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. Am. J. Primatol. 43:181–209, 1997. © 1997 Wiley-Liss, Inc.     

Evidence of gene flow between Sulawesi macaques

A pilot field study was conducted in Sulawesi (Indonesia) to assess the status of macaque populations on the island. Wild and captive animals were sampled, mainly in border areas between presumed different species. The five species investigated were Macaca maurus, M. tonkeana, M. hecki, M. nigrescens, and M. nigra, for which morphological and gene frequency data suggested the presence of hybridization zones. Some individuals within these zones showed intermediate or mosaic morphology between parental forms. These individuals also had intermediate gene frequencies for most of the polymorphic systems investigated. Karyotypes were identical in all species, and no cytogenetic barrier to hybridization existed between species. A review of the recent literature also provided evidence for hybridization between Sulawesi macaques. Clinical frequencies in both morphological and biomolecular traits perhaps can be best explained by the operation of gene flow between the various forms of macaques on the island. However, additional data are necessary before current classification schemes are revised. The unique opportunity and need of further study of Sulawesi macaques for a range of evolutionary questions is emphasized.     

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.     

Prevalence of enteric parasites in pet macaques in Sulawesi, Indonesia

On the Indonesian island of Sulawesi, nonhuman primate pets come into frequent contact with humans, presenting the possibility of zoonotic and anthropozoonotic disease transmission. We collected fecal samples from 88 pet macaques representing six of the seven macaque species currently recognized as endemic to Sulawesi (Macaca nigra, M. nigrescens, M. hecki, M. tonkeana, M. maura, and M. ochreata) as well as two non-endemic species (M. fascicularis and M. nemestrina) in order to determine the prevalence of intestinal parasitic infection in this population. Seven taxa of intestinal protozoa (Blastocystis hominis, Iodamoeba bütschlii, Entamoeba coli, Entamoeba hartmanni, Chilomastrix mesnili, Endolimax nana, and Retortamonas intestinalis) and three taxa of nematodes (hookworm, Trichuris spp., and Ascaris spp.) were detected. The overall parasitization rate was 59.1%. Commensal organisms predominated in this population. Parasitization was not statistically correlated with macaque age group, sex, species, or location, or with the owner's level of education. These findings are discussed in the context of primate pet ownership practices in Sulawesi.     

Cytogenetic study of Macaca tonkeana

A cytogenetic study of Macaca tonkeana shows that this species has a karyotype identical with that of Macaca fascicularis although there are sufficient morphological and ecoethological differences for the taxidermists to place these animals into two different species.     

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.     

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.     

短尾猴（Macaca arctoides）和猕猴跟骨的功能形态研究

本文从形态描述和统计入手,对短尾猴(macaca arctoides)和猕猴的跟骨进行了比较研究。结果表明,所研究的跟骨变量无论数值大小还是几何图形结构都存在一定差异。特别是跟骨最大宽、跟长、后距骨连结面长、跟骨高度及相对跟长存在显著性差异水平。猕猴跟骨变量间的相关关系比短尾猴的表现得更为紧密。据其形态与功能的关系,我们认为:与猕猴相较,短尾猴更适应于地栖生活。这似乎与短尾猴具更大的体重有关。     

Hematological values and parasite fauna in free-rangingMacaca hecki and theM. hecki/M. tonkeana hybrid group of Sulawesi Island, Indonesia

Hematological values and parasitological fauna of free-rangingMacaca hecki and the hybrid group betweenM. hecki/M. tonkeana of Sulawesi Island, Indonesia, were investigated. The hematological values, especially the red cell number (RBC), were lower than those of other macaque species, indicating that Sulawesi macaques are slightly anemic. Several parasites including Plasmodium sp., trombiculid mites, andTrichuris trichiura were identified. Although infection by Plasmodium was observed with considerable frequency, no clear relationship between its infection and the occurrence of anemia was found. Trombiculid mites and eggs ofAnatrichosoma sp. were detected in foci of the ears of most monkeys. The infection with a trombiculid mite is the first recorded occurrence in free-ranging wild Sulawesi macaques. Gastrointestinal parasites were identified from their eggs in fecal samples, where five species of nematoda and one trematoda species were found.     

The Human–Macaque Interface: Conservation Implications of Current and Future Overlap and Conflict in Lore Lindu National Park, Sulawesi, Indonesia

Here, I examine overlapping resource use of forest and cultivated resources by villagers and tonkean macaques (Macaca tonkeana) in Lore Lindu National Park, Sulawesi, Indonesia. An integrative research design was employed, using methods from primatology and cultural anthropology, in conjunction with quantitative measurements of cacao crop loss. The results indicate that the current patterns of overlapping resource use may not be severely affecting the tonkean macaques or villagers in Lindu. The research does, however, point to possible future difficulty if cacao crop raiding by macaques increases, and as changing socioeconomic trends and loss of traditional folklore result in further modification of macaque habitat. Successful strategies to ameliorate human–macaque conflict may require efforts aimed at the adoption of alternative buffer zone crops that use shade-management systems, the deliberate protection of important macaque food species, and increasing local tolerance to crop raiding by exploring the role of macaques in forest regeneration.     

食蟹猴和熊猴杂种F1的细胞遗传学研究

本工作采用染色体显带、睾丸组织学切片以及低渗铺张－硝酸银染色等方法较为详细地研究了食蟹猴和（Ｍ．ｆａｓｃｉｃｕｌａｒｉｓ）和熊猴（Ｍ．ａｓｓａｍｅｎｓｉｓ）种间杂种Ｆ１体细胞染色体的Ｇ带、Ｃ带、Ａｇ－ＮＯＲ、精母细胞联合复合体的结构、形态和行为以及精子发生。结果表明：（１）杂种亲本的染色体组具有高度的同源性;（２）杂种的精子发生过程完全正常;（３）食蟹猴和熊猴的种间生植屏障可能主要是生态隔离。此外     

The effects of hybridization on growth allometry and craniofacial form in Sulawesi macaques

The present research investigates the effects of hybridization between Macaca maurus and M. tonkeana on adult male form and patterns of growth allometry. Comparisons of adult hybrid mean phenotypic values with the adult averages of the parental species indicate a condition of heterosis for cranial vault length and crown-rump length. Negative heterosis is indicated for body mass. Regression parameters describing growth allometry are generated for four craniofacial measurement variables and one body measurement using both least squares and reduced major axis regression. Comparisons of hybrid and parental regression slopes and intercepts using analysis of covariance and t-tests suggest that there is a hybrid pattern of growth allometry characterized by an increase in regression slope values coupled with lower intercept values compared to those of the parental species and the parental averages for most regression parameters. Multivariate analyses of the adult and ontogenetic morphometric data indicate significant differences across species taxa in form and shape during development and adulthood. Our finding of significant differences between hybrids and their parental taxa in growth allometry and craniofacial form and shape during development challenges the assumption often made regarding the reproductive and taxonomic significance of observed ontogenetic divergence between Neandertals and modern humans. We propose that anthropological primatology, with its goal of developing nonhuman primate models for investigating human evolution, can provide a biologically relevant means by which to empirically estimate the taxonomic significance of morphological and ontogenetic divergence observed in the hominid fossil record.     

GENOMIC AND MORPHOLOGICAL ANALYSIS OF A SEMIPERMEABLE AVIAN HYBRID ZONE SUGGESTS ASYMMETRICAL INTROGRESSION OF A SEXUAL SIGNAL

Hybrid zones are geographic regions where differentiated taxa meet and potentially exchange genes. Increasingly, genomic analyses have demonstrated that many hybrid zones are semipermeable boundaries across which introgression is highly variable. In some cases, certain alleles penetrate across the hybrid zone in only one direction, recombining into the alternate genome. We investigated this phenomenon using genomic (genotyping‐by‐sequencing) and morphological (plumage reflectance spectrophotometry) analyses of the hybrid zone between two subspecies of the red‐backed fairy‐wren (Malurus melanocephalus) that differ conspicuously in a sexual signal, male back plumage color. Geographic cline analyses revealed a highly variable pattern of differential introgression, with many narrow coincident clines combined with several significantly wider clines, suggesting that the hybrid zone is a semipermeable tension zone. The plumage cline was shifted significantly into the genomic background of the orange subspecies, consistent with sexual selection driving asymmetrical introgression of red plumage alleles across the hybrid zone. This interpretation is supported by previous experimental work demonstrating an extra‐pair mating advantage for red males, but the role of genetic dominance in driving this pattern remains unclear. This study highlights the potential for sexual selection to erode taxonomic boundaries and promote gene flow, particularly at an intermediate stage of divergence.     

External characteristics and associated developmental changes in two species of Sulawesi macaques,Macaca tonkeana andM. hecki,with special reference to hybrids and the borderland between the species

The degree of intergradation between two species of Sulawesi macaques,Macaca tonkeana andM. hecki, was studied by examining the diagnostic external characteristics of more than 100 monkeys kept as pets by natives. Two possible hybrid monkeys were found and both originated from the borderland between the two species, located in the most proximal region of the northern peninsula of Sulawesi. The previously postulated wide area of integradation between the two species at the possible contact zone was, however, not recognized, and typical examples oftonkeana orhecki were found to be present on the two sides of a narrow “hybrid” zone which was defined by direct observations. Furthermore, despite considerable individual variations, we were able to allocate most monkeys to one or other of the species. Each of ten external characteristics of the members of both species more or less encompassed the individual variations, but may undergo changes with the development of the monkeys. The mechanisms of reproduction of hybrid monkeys and the maintenance of differences between the species are discussed.     

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.     

Copulatory behavior in a free-ranging population of stumptail macaques (Macaca arctoides) in Mexico

This paper presents copulatory data gathered on a free-ranging population of stumptail macaques (Macaca arctoides) in Mexico. The study found evidence for seasonal clumping of matings, with the peak in the month of February, and that matings are more common in the afternoon, when measuring diurnal changes. It also found that males require an average of one and a half mounts before ejaculating, and mating among females is distributed unequally, when the measurement is between those females that mated. Furthermore, male dominance rank and male-female affiliation are both positively correlated with mating frequency. Variations between this study and captive studies are minimal. The variances that do occur may be explained by differences in the research settings or the individual differences in the subjects' behavior across studies.     

Male life history in natural populations of Japanese macaques: Migration, dominance rank, and troop participation of males in two habitats

This paper compares male life history parameters of two populations of Japanese macaques (Macaca fuscata Blyth, 1875), studied without provisioning: Yakushima (M. f. yakui), a subtropical forest habitat in southwestern Japan, and Kinkazan (M. f. fuscata), a temperate, deciduous forest habitat in northeastern Japan. The males of the two sites experienced similar life histories with respect to several traits. Age at natal dispersal was at about 5 years. Average troop residence was about three years. Most males joined troops at the bottom of the rank order, although a few males joined troops at the top rank. Dominance ranks of males tended to rise with the death or departure of higher ranking males. Visiting males accounted for about 41% of observed mating at both sites. However, the two sites differed in the sex ratio of troops, partly because a larger proportion of males apparently lived outside of troops in the Kinkazan site compared to Yakushima. In particular, non-natal young males were absent from the main study troop at Kinkazan. Large within-species variation may exist in the degree to which males associate with troops.     

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.     

Fatal attack on an infant by an adult female tonkean macaque

We describe a fatal attack on a 10-month-old female infant by an adult female Tonkean macaque (Macaca tonkeana)in a semi-free-ranging group. During an intense conflict involving many group members, an adult female, the second most dominant in the group, attacked the infant of a lower-ranking female. The attacker remained near the victim for approximately 20 min, grabbing and biting it repeatedly, until the mother retrieved the infant. She died 2 days later. An autopsy revealed no lethal injury;the main cause of death was starvation or dehydration or both. We discuss social conditions under which a fatal attack by an adult female might occur.