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.     

Pelage Color Variation of Macaca arctoides and Its Evolutionary Implications

Stump-tailed macaques (Macaca arctoides) exhibit significant intraspecific variation in pelage color. Based on their pelage color and geographical distribution, they are classified into 2 subspecies: northern bright brown Macaca arctoides arctoides and southern black Macaca arctoides melanota. However, studies on the natural population are extremely scarce, and researchers have occasionally questioned the subspecific classification. We quantitatively examined pelage color variation of Macaca arctoides in 3 free-ranging populations in Thailand. Pelage color difference between populations is significant. The population distributed south of the Isthmus of Kra showed wide intrapopulational variation, including bright brown, dark brown, and completely black, whereas the northern populations primarily had dark brown hairs. Thus, we conclude that one cannot classify the color variants into subspecies. Further, we hypothesize that the distinctive polymorphism in southern Thailand resulted from geographical isolation caused by the Pleistocene eustatic fluctuations and subsequent recovery of land connection and subsequent gene flow.     

Morphometric analysis ofMacaca arctoides andM. thibetana in relation to other macaque species

As a first step in reviewing the classification of the two stump-tailed macaque species,Macaca arctoides andM. thibetana, as compared with other species of the genusMacaca, 72 linear dental and cranial variables of 11 macaque species were examined by morphometric analyses. The results indicate that the two stump-tailed species are the largest of the macaques and although rather similar overall, they exhibit significant differences in the pattern of variation in most of the five skull regions as shown by Principal Components and Canonical Variate Analyses. Euclidean Distances based on Canonical Variate scores indicate that the females ofM. arctoides andM. thibetana are more widely separated than eight other pairs of macaque species, and that the separations of the respective males are greater than those of three other pairs of species. These findings are consistent withFooden's classification of the stump-tailed macaques as two separate species (Fooden, 1976;Fooden et al., 1985). The present results suggest, as other researchers have proposed on the basis of external features, biochemistry and genetics, that the two stump-tailed macaque species andM. assamensis are closely related. The results also tentatively imply associations withM. fuscata andM. sylvanus but these require further study. The findings have implications for the assessment of the various Chinese Pleistocene macaque fossils.     

Tail length variation inMacaca fascicularis andM. mulatta

Based on collectors' measurements of 1,040 specimens, variation of relative tail length [RTL = (tail length/head and body length) × 100] has been studied inMacaca fascicularis andM. mulatta, two closely related species that replace one another in tropical Asia and subtropical Asia, respectively. RTL usually is greater than 90 inM. fascicularis and usually is less than 60 inM. mulatta; intermediate values occur in only 3.5% of specimens studied. Within each species, RTL is approximately equal in females and males. From infancy to adulthood, RTL tends to decline in both species. InM. fascicularis, RTL generally decreases with increasing latitude; inM. mulatta, RTL is approximately constant latitudinally. Where the geographic ranges of these two species meet at ca. 15°N in the Indochinese Peninsula, a few specimens have been collected in which RTL and dorsal pelage color are intermediate between those inM. fascicularis andM. mulatta. The observed pattern of variation suggests that the ranges ofM. fascicularis andM. mulatta formerly were separated by a zoogeographic barrier — perhaps during a Pleistocene glacial interval. After disappearance of the postulated barrier, the ranges of these two species apparently became contiguous and limited hybridization has occurred.     

<Emphasis Type="Italic">Macaca munzala</Emphasis>: A New Species from Western Arunachal Pradesh,Northeastern India<Superscript>*</Superscript>

Macaca, comprising 20 well-characterized species, represents the largest and one of the most ecologically and socially diverse of all the nonhuman primate genera. We report the discovery of a macaque that is new to science from the high altitudes of western Arunachal Pradesh, a biodiversity-rich state in northeastern India. We propose the scientific name Macaca munzala and the vernacular name Arunachal macaque for the species. It shares morphological characteristics independently with the Assamese macaque (Macaca assamensis) and with the Tibetan macaque M. thibetana; like them, it appears to belong to the sinica species-group of the genus. However, the species is distinctive in relative tail length, which is intermediate between those of Tibetan and Western Assamese macaques, the subspecies with which it is sympatric. It is also unique in its altitudinal distribution, occurring largely at altitudes between 2000 and 3500 m. We provide a morphological characterization of the species, report preliminary data on its field biology and discuss possible taxonomic identity in relation to the other closely-related species of Macaca.^*This paper is dedicated to Dr. A. J. T. Johnsingh for his immense contributions to the study and conservation of India’s wildlife and for being an inspiration to a whole generation of students.     

Identification of MHC class I sequences in four species of Macaca of China

Tibetan macaques (Macaca thibetana), stump-tailed macaques (M. arctoides), Assamese macaques (M. assamensis), and northern pig-tailed macaques (M. leonina) are four major species of Macaca in China. In order to effectively use these species in biomedical research, thorough investigations of their MHC immunogenetics are required. In this study, we identified MHC class I sequences using cDNA cloning and sequencing on a cohort of six M. thibetana, three M. arctoides, three M. assamensis, and three M. leonina derived from Sichuan and Yunnan provinces of China. Eighty new alleles were identified, including 26 MHC-A alleles, 46 MHC-B alleles, and 8 MHC-I alleles. Among them, Math-A1*126:01, Math-B*190:01, Math-B*191:01, Math-B*192:01, Maar-A1*127:01, Maar-A1*129:01, and Maas-A1*128:01 represent lineages that had not been reported earlier in Macaca. Phylogenetic analyses show that no obvious separation of lineages among these species of Macaca. This study provides important information about the MHC immunogenetics for the four major species of Chinese macaques and adds value to these species as model organisms in biomedical research.     

Phylogenetic Relationships of the Macaques (Cercopithecidae: Macaca), Inferred from Mitochondrial DNA Sequences

To study the phylogenetic relationships of the macaques, five gene fragments were sequenced from 40 individuals of eight species: Macaca mulatta, M. cyclopis, M. fascicularis, M. arctoides, M. assamensis, M. thibetana, M. silenus, and M. leonina. In addition, sequences of M. sylvanus were obtained from Genbank. A baboon was used as the outgroup. The phylogenetic trees were constructed using maximum-parsimony and Bayesian methods. Because five gene fragments were from the mitochondrial genome and were inherited as a single entity without recombination, we combined the five genes into a single analysis. The parsimony bootstrap proportions we obtained were higher than those from earlier studies based on the combined mtDNA dataset. Excluding M. arctoides, our results are generally consistent with the classification of Delson (1980). Our phylogenetic analyses agree with earlier studies suggesting that the mitochondrial lineages of M. arctoides share a close evolutionary relationship with the mitochondrial lineages of the fascicularis group of macaques (and M. fascicularis, specifically). M. mulatta (with respect to M. cyclopis), M. assamensis assamensis (with respect to M. thibetana), and M. leonina (with respect to M. silenus) are paraphyletic based on our analysis of mitochondrial genes.     

Seasonal changes in body weight of Macaca thibetana at Mt. Emei,China

This 1991–1992 study was designed to expand previous research on body weight (BW) in Tibetan macaques (Macaca thibetana) at Mt. Emei. Data on BW were collected in late autumn (LA) and late winter (LW) in groups ranging above 1,200 m. Over the winter, the BW fell significantly from a mean of 16.8 to 11.4 kg in females and from 19.5 to 17.0 kg in males. The previously reported BW means of 12.8 kg for females and 18.3 kg for males, measured in late spring, are near the center of the annual BW range for this species. In addition, with the sharper decline of female BW (?32% vs. ?13% seen in males), the sexual dimorphism (M /F ) in BW increased from 1.16 in LA to 1.49 in LW. This finding may be related to differential parental investment by two sexes. © 1994 Wiley-Liss, Inc.     

Baculum length and copulatory behavior in primates

The length of the baculum (os penis) was measured in 74 adult males representing 46 primate species. These data, and a review of previously published measurements, indicate that variation in baculum length among primates is related to taxonomic and behavioral differences. Thus, many New World monkeys have shorter bacula, relative to body weight, than Old World monkeys. The baculum is shorter in colobine monkeys than in cercopithecines. Among the great apes, reduction of the baculum is more pronounced in Pan and Gorilla than in Pongo. Very long bacula are found in some nocturnal prosimians (eg, Lorisidae) and also in Macaca arctoides. A comparison of baculum length relative to body weight was made in 34 species for which detailed information on copulatory behavi or was available. The presence of an elongated baculum was shown to correlate with copulatory patterns involving prolonged intromission and/or the maintenance of intromission during the postejaculatory interval (eg, Galago crassicaudatus, Loris tardigradus, M, arctoides). The evolutionary significance of these observations is discussed and it is suggeted that similar copulatory patterns may occur in species with elongated bacula (eg, Daubentonia, Perodicticus) for which behavioral data are lacking at present. The same hypothesis also applies to an extinct adapid primate which possessed a very large baculum.     

Wounding patterns in three species of captive macaques

The incidence of wounding in captive groups of rhesus (Macaca mulatta), pigtail (M. nemestrina), and stumptail (M. arctoides) macaques was studied for 21 months. Groups were monitored daily for evidence of wounding. Wounded animals were captured, treated by veterinary staff, and returned following recovery. Records were kept on the age, sex, and species of the recipient, along with the type and location of wound. In each species of macaque, adult males incurred the highest frequency of wounds and multiple wounds of any age-sex class. This contrasted with previously reported behavioral data indicating low frequencies of aggression received by adult males, especially contact aggression and bites. These discrepancies indicate wounding frequencies do not necessarily correspond with behavioral measures of aggression. Inhibition of aggression directed toward infants and the selective avoidance of bites directed to vital body regions were presented as possible mechanisms that modify intragroup aggression. Increased wounding in the birth season under captive conditions suggests that the pattern of increased wounding reported during the breeding season under freeranging conditions may reflect xenophobic responses to immigrating males, rather than direct male-male competition for estrous females.     

Macaca thibetana at Mt. Emei,China: III. Group composition

Data on group composition at the end of the 1986 birth season were collected from six groups of Macaca thibetana. All adult males, the members of group A, and some conspicuous animals were recognized individually. Fourhundred survey sessions were completed. The mean group size was 38.3 (SD = 13.8, range: 28–65); the number of adult females was the best correlate of total group size. The mean adult sex ratio (F:M) across groups was 3:1 (SD = 1.9, range: 1.5–6.5:1), which significantly deviated from 1:1. Sex ratios (F:M) in newborns, juveniles, and all members did not significantly deviate from 1. The ratio of immature animals to adults was 1.5 to 1 (average of groups); that is, 60% of the population was composed of immature animals, and the population was growing.     

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.     

Mandibular morphometrics among macaques: The case ofmacaca thibetana

Recent field studies suggest that Macaca thibetana,a large endemic Chinese macaque, may be quite folivorous, distinguishing it from most other macaque species, which tend to be primarily frugivorous. To understand how this diet affects its masticatory system, we conducted a comparative morphometric study of mandibular dimensions. We took linear measurements from male and female mandibles of this species as well as four other macaques—M. fascicularis, M. nemestrina, M. arctoides,and M. assamensis—and four species of Presbytis—P. obscura, P. rubicunda, P. cristata,and P. phayrei—and subjected to them to a variety of analyses. Based on analyses of variances and discriminant analyses on each sex individually, the mandible of M. thibetanacorresponds to expected patterns for folivorous primates with respect to its wide condyles and thick corpora. However, the height of the corpus and symphysis are lower, and the anteroposterior length of the condyle is longer than predicted for a folivore. In addition to interpretations specifically relating to M. thibetana,we also discuss the functional morphology of the other species in light of what is published about their diets.     

Macaca leonina has a wider niche breadth than sympatric M. mulatta in a fragmented tropical forest in southwest China

Niche differentiation has long been identified as an essential stabilizing mechanism for the coexistence of sympatric species. Using camera trapping data obtained during 2012–2016, we identified Macaca leonina and M. mulatta as the dominant macaque species in the Naban River Watershed National Nature Reserve (NRW-NNR), a tropical forest in southwestern China. In general, M. leonina exhibited a wider distribution and greater niche breadth than co-occurring M. mulatta. According to a fitted maximum entropy model (MaxEnt), M. leonina was predicted to predominantly occur in forest at higher elevation, whereas M. mulatta was predicted at lower elevation; the broadleaved evergreen forest was predicted as the most suitable vegetation for both species to inhabit, while the unsuitable area was bordered by rubber plantation, in which both food scarcity and human disturbance restricted the movement of macaques. Although the niches of these two species highly overlapped across space and time, we also found evidence for their spatiotemporal niche differentiation. When the two species inhabited independent areas with different elevations and vegetation, they maintained a similar activity pattern; however, in the zones of overlap, their activity patterns differed significantly. Further comparative field studies of these two macaques, considering other niche dimensions, are required to ensure their coexistence and long-term conservation.     

Non-seasonal breeding pattterns in stumptail macaques (Macaca arctoides)

This paper summarizes published reports of breeding patterns across the genusMacaca. Patterns range from strictly seasonal to non-seasonal. Data on sexual behavior and birth patterns are presented which confirm previous reports of non-seasonality forMacaca arctoides. In a captive colony, 63 births were recorded, and individuals were born during every month of the year. Heterosexual mounting activity was recorded over a two-year period and occurred during every month of that period. It is clear thatM. arctoides does not exhibit the seasonal cyclicity observed in some other macaque species.     

Ranging behavior ofMacaca thibetana at Mt. Emei,China

Food handouts from visitors to Mt. Emei, in The People’s Republic of China, have considerably increased the diversity of food available to an indigenous population of Macaca thibetana.Some 43% of the feeding time was spent at the trail area frequented by tourists. Ranging behavior was of two kinds: wandering around within the group’s most densely used areas and making peripheral excursions between the areas. Three kinds of trail-area use were observed: three-group overlapping, two-group overlapping, and exclusive. M. thibetanatended to use sheltered sites for sleeping, to ensure safety and/or to keep dry in a rainy habitat. Exclusively and successively used sleeping sites were noted. The average size of the home range per group was 3 km ²; the average population density for the entire range was 13/km², and the biomass was 109 kg/km². The population may be growing, a possibility that is also supported by previous analyses using data on group composition.     

Dominance style of Japanese macaques compared with rhesus and stumptail macaques

In the present study, we seek to relate dominance style with group cohesion in a captive group of Japanese macaques (Macaca fuscata). Social data were gathered on approach rate, result, and direction, aggression rate and intensity, grooming rate and direction, and conciliatory tendency. Data were collected using focal animal sampling and instantaneous scan sampling. Reconciliation data were collected using ad libitum observations of aggression with ten-minute post-conflict and matched-control focal observations. Data were compared to prior studies on rhesus (M. mulatta) and stumptail macaques (M. arctoides) living in similar environments. Each species demonstrated the presence of a formalized dominance hierarchy based on the teeth-baring display. The Japanese macaque group showed a lower rate of approach with a higher proportion of negative outcomes than either of the other species. Rates of aggression and reconciliation were also lower in the study troop, suggesting a strict hierarchy while maintaining an optimal nearest-neighbor distance. Overall, this group of Japanese macaques was less sociable than other groups of the same species, perhaps due to a history of individual removals. © 1995 Wiley-Liss, Inc.     

Temperament in Rhesus,Long‐Tailed,and Pigtailed Macaques Varies by Species and Sex

Temperament differs among individuals both within and between species. Evidence suggests that differences in temperament of group members may parallel differences in social behavior among groups or between species. Here, we compared temperament between three closely related species of monkey—rhesus (Macaca mulatta), long‐tailed (M. fascicularis), and pigtailed (M. nemestrina) macaques—using cage‐front behavioral observations of individually housed monkeys at a National Primate Research Center. Frequencies of 12 behaviors in 899 subjects were analyzed using a principal components analysis to identify temperament components. The analysis identified four components, which we interpreted as Sociability toward humans, Cautiousness, Aggressiveness, and Fearfulness. Species and sexes differed in their average scores on these components, even after controlling for differences in age and early‐life experiences. Our results suggest that rhesus macaques are especially aggressive and unsociable toward humans, long‐tailed macaques are more cautious and fearful, and pigtailed macaques are more sociable toward humans and less aggressive than the other species. Pigtailed males were notably more sociable than any other group. The differences observed are consistent with reported variation in these species’ social behaviors, as rhesus macaques generally engage in more social aggression and pigtailed macaques engage in more male–male affiliative behaviors. Differences in predation risks are among the socioecological factors that might make these species‐typical behaviors adaptive. Our results suggest that adaptive species‐level social differences may be encoded in individual‐level temperaments, which are manifested even outside of a social context. Am. J. Primatol. 75:303‐313, 2013. © 2012 Wiley Periodicals, Inc.     

Southward extension of the range ofmacaca thibetana

Based on results of recent fieldwork, the known geographic range of Macaca thibetanais extended approximately 55 km southward, to 23°48’N, in Jinxiu County, Guangxi Province, China.