- Duboscq, J., Micheletta, J. Macaca nigra in the Spotlight: Accounting for Diversity in Behavior, Ecology, and Conservation in Primates. Int J Primatol 44, 1026–1041 (2023). DOI. Abstract
Long-term studies of well-identified individuals and improved methodologies have advanced primate behavioral ecology, genetics, and physiology (Kappeler & Watts,
2012; Sheldon
et al.,
2022). However, model species are few and we need to focus on less studied taxa to assess the general validity of theoretical models and to account for the extraordinary level of variation in primate ecology and behavior (Bezanson & McNamara,
2019). In this Special Issue, we focus on such a primate species, moreover one that is Critically Endangered: the crested macaque
Macaca nigra. We also take this opportunity to celebrate 17 years of activity of a long-term project, the Macaca Nigra Project (MNP), in North Sulawesi, Indonesia, where the crested macaque is endemic. We start by retracing the history of the MNP, situating the project, the studies, and the species in its environment. We then take stock of past, present, and future research from various perspectives with nine original contributions. Now more than ever, this is important given the particular place of crested macaques in the primate radiation, and the bleak outlook for their survival. We also use the opportunity to celebrate the great resilience of people participating in the conservation of the species.
- Chanvin, M., Lamarque, F., Diko, N. et al. 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. Int J Primatol 44, 743–763 (2023) DOI. Abstract
In areas where primates are threatened, environmental education interventions are one decisive route to increase local population’s knowledge and thus encourage their positive attitudes and habits to be able to preserve the environment and wildlife on a local and global scale. This study assesses the impact of Tangkoko Conservation Education (TCE), the conservation education programme of the Macaca Nigra Project, running since 2011 in North Sulawesi for school children, teachers, and the local population. TCE’s aim is to help them improve their knowledge, 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 on pupils using questionnaires provided one month before and one month after a yearlong conservation education programme at school. Pupils’ knowledge and behaviour scores significantly increased after their participation in the programme. Their habits score also improved but this increase was not statistically significant. Female pupils scored significantly higher than male pupils 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 a formal analysis. Despite some limitations, this study demonstrates the positive impact of our programme on young people living in areas where primates are threatened. We hope that this research will inspire similar programmes based in Sulawesi.
- Bertrand, D.A., Berman, C.M., Agil, M. et al. Do Responses of Wild Macaca nigra to Crop Defense Resemble Responses to Predators?. Int J Primatol 44, 791–817 (2023). DOI. Abstract
Although conservation-minded researchers advocate that growers use a variety of methods to defend crops from wildlife, we know little about the effects of such methods on the targeted species. We assessed effects of nonlethal crop defense (CD) methods used in Tangkoko Reserve, Sulawesi, Indonesia, on potentially stress-related behavior of Critically Endangered (CR) wild, crested macaques (Macaca nigra). We examined responses of three groups exposed to different amounts of CD, both immediately after being targeted and when only exposed to cues of targeting elsewhere in the forest. We analyzed 630 h of data from 33 adults of both sexes by using Generalized Linear Mixed Models. When not targeted, all groups and both sexes displayed fewer self-directed behaviors, males showed fewer affiliative behaviors, and two groups decreased aggression in months with more CD. When we compared behavior immediately after targeting with behavior unassociated with targeting, males in the most frequently targeted group showed increased aggression, whereas both sexes in the moderately frequently targeted group showed increased self-directed behaviors. We suggest that when not targeted, groups show a degree of behavioral inhibition during months in which CD targeting is relatively frequent. When targeted, the two regularly targeted groups displayed behavior consistent with increased stress. However, the groups appeared to respond in qualitatively different ways. We tentatively suggest that the macaques’ behavioral responses to CD (inhibition in low-risk conditions and signs of stress and/or motivational conflict in moderate-risk conditions) resemble typical responses of primates to perceived predators posing varying degrees of risk.
- Rismayanti, R., Perwitasari-Farajallah, D., Cahyaningrum, E. et al. Exploring Strategic Functions of Sleeping Sites in Crested Macaques (Macaca nigra): Evidence from Intergroup Encounters. Int J Primatol 44, 722–742 (2023). DOI. Abstract
In gregarious animals, competition for resources, such as water, food, and shelter, is common. Sleeping sites are one such resource that also may serve strategic functions, such as food or group defense. We investigated whether groups of wild crested macaques (Macaca nigra) compete for sleeping sites and two potential strategic functions of these sites: food defense and group protection. We gathered data from three habituated groups (Pantai Batu 1, Rambo 1, and Rambo 2) in Tangkoko Nature Reserve in North Sulawesi, Indonesia. We collected information on sleeping site use between October 2015 and June 2016, for 192, 156, and 41 nights, for each group respectively. We recorded 229, 207, and 183 travel routes for the three study groups and used these to calculate their home ranges and core areas using Brownian Bridge Movement Models. We also documented 304 intergroup encounters (IGE) among the three habituated groups and their neighbors. We found that suitable sleeping sites for crested macaques are limited, frequently reused, and shared sequentially, but not used simultaneously. There was a strong link between core areas and sleeping site density. However, we found no significant relationship between high IGE risk areas and sleeping site density, nor between core or high IGE risk areas and sleeping site reuse frequency. The study found no correlation between the distance traveled post-encounter to sleeping sites and the encounter’s outcome or intensity. Overall, our study adds to the evidence that primates are selective in choosing sleeping sites, whose additional functions might be population specific.
- Martínez-Íñigo, L., Rismayanti, Engelhardt, A. et al. Factors Affecting the Outcome and Intensity of Intergroup Encounters in Crested Macaques (Macaca nigra). Int J Primatol 44, 696–721 (2023). DOI. Abstract
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.
- Kerhoas, D., Kulik, L., Perwitasari-Farajallah, D. et al. Do Wild, Male, Crested Macaques (Macaca nigra) Respond to the Screams of Infants Involved in Agonistic Interactions?. Int J Primatol 44, 626–648 (2023). DOI. Abstract
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.
- Joly, M., Tamengge, M., Pfeiffer, JB. et al. Climate, Temporal Abundance of Key Food Sources and Home Ranges of Crested Macaques (Macaca nigra) in Sulawesi, Indonesia: A Longitudinal Phenological Study. Int J Primatol 44, 670–695 (2023). DOI. Abstract
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.
- Duboscq, J., Micheletta, J., Perwitasari-Farajallah, D. et al. Investigating the Relationship Between Sociality and Reproductive Success in Wild Female Crested Macaques, Macaca nigra. Int J Primatol 44, 649–669 (2023). DOI. Abstract
Studying the link between sociality and fitness is valuable to understand the costs and benefits of sociality. In many species, sociality is positively linked to fitness: having more, stronger, more equitable or predictable affiliative relationships leads to higher reproductive success, greater survival, or longevity, at least in females. We tested this sociality-fitness link in wild, female, crested macaques, Macaca nigra, in Tangkoko, North Sulawesi, Indonesia. Over 15 years, we studied six groups and collected behavioral, ecological, and demographic data on 140 females. We modeled the annual probability that females gave birth as a function of grooming rate with other females, adjusting for a number of control variables. We found no evidence for an overall association between grooming and the probability of giving birth. Further exploration of the results revealed large uncertainties in the model estimates and substantial idiosyncratic variation within and between females, and to a lesser extent, years and groups. This may have to do with constraints imposed on grooming, on reproduction, or on both. Further investigations into the significance and sources of this variation will help to disentangle the pathways by which social interactions with other group members relate to fitness outcome.
- Higham, J.P. The Sexual Selection Landscape and Sexually-Selected Traits of the Crested Macaque (Macaca nigra). Int J Primatol 44, 613–625 (2023). DOI. Abstract
Sexual selection explains the evolution of traits that impact mating and reproductive success. Primates are an excellent system for studying sexually-selected traits, because they exhibit marked variation in mating systems, show evidence of intrasexual competition in both sexes, and mutual mate choice. Here, I discuss the sexual selection dynamic of the crested macaque (Macaca nigra) and its overall putative sexually-selected phenotype. Female crested macaque fertile phases are highly asynchronous, which alpha males monopolize, leading to high reproductive skew. Given the reproductive benefits to alpha status, males compete aggressively over dominance, with all observed alpha male replacements occurring via top-entry challenge competition. Infant disappearances increase after the arrival of a new alpha male, indicating potential infanticide from incoming males. Consistent with strong male-male contest competition, crested macaques exhibit marked body and canine size sexual dimorphism, with males being larger. Males exhibit small relative testis volume, indicating that indirect competition via sperm competition is not prevalent. Male-male relationships are mediated by social status signals, including loud calls and colorful genitals, and males largely avoid each other. Female-female relationships are generally affiliative with low levels of aggression. Females exhibit direct mate choice in the form of some consortship maintenance, and also exhibit a number of proceptive behaviors towards males, which increase in frequency markedly during fertile phases. Females exhibit traits that may facilitate indirect mate choice, including copulation calls and large sexual swellings. Our understanding of the species enables us to set the crested macaque into comparative context, and to characterize many of its traits as part of a holistic sexually-selected phenotype.