Detection of viruses from feces of wild endangered Macaca maura: a potential threat to moor macaque survival and for zoonotic infection.

BACKGROUND: To date, there is a scarcity of information and literature on Macaca maura health status relative to viral diseases. The objectives of the present study were to investigate on the potential spread of enteric and non-enteric viruses shed in the environment through a wild macaque feces and to understand the possible interrelation in the spread of zoonotic viruses in a poorly studied geographical area, the Sulawesi Island. This study will also contribute providing useful information on potential threats to the health of this endangered species. METHODS: The sampling was conducted between 2014 and 2016 in the Bantimurung Bulusaraung National Park, in the south of the Sulawesi Island and non-invasive sampling methods were used to collect fresh stools of the M. maura, one of the seven macaque species endemic to the island of Sulawesi, Indonesia. The population under study consisted in two wild, neighboring social macaque groups with partially overlapping home ranges; twenty-four samples were collected and examined using negative staining electron microscopy and a panel of PCR protocols for the detection of ten RNA and two DNA viruses. RESULTS: Viral particles resembling parvovirus (5 samples), picornavirus (13 samples) and calicivirus (13 samples) were detected by electron microscopy whereas the PCR panel was negative for the 12 viruses investigated, except for one sample positive for a mosquito flavivirus. The results did not correlate with animal sex; furthermore, because all of the animals were clinically healthy, it was not possible to correlate feces consistency with viral presence. CONCLUSIONS: As information on viral infections in wild moor macaques remains limited, further studies are yet required to identify the fecal-oral and blood transmitted potentially zoonotic viruses, which may infect the moor macaque and other macaque species endemic to the South Sulawesi Island.

Roadside monkeys: anthropogenic effects on moor macaque (Macaca maura) ranging behavior in Bantimurung Bulusaraung National Park, Sulawesi, Indonesia.

A growing body of research focuses on how anthropogenic factors affect the behavior and ecology of primates and their ecosystems. Infrastructural development, such as roads, is an increasingly pervasive anthropogenic impact that destroys primate habitat, affects the distribution and dispersal of primates, and facilitates human-primate interactions. At our field site in Bantimurung-Bulusaraung National Park, Sulawesi, Indonesia, a major road bisects the habitat of the endangered moor macaque (Macaca maura). Beginning in 2015, we observed a behavioral shift by our main study group: they began spending more time along the road foraging in trash pits and waiting for provisions from vehicles. Our objective in this study was to examine how access to anthropogenic foods has affected the group's ranging behavior by comparing ranging data collected before (2010-2011) and after the shift (2016-2017). In contrast to what we expected, home ranges were significantly larger and daily travel distance was significantly longer after the shift compared to before. As predicted, mean distance to the road decreased after the shift. These results likely reflect the irregular and spatially dispersed nature of provisioning at this site. The macaques appear to be attracted to the road because it presents opportunities to obtain palatable and energy-dense foods. Our results indicate that moor macaques are able to flexibly adjust their ranging behavior in response to anthropogenic impacts. However, given the risks of being in proximity to roads and humans, management of this emerging human-macaque interface is needed.

Dominance style predicts differences in food retrieval strategies.

In several species, rank predicts access to food, and subordinates may need specific behavioural strategies to get a share of resources. This may be especially important in despotic species, where resources are strongly biased in favour of dominants and subordinates may more strongly rely on specific tactics to maximize food intake. Here, we compared three macaque species with an experimental set-up reproducing feeding competition contest. Following our predictions, more tolerant species mostly retrieved food in the presence of others and were less dependent on specific tactics. Contrarily, subordinates in more despotic species more likely collected food (1) when dominants could not see food or (2) were attacking others, (3) while "dissimulating", or (4) "storing food". Our study reveals that dominance styles reliably predict the probability of using specific food retrieval tactics and provides important insights on the social conditions that might have led to the emergence of tactical deception.

Dominance style only partially predicts differences in neophobia and social tolerance over food in four macaque species.

Primates live in complex social systems with social structures ranging from more to less despotic. In less despotic species, dominance might impose fewer constraints on social choices, tolerance is greater than in despotic species and subordinates may have little need to include novel food items in the diet (i.e. neophilia), as contest food competition is lower and resources more equally distributed across group members. Here, we used macaques as a model to assess whether different dominance styles predict differences in neophilia and social tolerance over food. We provided familiar and novel food to 4 groups of wild macaques (N = 131) with different dominance styles (Macaca fuscata, M. fascicularis, M. sylvanus, M. maura). Our study revealed inter- and intra-specific differences in individuals' access to food, which only partially reflected the dominance styles of the study subjects. Contrary to our prediction, social tolerance over food was higher in more despotic species than in less despotic species. Individuals with a higher dominance rank and being better socially integrated (i.e. higher Eigenvector centrality) were more likely to retrieve food in all species, regardless of their dominance style. Partially in line with our predictions, less integrated individuals more likely overcame neophobia (as compared to more integrated ones), but only in species with more tolerance over food. Our study suggests that individual characteristics (e.g. social integration or personality) other than dominance rank may have a stronger effect on an individual's access to resources.

Activity budget, home range, and habitat use of moor macaques (Macaca maura) in the karst forest of South Sulawesi, Indonesia.

Primate behavior can be responsive to the different ecological pressures associated with different habitats, as well as to the effects of direct and indirect anthropogenic disturbance. The karst forest ecosystem of South Sulawesi (Indonesia) represents one of the few intact forests available for residual populations of the moor macaque, but our understanding of its habitat use is limited. In the present study, this gap in knowledge was addressed by observing the activity and habitat use of two groups of moor macaques and by assessing the suitability of different habitats in the karst forest. Through a fine-scale vegetation analysis of 1 ha of forest in Bantimurung Bulusaraung National Park, we identified the presence of two distinct habitats that differ in terms of forest structure and composition. The karst plain forest (KPF) provided a greater abundance and diversity of food resources than the karst tower forest (KTF). In addition, anthropogenic disturbance was high in the KPF but low in the KTF. Behavioral data collected via group scans indicate that the macaques devoted more time to feeding activities when in the KPF, suggesting an ability to adjust their feeding behavior to meet their nutritional needs. However, the larger of the two groups used the food-rich KPF more than expected, implying that the KTF may represent a valuable refuge for the smaller group, as it is a less risky portion of its home range. The results of this study therefore provide novel information on the ecology of moor macaques and their habitats that can inform conservation planning for remnant populations.

Interactions with humans are jointly influenced by life history stage and social network factors and reduce group cohesion in moor macaques (Macaca maura).

Human-wildlife encounters are becoming increasingly frequent across the globe, often leading people to interact with and feed wild animals and impacting animal behaviour and ecology. Although the nature of human-wildlife interactions has been well documented across a number of species, we still have limited understanding as to why some individual animals interact more frequently with humans than others. Additionally, we lack a comprehensive understanding of how these interactions influence animal social networks. Using behavioural data from a group of moor macaque monkeys (Macaca maura), we used permutation-based linear regression analyses to understand how life history and social network factors jointly explain interindividual variation in tendency to interact with humans along a provincial road in South Sulawesi, Indonesia. As our study group spent only a portion of their time in proximity to humans, we also examined how social network structure changes in response to human presence by comparing social networks in the forest to those along the road. We found that sex, individual network position, and associate network position interact in complex ways to influence individual behaviour. Individual variation in tendency to be along the road caused social networks to become less cohesive when in proximity to humans. This study demonstrates that nuanced intragroup analyses are necessary to fully understand and address conservation issues relating to human-wildlife interactions.