Organization of Group Members at Departure Is Driven by Social Structure in Macaca

Researchers have often explained order of progression of group members during joint movement in terms of the influence of ecological pressures but rarely that of social constraints. We studied the order of joining by group members to a movement in semifree-ranging macaques with contrasting social systems: 1 group of Tonkean macaques (Macaca tonkeana) and 1 group of rhesus macaques (M. mulatta). We used network metrics to understand roles and associations among individuals. The way the macaques joined a movement reflected the social differences between the species in terms of dominance and kinship. Old and dominant male rhesus macaques were more often at the front of the movement, contrary to the Tonkean macaques, which exhibited no specific order. Moreover, rhesus macaques preferred to join high-ranking or related individuals, whereas Tonkean macaques based associations during joining mostly on sexual relationships with a subgroup of peripheral males.     

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.     

Grooming site preferences determined by lice infection among Japanese macaques in Arashiyama

I investigated the effect of the density of louse eggs (Pedicinus obtusus andP. eurygaster) on grooming site preferences in Japanese macaques (Macaca fuscata). Louse eggs were more often found on the outer side of the body (upper back, lower back, outer arms, and outer legs) than on the inner side of the body (chest, belly, inner arms, and inner legs). Japanese macaques were more likely to be groomed on the outer side than the inner side of the body by allogrooming and autogrooming. Such grooming site preferences correlated with the distribution of louse eggs but not with the areas of body parts. Thus, the ecology of lice might affect grooming behavior of Japanese macaques. Five hundred and fifty louse eggs were estimated to parasitize an adult female Japanese macaque. Considering the intrinsic rate of natural increase of lice, monkeys need to be groomed almost every day. This suggests that Japanese macaques need grooming partners and form social bonds with others for everyday grooming.     

The evolution of “egalitarian” and “despotic” social systems among macaques

Recent studies of captive macaques have revealed considerable inter-species differences in dominance styles among females. In “egalitarian” species such as stumptail (Macaca arctoides) or tonkean macaques (M. tonkeana), social interactions are more symmetrical and less kin-biased than in “despotic” species such as Japanese (M. fuscata) or rhesus macaques (M. mulatta). Field observations of moor macaques (M. maurus), close relatives of tonkean macaques, suggest that tolerance during feeding characterizes their egalitarian dominance style in the natural habitat. Although it has been proposed that communal defense against other groups may be the main selective force in the evolution of egalitarian dominance style among females, few field data support this prediction. A game theory analysis showed that both an “egalitarian” strategy and a “despotic” strategy are possible evolutionarily stable strategies (ESS) under certain conditions. The difference in dominance styles might reflect the difference in ESS. This means that an egalitarian dominance style can emerge without strong between-group contest competition. A phylogenetic comparison among macaques suggests that despotic dominance styles very likely evolved from egalitarian dominance styles. In the future, primate socioecological studies should pay more attention to the evolutionary history of each species.     

A Voucher Specimen for <Emphasis Type="Italic">Macaca munzala</Emphasis>: Interspecific Affinities,Evolution, and Conservation of a Newly Discovered Primate

Sinha, A., Datta, A., Madhusudan, M. D., & Mishra, C. (2005. Macaca munzala: A new species from western Arunachal Pradesh, northeastern India. International Journal of Primatology, 26, 977–989) discovered Arunachal macaques (Macaca munzala), a species new to science, in the eastern Himalaya of Arunachal Pradesh in northeastern India. They depicted the holotype and paratypes of the species in photographs, and a specimen of the species had been unavailable for preservation and examination. In March 2005, we obtained an entire specimen of an adult male Macaca munzala, which we propose as a voucher specimen for the species. We provide detailed morphological and anatomical measurements of the specimen and examine its affinities with other macaques. Macaca munzala appears to be unique among macaques in craniodental size and structure, baculum, and aspects of caudal structure, while exhibiting affinities with the other members of the sinica-group to which it belongs. We summarize our insights on the origins and phylogeny of Macaca munzala. Finally, we review the current conservation status of the macaques, which are threatened by extensive hunting in the only 2 districts of Arunachal Pradesh where they are documented to occur.     

Outcast males and social structure among bonnet macaques (Macaca radiata)

Outcast males are a regular feature of rhesus (Macaca mulatta) and Japanese (M. fuscata) macaque societies but are rare among bonnet macaques (M. radiata). Apparently bonnets have other solutions than ostracism for their social problems. For example, in many troops the male-female ratio ranges from 0.7?1.0+; and, as the young adult males grow to full social and physical maturity, they remain in the troop and participate actively in social relationships. A few troops of bonnet macaques, however, have a network of social relationships which prevents the young males from being integrated into the social system; in some of these cases, male isolation occurs. A comparison of the social relations between males in bonnet macaque societies of both types suggests that societies with strong male-male bonds accommodate their growing males better than those with highly individual males.     

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.     

Social Behavior of Captive Indochinese and Insular Long-Tailed Macaques (Macaca fascicularis) Following Transfer to a New Facility

There are measurable differences in behavior, physiology, social organization, and geographic distribution within and between various species of macaques. We collected information on the social behavior of captive Macaca fascicularis from Indochina and island populations after they had been transferred to a new environment and new social groups. While some changes in behavior occurred over time, we found no decrease in high levels of agonistic behaviors. We interpret this finding in light of previous research reporting that long-tailed macaques show low levels of habitatuation to novelty and are highly aroused in comparison to other macaque species. We found predictable differences in behavior for males, females, and infants, in which infants played more, females had higher levels of contact proximity to other individuals, and males exhibited more sexual and threat behavior. A comparison of social behavior in long-tailed macaques from different origins indicate that Indochinese macaques are generally less affiliative and Indochinese males are more aggressive than their insular counterparts. Differences among macaque species, and within the fascicularis-group, should be considered in management of captive colonies and when interpreting research data.     

Sons of low-ranking female rhesus macaques can attain high dominance rank in their natal groups

Five adult and subadult sons of middle- and low-ranking female rhesus macaques (Macaca mulatta) were observed to hold high dominance rank in their natal groups during a 12-month study at Cayo Santiago, Puerto Rico. Three of these males also experienced high mating success during at least one mating season. These findings contrast with all previously published accounts of rank acquisition by natal male rhesus macaques in provisioned colonies, and they present a challenge to the hypothesis that natal transfer functions to increase male access to fertile females.     

Effects of six-day maternal separation on tonkean macaque infants

Maternal separation may induce a depressive state in infant macaques. However, this does not occur in all macaque species. From present hypotheses, it may be predicted that infants belonging to a species characterized by open and tolerant social relationships should not develop severe depressive symptoms. Tonkean macaques (Macaca tonkeana) stand as such a species. The goal of the study was to verify that the infant’s reaction to mother loss is related to the social environment. The mothers of eight 5- to 9-month-old infants were removed during 6-day experimental periods. Infants’ behavior was characterized by a mild initial protest stage, followed by a slight decrease in activity during later maternal separation, and quick recovery after the mother’s return. No despair stage occurred. During separation, group members compensated for mother’s absence by cradling the infants. That social networks determine the intensity of the infant’s response to separation has far-reaching implications with regard to the meaning of depression occurrence within social networks.     

A 15-year study of the association between dominance rank and reproductive success of male rhesus macaques

The reproductive success (RS) of 32 males in a captive group of rhesus macaques (Macaca mulatta) between 1978 and 1992 was determined using paternity exclusion analysis. Dominance rank of each male over age 4 was assessed at the end of each breeding season based on agonistic dyadic interactions. The dominance rank and RS of these males were strongly correlated whether or not subadult males were included. The high reproductive success of males that eventually reached alpha rank is primarily responsible for this outcome. These results support the theory that social dominance has evolved in genusMacaca by sexual selection but some changes in male dominance rank and RS during the 15-year period suggest that priority of access is not the sole focus for such selection.     

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.     

Distribution and Population Densities of Diurnal Primates in the Karst Forests of Phong Nha – Ke Bang National Park,Quang Binh Province,Central Vietnam

We studied the status and distribution of the diurnal primates in the Phong Nha – Ke Bang National Park (PNKB NP) from April to August 2007. In the past, researchers reported 9 primate species and subspecies for the karst forests of PNKB NP, which constitutes the most important protected area for the endangered Hatinh langur (Trachypithecus hatinhensis) in Vietnam. All 9 primate taxa are threatened due to hunting pressure and habitat loss. We applied line transect sampling in 4 areas. During a total of 117 transect inspections along 12 different transect routes, we confirmed 5 primate taxa and the analysis of population densities resulted in 2143 (±467) Hatinh langurs, 1316 (±871) red-shanked douc langurs (Pygathrix nemaeus), 930 (±489) stump-tailed macaques (Macaca arctoides), 986 (±883) eastern Assamese macaques (M. a. assamensis), and 18 (±18) southern white-cheeked crested gibbons (Nomascus siki) in the whole PNKB NP, which covers an area of ca. 85,000 ha. We could not detect the 2 nocturnal lorises, Bengal slow lorises (Nycticebus bengalensis) and pygmy slow lorises (N. pygmaeus), as well as rhesus macaques (Macaca mulatta) and northern pig-tail macaques (M. leonina). The distribution of the primates predominantly depended on human impact. We could not recognize a correlation between habitat constitution and abundance of primates. The population density estimates showed a much higher density of the Hatinh langur than previously assumed. Thus the importance of the PNKB NP for the conservation of this endangered langur increased significantly.     

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.     

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.     

Male rank,reproductive behavior,and reproductive success in free-ranging rhesus macaques

Paternity assessment through DNA fingerprinting by synthetic oligonucleotide probes was applied to one birth cohort in a social group of free-ranging rhesus macaques (Macaca mulatta) on Cayo Santiago. The 11 group males and 9 males from other groups were observed mating with the females. Paternity was determined for 11 of the 15 infants. Male dominance rank was not associated with reproductive success. High-ranking resident males (N=5) sired 27% of the infants born during a one-year study. Four of the 11 infants of known paternity were sired by males of other social groups. The four infants of unknown paternity were sired either by males not observed mating with the females or the low-ranking male who was not fingerprinted. Male dominance rank was not associated with reproductive activity during conception cycles. These results suggest that the effect of rank on male reproductive success is not a predictable correlation, but a conditional probability.     

Characterization of 47 MHC class I sequences in Filipino cynomolgus macaques

Cynomolgus macaques (Macaca fascicularis) provide increasingly common models for infectious disease research. Several geographically distinct populations of these macaques from Southeast Asia and the Indian Ocean island of Mauritius are available for pathogenesis studies. Though host genetics may profoundly impact results of such studies, similarities and differences between populations are often overlooked. In this study we identified 47 full-length MHC class I nucleotide sequences in 16 cynomolgus macaques of Filipino origin. The majority of MHC class I sequences characterized (39 of 47) were unique to this regional population. However, we discovered eight sequences with perfect identity and six sequences with close similarity to previously defined MHC class I sequences from other macaque populations. We identified two ancestral MHC haplotypes that appear to be shared between Filipino and Mauritian cynomolgus macaques, notably a Mafa-B haplotype that has previously been shown to protect Mauritian cynomolgus macaques against challenge with a simian/human immunodeficiency virus, SHIV_89.6P. We also identified a Filipino cynomolgus macaque MHC class I sequence for which the predicted protein sequence differs from Mamu-B*17 by a single amino acid. This is important because Mamu-B*17 is strongly associated with protection against simian immunodeficiency virus (SIV) challenge in Indian rhesus macaques. These findings have implications for the evolutionary history of Filipino cynomolgus macaques as well as for the use of this model in SIV/SHIV research protocols. Kevin J. Campbell and Ann M. Detmer contributed equally to this work.     

Identification of MHC class I sequences in Chinese-origin rhesus macaques

The rhesus macaque (Macaca mulatta) is an excellent model for human disease and vaccine research. Two populations exhibiting distinctive morphological and physiological characteristics, Indian- and Chinese-origin rhesus macaques, are commonly used in research. Genetic analysis has focused on the Indian macaque population, but the accessibility of these animals for research is limited. Due to their greater availability, Chinese rhesus macaques are now being used more frequently, particularly in vaccine and biodefense studies, although relatively little is known about their immunogenetics. In this study, we discovered major histocompatibility complex (MHC) class I cDNAs in 12 Chinese rhesus macaques and detected 41 distinct Mamu-A and Mamu-B sequences. Twenty-seven of these class I cDNAs were novel, while six and eight of these sequences were previously reported in Chinese and Indian rhesus macaques, respectively. We then performed microsatellite analysis on DNA from these 12 animals, as well as an additional 18 animals, and developed sequence specific primer PCR (PCR-SSP) assays for eight cDNAs found in multiple animals. We also examined our cohort for potential admixture of Chinese and Indian origin animals using a recently developed panel of single nucleotide polymorphisms (SNPs). The discovery of 27 novel MHC class I sequences in this analysis underscores the genetic diversity of Chinese rhesus macaques and contributes reagents that will be valuable for studying cellular immunology in this population.     

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.     

Female reproductive cycles and the sexual behavior of moor macaques (Macaca maurus) in their natural habitat,South Sulawesi,Indonesia

The female reproductive cycles and sexual behavior of moor macaques (Macaca maurus) were studied in their natural habitat. Female moor macaques showed repeated perineal swelling. The average cycle length was 36.2 days and the mean duration of swelling was 11.9 days. The estimated duration of gestation in two observed cases was 175 and 176 days, respectively. Females did not exhibit post-conception sexual swelling. Males appeared to ejaculate in multi-mounts. Serial mounting by the alpha male was concentrated on swelling females, while second- and third-ranking males sometimes mounted non-swelling females in series.