estimation, the same analyses of the above experiments were repeated by a different user. The estimation errors of positions of most body parts between the two experimenters were significantly smaller in the MCS-assisted estimation than in the manual estimation. Third, effects of methamphetamine (MAP) administration on the spontaneous behaviors of four monkeys were analyzed using the MCS. MAP significantly increased head movements, tended to decrease locomotion speed, and had no significant effect on total path length. The results were comparable to previous human clinical data. Furthermore, estimated data following MAP injection (total path length, walking speed, and speed of head rotation) correlated significantly between the two experimenters in the MCS-assisted estimation (r = 0.863 to 0.999). The results suggest that the presented MCS in monkeys is useful in investigating neural mechanisms underlying various psychiatric disorders and developing pharmacological interventions.     

Amino acids in the plasma of fasting Japanese monkeys (Macaca fuscata fuscata andM. f. yakui)

The plasma levels of 26 amino acids and related compounds were determined in five male and five female adult members of each of the two subspecies of Japanese monkeys,Macaca fuscata fuscata andM. f. yakui. Activities of L-asparaginase and histaminase in plasma were also measured.Numerous differences in amino acid levels between the sexes in the subspeciesfuscata were noted, with the female consistently exhibiting lower values. Few differences were observed between the sexes of the subspeciesyakui or between the two subspecies of Japanese monkeys. These monkeys were similar to other previously studied nonhuman primates in exhibiting measurable levels of 3-methylhistidine in plasma. There were numerous quantitative differences among Japanese monkeys and stump-tailed macaques, rhesus monkeys, chimpanzees, and man, with the Japanese monkeys usually exhibiting higher plasma levels.L-asparaginase activity was not detectable in these Japanese monkeys. Histaminase activity was similar to that previously measured in pig-tailed macaques and chimpanzees, lower than that in rhesus monkeys and stump-tailed macaques, and higher than that in man.     

Traditions in monkeys

Traditions, defined as relatively long‐lasting behavioral practices shared among members of a group partly via social learning, were studied in monkeys, specifically Japanese macaques, before being studied in great apes. Although apes and humans may share some social learning capacities that are absent in monkeys, a complete understanding of the roots of human culture requires attention to the socioecological conditions favoring traditions, however generated, in animals generally and in multiple behavioral domains. Using the four criteria of intergroup variation, observation of the origin and spread of a novel behavior, dissemination patterned according to age or kinship, or individuals' close observation of others' performance of the behavior before engaging in it, over twenty‐five behaviors have been nominated as traditions in free‐ranging monkey populations. Tolerant gregariousness has been proposed to increase the likelihood of the emergence of traditions in any behavioral domain. Omnivory and extractive foraging should favor the emergence of foraging‐related traditions; strong cooperative relationships and flexible coalitionary structure should favor the emergence of social conventions that function to test social bonds. These conditions are taxonomically widespread. Thus, the current restriction of most reported free‐ranging monkey traditions to two taxa (Macaca fuscata and Cebus) is likely to reflect variation in primatologists' research goals, methods, and concepts rather than real interspecific variation in the propensity to generate traditions.     

The development of small primate models for aging research

Nonhuman primate (NHP) aging research has traditionally relied mainly on the rhesus macaque. But the long lifespan, low reproductive rate, and relatively large body size of macaques and related Old World monkeys make them less than ideal models for aging research. Manifold advantages would attend the use of smaller, more rapidly developing, shorter-lived NHP species in aging studies, not the least of which are lower cost and the ability to do shorter research projects. Arbitrarily defining "small" primates as those weighing less than 500 g, we assess small, relatively short-lived species among the prosimians and callitrichids for suitability as models for human aging research. Using the criteria of availability, knowledge about (and ease of) maintenance, the possibility of genetic manipulation (a hallmark of 21st century biology), and similarities to humans in the physiology of age-related changes, we suggest three species--two prosimians (Microcebus murinus and Galago senegalensis) and one New World monkey (Callithrix jacchus)--that deserve scrutiny for development as major NHP models for aging studies. We discuss one other New World monkey group, Cebus spp., that might also be an effective NHP model of aging as these species are longer-lived for their body size than any primate except humans.     

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。     

A photogrammetric method to evaluate nutritional status without capture in habituated free-ranging Japanese macaques (Macaca fuscata): a pilot study

The quantification of nutritional status (e.g., total body fat) of animals is difficult, because the linear dimension (body length) required for the calculation of proxy parameters, such as the physique or body mass indices, cannot be measured without capture. One solution is photogrammetry of body length, provided the following two criteria are met: (1) the camera axes and subject are oriented vertically, and (2) anatomical landmarks are easily identified with low measurement error. By modifying Mori’s (Primates 20:371–397, 1979) approach, we devised an accurate photogrammetric method that uses a horizontal bar with an attached ruler for the monkey to traverse, and the anatomical landmarks of the eye and upper border of the ischial callosity to measure body length. We tested the applicability of this method on 11 adult female, habituated, free-ranging Japanese macaques (Macaca fuscata). Somatometric body length (crown–rump length and anterior trunk length) was statistically compared with the body length obtained using photogrammetry. The significant correlation of the photogrammetric body length with each somatometric measurement verified that the former could be employed to calculate various indices that are used to characterize fat mass (nutritional status) in Japanese macaques. The advantages and disadvantages of photogrammetry are also discussed.     

Comparison of masticatory morphology between Rhinopithecus bieti and R. roxellana

The masticatory apparatus for two endemic species of golden monkey in China, Rhinopithecus bieti and Rhinopithecus roxellana, were compared with those of macaques, Macaca and leaf monkeys, Presbytis. Multivariate analyses demonstrated that the two golden monkey species are distinct. Interspecies allometric analyses revealed that golden monkeys differ in their masticatory apparatus from both macaques and leaf monkeys. The prominent symphysial fusion, corpus, and sagittal condylar dimension of R. roxellana may produce efficient biting force on the incisal and posterior canine teeth, with the heavy reaction force born on the temporomandibular joint. However, the well-developed bizygamatic width and mandibular height in R. bieti suggest that posterior canine function is similarly prominent in R. roxellana, while incisal function is not. © 1995 Wiley-Liss, Inc.     

三种笼养灵长类活动时间分配的比较研究

采用焦点动物法和连续记录法对3种笼养灵长类活动时间分配进行比较研究。结果表明,川金丝猴Rhi-nopithecus roxellanae和熊猴Macaca assamensis用于休息的时间多于猕猴Macaca mulatta,移动时间则相反;川金丝猴和猕猴用于理毛的时间多于熊猴。不同性别年龄组之间的活动时间分配有差异,主要表现在川金丝猴母亲用于理毛的时间明显多于成年儿子,用于玩耍的时间则相反;猕猴成年雄性的移动时间和理毛时间多于成年雌性,玩耍时间则少于成年雌性;熊猴成年雌性的移动时间多于成年雄性,与成年个体相比,幼体花更多的时间用于玩耍,而相应的减少了其休息时间。