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.     

Determining genetic background in captive stocks of cynomolgus macaques (Macaca fascicularis)

Background As in other model organisms, genetic background in the non‐human primates Macaca mulatta and Macaca fascicularis is an experimental variable that affects the response of other study variables. Genetic background in model organisms is manipulated by breeding schemes but is generally pre‐determined by the source population used to found captive stocks. In M. fascicularis three such sources have been distinguished, however, these are not routinely taken into consideration when designing research. Methods We exemplify a mitochondrial DNA (mtDNA)‐based strategy to trace the maternal geographic origins of M. fascicularis animals of unspecified origins. Results Macaca fascicularis of unspecified origins kept at primate research centers carry mtDNA haplotypes representing all three major genetic subdivisions. Conclusions We suggest that the genetic background of study animals could be better specified in the future using an mtDNA‐based approach, which would enable informed selection of study animals and help reduce variation within and among studies.     

Structural differentiation of microhabitats of sympatricmacaca fascicularis andM. nemestrina in East Kalimantan,Indonesia

Macaca nemestrina andM. fascicularis coexist through much of their geographic ranges in Southeast Asia, but locally they segregate into drier hilly terrain and wetter alluvial riverine terrain respectively. SinceM. fascicularis travel arboraally andM. nemestrina, travel terrestrially, structural characteristics of habitats on the two different substrates may explain local segregation of these two species. This paper reports measures comparing habitat structure ofM. fascicularis fascicularis andM. nemestrina nemestrina at the Mentoko site in East Kalimantan, Indonesia. Results show that (1) ground cover is thicker; (2) there are fewer gaps in the canopy; and (3) the foliage of the canopy is more dense in habitat occupied by arborealM. f. fascicularis than in habitat occupied byM. n. nemestrina. These differences in habitat structure appear to explain segregation of the two species at the Mentoko. Similar differences in habitat may permit coexistence of the two species throughout their geographical ranges.     

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.     

Polyspecific groups of macaques on the kowloon peninsula,new territories,Hong Kong

Three polyspecific groups of free-ranging macaques were observed in July and August of 1980 and 1981 in the forests of the New Territories of mainland Hong Kong. Two groups were composed of rhesus monkeys (Macaca mulatta) and long-tailed or crab-eating monkeys (M. fascicularis), and one group was composed of both the former plus Japanese macaques (M. fuscata). All three groups contained hybrids between M. mulatta and M. fascicularis. This combination of species within the same social group is an unusual circumstance in natural habitats, and it offers a unique opportunity for field studies in primate ecology and behavior.     

Geometric characters of the radius and tibia in <Emphasis Type="Italic">Macaca mulatta</Emphasis> and <Emphasis Type="Italic">Macaca fascicularis</Emphasis>

We performed comparative analyses of four cross-sections of the distal radius and tibia in two species of macaque to clarify the relationships between bone morphology and locomotor type. The lengths of bones and five bone geometric properties in each section were examined and compared separately in both female and male Macaca mulatta and Macaca fascicularis. In M. mulatta, there were no significant gender-specific differences in either the radius or the tibia. In contrast, the radius and tibia of male M. fascicularis had greater geometric parameters in the 20% and 40% positions relative to the 5% and 10% positions from the distal end than those of their female counterparts. The radius and tibia of M. mulatta were relatively longer than those of M. fascicularis, and the sectional parameters of the tibia of M. mulatta were relatively larger than those of M. fascicularis. Standardization of the log-transformed bone length between the species revealed larger radial cortical bone areas in M. fascicularis. In contrast, there were minimal differences in the tibial cortical bone areas between the two species. This study suggests that the observed distinctions in bone geometry in female and male M. fascicularis may be due to gender-specific differences in the muscle weights of the forearm and calf, which may underlie the divergence in the leaping abilities of females and males of this species. Taken together, these results of interspecies comparisons may be related to the fact that arboreal primates such as M. fascicularis undergo compressive mechanical stress due to the forelimb lead that occurs as the animal descends a sloping trunk or bridges a tree gap downward, while terrestrial primates such as M. mulatta move on nearly flat substrates. Differences in fore- and hind-limb bone properties between the two species are discussed with regard to functional morphology and locomotor type.     

Tail-Length Evolution in Fascicularis-Group Macaques (Cercopithecidae: Macaca)

In the four species of macaques that constitute the fascicularis-group, relative tail length generally decreases with increasing latitude, in accord with Allen's Rule. Although this generalization applies to Macaca mulatta in the northern part of its range—north of ca. 26°N, it does not apply south of ca. 26°N, where the tail is anomalously short in Macaca mulatta. This suggests that the anomalously short-tailed population of Macaca mulatta did not originate within its present latitudinal range, but instead dispersed there from farther north. The anomalously short-tailed population apparently replaced a now-extinct longer-tailed population, from which founders of insular Macaca cyclopis previously had been derived. Southward dispersal of the anomalously short-tailed population of Macaca mulatta, and correlated extinction of the longer-tailed population that it apparently replaced, may have been induced by a major glacial advance.     

Patterns of sexual behavior in male macaques

One large social group of each of three species of macaques (Macaca mulatta, M. fascicularis, M. radiata), housed in half-acre field cages at the California Primate Research Center, were observed for a total of 150 h. Data on sexual behavior and dominance interactions were recorded by pairs of experienced observers using a focal animal technique. Single or multiple mount-to-ejaculation sequences, number of thrusts per mount, number of mounts per sequence, duration of mounts per sequence, duration of sequences, social rank and frequency of sexual activity were recorded for each adult male. M. mulatta used a multiple mount-to-ejaculation (MME) pattern in 91% of their copulations. M. radiata used a single mount-to-ejaculation (SME) pattern in 91% of their copulations. M. fascicularis used both patterns—53% MME and 47% SME. A positive correlation was found between rank and sexual activity in fascicularis and mulatta males. A negative correlation between rank and sexual activity was found in radiata males and also a positive correlation between rank and age indicating that the youngest and most subordinate radiata males were the most sexually active males. In reviewing the literature, a relationship between degree of intermale competition, intermale tolerance and type of mounting pattern was revealed. Macaque species that primarily use an SME pattern also show sa high degree of intermale tolerance and little interrnale competition. Macaque species that primarily use an MME pattern typically show a high degree of intermale competition and a low degree of intermale tolerance. Possible events leading to such relationships are discussed.     

Quantitative analyses of cross-sectional shape of the distal radius in three species of macaques

I conducted quantitative analyses of the cross-sectional shape of the distal radial shaft in three species of macaques, which differ in locomotor behavior: semi-terrestrial Japanese macaques (Macaca fuscata), arboreal long tailed macaques (M. fascicularis), and relatively terrestrial rhesus macaques (M. mulatta). I took CT scans of the distal radial shafts of a total of 180 specimens at the level of the inferior radio-ulnar articulation. From each CT image, the periosteal outline of the radius was traced automatically by a digital imaging technique. I determined five points (landmarks) on the outline by developing a standardized morphometric technique. Bone surface lengths were measured by using these landmarks and their soft tissue correlates were investigated. The results of this study were as follows: (1) Semi-terrestrial M. fuscata has features that are approximately intermediate between those of the other two species. M. fuscata has a relatively small groove for M. abductor pollicis longus and a large groove for Mm. extensor carpi radialis longus et brevis. These characters resemble those of M. fascicularis. On the other hand, the ulnar notch of M. fuscata is relatively large, a character which is similar to that of M. mulatta. Moreover, compared to the other two macaques, the surface of the flexor muscles of M. fuscata is intermediate in size. (2) The more terrestrial M. mulatta has a relatively large groove for M. abductor pollicis longus and a small groove for Mm. extensor carpi radialis longus et brevis. Moreover, M. mulatta has a relatively large ulnar notch and a small surface for the flexor muscles. (3) The arboreal M. fascicularis has similar features to those of M. fuscata for the first and second relative size index. However, in the ulnar notch, M. fascicularis has a peculiar character and the surface for the flexor muscles is relatively large compared to those of the other two species. These results can be interpreted in terms of positional habits and presumed functional demands. A form-functional study by Lemelin and Schmitt also corroborates the interpretations of the present study. Thus, the distal region of the forearm strongly reflects muscular development and joint resultant force, and is an important region for investigating locomotor adaptations in primates. The present study reveals the possibility of using this type of morphometric analysis for reconstructing the positional behavior of fossil primates.     

山西蟒河国家级自然保护区猕猴食源植物区系特征

于2012~2013年,以样带法、样方法和无样地法相结合,分4次对蟒河国家级自然保护区猕猴栖息地食源植物种类进行了实地调查,并分析了其区系特征。研究发现:(1)蟒河保护区猕猴栖息地内有维管植物659种,隶属102科374属,其中54科126属261种为猕猴的食源植物,占猕猴栖息地植物科、属、种总数的52.94%、33.69%和39.61%;蔷薇科是食源植物中包含种类最多的科,有16属39种,其次为豆科,含11属23种。(2)蟒河保护区内猕猴食源植物区系特征为:食源植物所在科有6个分布型和2个变型,所在属有13个分布型和6个变型;在属的分布类型中,温带性质分布类型的属占优势,有75个,占总属数的66.96%,其中北温带分布类型的属46个,占总属数的41.07%;热带性质分布类型的属有24个,地中海区、中亚、东亚和中国特有分布成分的属共有13个,分别占总属数的21.43%和11.61%,说明蟒河保护区内猕猴食源植物区系为暖温带性质。     

Ancient genome‐wide admixture extends beyond the current hybrid zone between Macaca fascicularis and M. mulatta

Macaca fascicularis and Macaca mulatta are two of the most commonly used laboratory macaques, yet their genetic differences at a genome‐wide level remain unclear. We analysed the multilocus DNA sequence data of 54 autosomal loci obtained from M. fascicularis samples from three different geographic origins and M. mulatta samples of Burmese origin. M. fascicularis shows high nucleotide diversity, four to five times higher than humans, and a strong geographic population structure between Indonesian‐Malaysian and Philippine macaques. The pattern of divergence and polymorphism between M. fascicularis and M. mulatta shows a footprint of genetic exchange not only within their current hybrid zone but also across a wider range for more than 1 million years. However, genetic admixture may not be a random event in the genome. Whereas randomly selected genic and intergenic regions have the same evolutionary dynamics between the species, some cytochrome oxidase P450 (CYP) genes (major chemical metabolizing genes and potential target genes for local adaptation) have a significantly larger species divergence than other genes. By surveying CYP3A5 gene sequences of more than a hundred macaques, we identified three nonsynonymous single nucleotide polymorphisms that were highly differentiated between the macaques. The mosaic pattern of species divergence in the genomes may be a consequence of genetic differentiation under ecological adaptation and may be a salient feature in the genomes of nascent species under parapatry.     

A comparison of the behavior of Macaca fascicularis and Macaca mulatta in relation to the menstrual cycle

Observations on oppositely sexed pairs of M. fascicularis and M. mulatta revealed certain differences. M. fascicularis showed single-mount copulations, higher potency, less grooming activity, and milder but more frequent aggressive exchanges than the rhesus monkey. These differences might be due to the lower dominance gradient between the sexes and less sexual dimorphism in M. fascicularis than in M. mulatta. There were changes in the sexual, grooming, and aggressive interaction in relation to the menstrual cycle, indicating the suitability of M. fascicularis for hormone-behavior studies. Comparison of data from 30 and 60 min tests showed that important behavioral changes did not become apparent unless animals were given enough time to interact.     

NRAMP1 polymorphism in a hybrid population between Japanese and Taiwanese macaques in Wakayama, Japan

A macaque population produced by the hybridization of native Japanese macaques (Macaca fuscata) and introduced Taiwanese macaques (M. cyclopis) in Wakayama Prefecture was shown to possess three DNA haplotypes of the natural resistance-associated macrophage protein 1 (NRAMP1). Based on genotyping and comparison with M. fuscata populations, it was revealed that the introduced M. cyclopis population was polymorphic for the NRAMP1 locus. Extensive crossbreeding of the introduced species with the native species was confirmed using this genetic marker and the proportion of M. cyclopis genes was 57.4%. Results of statistical tests suggested non-random mating in the hybrid population.     

The high genetic homology of threeMacaca fascicularis and twoMacaca mulatta subspecies on the basis of their highly repeated DNA restriction patterns

We have studied highly repeated DNA sequences of three subspecies ofM. fascicularis (M.f. philippinensis M.f. mordax, M.f. fusca) and of two subspecies ofM. mulatta (M.m. lasiotus, M.m. mulatta). Restriction patterns were obtained after digestion with 9 restriction endonucleases and evidenced after southern blotting and hybridization with Bam HI satellite DNA fragments fromM. fascicularis subspecies. M. fascicularis andM. mulatta subspecies studied, present morphological differences but indistinguishable karyotypes: highly repeated DNA analysis, resulting in the same restriction patterns for all the restriction sites studied with highly repeated DNA probes characteristic of the threeM. fascicularis subspecies, gave arguments in favour of the high genetic homology ofM.f. philippinensis, M.f. mordax, M.f. fusca on one side, andM.m. lasiotus andM.m. mulatta on the other, which can be distinguished only on the basis of morphological criteria.     

陕西米仓山国家级自然保护区猕猴的分布及种群数量调查

2013年8至12月,对陕西省米仓山国家级自然保护区境内野生猕猴的种群数量及其社会结构进行调查,并估测该物种栖息环境的偏好性。通过在预先选取的样区域内采用"V"型路线调查法调查,发现该区域生活12群,共有460—500只野生猕猴。结合对其中5个猴群长时间的持续跟踪观察,统计得出成年个体占45.93%,未成年个体占34.45%,幼仔占19.61%,成年与未成年比例为1.33,成年雄雌的比例为0.36。并证实猕猴倾向于选择海拔700—1600m裸露的悬崖峭壁、平缓山坡农田带上缘、灌丛-森林带和半山中部及以上区域的阔叶林带下缘活动。     

Heart rate patterns under stress in three species of macaques

Cardiac responses during one hour exposures to three stressful experimental conditions were compared among juvenile females of three species of the genus Macaca (M. mulatta, M. radiata, and M. fascicularis). M. fascicularis showed the highest overall heart rate, and M. mulatta the lowest, in all three conditions. The principal difference between species was in the pattern of change in heart rate over the test sessions. Heart rate declined during the hour for all three species in the first two conditions (home cage novel environment), and the change was most rapid in M. mulatta and slowest in M. fascicularis. In the third and most stressful condition (physical restraint), each species showed a distinct temporal pattern. Heart rate increased over the hour in M. fascicularis, declined in M. radiata, and increased rapidly then declined gradually in M. mulatta. Individual differences in heart rate tended to be consistent within and across conditions. Correlations between behavioral measures of somatic activity and heart rate were generally modest. The results are in accord with other behavioral and physiological differences obtained for the same subjects, and suggest that responses to environmental stimuli reflect fundamental aspects of temperament that may vary substantially even among closely related species. © 1994 Wiley-Liss, Inc.     

Structure and composition of the oral mucous membrane on the lips and cheeks of the monkey,Macaca fascicularis

Summary In seven monkeys (6 Macaca fascicularis, 1 M. mulatta; 2.4±0.6 kg in weight) the labial and buccal mucosae were studied morphologically and quantitatively. Following fixation by perfusion, the upper and lower lips and entire cheeks were dissected free and processed for light-, scanning and transmission electron microscopy. Established programs (HISTOMEP, MUMANA II) and appropriate morphometric techniques were used to estimate, at the light-microscopic level, the epithelial thickness, the width of the combined lamina propria/submucosa, and the volumetric composition of the gland-containing portions of lip and cheek mucosae. The cheek epithelium was more than twofold thicker than the lip epithelium, on the average 0.46±0.04 and 0.21±0.02 mm, respectively, with no differences related to sex or topographical sites. The combined lamina propria/submuscosa was 1.32 ±0.19 and 1.50±0.26 mm in width in cheeks and lips, respectively. The main mucosal constituents at both sites were glandular and connective tissue, and lymph follicles associated with secretory ducts. In lips, the volume of plasma cells around gland acini correlated positively with the amount of lymphoid tissue present around topographically related ducts. It is suggested that the duct/ lymph follicle assembly may serve as a local antigen-recognition system.

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Zusammenfassung Die Lippen- und Wangenmukosa wurde an 7 Affen (6 M. fascicularis, 1 M. mulatta; 2,4±0,6 kg schwer) morphologisch und quantitativ untersucht. Nach einer Perfusionsfixation wurden Ober- und Unterlippen sowie ganze Wangen herauspräpariert und für Untersuchungen im Licht-, Raster und Transmissionselektronenmikroskop vorbereitet. Bestehende Programme (HISTOMEP, MUMANA II) und morphometrische Standardmethoden wurden verwendet, um lichtmikroskopisch die Epitheldicke, die Breite der kombinierten Lamina propria/Submukosa und die volumetrische Zusammensetzung der drüsenhaltigen Abschnitte der Lippen- und Wangenschleimhaut zu ermitteln. Das Wangenepithel war mehr als zweifach dicker als das Lippenepithel (0,46±0,04 und 0,21±0,02mm); die Epitheldicke war unabhängig von Geschlecht und Topographie. Die kombinierte Lamina propria/ Submukosa war im Wangenbereich 1,32±0,19, im Lippenbereich 1,50± 0,26 mm breit. Die Hauptelemente der Lippen- und Wangenschleimhaut sind Drüsen- und Bindegewebe sowie mit Ausführungsgängen assoziierte Lymphfollikel. In der Lippen-, nicht aber in der Wangenschleimhaut, ist das Volumen der die Drüsenacini umlagernden Plasmazellen positiv korreliert mit der Menge der Lymphfollikel an den benachbarten Ausführungsgängen. Es wird vermutet, daß das Ausführungsgang/Lymphfollikel-System zur lokalen Erkennung von Antigenen dienen könnte.

     

Macaque Masseter Muscle: Internal Architecture,Fiber Length and Cross-Sectional Area

Models of mastication require knowledge of fiber lengths and physiological cross-sectional area (PCS): a proxy for muscle force. Yet only a small number of macaques of various species, ages, and sexes inform the previous standards for masseter muscle architecture. I dissected 36 masseters from 30 adult females of 3 macaque species—Macaca fascicularis, M. mulatta, M. nemestrina—using gross and chemical techniques and calculated PCS. These macaques have mechanically similar dietary niches and exhibit no significant difference in masseter architecture or fiber length. Intramuscular tendons effectively compartmentalize macaque masseters from medial to lateral. Fiber lengths vary by muscle subsection but are relatively conservative among species. Fiber length does not scale with body size (mass) or masseter muscle mass. However, PCS scales isometrically with body size; larger animals have greater force production capabilities. PCS scales positively allometrically with facial size; animals with more prognathic faces and taller mandibular corpora have greater PCS, and hence force, values. This positive allometry counters the less efficient positioning of masseter muscles in longer-faced animals. In each case, differences in PCS among species result from differences in muscle mass not fiber length. Masseter PCS is only weakly correlated with bone proxies previously used to estimate muscle force. Thus predictions of muscle force from bone parameters will entail large margins of errors and should be used with caution.     

Differentiall behavioral and adrenocortical responses to stress among three macaque species

Behavioral and adrenocortical responses of rhesus (Macaca mulatta), bonnet (M. radiata), and crabeating (M. fascicularis) macaques were compared in their home cages, during exposure to novelty and during physical restraint. Both behavioral and adrenocortical responses differentiated species in each condition. In all conditions, post-test corticosteroid levels were highest for crabeaters and lowest for rhesus. Rhesus were the most active behaviorally, and bonnets were the most passive, while crabeaters exhibited the greatest signs of behavioral disturbance. Relationships between adrenocortical and behavioral responses varied between groups. Both adrenocortical and behavioral profiles were in accord with the behavior of these three species under more natural conditions. The role of psychophysiological responses in general behavioral dispositions toward the environment is discussed. It is concluded that behavioral dispositions, inclusive of psychophysiological responses, may vary qualitatively even among closely related primate species.     

<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.