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.     

Y-Chromosome and Mitochondrial Markers in Macaca fascicularis Indicate Introgression with Indochinese M. mulatta and a Biogeographic Barrier in the Isthmus of Kra

This is the first report of Y-chromosome introgression between primate species. We sequenced 3.1 Kb of Y-chromosome DNA and 1.5 Kb of mtDNA for 27 macaques of Fooden's (Folia Primatol. [1976] 25: 225–236) fascicularis species group and 5 outgroup taxa (Macaca sylvanus, Papio hamadryas, Theropithecus gelada, Allenopithecus nigroviridis, and Cercopithecus mona). Phylogenies constructed separately for the paternal and maternal data sets show a Y-chromosome paraphyly among lineages of Macacafascicularis, but a mitochondrial monophyly for the same individuals. The Y-chromosome topology depicts Indochinese Macaca fascicularis haplotypes joining with those of M. mulatta, followed by M. cyclopis and M. fuscata, before clustering with a clade of lineages of M. fascicularis from peninsular Malaysia, Indonesia, and the Philippines. These contrasting patterns of mitochondrial and Y-chromosome DNA, evaluated in the context of the evolutionary consequences of macaque sex-biased dispersal, present strong evidence for contemporary hybridization between Macaca fascicularis and M. mulatta in Indochina and a biogeographic barrier in the Isthmus of Kra.     

Male external genitalia and systematic relationships of the Japanese macaque (Macaca fuscata Blyth, 1875)

Penial morphology was studied in six preserved specimens of the Japanese macaque,Macaca fuscata. Structure of the glans penis and baculum inM. fuscata is essentially similar to that in the rhesus macaque,M. mulatta. With age the skin of the penis inM. fuscata apparently becomes progressively more darkly and extensively pigmented, and the baculum becomes progressively longer. One immature specimen examined, with penial skin unpigmented and baculum cartilaginous, appears to be abnormally retarded in penial development. Penial morphology suggests that the allopatric speciesM. fuscata, M. mulatta, M. cyclopis, andM. fascicularis constitute a closely interrelated group. Contrary to a previous report, there is no evidence that penial morphology inM. fuscata is transitional to that inM. radiata andM. sinica. InM. fuscata, M. mulatta, andM. fascicularis, latitudinal variation of body size and relative tail length conforms toBergmann's rule andAllen's rule; external proportions in three specimens ofM. cyclopis only partly conform to this pattern.     

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.     

Morphological and Body Color Variation in Thai <Emphasis Type="Italic">Macaca fascicularis fascicularis</Emphasis> North and South of the Isthmus of Kra

Long-tailed macaques (Macaca fascicularis fascicularis) are widely distributed in Southeast Asia and are morphologically and genetically (Tosi et al. in International Journal of Primatology 23:161–178, 2002) distinguishable on either side of the Isthmus of Kra (ca. 10.5°N). We compared the somatometry and body color of 15 local populations of long-tailed macaques in Thailand distributed over areas from 6.5°N to 16.3°N and also a Thai rhesus macaque population at 17.2°N. Limb proportions and body color variation follow the geographical trend. However, contrary to a previous report, body size does not decrease with latitude in the northern group and also in the southern (southerly distributed) rhesus macaque. Relative tail length (RTL) and color contrast in yellow between the back and thigh are the sole traits that distinctively separate the 2 groups: the southern group has a long relative tail length (RTL >125%) and small color contrast, whereas the northern group has a short RTL (<120%) and large color contrast. The southern rhesus macaques appear to have somatometric and body color traits that follow the geographical trend in long-tailed macaques, though they maintain their distinctive species-specific traits of shorter RTL (ca. 55%), shorter relative facial length, and a bipartite body color pattern. Researchers assume that the northern group of long-tailed macaques and the southern rhesus macaques had undergone partial introgression with each other. Montane refugia present during the glacial period are localities in which introgression occurred in long-tailed macaques.     

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.     

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.     

Further report on object manipulation in non-human primates: A comparison within 13 species of the genusMacaca

Thirteen captive species of the genusMacaca were presented with certain non-edible objects and the subsequent manipulation was observed. The following results were obtained: (1) Thefascicularis group species displayed a great variety in rolling the manipulandum, which has been reported to be one of the actions characterizing cercopithecine species; (2) manipulating the object with one finger was typical of thesilenus-sylvanus andsinica groups, whereas use of the fingers moving opposably was common to all species ofMacaca; (3) secondary manipulations in relation to the wire-mesh were observed only inM. silenus, M. sinica, andM. nemestrina, whereas those in relation to water were common to allMacaca species; and (4) within-subgroup differences were great in thesilenus-sylvanus andsinica groups as compared to thefascicularis group.     

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.     

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。     

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.     

Variation within and among the chloroplast genomes ofMelaleuca alternifolia andM. linariifolia (Myrtaceae)

Melaleuca alternifolia andM. linariifolia are commercially important Australian species harvested for their essential oils. Both species have relatively narrow and disjunct distributions on the central coast of eastern Australia. Variation in the chloroplast genome was assessed for eight individuals from each of twelve populations, representing the species' geographic range. Low nucleotide diversity withinM. alternifolia contrasted with high nucleotide diversity inM. linariifolia. CpDNA data are consistent with the southern population ofM. alternifolia being a hybrid population withM. linariifolia. The two species are sympatric in this region. Variation inM. linariifolia was geographically structured, with northern populations differing from southern populations by seven restriction site mutations, five length mutations and an inversion. There was no evidence of hybridisation of the cp genome of northernM. linariifolia with the partially sympatric speciesM. trichostachya. Intra- and interspecific variation in the chloroplast genomes ofM. alternifolia, M. linariifolia, andM. trichostachya indicate considerable potential for the use of intraspecific cpDNA studies in examining phylogenetic relationships in melaleucas.     

Ecological wood anatomy of NepaleseRhododendron (Ericaceae). 2. Intraspecific variation

The intraspecific relationship of selected wood anatomical characters with stem diameter, plant height, and altitude was investigated in four NepaleseRhododendron species:R. anthopogon, R. lepidotum, R. campanulatum, andR. arboreum, i.e., two shrubs, one subtree, and one tree. We studied 23 to 27 specimens for each species.R. anthopogon grew from 3,380 to 4,950 m,R. lepidotum from 2,060 to 4,720 m,R. campanulatum from 2,790 to 4,140 m, andR. arboreum from 1,430 to 3,460 m. Multiple regression analysis and actual distribution of character values show that the wood anatomical characters having a significant correlation with non-anatomical factors differ between species. The number of significant characters are two inR. anthopogon andR. campanulatum, five inR. lepidotum, and nine inR. arboreum and tends to be small in species having smaller altitudinal ranges. Average pore area, most strongly correlated with non-anatomical factors in interspecific variation, is significantly correlated only inR. lepidotum andR. arboreum. The general trends in intraspecific variation among four NepaleseRhododendron species differ from the trends found in interspecific variation within the genus and are characteristic of each species.     

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.     

Allozymic variation in four Indian species of genusMus: A comparative analysis

The present study focusses on allozyme variation in the commensal house mouseMus musculus, the pygmy field miceM. booduga andM. terricolor, and the spiny mouseM. platythrix. Genetic heterozygosity was estimated using a set of 24 polymorphic biochemical genetic markers. The extent of variability present inM. booduga, M. terricolor andM. platythrix has been compared with that in theM. musculus complex. Levels of allozyme variation at species level indicate thatM. musculus has the maximum heterogeneity, followed byM. booduga andM. terricolor, whileM. platythrix shows comparatively homogeneous genetic make-up. Gene frequency data have been used to trace phylogenetic relationships among these four 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.     

Embryology of JapaneseMitella (Saxifragaceae) and its taxonomic significance

The embryo sac formation, endosperm formation, and embryo development in all species of JapaneseMitella andM. diphylla of North America were studied. Monosporic 8-nucleate embryo sac formation of thePolygonum type was found in all the species. In endosperm formation, the Cellular type was found in all species of sect.Mitellaria, and the Helobial type inM. nuda, M. diphylla, andM. integripetala. The Helobial type inM. integripetala was somewhat aberrant and approximated to the Cellular type. In embryo development, three types were distinguishable in sect.Mitellaria: Type A (most of the species), Type B (M. acerina) and Type C (M. pauciflora andM. furusei var.furusei). Type B is an intermediate type between A and C.Mitella integripetala also shows Type A, and the types ofM. nuda andM. diphylla are similar to Type A, except for the shape of suspensor. From outgroup comparison, Type A is suggested to be primitive and Type C to be most derivative in sect.Mitellaria. The affinity of some species in sect.Mitellaria is discussed from the embryogenic data obtained.     

Allozyme variation in relation to morphology and taxonomy inMedicago sect.Spirocarpos subsect.Intertextae (Fabaceae)

Medicago intertexta andM. ciliaris have been controversially recognized as separate species. The only reliable diagnostic character, gland-tipped trichomes on the fruits inM. ciliaris, is controlled by presence of a single dominant allele, and such one-character taxonomies are debatable. Contributing to the difficulty,M. muricoleptis andM. granadensis, the other two species ofMedicago sectionSpirocarpos subsectionIntertextae, are sometimes confusingly similar toM. intertexta or to each other. Allozyme differences provided 95% verification of the suitability of the gland-tipped trichome character for separatingM. intertexta andM. ciliaris, thus corroborating their recognition as separate taxa. Several measures of allozyme variation indicated thatM. intertexta is more polymorphic than its sister species. Heterozygosity was also highest inM. intertexta, suggestive of a higher outcrossing rate, which is also consistent with larger floral size. Heterozygosity ofM. intertexta was concentrated in Sicily and nearby countries. Taxonomic difficulties in identifying SicilianM. intertexta are well known, and may be the result of interspecific hybridization and introgression.Medicago muricoleptis differed from the above two species in the frequency of several alleles, whileM. granadensis possessed numerous unique alleles consistent with its complete absence of genetic exchange with the other three substantially interfertile species.     

DNA evidence for multiple origins of intergeneric allopolyploids in annualMicroseris (Asteraceae)

Seventy populations of North American annualMicroseris, Stebbinsoseris, andUropappus species were examined for chloroplast and nuclear ribosomal DNA restriction site variability to determine the origin of the allotetraploid speciesS. heterocarpa andS. decipiens. Previously identified chloroplast DNA restriction site variants were used in concert with restriction site variation forNco I in the nuclear-encoded ribosomal DNA repeat. The presence of two, mutually exclusive restriction site gains were observed in diploid populations ofM. douglasii; these same variants were also found in populations of allotetraploidS. heterocarpa, indicating mutiple origins of this species from different maternal diploid populations ofM. douglasii. Variation in the rDNA repeat between the diploid annual species and the putative paternal genome ofU. lindleyi was found to be additive inS. heterocarpa. A similar relationship was observed for the origin ofS. decipiens; cpDNA restriction site variants found inM. bigelovii andM. douglasii were present inS. decipiens. The rDNANco I variants also were additive in this purported allotetraploid. These results confirm the reticulate evolutionary pattern inStebbinsoseris and provide another example of multiple origins of intergeneric allopolyploids.     

Hemoglobin polymorphism in macaques with reference to the evolution ofMacaca fascicularis andMacaca mulatta

Blood samples were collected fromMacaca fascicularis andMacaca mulatta living in indoor breeding groups and investigated electrophoretically. Hemoglobin polymorphism was observed in both species. Isoelectric focusing was performed on urea denaturated samples to test the hypothesis of a site duplication at theα-chain locus inM. fascicularis (Barnicot et al., 1970). The results of our investigations do not support the above mentioned hypothesis. Only one locus coding theα-chain was detected, and this is under the control of two alleles. Evolutionary events at the molecular level are discussed, as well asWheatley's hypothesis (1980) that malaria was an important force behind divergence in both species. InM. fascicularis hemoglobin variants might be similarily connected with malaria resistance as in man. We suggest that this was not an important process behind speciation in macaques.