Macaca Nigra Research Articles

Social bonds affect anti-predator behaviour in a tolerant species of macaque,Macaca nigra

Enduring positive social bonds between individuals are crucial for humans' health and well being. Similar bonds can be found in a wide range of taxa, revealing the evolutionary origins of humans' social bonds. Evidence suggests that these strong social bonds can function to buffer the negative effects of living in groups, but it is not known whether they also function to minimize predation risk. Here, we show that crested macaques (Macaca nigra) react more strongly to playbacks of recruitment alarm calls (i.e. calls signalling the presence of a predator and eliciting cooperative mobbing behaviour) if they were produced by an individual with whom they share a strong social bond. Dominance relationships between caller and listener had no effect on the reaction of the listener. Thus, strong social bonds may improve the coordination and efficiency of cooperative defence against predators, and therefore increase chances of survival. This result broadens our understanding of the evolution and function of social bonds by highlighting their importance in the anti-predator context.

Immunohistochemical and morphological features of a small bowel leiomyoma in a black crested macaque (Macaca nigra)

BackgroundSpontaneous gastrointestinal neoplasms in non-human primates are commonly seen in aged individuals. Due to genetic similarities between human and non-human primates, scientists have shown increasing interest in terms of comparative oncology studies.Case presentationThe present study is related to a case of an intestinal leiomyoma in a black crested macaque (Macaca nigra), kept on captivity by Matecaña Zoo, Pereira City, Colombia. The animal had abdominal distension, anorexia, vomiting, diarrhea and behavioral changes. Clinical examination showed an increased volume in the upper right abdominal quadrant caused by a neoplastic mass. The patient died during the surgical procedure. Necropsy revealed several small nodules in the peritoneum with adhesion to different portions of the small and large intestines, liver, stomach and diaphragm. Tissue samples were collected, routinely processed and stained by H&E. Microscopic examination revealed a mesenchymal tumor limited to tunica muscularis, resembling normal smooth muscle cells. Neoplastic cells were positive for alpha-smooth muscle actin and vimentin, and negative for cytokeratin AE1/AE3 by immunohistochemistry. Those morphological and immunohistochemical findings allowed to diagnose the intestinal leiomyoma referred above.ConclusionNeoplastic diseases in primates have multifaceted causes. Their manifestations are understudied, leading to a greater difficulty in detection and measurement of the real impact provides by this disease.

Testing the oxidative stress hypothesis of aging in primate fibroblasts: is there a correlation between species longevity and cellular ROS production?

The present study was conducted to test predictions of the oxidative stress theory of aging assessing reactive oxygen species production and oxidative stress resistance in cultured fibroblasts from 13 primate species ranging in body size from 0.25 to 120 kg and in longevity from 20 to 90 years. We assessed both basal and stress-induced reactive oxygen species production in fibroblasts from five great apes (human, chimpanzee, bonobo, gorilla, and orangutan), four Old World monkeys (baboon, rhesus and crested black macaques, and patas monkey), three New World monkeys (common marmoset, red-bellied tamarin, and woolly monkey), and one lemur (ring-tailed lemur). Measurements of cellular MitoSox fluorescence, an indicator of mitochondrial superoxide (O2(·-)) generation, showed an inverse correlation between longevity and steady state or metabolic stress-induced mitochondrial O2(·-) production, but this correlation was lost when the effects of body mass were removed, and the data were analyzed using phylogenetically independent contrasts. Fibroblasts from longer-lived primate species also exhibited superior resistance to H(2)O(2)-induced apoptotic cell death than cells from shorter-living primates. After correction for body mass and lack of phylogenetic independence, this correlation, although still discernible, fell short of significance by regression analysis. Thus, increased longevity in this sample of primates is not causally associated with low cellular reactive oxygen species generation, but further studies are warranted to test the association between increased cellular resistance to oxidative stressor and primate longevity.

MITOCHONDRIAL DNA (MTDNA) VARIATION OF SULAWESI BLACK MACAQUE (Macaca nigra) LIVED IN TWO NATIONAL PARKS (TANGKOKO AND DUA SAUDARA) OF NORTH SULAWESI

Hypervariable II (HVII) regions of mitochondrial DNA (mtDNA) D-loop regions of Macaca nigra lived in Tangkoko and Dua Saudara National Parks have been analysed. An approximately 600 base pairs (bp) of HVII regions was sequenced to characterize genetic variation among 20 samples of Macaca nigra lived in Tangkoko and Dua Saudara National Parks. Using an outgroup of Macaca fascicularis of Kalimantan, a neighbor-joining and maximum parsimony trees both identified that all DNA samples of Macaca nigra were arranged in similar cluster. The low nucleotide diversity among samples of Macaca nigra in Tangkoko and Dua Saudara suggests either there is a direct mix among species or that they may have similar ancestor among them.

Friendship affects gaze following in a tolerant species of macaque, Macaca nigra

Gaze following, the ability to follow the direction in which others are looking, is thought to allow individuals to acquire valuable information from their physical and social environment. Recent studies, using artificial stimuli, showed that gaze following can be modulated by social factors such as dominance or social context, suggesting the importance of integrating these factors in future cognitive studies to understand better the evolution and function of gaze following. Whether this finding still holds true when animals are tested with conspecifics is unknown. Moreover, additional social factors remain to be tested. Testing live conspecifics, we show that friendship (i.e. strong positive bonds between individuals) improved gaze-following responses in a tolerant primate: the crested macaque. Subjects did not follow the gaze of friends more often, but in dyads characterized by a high friendship index, subjects were quicker to react to gaze cues. The increased social tolerance characteristic of crested macaques’ social relationships may lessen the constraints imposed by dominance and kinship, thus allowing sociocognitive abilities to be better used among friends. Together with previous findings, our results suggest the importance of relationship quality and species’ social style in shaping primate cognition.

A comparative network analysis of social style in macaques

In group-living species, individuals gain significant advantages from establishing an extensive network of social relationships. This results in complex organizations that are difficult to quantify in a comprehensive manner. In this respect, network analyses are an ideal means to pinpoint the overall properties of social structures, and the place of each individual within these structures. We used network measurements to investigate cross-species variations in the social style of macaques, and studied 12 groups from four species. Two species (Macaca mulatta, Macaca fuscata) were characterized by a relatively weak social tolerance, a steep gradient of dominance and a strong preference for kin. The other two species (Macaca nigra, Macaca tonkeana) were known to display higher levels of tolerance, relaxed dominance and low kinship bias. We used a centrality index based on eigenvector centrality to show that in a comparison of intolerant and tolerant species, top-ranking individuals were more central than other group members in the former species than the latter. We also found that networks had higher modularity in intolerant species, indicating that kin-related partners interacted more frequently in subgroups of these species than in those of tolerant species. Consistently, the matrix of body contacts was more strongly correlated with the kinship matrix in intolerant species. This study demonstrates the efficiency of network methodology in detecting fine and overall contrasts in social structures, and also reveals novel dimensions in the social style of macaques.

Pemetaan Distribusi dan Densitas Monyet Hitam Sulawesi (Macaca Nigra) di Sulawesi Utara

A study on mapping of distribution and population of Sulawesi crested black macaques ( Macaca nigra ) has been carried out to evaluate the current condition of distribution and density. This research was conducted from January to November 2009 at 24 locations in North Sulawesi Province. Determination of M. nigra distribution was based on the information provided by people surrounding the sites and field observation. Line transect was used to evaluate the density of the monkey with the length based on the habitat condition and the width was 100 m. The results showed that monkeys were not found at all of the locations and based on categories, high density of monkey was only found at Tangkoko-Batuangus Nature Reserve Two serious problems responsible to monkey population decreasing were hunting for consumption and habitat destruction. It can be concluded that distribution of M. nigra in North Sulawesi is meta-population and the current status of the species as critically endangered is accepted; the conservation of this species depends on the active management and terminating the factors of population decreasing.

The endemic seven: Four decades of research on the Sulawesi macaques

AbstractThe oceanic island of Sulawesi, Indonesia, has long been of interest to scholars, including one of the leading evolutionary thinkers of the nineteenth century: Alfred Russell Wallace. During his explorations of the Malay archipelago, Wallace1 was particularly struck with the ecology of Sulawesi (formally Celebes), noting the depauperate, yet distinctive nature of its fauna. It was home to members of both Asian and Australian faunas. Today, the asymmetrical four‐armed island of Sulawesi is regarded as the center of Wallacea, a unique biogeographical zone where endemism levels are incredibly high.2 Of the 127 mammals indigenous to Indonesia, 79 (62%) are endemic to Sulawesi. Among these are seven species of the genus Macaca,3 the most geographically widespread and ecologically diverse of nonhuman primate genera. In this paper, I trace the history and development of the major research trends on these endemic primates over the last four decades since Fooden's3 landmark 1969 publication. These research trends include origin, speciation, and taxonomy; socioecology and behavior; ecology and conservation; and, most recently, the human‐macaque interface.

Loud calls in male crested macaques, Macaca nigra: a signal of dominance in a tolerant species

Compared to other mammals, sexual signals occur particularly often within the primate order. Nevertheless, little is known so far about the pressures under which these signals evolved. We studied loud calls in wild crested macaques to examine whether these are used as a sexual signal, particularly as a signal of dominance, in this species. Since the structure of loud calls may be influenced by the context in which they are uttered, we tested for contextual differences in call structure. Only males uttered loud calls and analysis of 194 loud calls given by 15 males showed that call structure encoded the caller's identity as well as his social status. Dominance rank was also reflected in the frequency with which males called with alpha males calling most often. The structure of loud calls, however, was not influenced by context. Our findings consolidate the assumption that, in crested macaques, loud calls serve as a signal of dominance, most probably used to prevent contests between males for mates. We herewith provide the first direct evidence for a signal of dominance in a tolerant primate species and discuss why this signal occurs in only one sex.

The ischial callosities of Sulawesi macaques

Sulawesi island has a high level of endemism, including the seven species of monkey from the genus Macaca (macaques). These monkeys have a pair of sitting pads, termed ischial callosities that have diverse shapes and previously were described verbally only. Although useful, these verbal descriptions cannot fully describe shape variation and are somewhat subjective, and cannot directly be used to analyze relationships among species. Here, we report a quantitative analysis of shape of Sulawesi macaque ischial callosities using geometric morphometric tools to optimally describe shape variation and objectively reconstruct general pattern of callosity shapes. By quantification of shape variation, we compare the relationships of each Sulawesi macaque species with each other and with the two geographically neighboring macaque species, M. nemestrina and M. fascicularis, by consensus coordinates of the callosity outlines. The Sulawesi macaques have a wider degree of variation compared with M. fascicularis and M. nemestrina; variation exists in the dorsal part and in the bending of the callosity. There are three general types of callosity shape in Sulawesi macaques: oval without bending (M. tonkeana and M. maurus), oval with outward bending (M. ochreata and M. brunnescens), and oval or reniform with inward bending (M. hecki, M. nigrescens, and M. nigra). These types are congruent with their geographical distribution. The pathway of shape change may have started from oval without bending in the center and the southern peninsula, to outward bending in the southeastern species, and to oval or reniform with inward bending in the northern species.

Distress prevention by grooming others in crested black macaques.

Allogrooming is probably one of the most common and most studied social behaviours in a variety of animals. Whereas the short-term benefits for the groomee have often been investigated, little is known about the effects for the groomer. Our study focused on the short-term effects of grooming another group member in seven adult female crested black macaques (Macaca nigra). We found reductions in self-directed behaviour, an indicator of anxiety, and aggressive tendencies soon after grooming, when compared to matched-control periods. These findings can be interpreted as evidence of distress prevention, possibly mediated by an increase in tolerance. Indeed, a former groomee was more likely to be the nearest neighbour of the former groomer in the 10 min after grooming ended. Thus, the role of grooming in short-term distress alleviation can be applicable to the groomer as well as the groomee. These short-term effects, together with the longer-term effects of large and/or strong grooming networks confirm that grooming, as well as receiving grooming, has great importance for social dynamics.

LAMA KEBUNTINGAN MONYET HITAM SULAWESI (Macaca nigra) DI CAGAR ALAM TANGKOKO-BATUANGUS, SULAWESI UTARA

A research about gestational length of Sulawesi crested black macaque (Macaca nigra) has conducted to determine the length between conception and birth. Five adult females of Rambo II Group at Tangkoko-Batuangus Nature Reserve, North Sulawesi, were used as samples. Data collection used focal animal sampling to observe the sex swelling cycle and the time when they gave birth. The length of gestation was determined by counting the time duration between middle fully swollen until giving birth. Data was analyzed descriptively to count the mean and standard deviation. Result showed that the gestational length of Sulawesi crested black macaque was 183.6 ± 11.6 days. From this result can be concluded that the gestational length of this species is longer than other Macaca species.

Radiographic measurement of the cardiothoracic ratio in pet macaques from Sulawesi, Indonesia

The relative size of the heart, as measured by the cardiothoracic ratio, is often used as an index of ventricular hypertrophy—an important measure of myocardial pathophysiology in human primates. Despite its widespread use in human medicine, use of the cardiothoracic ratio in nonhuman primate veterinary medicine has been poorly documented. This report describes the results of our radiographic study of the cardiothoracic ratio in a sample of pet monkeys from Sulawesi, Indonesia. We assessed the effects of age and sex on cardiothoracic ratios, and compared our estimates with those presented in the literature for the Formosan macaque ( Macaca cyclopis). Our results indicated a significant difference between the Sulawesi macaque species groupings in cardiothoracic ratios. Sex and age-related differences were not significant. Comparisons of cardiothoracic ratios with published ratios indicated similarity between M. cyclopis and Macaca nigra, but not between M. cyclopis and Macaca tonkeana.

A coalescent framework for comparing alternative models of population structure with genetic data: evolution of Celebes toads

Isolation of populations eventually leads to divergence by genetic drift, but if connectivity varies over time, its impact on diversification may be difficult to discern. Even when the habitat patches of multiple species overlap, differences in their demographic parameters, molecular evolution and stochastic events contribute to differences in the magnitude and distribution of their genetic variation. The Indonesian island of Sulawesi, for example, harbours a suite of endemic species whose intraspecific differentiation or interspecific divergence may have been catalysed by habitat fragmentation. To further test this hypothesis, we have performed phylogenetic and coalescent-based analyses on molecular variation in mitochondrial and nuclear DNA of the Celebes toad (Bufo celebensis). Results support a role for habitat fragmentation that led to a population structure in these toads that closely matches distributions of Sulawesi macaque monkeys. Habitat fragmentation, therefore, may also have affected other groups on this island.

Daytime birth of a baby crested black macaque (Macaca nigra) in the wild

In mammals, which give birth to more or less dependent offspring, parturition usually takes place during the animals' resting period and in a secure environment. We report here the first direct and documented observation of a daytime birth of a wild baby crested black macaque, Macaca nigra, in the Tangkoko Batuangus Nature Reserve, North Sulawesi, Indonesia. We further consider the parturition time as a female reproductive strategy in a broader evolutionary framework.

Variation of the melanocortin 1 receptor gene in the macaques

Melanocortin 1 receptor (MC1R), a G-coupled seven-transmembrane receptor protein, plays a key role in the regulation of melanin synthesis in mammals. Sequence variation of the MC1R gene (MC1R) has been associated with pigmentation phenotypes in humans and in several animal species. The macaques (genus Macaca) are known to show a marked inter-specific variation in coat color although the causative genetic variation remains unclear. We investigated nucleotide sequences of the MC1R in 67 individuals of 18 macaque species with different coat color phenotypes including black and agouti. Twenty-eight amino acid replacements were identified in the macaques, but none of these amino acid replacements could explain the black coat color of Macaca silenus and the Sulawesi macaque species. Our molecular evolutionary analysis has revealed that nonsynonymous substitution/synonymous substitution (dN/dS) ratio of the MC1R has not been uniform in the macaque groups and, moreover, their coat color and dN/dS ratio were not related. These results suggest that the MC1R is unlikely to be responsible for the coat color variation of the macaques and functions of MC1R other than pigmentation might be associated with the different selective pressures on the MC1R in macaques.

Social play in crested and japanese macaques: Testing the covariation hypothesis

Most studies about social play have focused on its function in aiding socialization. It is not known whether play patterns vary by species according to specific adult social relationships. To test whether there is covariation between the form of play interactions and adult relationships, we studied social play in Japanese macaques (Macaca fuscata) and crested macaques (Macaca nigra). Comparative studies have shown that whereas low levels of tolerance and strict hierarchies characterize Japanese macaques, crested macaques display greater tolerance and relaxed dominance. The results showed that the former prefer less risky games, with minimal physical contact, ease of escape and a small number of play partners. The play bouts of the latter species involve closer contact and more partners. We conclude that play patterns covary with specific social style. Play patterns could have been selected for to introduce youngsters to their future social environment.

Distribution ofMacaca ochreataand Identification of MixedOchreata-TonkeanaGroups in South Sulawesi, Indonesia

We collected data on the distribution of booted macaques (Macaco ochreata) in Faruhumpenai Nature Reserve in South Sulawesi, Indonesia, in order to assess its conservation status. Methodology included censuses conducted along piecewise linear transects established at two sites from April—July 2006. The total distance walked was 45 km for the Matano site, and 20 km for the Kasintuwu site. Group density of booted macaques at the Matano site was 0.97–1.56 per km2. At the Kasintuwu site, we encountered groups of booted macaques and Tonkean macaques (Macaca tonkeana), as well as mixed groups of tonkeana and ochreata. The group density of booted macaques was 1.45–2.00 per km2. Overall macaque group density (i.e., Macaca spp.) at this site was 3.25–4.00 per km2. Our study demonstrated that two species of Sulawesi macaques, M. tonkeana and M. ochreata, as well as mixed tonkeana-ochreata groups occur in the forests in and surrounding Faruhumpenai Nature Reserve. The results confirm a more extensive range of M. ochreata than was previously recognized; one that extends further north and northwest than the provincial boundary of south and southeast Sulawesi. The conservation status of booted macaques may, therefore, not be as precarious as previously thought, since their habitat is protected in not only two large conservation areas in Southeast Sulawesi (Rawa Aopa National Park and Tanjung Peropa Game Reserve), but also in South Sulawesi in the Faruhumpenai Nature Reserve. Nonetheless, because cacao is frequently planted on the borders of these protected forests, human-macaque conflict resulting from crop raiding may eventually pose a threat.

Investigation of the role of the agouti signaling protein gene (ASIP) in coat color evolution in primates

We investigated variation in the gene encoding the agouti signaling protein (ASIP) in relation to coat color evolution in primates. We found little evidence that mutations in the coding region of ASIP have been involved in color changes among closely related primate species. Among many closely related species with differing coat color, the coding region of ASIP was identical. In two cases (Sulawesi macaque and black lion tamarin) where species with almost completely black coat color had derived point mutations in exon 4 of the ASIP coding sequence, the same mutations did not alter coloration in other mammals and so probably do not affect ASIP function. Evolutionary reconstructions of two key phenotypes that are typically related to ASIP function--transverse phaeomelanin bands on hairs and pale ventral coloration--showed that these usually evolved concurrently, suggesting that loci acting downstream of ASIP may be involved. Analysis of dN/dS ratios revealed a likely change in functional constraint on ASIP following loss of agouti-banded hairs + pale ventral coloration, particularly in catarrhine primates (humans, apes, and Old World monkeys). Together with previous results on a lack of association of coat color with MC1R variation, these results suggest that other loci probably have an important role in primate coat color evolution.

Phylogeny of primate T lymphotropic virus type 1 (PTLV-1) including various new Asian and African non-human primate strains

To further unravel intra- and interspecies PTLV-1 evolution in Asia and Africa, we phylogenetically analysed 15 new STLV-1 LTR and env sequences discovered in eight different Asian and African non-human primate species. We show that orang-utan STLV-1s form a tight, deeply branching monophyletic cluster between Asian STLV-1 macaque species clades, suggesting natural cross-species transmission. Novel viruses of Macaca maura, Macaca nigra and siamang cluster with other Sulawesian STLV-1s, demonstrating close relatedness among the STLV-1s in these insular species and suggesting cross-species transmission to a siamang in captivity. Viruses from Western chimpanzees and a Western lowland gorilla cluster within the HTLV-lb/STLV-1 clade, the latter close to a human strain, indicative of zoonosis. A new STLV-1 from Cercopithecus ascanius differs from the published STLV-Cas57, explainable by the existence of five geographically separated subspecies. Barbary macaques, not yet described to be STLV-infected, carry a relatively recent acquired, typical African STLV-1, giving us no clue on the phylogeographical origin of PTLV-1.