The stumptail macaques of China

The stumptail macaque species Macaca thibetana and Macaca arctoides replace one another from north to south in subtropical and tropical China. These species differ in external and cranial characters. Neonatal pelage color is pale grayish-brown in M. thibetana and whitish in M. arctoides. In adults, ventral pelage is whitish in M. thibetana and brown in M. arctoides. The forehead and cheeks are thickly furred in adult M. thibetana and bald in M. arctoides. Facial skin color typically is sexually dimorphic in M. thibetana—buffy in males and reddish in females—and monomorphic in M. arctoides—reddish in both sexes. Head and body length, weight, relative tail length, and relative ear length all tend to average greater in M. thibetana than in M. arctoides. Skull length, rostral-postrostral ratio, and relative canine length in males average greater in M. thibetana. than in M. arctoides; relative zygomatic breadth and relative bimalar breadth average greater in M. arctoides than in M. thibetana. Reproductive anatomy in both sexes is strikingly divergent in these two species. Although these species are adapted to different climatic zones, many aspects of their natural history are generally similar, as far as is now known. One apparent behavioral difference is that M. thibetana usually sleeps in caves or rocky crevices, while M. arctoides usually sleeps in trees.     

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.     

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.     

Copulatory behavior in relation to anatomical characteristics of three macaques

Anatomy of copulatory organs and patterns of copulatory behavior were studied in three species of Macaca. The copulatory behavior of the rhesus monkey (M. mulatta) and crab-eating macaque (M. fascicularis) were similar. Mounting time was longer in stump-tailed macaque (M. arctoides) (48 seconds) than in the rhesus monkey or crab-eating macaque (8.5 seconds). Species differences were correlated with anatomical differences in the female and male reproductive organs. In the stump-tailed macaque the male has a relatively long penis, and the female has an elaborate vestibular colliculus in the vestibule. Both rhesus and crab-eating macaques have a short penis, and the female has no vestibular colliculus. Under scanning electron microscope, cone-like projections (3–4 mm) were observed on the surface of the glans and corpus penis of M. arctoides. In M. fascicularis shorter projections (0.05–0.1 mm) were observed on the glans penis but not the corpus penis.     

Responses to urinary stimuli in pigtailed (Macaca nemestrina) and stumptailed (Macaca arctoides) macaques

Responses to different urine samples were studied in pigtailed (M. nemestrina) and stumptailed (M. arctoides) macaques. Both species exhibited more interest towards urine samples from their own species than neutral stimuli. Responses towards urine samples from other macaque species did not significantly differ from those towards neutral stimuli. In stumptailed macaques, no differential interest was observed between urine samples from a known (the adult male of the group) and an unknown adult male conspecific.     

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.     

Genetic polymorphism of alpha-1-antitrypsin in macaque species

Thirty-two phenotypes of alpha-1-antitrypsin (al-AT) controlled by 18 codominant alleles of PI_mac locus were identified by isoelectric focusing in 1.121 macaques of nine species. In terms of al-AT polymorphism macaque species vary markedly from nearly monomorphic (Macaca mulatta, M. arctoides) to highly polymorphic (M. nemestrina, M. fascicularis). Only 4 of 18 PI_mac alleles are common for two or more macaque species, the rest of the alleles are species-specific.     

Taxonomy and evolution of thesinica group of macaques: I. Species and subspecies accounts ofMacaca sinica

Based on study of 116 museum specimens and review of relevant literature, a new species account ofMacaca sinica, the Sri Lanka toque macaque, is presented. External and cranial characters of the species are described and analyzed. A summary of natural history of the species includes information on habitats, arboreal-terrestrial preferences, predators, diet, relations with other primate species, density, troop size and composition, home range area, and reproductive biology. Two subspecies ofM. sinica are recognized, northernM. s. sinica (Linnaeus, 1771) and southwesternM. s. aurifrons (Pocock, 1931). Geographic ranges of these two subspecies meet in a 50–200 km broad contact zone in which representatives of both subspecific phenotypes are encountered (35s. sinica phenotypes; 8s. aurifrons phenotypes in 43 contact zone specimens examined). An annotated gazetteer of known macaque localities in Sri Lanka provides information concerning available museum specimens and field reports by collectors or observers. Comparative study of three remaining species in thesinica group (M. radiata, M. assamensis, & M. thibetana) is in progress. This research was partly supported by National Institutes of Health MBS Grant No. RR-08043 to Chicago State University.     

Species differences of male loud calls and their perception in sulawesi macaques

Playback experiments were conducted to investigate interspecific discrimination of male loud calls in Sulawesi macaques. Loud calls of four macaque species living in Sulawesi (Macaca tonkeana, M. maurus, M. hecki, andM. nigrescens) and a control stimulus (an 8-sec frequency modulated sound) were played back to semi-free-ranging Tonkean macaques (M. tonkeana). A preliminary acoustic analysis indicated that the calls of these four species differ in some spectral and temporal features. In the playback experiments, Tonkean macaques responded in a similar manner to conspecific calls and calls of two other species,M. maurus andM. hecki. In contrast, animals responded more weakly to the call ofM. nigrescens and the control stimulus. Males responded more strongly than females to all stimuli, while females appeared to be more discriminating for species differences than males. Analyses on the acoustic features of loud calls suggested that high frequency, wide frequency range, and repetition of sound units at a high rate elicit quick responses from animals.     

Genetic characterization of long-tailed macaques (Macaca fascicularis) on Tabuan Island Indonesia

Protein and mitochondrial DNA variations (D-loop region PCR-RFLP) were analyzed for 7 serum and 40 clot samples collected from long-tailed macaques (Macaca fascicularis) living on Tabuan Island, Indonesia. Protein polymorphisms were examined electrophoretically for 5 and 12 kinds of protein in serum and erythrocytes, respectively. Each of the protein loci tested showed a monomorphic pattern. Polymorphisms were detected in the analysis of the D-loop-containing region of mtDNA (PCR-RFLP) using 32 restriction endonucleases. Two haplotypes, differing 1.03% in sequence divergence were observed, and both were previously undetected in other local populations. Based on genetic features and differences in pelage color as outlined inFooden's (1995) morphological analysis, the present results suggest that long-tailed macaques on Tabuan Island are a unique population. From the genetic analyses performed here, Tabuan monkeys are considered to be the same species group as those populations of Sumatra and Java (Fooden, 1995).     

Vocal communication of wild bonnet macaques (Macaca radiata)

Field observations and spectrographic analyses of sound recordings of South Indian bonnet macaques revealed a vocal repertoire of at least 25 basic patterns. The repertoire consists of well separated sound classes and acoustic categories connected by structural intergradation. Besides structural variations within and between different elements of the repertoire, the vocal system ofMacaca radiata is characterized by regular combinations of particular basic patterns. These combinations occurred not only between calls of similar structure and function but also between calls usually emitted in entirely different social contexts. According to the qualitative analysis, sex-specific asymmetries of the vocal behaviour were less pronounced than age-dependent characteristics. The comparison of clear call vocalizations ofMacaca radiata andM. fuscata revealed significant species-specific differences on the structural and the behavioural level. Evaluations of the structural features of alarm calls of various macaque species imply marked differences between members of thefascicularis group andsinica group on one hand and thesilenus group andarctoides group on the other.     

<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.     

The borderlands and possible hybrids between three species of macaques,M. nigra,M. nigrescens,andM. hecki,in the northern peninsula of Sulawesi

The borderlands between three species of macaques,Macaca nigra, M. nigrescens, andM. hecki, which live on the northern peninsula of Sulawesi were surveyed mainly via observations of pet monkeys kept by local people. The borderlands between these species could be delineated. Some monkeys of peculiar appearance and/or with mixtures of the external characteristics of two species were found in the borderlands between the respective pairs of species. However, such possibly hybrid monkeys were seen or originated only in the very limited areas where the species might come into contact with each other.     

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.     

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.     

Species recognition by five macaque monkeys

Sixteen monkeys of five macaque species (Macaca fuscata fuscata, M. mulatta, M. radiata, M. nemestrina, andM. arctoides) pressed a lever to see a variety of pictures (35 mm slides) of seven macaque species including their conspecifics. The subjects were allowed to see the same picture for the duration of the lever press and were able to see the same picture repeatedly by pressing the lever within 10 sec after the previous release of the lever. When 10 sec passed after releasing the lever, the next picture was set on the slide projector. All monkeys exceptM. arctoides and two infantM. fuscata fuscata pressed the lever to see their conspecifics for the longest duration. For all of the adult subjects, a multivariate analysis of variance (MANOVA) based on the mean duration of lever pressing responses (D) and the mean interval between the responses (I) revealed that the data for conspecific stimuli were distributed at significantly different locations from those for at least one of six close species on a two-dimensional space constructed with D and I. These results suggest that adult macaque monkeys visually discriminate their conspecifics from close species based on the still images of them.     

Morphological studies on the Sulawesi macaques I: Phyletic analysis of body color

The body color of Sulawesi macaques was measured quantitatively and compared among the different monkeys. As a result, divergence models for extant Sulawesi macaques, withtonkeana as the starting point and fading as the sole direction of color change, were inferred as follows: (1) fading slightly on the upper half of the body—nigra, fading more on the proximal part of the body—nigrescens; (2) fading over the whole body—maura; (3) fading greatly on the legs—hecki; and (4) fading on the distal part of the body—ochreata, fading more over the whole body, including the proximal part of the body—brunnescens. The color changed progressively in the order of (1) through (4). The divergence model, excluding the position ofhecki (3), supports the speciation model ofFooden (1969). If the proto-Sulawesi macaques had a body color pattern similar to the livingnemestrina, darkening would have been necessary for the evolution of the Sulawesi macaques after their immigration, and it may have been acquired as an adaptation to the ground (forest floor) living nature of the Sulawesi macaques, together with influences deriving from the insularity and/or from the absence of predators.     

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.