Macaca Nigra Research Articles

Successful adoption of non-orphaned infant by a parous, nursing female in yaki (Sulawesi crested macaque)

Abstract Adoption is an unusual behaviour across taxa, and for adoption to be successful, with the infant surviving to independence, the adoptive parent must be able to provide appropriate nutrition and care. Successful adoption has now been reported in several nonhuman primate species and here we add a case in wild yaki (Sulawesi crested macaque, Macaca nigra). We observed the adoption of an approx. 2-week-old infant by a female with her own approx. 3-week-old infant who went on to carry, nurse, and care for both infants until they both became independent. The adoptive and biological mother had each previously raised the same number of offspring (5). There was no evidence of aggressive transfer and we did not observe any attempts by the adopted infant’s biological mother to retrieve her. The biological mother went on to have another infant 8 months later while the adoptive mother was still caring for her other infant. This case may reflect some of the health costs and reproductive benefits of adoption for nonhuman primates.

Otolithiasis in the Animal Kingdom: A Retrospective Analysis.

If otolithiasis can be demonstrated to affect multiple species, it may be possible to identify an experimental animal for prospective study of this entity. Otolithiasis refers to dislodged otolithic matter within the confines of the membranous labyrinth that has the potential to cause clinical symptoms. The mechanism involves separation of free-floating otoconia that can affect the hearing and balance functions of the ear. While this process is known to occur in humans, it is uncertain if other species are affected. The published images of 37 whole-mount specimens of mammalian labyrinths were identified for retrospective examination. These were evaluated stereographically for the presence of calcareous material in abnormal locations within the membranous labyrinth. Thirty normal labyrinth specimens were found, exemplified by that of the Cape sea lion. Seven pathologic specimens were found, including a human, a black ape, a yellow-faced baboon, a hocheur monkey, a collie dog, a common sheep, and a common hare. Abnormal accumulations of calcareous material were found at one or more sites, more frequently in the utricle and canal system and less frequently in the endolymphatic and cochlea ducts. Otolithiasis appears to occur in other animal species besides the human. Abnormal calcareous material was found in various locations within the membranous labyrinth of affected animals. One or more of these might serve as an animal model to prospectively study the phenomenon of otolithiasis.

Integration-free induced pluripotent stem cells from three endangered Southeast Asian non-human primate species

Advanced molecular and cellular technologies provide promising tools for wildlife and biodiversity conservation. Induced pluripotent stem cell (iPSC) technology offers an easily accessible and infinite source of pluripotent stem cells, and have been derived from many threatened wildlife species. This paper describes the first successful integration-free reprogramming of adult somatic cells to iPSCs, and their differentiation, from three endangered Southeast Asian primates: the Celebes Crested Macaque (Macaca nigra), the Lar Gibbon (Hylobates lar), and the Siamang (Symphalangus syndactylus). iPSCs were also generated from the Proboscis Monkey (Nasalis larvatus). Differences in mechanisms could elicit new discoveries regarding primate evolution and development. iPSCs from endangered species provides a safety net in conservation efforts and allows for sustainable sampling for research and conservation, all while providing a platform for the development of further in vitro models of disease.

Conservation Yaki (Macaca nigra): The role of PT PGE TBK Lahendong Area on endemic wildlife conservation in North Sulawesi

This article discusses the role of Pertamina Geothermal Energy (PGE) Tbk. Area Lahedong in the Corporate Social Responsibility (CSR) program for the conservation of Yaki (Macaca nigra) in Tomohon City, North Sulawesi Province. The Yaki is endemic to North Sulawesi and is included in the Critically Endangered category on the red list of the International Union for Conservation of Nature and Natural Resources (IUCN). Every company has the obligation to carry corporate social and responsibility (CSR) in its operational area as has been regulated in the act of Corporation (PT) No. 40/2007. Throughout these years the company CSR programme often just aimed at people but often forgot that the surrounding environment also needed attention. Biodiversity conservation becomes crucial as it will give a positive impact to the sustainability of human life in the present as well as in the future. This study uses a descriptive qualitative method where data collection is carried out by observation, interviews, and documentation. The selection of informants was determined by purposive sampling. PGE Tbk. Area Lahedong is collaborating with the Yayasan Masarang and the Tasikoki Wildlife Rescue Center to carry out this conservation activity. The program will be implemented from 2020 until the release of 8 Yaki in 2023 and will continue again for the conservation of other Yaki groups. PGE Tbk. The Lahendong area has a role to accommodate activities during this program. Through this program, in addition to having an impact on increasing the Yaki population in their habitat, it can also become a media campaign for Yaki conservation to the public that Yaki are not food and must be preserved together as endemic animals to North Sulawesi.

Characteristics of sleeping sites and sleeping trees selected by Celebes crested macaques (Macaca nigra) in Tangkoko, North Sulawesi, Indonesia

Abstract. Qomariyah IN, Perwitasari-Farajallah D, Iskandar E, Berthier JM. 2023. Characteristics of sleeping sites and sleeping trees selected by Celebes crested macaques (Macaca nigra) in Tangkoko, North Sulawesi, Indonesia. Biodiversitas 24: 6200-6208. Research on the selection of sleeping sites is imperative in providing information on the fitness and survival of a species. We investigated the characteristics of the sleeping sites and the sleeping trees selected by wild Celebes crested macaques (Macaca nigra Desmarest 1822) in North Sulawesi, Indonesia, as well as their spatial and temporal use. The study was conducted in two groups of macaques for nine months (187 study days) from September 2020 to June 2021. These macaques avoided using the same sleeping site on consecutive nights. Two predator encounters (Python reticulatus Schneider 1801) were recorded near the sleeping sites, but pythons caught no monkeys during the study period. The macaques used 58 trees from 13 species as sleeping trees, of which 79% of the sleeping trees were also food trees. M. nigra chose sleeping trees with higher diameter, height, and a bigger Important Value Index than the surroundings. The average distance between sleeping trees and feeding trees in the morning and evening were 203 m and 127 m, respectively. These results suggest that optimal foraging strategy and predator avoidance are important factors in selecting sleeping sites, providing a broader understanding of the habitat preferences of the Critically Endangered M. nigra.

Effects of Tourist and Researcher Presence on Fecal Glucocorticoid Metabolite Levels in Wild, Habituated Sulawesi Crested Macaques (Macaca nigra).

Ecotourism managers and researchers often assume that apparently habituated primate groups no longer experience adverse consequences of prolonged exposure to tourists or researchers. We examined the effects of tourists and researchers on fecal glucocorticoid metabolite output (FGCM) in three critically endangered, wild crested macaque (Macaca nigra) groups in Tangkoko Nature Reserve, Sulawesi, Indonesia. We assayed FGCM from 456 fecal samples collected from thirty-three adults. Tourists can walk through and among macaque groups freely. Hence, we examined the possible effects of tourists both (1) in the reserve when away and not interacting with the study groups and (2) when they were present within the macaque groups. Generalized Linear Mixed Model (GLMM) analysis indicated that when tourists were present in the forest, but not directly among the macaques, FGCM levels in the macaque tourism groups were higher in months with more tourists. When tourists were among the macaque groups, some female macaques experienced rises and subsequent postexposure decreases in FGCM levels, consistent with predictions for acute stress. Male FGCM levels increased with tourist numbers within the group. Nevertheless, they were not significantly different from levels during undisturbed or postexposure conditions. FGCM responses related to researchers in groups varied by group, sex, and tourist presence. However, the temporal patterning of FGCM responses showed little evidence of chronic stress from tourism at this site.

Topography of cranial foramina and anaesthesia techniques of cranial nerves in selected species of primates (Cebidae, Cercopithecidae, Lemuridae) – part I – osteology

BackgroundConductive anaesthesia of the nerves around the head is one of the methods of intraoperative pain relief (under deep anaesthesia but before proceeding with the procedure). Performing this procedure on primates is especially challenging for the veterinarian, due to their cranial anatomy and topography, which has more in common with the human skull than with the skulls of other animals. Knowledge of key bony structures, including cranial foramina, is essential for effective anaesthesia of the cranial nerves.ResultsIn this study, the differences in the topography of the cranial foramina in eight selected species of primates were examined: Angola colobus (Colobus angolensis), Celebes crested macaque (Macaca nigra), L’Hoest’s monkey (Allochrocebus lhoesti), baboon (Papio cynocephalus), buff-bellied capuchin (Sapajus xanthosternos), black-and-white ruffed lemur (Varecia variegata), crowned lemur (Eulemur coronatus), and a ring-tailed lemur (Lemur catta) coming from the Wroclaw Zoological Garden (Poland). The cranial nerves running through the foramina have also been described and their anaesthesia techniques against bone points have been tested to relieve post-operative pain in the area of the head supplied by these nerves.ConclusionThe tests carried out show differences in the topography of the cranial foramina, and therefore also differences in the methods of injection, so the results obtained in this study may be useful in veterinary medicine, especially for practising veterinarians.

Factors Affecting the Outcome and Intensity of Intergroup Encounters in Crested Macaques (Macaca nigra)

Conspecific animal groups often compete for access to fitness-enhancing resources. The more valuable the resource at stake is, the greater the costs groups can afford to outcompete their neighbours, leading to between-group conflicts. We investigated what factors affected intergroup encounter outcome (win, loss, or draw) and intensity (level of aggression and duration) in wild, crested macaques (Macaca nigra). We collected data on 158 dyadic intergroup encounters among three groups of crested macaques in Tangoko Nature Reserve (Indonesia) between November 2015 and July 2016. Intergroup encounters were more likely to have a clear winner the larger the group size difference was between the opposing groups and when both groups rarely used the intergroup encounter location. Groups tended to win in specific parts of their home range, regardless of the numerical advantage, the frequency of use of the intergroup encounter location and its distance to the closest core area. Most encounters involved aggression, but contact aggression was rare. None of our candidate predictors helped to explain the differences in intergroup encounter escalation. Male intergroup aggression was more common than female intergroup aggression. The probability of female and male participation in intergroup aggression increased with the participation of the other sex. Males chased and attacked females in their group (i.e., herded them) in most encounters. Our study suggests that intragroup sexual conflict occurs during intergroup encounters in crested macaques. More detailed and longer studies on intergroup participation may help to understand the factors behind crested macaque intergroup encounter outcome and intensity.

Macaca nigra in the Spotlight: Accounting for Diversity in Behavior, Ecology, and Conservation in Primates

Macaca nigra in the Spotlight: Accounting for Diversity in Behavior, Ecology, and Conservation in Primates

Do Responses of Wild Macaca nigra to Crop Defense Resemble Responses to Predators?

Do Responses of Wild Macaca nigra to Crop Defense Resemble Responses to Predators?

Intrageneric taxonomic distinction based on morphological variation in the macaque (Macaca) skeleton.

Taxonomic classification is important for understanding the natural world, yet current methods for species assessment often focus on craniodental morphology rather than the entire skeleton. Moreover, it is currently unknown how much variation could, or should, exist intragenerically. Here, we tested whether taxonomy can be accurately predicted based on patterns of morphological variation in macaques (H1 ) and whether postcranial bones reflect subgeneric macaque taxonomy similarly, or better, than the cranium (H2 ). Data included 3D scans of cranial and postcranial bones for eight macaque species (Macaca arctoides, Macaca fascicularis, Macaca fuscata, Macaca mulatta, Macaca nemestrina, Macaca nigra, Macaca radiata, and Macaca sylvanus). Fixed anatomical and semilandmarks were applied to scans of eight skeletal elements (crania = 45; mandible = 31; scapula = 66; humerus = 38; radius = 33; os coxa = 28; femur = 40; tibia = 40). For each skeletal element, regression analyses were performed to minimize the effects of sexual dimorphism. Between-groups principal components analysis was used to visualize the major patterns of among-species morphological variation, while the strength of correct taxon classification was measured with discriminant function analysis. Results suggested accepting the alternate hypothesis that different macaque species can be distinguished morphologically. Both cranial and many postcranial elements appeared to possess a taxonomic signal, and the limb bones-especially the upper limb-are reported to be more useful for taxonomic assessment than previously realized. Theoretically, certain behaviors and/or ecogeographical factors, as well as phylogeny, influenced skeletal morphology in macaques, likely contributing to taxonomic distinctions among different species.

Do Wild, Male, Crested Macaques (Macaca nigra) Respond to the Screams of Infants Involved in Agonistic Interactions?

Males may increase their fitness by providing care to offspring or to unrelated infants of female “friends” to maximise future mating. The potential for paternal care depends on paternity certainty, particularly in multi-male, multi-female groups with polygynandrous mating. In crested macaques (Macaca nigra), there seems to be high potential for paternity certainty and need for paternal protection. However, male-mother affiliation (or “friendships”), not paternity, predicts male-infant affiliation, questioning whether males can identify their offspring reliably. Using a Bayesian approach, we investigated male responses to infant screams (N = 2,637) emitted during agonistic interactions with males being the friend of the infant, the friend of the infants’ mother, and/or the father of the infant. Overall, male responses to infant screams were low. Bayesian estimates showed considerable uncertainty; hence, results should be interpreted cautiously. However, males were slightly more likely to react if the infant or its mother was a friend of the male or if the infant was his offspring. Additionally, higher-ranking males were slightly more likely to respond than lower-ranking ones, and screams from infants of lower-ranking females were more likely to be responded to. This might indicate that males assess paternity based on their rank and that they assess the need to intervene. Given the limitations of our study and the uncertainty surrounding our results, future studies are needed before we can draw solid conclusions for crested macaques. Overall, our results are in line with other studies suggesting that male primates provide care to related and unrelated infants.

Climate, Temporal Abundance of Key Food Sources and Home Ranges of Crested Macaques (Macaca nigra) in Sulawesi, Indonesia: A Longitudinal Phenological Study

Climate change is associated with more frequent extreme weather conditions and an overall increase in temperature around the globe. Its impact on individual ecosystems is not yet well known. Long-term data documenting climate and the temporal abundance of food for primates are scarce. We used long-term phenological data to assess climate variation, fruit abundance and home range sizes of the endemic and Critically Endangered crested macaques (Macaca nigra) in Tangkoko forest, Sulawesi, Indonesia. Between January 2012 and July 2020, every month, we monitored 498 individual trees from 41 species and 23 families. We noted each tree’s phenophase and assessed variation in climate (daily temperature and rainfall) and fruit abundance. We also investigated whether individual trees of known key food sources for macaques (New Guinea walnut trees, Dracontomelon spp, two species, N = 10 individual trees; fig trees, Ficus spp, four species, N = 34, and spiked peppers, Piper aduncum, N = 4) showed regular and synchronised fruiting cycles. We used 2877 days of ranging data from four habituated groups to estimate home ranges between January 2012 and July 2020. We created models to evaluate the impact of ecological factors (temperature, rainfall, overall fruit abundance, fig abundance). We found that the temperature increased in Tangkoko forest, and the overall fruit abundance decreased across the study. Top key fruits showed different trends in fruiting. Figs seem to be present year-round, but we did not detect synchrony between individuals of the same species. The macaque home ranges were about 2 km2. Monthly temperature was the main predictor of home range size, especially in disturbed forest with previously burnt areas. This information will help to further monitor changes in the macaques’ habitat, and better understand ranging and foraging strategies of a Critically Endangered species and hence contribute to its conservation.

Investigating the Relationship Between Sociality and Reproductive Success in Wild Female Crested Macaques, Macaca nigra

Investigating the Relationship Between Sociality and Reproductive Success in Wild Female Crested Macaques, Macaca nigra

The influence of feeding routines on the behavior of zoo-housed Sulawesi crested black macaques (Macaca nigra).

Many species thrive in captivity, yet there is still much to be assessed regarding the often-unknown stressors present that can compromise welfare. Uncovering such stressors is of paramount importance if we are to ensure the zoo environment provides the highest levels of animal welfare that will contribute to species conservation. Zoo-housed primates are subject to many potential stressors, including daily husbandry routines which they may find aversive or habituate to, regardless of their outcome. The specific aim of this study was to assess the behavioral responses to daily husbandry feeding routines on a total of 33 Sulawesi crested black macaques (Macaca nigra), across two different UK zoological collections. Group scan sampling was used to record behaviors for 30-minperiods before feeding (BF), for 30 min after feeding (AF), which we began 30 min after feed provision, and for 30 min when no feeding occurred (NF). The feeding condition significantly influenced behaviors recorded and post-hoc comparisons showed that BF conditions produced significantly higher frequencies of food anticipatory related activity (FAA). Furthermore, during BF periods, behaviors associated with FAA increased during the 15 min closer to a feed. This research finds that temporal feeding events cause changes in the behavior of two independent groups of crested macaques, indicative of food anticipation activity, during 30-minperiods leading up to a feed. These results have implications for how animal keeper routines and advertised zoo feeds are managed for this species within zoological collections.

The Link Between Personality, Subjective Well-being, and Welfare in Zoo-Housed Sulawesi Crested Macaques (Macaca nigra)

The Link Between Personality, Subjective Well-being, and Welfare in Zoo-Housed Sulawesi Crested Macaques (Macaca nigra)

Ten Years of Positive Impact of a Conservation Education Program on Children's Knowledge and Behaviour Toward Crested Macaques (Macaca nigra) in the Greater Tangkoko Area, North Sulawesi, Indonesia

In areas where primates are threatened, environmental education interventions are a key way to increase the local population’s knowledge of their environment and encourage positive attitudes and habits to preserve the environment and wildlife on a local and global scale. This study assesses the impact of Tangkoko Conservation Education (TCE), the Macaca Nigra Project’s conservation education programme, running since 2011 in North Sulawesi for school children, teachers, and the local population. TCE’s goal is to help people increase their knowledge of their environment and develop more positive habits and behaviours towards their local environment, especially the Critically Endangered and endemic crested macaques (Macaca nigra). We measured the efficacy of TCE’s programme for pupils using questionnaires provided one month before and one month after a year-long conservation education programme at school. Pupils’ knowledge and behaviour scores increased significantly after their participation in the programme. Their habits score also increased but this increase was not statistically significant. Girls scored significantly higher than boys in terms of positive behaviour towards wildlife. Children participating in the programme more than once seemed to obtain higher scores in their second participation, although the sample size was too small for formal analysis. Despite some limitations, this study demonstrates the positive impact of our programme on young people living in an area where primates are threatened. We hope that this research will inspire similar programmes in Sulawesi and elsewhere by providing methods and activities to help prevent primate extinction.

The Sexual Selection Landscape and Sexually-Selected Traits of the Crested Macaque (Macaca nigra)

The Sexual Selection Landscape and Sexually-Selected Traits of the Crested Macaque (Macaca nigra)

The existence of black macaque (Macaca nigra) population in Bogani Nani Wartabone National Park, Bolaang Mongondow, North Sulawesi of Indonesia: The valuable economical investment of the endemic fauna in the forest environmental sustainability

The existence survey of the black macaque (Macaca nigra) population was conducted at the Bogani Nani Wartabone National Park (BNWNP), Bolaang Mongondow, and North Sulawesi of Indonesia from December 2021 to November 2022. The survey using line transect by ‘Complete Count’ method was used to determine population size. The direct observations and questionnaire surveys of the local people were applied to identify the potential threats to the macaque existence. The population comprised 183 individuals from four multimale-multifemale groups and fourteen solitary individuals. The group density was 1.22 groups/km2, and the group size ranged from 34 to 55 individuals (mean of 42.25 ± 9.53). The mean ratio of adults to non-adults were 1:1.35, and the adult male to female ratio was 1:0.96. Macaca nigra was observed to forage and sleep inside range forest adjacent to the limited production forest. The survival of the macaque was threatened by the habitat loss, fragmentation, illegal logging and illegal mining. Other local human activities in opening forest for clove plantation were identified as potential stressors. Therefore, it should be recommended strictly to implement the existing management plan by the Directorate General of Natural Resources Conservation of the Republic of Indonesia. The monitoring and strengthening the capacity of forest departmental staffs should be focused to conserve the endemic fauna including M. nigra and flora vegetation of the animals’ habitats as the valuable economical investment in the forest environmental sustainability of the BNWNP.

RECTAL PROLAPSE IN THE SULAWESI CRESTED BLACK MACAQUE (MACACA NIGRA): MORBIDITY, MORTALITY, AND RISK FACTORS.

Empirical data suggest that rectal prolapse (RP) is common in captive Sulawesi crested black macaques (Macaca nigra) in Europe, resulting in the euthanasia of animals that experience repeat occurrences. However, the prevalence, etiology, and risk factors of RP remain unidentified. The aims of this retrospective study were to assess the morbidity and mortality of RP, to provide an overview of management practices, and to identify risk factors for RP in this species. A questionnaire was sent to all European Ex situ Programme institutions that housed M. nigra between 01 January 2014 and 31 December 2020. Zoological Information Management System medical records and the studbook were used to obtain additional information. The questionnaire had a response rate of 65%, accounting for 204 animals. Of these animals, 25 (12.3%) suffered from at least one RP event during the study period and recurrence was noted in 72%. The majority of prolapses reverted naturally, but 28% of afflicted animals were euthanized for this ailment. Institutions with M. nigra with high frequencies of diarrhea (P= 0.035), those that provided diets of ≥90% vegetables and high-fiber pellet (P < 0.001), and those with more male than female M. nigra (P < 0.001) had increased odds of RP. Institutions that provided fruits daily (P < 0.002) had reduced odds of having RP cases. Although correlation of RP with diet was identified, confounding cannot be excluded, and a detailed dietary analysis needs to take place before altering feeding practices. Acute stressors and detection of protozoa in fecal samples were common findings before an RP event. Demographic analysis indicated that aged females, young males, and subordinate individuals were most affected by this condition. Where tested during an RP intervention, animals had low serum levels of vitamin D. Pedigree analysis hinted at genetic predisposition in this species and requires further investigation.