The Influence of Age,Sex, and Rank on Yawning Behavior in Two Species of Macaques (Macaca fascicularis and M. fuscata)

Yawning behavior was studied in two species of macaques: the long-tailed macaque (Macaca fascicularis) and the Japanese macaque (M. fuscata). Japanese macaques yawned much more than long-tailed macaques. Age, sex, and dominance rank exerted different effects on yawning in the two species. In the long-tailed macaques, sex differences in frequency of yawning emerged only after sexual maturity; yawning rates increased significantly in both males and females as they reached sexual maturity; and, among males, dominance rank was positively correlated with frequency of yawning. Differently, in the Japanese macaques, males, both mature and immature, yawned more than same-aged females; sexual maturity was associated with an increase in yawning in males only; and male rank did not correlate with the frequency of yawning. Regardless of interspecific differences, the overall results supported only in part the finding that, in Old World monkeys, yawning is largely influenced by plasma concentrations of androgens. There was evidence that social factors were also important in influencing the age-sex class distribution of yawning.     

Plasma cholesterol levels in free-ranging macaques compared with captive macaques and humans

Plasma total cholesterol in free-ranging Japanese macaques (Macaca fuscata) on Koshima islet and in free-ranging long-tailed macaques (Macaca fascicularis) at Pangandaran in Indonesia was found to occur at very low levels compared with captive macaques and humans. Although total cholesterol levels in captive macaques were lower than humans, differences in HDL cholesterol levels were only small. In both sexes of wild and captive Japanese macaques, total cholesterol levels decreased from birth through to young adulthood but then increased in adult females of the captive group. In contrast, the value for adult females of the wild troop remained at a low level. Low TCH levels in adult females of the wild Japanese macaque troop may be due to a low energy intake and may have caused a delay in the onset of sexual maturation. Plasma TCH levels increased with the addition of 0.1% dietary cholesterol over six weeks in captive long-tailed macaques. That the cholesterol value after six weeks was dependent on cholesterol levels prior to supplementation indicates that captive macaques are slightly saturated with cholesterol.     

Social Relationships in Free-Ranging Male Macaca arctoides

Macaque social relationships differ greatly between species. Based on captive studies that focus mainly on females, researchers have classified stumptail macaque (Macaca arctoides) social relationships as tolerant, as indicated by a high rate of affiliation, frequent aggression, and symmetrical conflicts. To accumulate more data on male social relationships, which are relatively understudied, and to generate comparative data, we investigated male social relationships in a provisioned group of 68 free-ranging, naturally dispersing stumptail macaques in southern Thailand. We collected continuous focal animal and ad libitum data on 7 adult and 2 subadult males, recording social behavior during 283 contact hours between December 2006 and March 2007. Stumptail macaques of this population were less tolerant than predicted based on previous studies on captive groups: Rates of spatial proximity, affiliation, and aggression were low, most males directed affiliative behavior toward higher-ranking males, and conflicts were generally of low intensity and relatively asymmetrical. Thus, male stumptail macaques of the focal group appear to differ in their social style from a previous study of a captive group that mainly comprised of females. In some traits, they are even more intolerant than rhesus macaques, an intensively studied intolerant macaque species. We also compare our data on stumptail macaque males to those on other male macaques, but available data are too sparse to draw final conclusions.     

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.     

Positional behavior of free-ranging Japanese macaques (<Emphasis Type="Italic">Macaca fuscata</Emphasis>)

Positional behavior was quantitatively studied in identified free-ranging Japanese macaques (Macaca fuscata). Five male and 11 female adults were observed in a forested mountain habitat. Data were analyzed for proportion of bout distance, number and time of each locomotion and postural type. Japanese macaques are semiterrestrial, and mainly walk and run quadrupedally. This supports the notion that Macaca are generally quadrupeds. Sex differences in positional behavior were found in the preference of substrate and types of positional behavior. Males and females tend to be terrestrial and arboreal, respectively. Males leap more frequently and longer in distance than do females when they are feeding in trees. These sex differences are considered to be related to differences in morphology, food choice, social activity, and the nursing of infants. Frequencies of leaping and the distance covered by leaping in Japanese macaques are more than those of long-tailed macaques which are arboreal quadrupeds. However, Japanese macaques leap shorter distances at a time than do long-tailed macaques, which indicates that body size may be related to leaping distance more than the frequency of leaping and the distance covered by leaping. Japanese macaques are not as specialized for terrestrial locomotion as pig-tailed macaques. They use both terrestrial and arboreal supports, and are considered to be semi-terrestrial quadrupeds, somewhere between the arboreal long-tailed macaque and the terrestrial pig-tailed macaque. Electronic Publication     

Social development in three species of macaque (Macaca mulatta, M. fascicularis, M. tonkeana): A preliminary report on the first ten weeks of life

The development of social relations was studied in 11 infant monkeys over the first ten weeks of life : 5 subjects in a rhesus macaque group ($\text{Macaca mulatta}$), 3 in a long-tailed macaque group ($\text{M. fascicularis}$) and 3 in a Tonkean macaque group ($\text{M. tonkeana}$). Tonkean infants were found to interact with many different group members because of the permissiveness of their mothers, while social contacts of rhesus and long-tailed infants are less varied due to the restrictiveness of their mothers. These differences were consistent with patterns of adult-adult interactions, Tonkean macaques showing less intense agonistic interactions than the other two species.     

On the directional orientation of female presents inMacaca fascicularis

The directional orientation of female presents in a captive group of long-tailed macaques (Macaca fascicularis) is markedly dependent upon the sex of the potential recipient. Females present in the ‘standard’ mode significantly more often than in the ‘sideways’ mode to males, with the opposite pattern prevailing to other females.     

Body Size and Proportions and Pelage Color of Free-Ranging Macaca mulatta from a Zone of Hybridization in Northeastern Thailand

Rhesus (Macaca mulatta) and long-tailed (M. fascicularis) macaques belong to the same species, and are parapatric within a zone that lies between 15° and 20° N on the Indochinese peninsula. Researchers have reported probable hybrids between the 2 species from that zone, but have not studied the extent of introgression. To test for phenotypic evidence of hybridization, we collected body mass, morphometrics (body size and proportions), and pelage color readings from free-ranging rhesus living close to the zonal boundary at Wat Tham Pa Mak Ho (WTPMH), Wang Saphun district, Loei province, northeastern Thailand (17°14′N, 101°47′E). Female WTPMH rhesus macaques (n =12) were 10–20% smaller, but with a greater relative tail length than the captive Chinese or Indian female rhesus. Female WTPMH were larger than the free-ranging long-tailed macaques, but with similar limb proportions and a shorter relative tail length. The WTPMH rhesus macaques also displayed the bipartite pelage color pattern typical of Macaca mulatta . The evidence suggests slight contribution of long-tailed macaques to the gene pool of the WTPMH population. Further sampling of other macaque populations within the zone and genetic analysis are essential to address better the question of hybridization. Determination of the distribution and range of biobehavioral variation of macaques within the zone is urgently needed, because their habitat is being rapidly destroyed by deforestation, and their demography and social structure are threatened by artificial disturbance.     

Male Social Behavior and Dominance Hierarchy in the Sulawesi Crested Black Macaque (Macaca nigra)

In a 6-week study of the social behavior of wild Sulawesi crested black macaques (Macaca nigra), we found a linear and transitive dominance hierarchy among the six adult males in one social group. Dominance rank, as determined by the direction of supplantations, correlated strongly with percentage of time near more than four neighbors, frequency of grooming received from adult females, and percentage of time with an adult female as nearest neighbor. These results suggest that high-ranking males are socially attractive. Adult females sexually solicited high-ranking males more often than low-ranking males, but frequency of copulation was not correlated with dominance rank. Frequency and intensity of aggression between males are strongly correlated with rank distance, but aggression toward females was greatest for mid-ranking males. Males of all rank displayed significantly more aggression toward sexually receptive females than toward females in other estrous states. These data indicate that male Sulawesi crested black macaques display a social organization similar to that reported for multimale groups in other macaque species rather than the egalitarian social organization described for female Sulawesi macaques.     

Hybridization and Stratification of Nuclear Genetic Variation in Macaca mulatta and M. fascicularis

We used genotypes for 13 short tandem repeats (STRs) to assess the genetic diversity within and differentiation among populations of rhesus macaques (Macaca mulatta) from mainland Asia and long-tailed macaques (M. fascicularis) from mainland and insular Southeast Asia. The subjects were either recently captured in the wild or derived from wild-caught founders maintained in captivity for biomedical research. A large number of alleles are shared between the 2 macaque species but a significant genetic division between them persists. The distinction is more clear-cut among populations that are not, or are unlikely to have recently been, geographically contiguous. Our results suggest there has been significant interspecific nuclear gene flow between rhesus macaques and long-tailed macaques on the mainland. Comparisons of mainland and island populations of long-tailed macaques reflect marked genetic subdivisions due to barriers to migration. Geographic isolation has restricted gene flow, allowing island populations to become subdivided and genetically differentiated. Indonesian long-tailed macaques show evidence of long-term separation and genetic isolation from the mainland populations, whereas long-tailed macaques from the Philippines and Mauritius both display evidence of founder effects and subsequent isolation, with the impact from genetic drift being more profound in the latter.     

Prevalence of glucose intolerance in free-ranging Macaca fascicularis of Mauritius

Oral glucose tolerance tests (OGTTs) were carried out on 30 free-ranging long-tailed macaques (Macaca fascicularis) on the island of Mauritius, following the suggestion that severe glucose intolerance and diabetes mellitus might be prevalent in this macaque population. OGTTs revealed no evidence of frank diabetes mellitus in the sample. However, 13% of individuals showed impaired glucose tolerance, with preserved insulin secretion, suggesting the presence of the target tissue resistance to insulin characteristic of human noninsulin-dependent diabetes mellitus (NIDDM). The macaques with impaired glucose tolerance were neither obese nor aged. Glucose levels at all time points of the OGTT in normal macaques in our free-ranging sample were lower than reported in captive populations, perhaps due to greater physical activity. Our observations demonstrate that a genetic predisposition to glucose intolerance does exist in M. fascicularis, and that this condition, well documented in laboratory macaques, is not simply an artifact of captivity.     

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.     

Evaluating Dominance Styles in Assamese and Rhesus Macaques

Researchers have suggested that several types of agonistic and affiliative behavior covary as a set of species-specific traits, and have used the term dominance style to describe the covariation. We compared measures of dominance style between a group of Assamese macaques (Macaca assamensis) and a group of rhesus macaques (M. mulatta), though kinship information was unknown. Assamese and rhesus female-female dyads each showed a low proportion of counter aggression and a low conciliatory tendency, suggesting that they have despotic social relationships. They also showed a despotic pattern on several other types of agonistic and affiliative behavior, such as approach outcomes and grooming distributions, which is consistent with the covariation of dominance style traits. Assamese male-male dyads showed relatively high levels of reconciliation and counter aggression versus other macaque males portrayed in the literature, suggesting that Assamese males have a tolerant dominance style. Insofar as macaque dominance style depends on the behavior of females, we suggest that Assamese macaques, like rhesus macaques, have despotic social relationships, which contrasts with evidence of a strong correlation between phylogeny and dominance style in macaques. Further, our results indicate that strong male bonding and tolerant dominance relationships among males are independent of female dominance style. Lastly, some measures of agonistic behavior, such as rate of aggression or proportion of bites, are likely altered in competitive environments and thus are not useful indicators of dominance style.     

A pilot study of the social correlates of levels of urinary cortisol,prolactin, and testosterone in wild long-tailed macaques (Macaca fascicularis)

Urine samples were collected from individuals in a wild population of Sumatran long-tailed macaques (Macaca fascicularis), and the levels of cortisol, immunoreactive prolactin, and (for males) testosterone were determined. The amount of foraging during the 2 hr preceding urine collection were found to affect the levels of urinary cortisol, but not those of the other hormones. Immigration into a new group and having one's infant kidnapped led to increased levels of cortisol. Levels of cortisol and testosterone were correlated both within and between individuals, whereas prolactin varied independently. The effects of age, reproductive status, and social rank on the mean values of individuals were also examined. Lactating females had higher prolactin levels than non-lactating ones; reproductive state interacted with the age effect on prolactin and possibly cortisol. No effects of social status were found in spite of a small, but consistent effect of rank on birth rate in this population. Among males, age and rank are strongly linked. The low ranking old males had increased levels of cortisol, even though the younger high-ranking males were involved in the fiercest conflicts.     

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.     

Effects of group composition on agonistic behavior of captive pigtail macaques,Macaca nemestrina

We surveyed agonistic behaviors of 20 captive groups of pigtail macaques (Macaca nemestrina) housed under identical spatial conditions. Fifteen groups contained one male each; the other five groups contained no adult males. Groups included six to twelve adult females, some of which had infants with them. We found no relationship between social density of groups and incidence of agonistic behavior, but significantly more contact aggression (grab, hit, push, bite) and noncontact aggression (chase, open-mouth “threat,” bark vocalization) occurred among females in groups containing no males than in those containing one male each. Apparently, males played an important role in the inhibition of intragroup conflict. We also found that females in groups containing males exhibited less noncontact aggression if infants were present than if no infants resided in their groups. Thus, competition of females over infants must not have been an important constituent of intragroup conflict under the conditions of this survey.     

Status and Distribution of Macaca fascicularis umbrosa in the Nicobar Islands, India

We surveyed the distribution and status of the long-tailed macaque (Macaca fascicularis umbrosa) in the Nicobar Islands of India. Long-tailed macaques live on 3 islands: Great Nicobar, Little Nicobar and Katchal. There are a total 788 groups. Group size ranged from 25 to 56 individuals with a mean size of 36. Long-tailed macaques are a multimale-multifemale society. Adult males, adult females and immatures constituted 9.7 per cent, 43.2 per cent and 47.1 per cent of the population, respectively. A fairly high ratio of immatures to adult females indicates a healthy population turnover. Vegetation parameters including tree density, canopy cover, canopy height and basal area indicated a still healthful habitats on all the 3 islands. We observed a few threats to the macaques. Measures should be undertaken to ensure survival of the Nicobar subspecies.     

Development in Japanese macaques (Macaca fuscata): Sexually dimorphic behavior during the first year of life

We have documented several sexually dimorphic patterns of behavior that develop during the first year of life in infant Japanese macaques and their mothers. Mothers treated their infants differently by sex—mothers of males broke contact with them and retrieved them more frequently than did mothers of females. And mothers of male infants moved more frequently than did mothers of female infants. Male infants played more, played in larger groups, and mounted more frequently; female infants groomed and spent more time close to other monkeys in larger social groups than did males. Female infants were also punished by other group members more frequently than were male infants. We conclude that male and female Japanese macaque infants receive differential treatment early in life by both their own mothers and other animals, and males and females in turn treat their mothers and other animals differently. There appears to be a reciprocal relationship between the behavior of infants, mothers and other social partners that contributes to the development of sexually dimorphic patterns of behavior.     

Fishing in Macaca fascicularis: A Rarely Observed Innovative Behavior

Observations of fishing behavior in nonhuman primates are rare and isolated, and there is no prior published observation on the behavior in long-tailed macaques (Macaca fascicularis). We observed fishing behavior in 3 groups of long-tailed macaques from 2 separate study sites in North Sumatra and East Kalimantan, Indonesia. We propose that the behavior is rare and fulfills the requirements for classification as innovation. Further, all of the fishing individuals were watched by other members of their group, with their actions inciting attempts at fishing by them. We consider the possibility that the behavior has the potential to become cultural within the populations.     

Symmetrical patterns in non-agonistic social interactions found in unprovisioned Japanese macaques

Non-agonistic social interactions in an unprovisioned troop of Japanese macaques (Macaca fuscata yakui) were analyzed with the spacing between individuals, leading-following interactions, and exchange of social grooming. The most frequent interactions were found between kin-related females. Unrelated females stayed with one another rather frequently, but rarely exchanged social behaviors. Interactions between males and females were infrequent though they were occasionaly observed between high-ranking males and high-ranking females. Very frequent exchange of grooming was observed between males, and even high-ranking males exchanged grooming more frequently with males than with females. Most non-agonistic social interactions in the study troop were based on bidirectional exchange of social behaviors, in which no clear tendency relevant to dominance or sex was found; while in provisioned Japanese macaque troops, associations between males and females, between unrelated females, and between males were formed mainly be subordinates' active roles in associative behaviors. This seems relevant to the idea that dominance grealty influence social life in provisioned troops. The present study provides guidelines for interspecific comparison of social interaction patterns of macaque species.