Hybridization and population genetics of two macaque species in Sulawesi, Indonesia.

This study investigates hybridization and population genetics of two species of macaque monkey in Sulawesi, Indonesia, using molecular markers from mitochondrial, autosomal, and Y-chromosome DNA. Hybridization is the interbreeding of individuals from different parental taxa that are distinguishable by one or more heritable characteristics. Because hybridization can affect population structure of the parental taxa, it is an important consideration for conservation management. On the Indonesian island of Sulawesi an explosive diversification of macaques has occurred; seven of 19 species in the genus Macaca live on this island. The contact zone of the subjects of this study, M. maura and M. tonkeana, is located at the base of the southwestern peninsula of Sulawesi. Land conversion in Sulawesi is occurring at an alarming pace; currently two species of Sulawesi macaque, one of which is M. maura, are classified as endangered species. Results of this study indicate that hybridization among M. maura and M. tonkeana has led to different distributions of molecular variation in mitochondrial DNA and nuclear DNA in the contact zone; mitochondrial DNA shows a sharp transition from M. maura to M. tonkeana haplotypes, but nuclear DNA from the parental taxa is homogenized in a narrow hybrid zone. Similarly, within M. maura divergent mitochondrial DNA haplotypes are geographically structured but population subdivision in the nuclear genome is low or absent. In M. tonkeana, mitochondrial DNA haplotypes are geographically structured and a high level of nuclear DNA population subdivision is present in this species. These results are largely consistent with a macaque behavioral paradigm of female philopatry and obligate male dispersal, suggest that introgression between M. maura and M. tonkeana is restricted to the hybrid zone, and delineate one conservation management unit in M. maura and at least two in M. tonkeana.

The effects of feeding an Asian or Western diet on sperm numbers, sperm quality and serum hormone levels in cynomolgus monkeys (Macaca fascicularis) injected with testosterone enanthate (TE) plus depot medroxyprogesterone acetate (DMPA).

The aim of this study was to elucidate the effects of an Asian diet compared to a Western diet on sperm numbers and quality, and serum hormones in cynomolgus monkeys (Macaca fascicularis) injected with testosterone enanthate (TE) plus depot medroxyprogesterone acetate (DMPA). Thirty male monkeys were divided into three groups of ten animals each. The first group (control) was fed with standard diet 'monkey chow' (9% fat, 13% protein, 78% carbohydrate); the second group was fed an 'asian' diet (15% fat, 15% protein, 70% carbohydrate); the third group was fed a 'Western' diet (35% fat, 25% protein, 40% carbohydrate). These diets were administered from the beginning (adaptation) until the experiment was terminated. Three months after the adaptation period, all groups were injected with 20 mg TE (once per week) and 25 mg DMPA (once every 6 weeks) for 18 weeks, while TE injections were continued for another 6 weeks. There were no differences in sperm numbers and quality, or in hormone levels between the first and second groups. In both of these groups azoospermia was achieved in 100% of animals, while in the third group only 70% achieved azoospermia. In all 3 groups, spermatozoa were once again detectable by week 33. However, by the end of the study at week 39, sperm numbers in the first and second groups reached only severe oligozoospermia (two animals remained azoospermic in the first group) while in the third group, numbers had returned to normozoospermia. The quality of spermatozoa during and after the treatment in the third group was better than in the first and second groups. Hormone concentrations decreased more rapidly in both the first and second groups, compared to the third group, while the recovery period was slower in the first and second groups, compared to the third group. It is concluded that different formula diets result in differential decreases in sperm numbers and quality, and in hormone concentrations in M. fascicularis injected with TE in combination with DMPA. Animals fed with either monkey chow or an Asian diet exhibited more severe and prolonged decreases in these parameters than did animals fed with a Western diet.

Islet cell antibodies in Sulawesi macaques.

Older monkeys of the Sulawesian species Macaca nigra spontaneously develop a lesion in the pancreatic islets of Langerhans in which there is deposition of amyloid and gradual degeneration of all cells, which can lead eventually to development of diabetes mellitus. Islet cell antibodies (ICA), formed in response to the release of cellular antigens, can be used to detect the islet lesion and to monitor the progression of each monkey toward diabetes. Numerous M. nigra and one M. tonkeana in captivity have been tested, but it is unknown whether the islet lesion occurs in monkeys in their natural habitat of Sulawesi. Blood samples collected from M. maurus, M. tonkeana, and hybrid M. maurus/tonkeana were assayed for ICA. When all monkeys were considered together, 33% had ICA positive against beta cells and 14% had ICA positive against alpha and/or D cells. Appearance of ICA in blood of males was virtually the same as in females. These results are similar to those found in M. nigra examined in captivity. Since all Sulawesian species share a common genetic heritage, these results would support the appearance of this lesion in their natural habitat. Cause(s) for formation of the lesion and eventual development of diabetes are unknown. There may be genetic factors or genetic predisposition to environmental factors. If environmental factors are responsible, then they must be present not only in the wild, but either carried with the monkeys or universally available, since M. nigra born in captivity also develop the lesion and diabetes after physical maturity at ca. 7+ years.

Population densities of Sulawesi crested black macaques (Macaca nigra) on Bacan and Sulawesi, Indonesia: effects of habitat disturbance and hunting.

Population surveys of Sulawesi crested black macaques (Macaca nigra) were conducted on the Indonesian islands of Sulawesi and Bacan in 1992-1994 to assess the status of natural populations and determine habitat and anthropogenic factors affecting their population densities. We surveyed five sites for primates, including undisturbed and disturbed habitats. Data were collected on habitat structure and composition at two undisturbed and one disturbed forest site in which the primates were surveyed. The highest density of macaques was found in primary forest at Gunung Sibela Nature Reserve on Bacan (170.3 individuals/km2). Population density in logged forest on Bacan was high but significantly less than primary forest (133.4 individuals/km2). The high density of crested black macaques in primary forest on Bacan is best explained by the high carrying capacity found in primary forest. The lower food quantity and quality of food resources found in logged forest correlated with lower primate densities compared to primary forest. However, the large population of macaques in logged forest demonstrates the conservation value of such forest. Densities on Sulawesi at Tangkoko-Batuangas-DuaSudara Nature Reserve (TBDS) showed a continuing decline since earlier surveys. Primate densities were highest near the protected center of Tangkoko Reserve (66.7 individuals/km2). The peripheral areas of Batuangas and DuaSudara, even though adjacent and continuous, showed lower population densities of 46.4 and 23.5 individuals/km2, respectively. The best explanation for the continued decline of Macaca nigra populations at TBDS is hunting. Unless conservation measures are implemented immediately, M. nigra on Sulawesi risks extinction in the near future.

Phylogeographic analysis of pigtail macaque populations (Macaca nemestrina) inferred from mitochondrial DNA.

Mitochondrial DNA variation was surveyed in nine populations of the pigtail macaque (Macaca nemestrina), covering all three recognized subspecies in Southeast Asia. To do this, a 2,300 base pair fragment spanning the mitochondrial NAD 3 and NAD 4 genes and flanking tRNA subunits leucine and glycine was targeted for amplification and digested with a battery of 16 restriction endonucleases. Out of a total of 107 individuals, 32 unique haplotypes could be distinguished. Parsimony and neighbor-joining analyses grouped the haplotypes into five strongly supported assemblages representing China/Thailand, Malaysia, Sumatra, Borneo, and Siberut. These results indicate that the mainland and island mtDNA haplotypes are strictly and uniquely limited to the geographic ranges of the recognized morphological subspecies. Cladistic and neighbor-joining analyses indicate that inferred phylogenies of mtDNA haplotypes are congruent with subspecies designations. Furthermore, in support of morphological studies, results indicate that the Mentawai macaque is most likely not a distinct species but a subspecies of M. nemestrina.

Confirmation and location of the hybrid zone between wild populations of Macaca tonkeana and Macaca hecki in central Sulawesi, Indonesia.

Reports of hybridization between Macaca tonkeana and Macaca hecki were investigated in Central Sulawesi, Indonesia. We defined sets of morphological traits that were diagnostic for M. tonkeana and M. hecki and then located an areas where animals had intermediate or mosaic features. Hybridization as indicated by morphology was detected between M. tonkeana and M. hecki. The hybrid zone appeared to be strongly centered at the road that crosses the isthmus of Central Sulawesi from Tawaeli to Toboli. Macaques in this region were not morphologically uniform; animals from the western area of the Tawaeli-Toboli road resembled M. hecki, while animals from the eastern area resembled M. tonkeana. The hybrid zone was found to be smaller than previously thought, with maximum dimensions of approximately 15 and 7.5 km. Clines for diagnostic morphological features were broadly coincident, suggesting that the hybrid zone originated by secondary contact. Analysis of three museum specimens collected in 1916 provided evidence that the hybrid zone has been in existence since at least then. The narrow width of the hybrid zone, along with its age, suggested that some prezygotic or postzygotic barrier must exist to full introgression between M. tonkeana and M. hecki.

Morphometric analyses of Ateles: systematic and biogeographic implications.

This study examined the cranial and dental morphometric patterns among South American spider monkey taxa (Ateles), using various multivariate data reduction techniques to corroborate or falsify the predictions of alternative vicariance or parapatric models for explaining neotropical biodiversity. Data from 284 specimens were standardized to eliminate sex differences and then transformed by factor analysis to obviate the effects of body size on shape relationships. We found the independent discriminant analyses of dental and cranial data to be not at all dissimilar, nor did body size appear to distort geographical relationships. Thus a pooled data set of 50 measurements was further reduced by cluster analysis to produce a dendrogram of taxonomic relationships that is discordant with current classification. Three independent taxa are indicated, with the Guianan samples being most distinct, followed by the animals of northwest Venezuela and adjacent Colombia. Elsewhere, the samples describe a cline of relationships around Amazonia that resembles a ring species. Of particular interest is the apparent clinal intergradation across major tributaries of the Amazon, which is inconsistent with the concept of these rivers as barriers in their present form. Instead these observations, and the congruence between the multivariate clusters and previously identified centers of endemism, support both tierra firme and forest refugia models of historical biogeography. However, the latter model is somewhat falsified within Amazonia by character stability for alternative pelage patterns on opposite sides of the same major rivers that showed morphometric intergradation, but not as predicted within the refugia. This parapatric enhancement of pelage differences, which originated presumably in allopatry, suggests a mechanism of incipient speciation by frequency-dependent assortative mating with no apparent hybrid disadvantage or disruption of widespread gene flow.

Population survey of macaques in northern Sulawesi.

A field survey of 25 sites in Sulawesi Utara (north Sulawesi) in 1987 and 1988 found macaques in 16 of these sites. The most viable population of Macaca nigra was found in the Tangkoko reserve at an estimated density of 76.2 monkeys/km2, which is less than one-third the abundance reported in the late 1970s by the MacKinnons. The adjacent reserves of Batuangus and Duasudara had only 22 monkeys/km2, yielding a population estimate for these three contiguous reserves of only 3,655 individuals. Maccaca nigrescens were found in the central and western portions of Dumoga-Bone National Park in densities of 15.5 and 16.4 monkeys/km2, significantly below the density of 27/km2 reported by the MacKinnons. The more peripheral areas of Dumoga-Bone had only 8.15 monkeys/km2, yielding a population estimate of M. nigrescens in Dumoga-Bone of less than 34,000. Our total population estimate for M. nigra and M. nigrescens combined is less than 50,000 individuals, which is considerably below that reported in recent litreture. M. hecki were observed in only two locations, Tangale and Panua Reserves, at low densities of 3.3 to 5.2 monkeys/km2, suggesting its range and abundance have declined since the observations of Groves (pp. 84-124 in THE MACAQUES: STUDIES IN ECOLOGY, BEHAVIOR AND EVOLUTION. D. G. Lindburg, ed. New York, Van Nostrand Reinhold, 1980). Several factors have contributed to population decline in these species: habitat shrinkage, increasing human population pressure, and drought conditions. Group sizes were significantly smaller in our study than in previous ones, and we found a shortage of juveniles and infants.