Radiation and phylogeography in the Japanese macaque, Macaca fuscata

The Japanese macaque (Macaca fuscata) presumably differentiated from eastern rhesus macaque (Macaca mulatta) populations during the Pleistocene and the two species are closely related. In order to analyse speciation and subspeciation events in the Japanese macaque and to describe historical and current relationships among their populations, we sequenced and analysed a fragment of 392bp of mitochondrial DNA (mtDNA) control region in 50 individuals belonging to six populations of Japanese macaque and compared these sequences with 89 eastern rhesus macaque control region sequences from GenBank/EMBL database. There were high genetic similarities between both species and only two positions were fixed within each species, which supports the inclusion of the Japanese macaque in a single species with eastern populations of rhesus macaques. Japanese macaque ancestors colonised Japan after the separation of the two species, estimated at between 0.31 and 0.88 million years ago (Mya). The star-like phylogeny, multimodal mismatch distribution, and lack of correlation between geographic and genetic distances are in accordance with a rapid dispersion of macaques throughout the archipelago after the arrival into Japan. The species shows low genetic variation within populations and high levels of genetic differentiation among populations with no mtDNA haplotype shared across populations. Genetic distances between Yakushima macaques (Macaca fuscata yakui) and any other population of Macaca fuscata fuscata subspecies are comparable to the distances between populations of Honshu, Awajishima, and Kyushu, not supporting the classification of Yakushima macaques as a different subspecies.     

Postconflict Behavior Among Male Japanese Macaques

Reconciliation was first described more than 20 years ago. Since then, it has been observed in many mammals (mainly primates) but data on postconflict behavior among males are still scarce because they usually aggressively compete for mating partners, rarely maintain amicable relationships with one another. Accordingly, reconciliation is expected to occur at low rates. Although this is true for Japanese macaque males, the subspecies on Yakushima Island (Macaca fuscata yakui) seems to represent an exception as grooming among males occurs often. We analyzed postconflict behavior among them and discuss the possible factors that may favor the occurrence of grooming and reconciliation. Selective attraction between former opponents—reconciliation—occurred soon after conflicts. Consolation—affiliative interactions between a focal animal and group members other than the former opponents occurring earlier in PCs than in MCs—was absent among males. Conciliatory tendency is higher for Yakushima macaque males (0.31) versus that in studies on the other subspecies Macaca fuscata. We discuss differences in the behavioral ecology of the 2 subspecies, the ecological and social factors that may favor the occurrence of reconciliation, and the possible benefits that males gain from grooming exchange and reconciliation.     

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.     

Craniofacial growth of fetal Macaca nemestrina: A cephalometric roentgenographic study

The prenatal growth of the macaque craniofacial skeleton is described using lateral radiographs of 82 fetal and 25 neonatal Macaca nemestrina whose known gestational ages range from 50 to 186 days. The ossification sequence of the craniofacial bones resembles that in the human fetus. During gestation, the macaque neurocranium loses its round, globular shape, becoming flattened and elongated in an anteroposterior direction. In contrast, the morphologic pattern of the face is established early in fetal life, and little change takes place during the remaining prenatal period. The macaque craniofacial dimensions develop along the general skeletal growth pattern, unlike the human craniofacial dimensions, which follow an intermediate pattern between the neural and general skeletal patterns. However, despite minor differences, the macaque and human fetal faces follow the same basic patterns of growth.     

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.     

Morphological studies ofMacaca fuscata

Dermatoglyphics of the foot of two groups of Japanese monkey (Macaca fuscata fuscata of Takasakiyama, Oita Prefecture andMacaca fuscata yakui of Yakushima, Kagoshima Prefecture) were examined. All the fingerprints of the foot consist of a whorl type. Concerning plantar patterns and ridge directions in the sole, there are some differences between both groups. Common to both groups, we find that three kinds of interdigital pattern (II, III, and IV) and proximal thenar pattern (Th^p) are usually of the non-whirling type. This comparatively low frequency of occurrence of a whirling type may be regarded as a characteristic of this species (Macaca fuscata).     

Symmetrical patterns in non-agonistic social interactions found in unprovisioned Japanese macaques

Non-agonistic social interactions in an unprovisioned troop of Japanese macaques (Macaca fuscata yakui) were analyzed with the spacing between individuals, leading-following interactions, and exchange of social grooming. The most frequent interactions were found between kin-related females. Unrelated females stayed with one another rather frequently, but rarely exchanged social behaviors. Interactions between males and females were infrequent though they were occasionaly observed between high-ranking males and high-ranking females. Very frequent exchange of grooming was observed between males, and even high-ranking males exchanged grooming more frequently with males than with females. Most non-agonistic social interactions in the study troop were based on bidirectional exchange of social behaviors, in which no clear tendency relevant to dominance or sex was found; while in provisioned Japanese macaque troops, associations between males and females, between unrelated females, and between males were formed mainly be subordinates' active roles in associative behaviors. This seems relevant to the idea that dominance grealty influence social life in provisioned troops. The present study provides guidelines for interspecific comparison of social interaction patterns of macaque species.     

Observation of a wild Japanese macaque mother pacifying her distressed infant with an acorn

This is the first report on an observation of food transfer by a mother to her offspring in wild Japanese macaques (Macaca fuscata yakui). On November 6, 1996, an adult female wild Japanese macaque stopped grooming her 1.5–1.6 yr old daughter in order to be groomed by a young male. Her daughter protested loudly for about 1 min. In response to her daughter's protest, the mother picked up a mature nut ofQuercus phillyraeoides that was lying near her right hand, and placed it in the daughter's mouth. The daughter's cries were immediately muffled and she silently ate the acorn's contents, and spat out the pericarp. We inferred that the daughter wanted to be groomed by her mother, not to receive food. This reported example of treatment resembling tool using behavior in response to an emotional outcry was precipitated by mother-offspring conflict in the natural habitat.     

Seasonal variation in the feeding behavior and diet of Japanese macaques (Macaca fuscata yakui) in lowland forest of Yakushima

The feeding behavior of the southern subspecies of Japanese macaque (Macaca fuscata yakui) was studied over a period of 18 months in warm temperate broad-leaved forest on the island of Yakushima, Japan. Focal animal data were collected for the eight adults in the troop. Over a full annual cycle, 35.0% of foraging on identified foods was on leaves and shoots, 30.2% on fleshy fruit, 13.2% on seeds, and 5.5% on flowers. Invertebrates and other animal matter accounted for 10.3% of foraging and fungi for 4.6%. There was marked seasonal variation in the use of different food categories, and seeds, leaves, fleshy fruit, and animal matter were each predominant at different times of year. There was also evidence of annual cyclicity in patterns of foraging on all major food types. The monkeys spent less time moving and ate a greater variety of foods when feeding on leaves than when feeding on fruit and seeds, or on insects. Time spent foraging was positively correlated with diversity of the diet, but there was no simple relationship between time spent foraging and the predominant food type. This suggests that a wide variety of foods takes longer to harvest and process, irrespective of the food type. The diet of the study troop was flexible and could not be assigned to a simple dietary category, such as frugivorous or folivorous. If these data are representative of the subspecies, the Yakushima macaque is much more of a dietary generalist than most primates for which there are adequate data. Am. J. Primatol. 43:305–322, 1997. © 1997 Wiley-Liss, Inc.     

Inter-male associations in a wild Japanese macaque troop on Yakushima Island,Japan

Adult male association and its annual change were studied in a wild population of Japanese macaques (Macaca fuscata yakui) on Yakushima Island, Japan. Unlike many other Japanese macaque troops, adult troop males frequently maintained proximity and exchanged grooming with one another in both the mating and non-mating seasons, and the dominance relationship rarely appeared in such inter-male associations. The few cases of agonistic interactions occurred mostly when estrous females or food resources were immediately concerned. Although troop males were very intolerant to newly appeared solitary males (new males) during the mating season, close associations were formed between troop males and new males as soon as the mating season terminated. The consort of new males and lower-ranking troop males with estrous females was frequently disturbed, but these males could copulate no less frequently than higher-ranking males. A comparison among macaque species suggests the existence of two forms of inter-male association: (1) the frequent association based on the symmetrical exchange of social behaviors; and (2) the infrequent and asymmetrical association related to the dominance relationship. The form of inter-male association seems to be influenced by whether or not males can keep close associations with females throughout the year.     

Vocal communication of tonkean macaques in confined environments

Vocal recordings of one semi-free-ranging group and one captive group of Tonkean macaques (Macaca tonkeana) were used to establish the vocal repertoire of the species. Only the alpha male of the groups uttered a very distinctive loud call. Localization variants of coo calls were found. Alarm calls given by this species were acoustically similar to those by Japanese, rhesus, and long-tailed macaques (M. fuscata, M. mulatta, andM. fascicularis). Adult females uttered a specific variant of vocalizations during sexual morphological changes. The repertoire of agonistic vocalizations was more variable than that of any other macaque species investigated. These characteristics were discussed with reference to previous studies on vocalizations of macaque species.     

Cranial adaptation to a high attrition diet in Japanese macaques

Primates with diets that require greater occlusal forces to process exhibit anteroposteriorly shorter, vertically deeper faces, more anteriorly placed masseter attachment areas, and broader, taller mandibular corpora compared to closely related species/populations. Japanese macaques (Macaca fuscata)eat different, perhaps mechanically tougher to process, foods than other macaques do. Accordingly, they should exhibit structural features of the skull related to dissipating great occlusal loads. To test this hypothesis I compared cranial variables amongst wild-caught, adult female skulls (n = 85) of M. fuscataand three other macaque species (M. mulatta, M. fascicularis,and M. nemestrina)and applied least-squares and reduced-major-axis regression analysis and principal components analysis (PCA) to 17 cranial variables reflecting facial, vault, and mandibular dimensions. When scaled for size, the Japanese macaque has a vertically deeper and anteroposteriorly shorter face,a broader but not taller mandibular corpus, and a more anteriorly placed masseter muscle than the other three macaques do. The first PCA axis isolates variation due to a suite of characters related to mechanical efficiency in dissipating occlusal loads (vertically deep face and broad corpus) and differentiates the Japanese macaques from the other species. This, coupled with reported dietary differences among species, suggests that Japanese macaques are selected for dissipating greater occlusal loads than other macaques are. The presence of a narrow mandible relative to cranial breadth and a hyperrobust mandibular corpus width suggests that axial torsion is a significant influence in the masticatory regime of M. fuscata.The lack of an increase in corpus height indicates that parasagittal bending is not as significant an influence. Geographic and climatic influences cannot account for the patterns of variation between M. fuscataand the other macaques.     

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.     

Relation between age–sex classes and dietary selection of wild Japanese monkeys

Dietary selection by wild Japanese monkeys (Macaca fuscata yakui Kuroda) was examined in relation to body size. The monkeys were classified into three age–sex categories: adult males, adult females and immatures excluding suckling infants. Time spent feeding did not differ between age–sex classes, although time spent moving was longer in lighter classes. Heavier individuals fed relatively more on mature leaves, while lighter individuals fed on insects more frequently. Mature leaves were more abundant but had lower energy content than other food items in the forest. Heavier monkeys seemed to feed on greater amounts of lower quality food in this species. This finding agrees with the Jarman–Bell principle on ungulates.     

Coprophagy-related interspecific nocturnal interactions between Japanese macaques (<Emphasis Type="Italic">Macaca fuscata yakui</Emphasis>) and sika deer (<Emphasis Type="Italic">Cervus nippon yakushimae</Emphasis>)

The influence of sympatric large animals on the sleeping behavior of primates in the wild is still largely unknown. In this study, we observed behaviors of wild Japanese macaques (Macaca fuscata yakui) at their sleeping sites, using a highly sensitive video camera. We found evidence of nocturnal interspecific interactions, such as agonistic interactions, between Japanese macaques and sika deer (Cervus nippon yakushimae). Deer approached sleeping clusters of macaques, which slept on the ground, to eat their feces or unidentified materials near the sleeping clusters, and as a result, the macaques were often quickly displaced from their sleeping site. There was a significant difference in the occurrence of macaque–deer agonistic interactions between seasons. Our results suggested that the size of the sleeping cluster, the number of adult macaques in the cluster, and the existence of adult males in the cluster did not influence the occurrence of the agonistic interactions. Finally, we discuss the influence of this interaction on macaques and speculate on the influential factors leading to nocturnal coprophagy of macaques’ feces by deer.     

Genetic differences among subspecies of the saddle-back tamarin (Saguinus fuscicollis):evidence from hybrids

The subspecies of saddle-back tamarins (Saguinus fuscicollis) are known to be chromatically and morphologically diverse but little is known of the genetic basis for the observed morphological variation. The morphology of first generation subspecific hybrids can be compared to that of the parental subspecies to provide information on the extent and nature of genetic differences in morphology between subspecies. We compare two groups of saddle-back tamarin hybrids (S. f. illigeri × S. f. lagonotus and S. f. illigeri × S. f. leucogenys) to pure-bred members of their parental subspecies. These crosses were examined for heterosis, caused by allele frequency differences between the subspecies in combination with directional dominance. Thirty-nine craniofacial measurements were derived from three-dimensional coordinates of landmarks on 355 adult tamarin skulls. These measurements were corrected for sex differences and differences due to environment (wild-derived vs. laboratory-born) prior to analysis of hybridity. Sex differences were minimal for these traits. Environment had a more significant effect on craniofacial morphology. Laboratory environments produce larger faces but smaller orbits, anterior cranial vaults, and cranial bases. Significant heterosis was found for many individual traits and for the first principal component representing size and size-related shape measurements in the S. f. illigeri × S. f. lagonotus cross. The smaller samples involved in the S. f. illigeri× S. f. leucogenys cross led to a much lower number of statistically significant results, although most traits did display heterosis. Heterosis for craniofacial size was nearly statistically significant. These results suggest that there are large differences in allele frequencies among these subspecies of saddle-back tamarin for genes affecting craniofacial morphology. Based on these data we suggest that these subspecies are likely to be independent, largely isolated, evolutionary units. © 1993 Wiley-Liss, Inc.     

Genetic variability in macaques: Correlations between biochemical and dermatoglyphic systems

The palmar dermatoglyphics of four groups of macaque, Macaca nemestrina, M. fuscata yakui, M. f. fuscata and M. fascicularis, were compared, and the genetic affinities of the four groups were assessed using a dermatoglyphic mean square distance measure. According to this measure the two subspecies of M. fuscata were dermatoglyphically more distant from one another than was M. fuscata fuscata from M. nemestrina, suggesting that the two insular populations of M. fuscata had evolved in genetic isolation. The distributions of specific dermatoglyphic patterns were then compared with the frequency distributions of alleles at different protein structural loci in other macaque populations. The results of the comparison were consistent in that insular populations showed reduction in variability for both kinds of systems. The implications of this correlation are discussed in terms of population size and natural selection.     

Age changes of the carpal bones in macaques: Application of the fourier analysis on the radiographs

A method based on the Fourier analysis is proposed, which describes and analyzes the contour morphology of carpal bones by separating morphology into factors of shape and size. Here, “size” refers to the average diameter of the contour. The “shape” is expressed byshape factors which are derived from the Fourier series and the “shape” of a monkey is expressed by ashape index which is calculated fromshape factors. The age change in the morphology of the lunate and capitate ofMacaca fuscata fuscata was analyzed by this method. The development of “shape” approximately completes by 3 years of age, whereas increase in “size” begins its spurt at that age as do body weight and anterior trunk length. By applying this method to other macaque species, it was found thatM. mulatta, M. f. yakui andM. cyclopis exhibit similar patterns of growth and development of carpal bones to those ofM. f. fuscata. Patterns found inM. fascicularis differ in that its bones develop faster than in the other macaques with respect to the “shape,” but remain small with respect to the “size.”     

Reappraisal of <Emphasis Type="Italic">Macaca speciosa subfossilis</Emphasis> from the Late Pleistocene of Northern Vietnam Based on the Analysis of Cranial Anatomy

Jouffroy (Bulletin du Muséum National d'Histoire Naturelle. Série 2 31:209–216, 1959) described Macaca speciosa subfossilis on the basis of her study of the external anatomy of a nearly complete cranium (PV F1; Muséum national d’Histoire naturelle, Paris) found in the Late Pleistocene cave deposits, Thung-Lang, northern Vietnam. Whereas Jouffroy (Bulletin du Muséum National d'Histoire Naturelle. Série 2 31:209–216, 1959) considered it to belong to an ancestor of Macaca arctoides or M. thibetana, Fooden (Journal of Human Evolution 19:607–686, 1990) reexamined the facial anatomy and assigned it to the extant species M. arctoides. We used computed tomography images to reevaluate the phylogenetic position of Macaca speciosa subfossilis by comparing the external and internal features of PV F1 with those of the crania of the extant macaque species. PV F1 shows a lower degree of preorbital concavity than Macaca arctoides, M. assamensis, and M. thibetana, but shares an anteriorly directed malar as seen in the crania of the two former species. The size of the molars of PV F1 falls within a range such that the cranium may be assigned to any of the five species of Macaca arctoides, M. assamensis, M. thibetana, M. mulatta, and M. nemestrina. An analysis of the internal structure of the cranium reveals that only PV F1 and the cranium of Macaca arctoides have a pear-shaped nasal cavity expanding laterally at both the anterior and posterior regions. Such a feature is probably a derived condition in the macaque lineage, suggesting a close relationship between Macaca speciosa subfossilis and M. arctoides. This finding supports the paleobiological scenario that the members of the lineage of Macaca arctoides diverged from the other members of Asian macaques and became distributed in northern Vietnam as early as the Late Pleistocene.     

Ultrasonic assessment of pregnancy and fetal development in three species of macaque monkeys

Serial ultrasonic assessments of gestational sac (GS) and fetal biparietal diameter (BPD) were performed in the Japanese monkey (Macaca fuscata fuscata), rhesus monkey (Macaca mulatta), and crab-eating monkey (Macaca fascicularis). In the Japanese monkey, GS increased linearly for 3-8 weeks, whereas BPD increased in a linear-quadratic manner over 8 weeks to term. Ultrasonic assessments of spontaneously aborted fetuses with BPD growth retardation and diagnosis of a pelvic chocolate cyst also were reported.