Flexible use of simple and combined calls in female Campbell's monkeys

Research has been funded by the French Ministry of Research, the French University Institute (IUF), the National Agency for research (ANR ‘Orilang’) and the European Union's Seventh Framework Programme (FP7/2007-2013) / ERC grant agreement n° 283871 (prilang).Call combinations allow animals to expand the communicative power of small repertoires with acoustically inflexible elements. In Campbell's monkeys, Cercopithecus campbelli, males possess a small repertoire of calls that can be merged to an acoustically invariable suffix and which are concatenated into various sequences, mainly in response to external disturbances. The vocal repertoire of adult females has been less well studied although it is much richer, containing both alarm and various social calls. In particular, females possess a low-pitched contact call, produced either alone or merged with a high-pitched, arched unit. Combined contact calls are identity-richer and easier to detect than simple calls. Here, we investigated the socioecological factors that determined the production of single and combined utterances and found that combined utterances were more common when identity was relevant such as in mixed-species associations and during socially important vocal exchanges. In contrast, single calls were used mainly when predation risk was high, as part of this species' generally cryptic antipredator strategy. We discuss these finding in the light of current theories regarding the evolution of combinatorial signalling.PostprintPeer reviewe

Social and Ecological Correlates of Parasitic Infections in Adult Male Gray-Cheeked Mangabeys (Lophocebus albigena)

International audienceIntestinal parasites may constitute an important evolutionary and ecological force. We aimed to identify social, physiological, and environmental factors that correlate with intestinal parasite infections in adult male gray-cheeked mangabeys (Lophocebus albigena). We analyzed 102 fecal samples collected from 18 adult males over 19 mo for the incidence (proportions of samples with parasites) and intensity (total number of parasites per gram of feces) of infection of nematodes relative to social status, fecal glucocorticoid and testosterone metabolites, group size, and rainfall, all of which are factors that earlier studies suggested can be important mediators of parasite load. Parasite incidence was greater in immigrant males compared to low- and high-ranking males whereas parasite intensity was greater in immigrant males and low-ranking males compared to high-ranking males. Fecal samples with more parasites had higher concentrations of fecal glucocorticoid and testosterone metabolites than those with fewer parasites. As immigrant males had a greater incidence of parasites and higher concentrations of both metabolites than resident males, this profile appears to fit immigrant males best. We also found higher nematode intensities in mid-sized groups and during periods with more rainfall. Our results suggest that it will be fruitful for future studies to explore the role of immigrant males as spreaders of intestinal parasites

Implementing social network analysis to understand the socioecology of wildlife co-occurrence and joint interactions with humans in anthropogenic environments

This is an accepted manuscript of an article published by Wiley in Journal of Animal Ecology on 28/08/2021, available online: https://doi.org/10.1111/1365-2656.13584 The accepted version of the publication may differ from the final published version.Human population expansion into wildlife habitats has increased interest in the behavioural ecology of human-wildlife interactions. To date, however, the socio-ecological factors that determine whether, when or where wild animals take risks by interacting with humans and anthropogenic factors still remains unclear. 2.We adopt a comparative approach to address this gap, using social network analysis (SNA). SNA, increasingly implemented to determine human impact on wildlife ecology, can be a powerful tool to understand how animal socioecology influences the spatiotemporal distribution of human-wildlife interactions. 3.For 10 groups of rhesus, long-tailed, and bonnet macaques (Macaca spp.) living in anthropogenically-impacted environments in Asia, we collected data on human-macaque interactions, animal demographics, and macaque-macaque agonistic and affiliative social interactions. We constructed ‘human co-interaction networks’ based on associations between macaques that interacted with humans within the same time and spatial locations, and social networks based on macaque-macaque allogrooming behaviour, affiliative behaviours of short duration (agonistic support, lip-smacking, silent bare-teeth displays, and non-sexual mounting), and proximity. 4.Pre-network permutation tests revealed that, within all macaque groups, specific individuals jointly took risks by repeatedly, consistently co-interacting with humans64within and across time and space. GLMMs revealed that macaques’ tendencies to co-interact with humans was positively predicted by their tendencies to engage in short-duration affiliative interactions and tolerance of conspecifics, although the latter varied across species (bonnets>rhesus>long-tailed). Male macaques were more likely to co-interact with humans than females. Neither macaques’ grooming relationships nor their dominance ranks predicted their tendencies to co-interact with humans. 5.Our findings suggest that, in challenging anthropogenic environments, less (compared to more) time-consuming forms of affiliation, and additionally greater social tolerance in less ecologically flexible species with a shorter history of exposure to humans, may be key to animals’ joint propensities to take risks to gain access to resources. For males, greater exploratory tendencies and less energetically demanding long-term life-history strategies (compared to females), may also influence such joint risk-taking. From conservation and public health perspectives, wildlife connectedness within such co-interaction networks may inform interventions to mitigate zoonosis, and move human-wildlife interactions from conflict towards co-existence.The authors were supported by the U.S. National Science Foundation (Grant no. 1518555) awarded to PI McCowan

Individuals in urban dwelling primate species face unequal benefits associated with living in an anthropogenic environment

In primates, living in an anthropogenic environment can significantly improve an individual’s fitness, which is likely attributed to access to anthropogenic food resources. However, in non-professionally provisioned groups, few studies have examined whether individual attributes, such as dominance rank and sex, affect primates’ ability to access anthropogenic food. Here, we investigated whether rank and sex explain individual differences in the proportion of anthropogenic food consumed by macaques. We observed 319 individuals living in nine urban groups across three macaque species. We used proportion of anthropogenic food in the diet as a proxy of access to those food resources. Males and high-ranking individuals in both sexes had significantly higher proportions of anthropogenic food in their diets than other individuals. We speculate that unequal access to anthropogenic food resources further increases within-group competition, and may limit fitness benefits in an anthropogenic environment to certain individuals.This work was supported by the U.S. National Science Foundation (Grant no. 1518555)

Impact of individual demographic and social factors on human-wildlife interactions: a comparative study of three macaque species

© 2020 The Authors. Published by Springer Nature. This is an open access article available under a Creative Commons licence. The published version can be accessed at the following link on the publisher’s website: https://doi.org/10.1038/s41598-020-78881-3Despite increasing conflict at human-wildlife interfaces, there exists little research on how the attributes and behavior of individual wild animals may influence human-wildlife interactions. Adopting a comparative approach, we examined the impact of animals’ life-history and social attributes on interactions between humans and (peri)urban macaques in Asia. For 10 groups of rhesus, long-tailed, and bonnet macaques, we collected social behavior, spatial data, and human-interaction data for 11-20 months on pre-identified individuals. Mixed-model analysis revealed that, across all species, males and spatially peripheral individuals interacted with humans the most, and that high-ranking individuals initiated more interactions with humans than low-rankers. Among bonnet macaques, but not rhesus or long-tailed macaques, individuals who were more well-connected in their grooming network interacted more frequently with humans than less well-connected individuals. From an evolutionary perspective, our results suggest that individuals incurring lower costs related to their life-history (males) and resource-access (high rank; strong social connections within a socially tolerant macaque species), but also higher costs on account of compromising the advantages of being in the core of their group (spatial periphery), are the most likely to take risks by interacting with humans in anthropogenic environments. From a conservation perspective, evaluating individual behavior will better inform efforts to minimize conflict-related costs and zoonotic-risk

Long-term Site Fidelity and Individual Home Range Shifts in Lophocebus albigena

We investigated long-term site fidelity of gray-cheeked mangabey (Lophocebus albigena) groups in Kibale National Park, Uganda. Concurrently, we monitored shifts in home range by individual females and subadult and adult males. We documented home range stability by calculating the area of overlap in successive years, and by recording the drift of each group’s monthly centroid from its initial location. Home ranges remained stable for 3 of our 4 groups (overlap over 10 yr >60%). Core areas were more labile, but group centroids drifted an average of only 530 m over the entire decade. Deviations from site fidelity were associated with dispersal or group fission. During natal dispersal, subadult males expanded their home ranges over many months, settling ≤4 home ranges away. Adult males, in contrast, typically dispersed within a few days to an adjacent group in an area of home range overlap. Adult males made solitary forays, but nearly always into areas used by their current group or by a group to which they had previously belonged. After secondary dispersal, they expanded their ranging in the company of their new group, apparently without prior solitary exploration of the new area. Some females also participated in home range shifts. Females shifted home ranges only within social groups, in association with temporary or permanent group splits. Our observations raise the possibility that male mangabeys use a finder-joiner mechanism when moving into new home ranges during secondary dispersal. Similarly, females might learn new resource locations from male immigrants before or during group fission

Correlations between Social Context and Fecal Glucocorticoid Metabolite Concentrations in Free-ranging Female Gray-cheeked Mangabeys (Lophocebus albigena) in Kibale National Park, Uganda

International audienceAn elevated concentration of glucocorticoids is an indicator of stress, and chronically high glucocorticoid levels are often associated with poor health and reduced fertility.We explored conditions that might be stressors in the lives of adult female gray-cheeked mangabeys (Lophocebus albigena) by measuring fecal glucocorticoid metabolites (fGCM) concentrations. During a six-month study we collected 109 fecal samples from 28 adult females from five groups in Kibale National Park, Uganda. We examined fecal fGCM levels of individual females relative to their own reproductive status (cycling or not cycling) and that of other females and to the presence of newcomer (immigrant) males. We found elevated fGCM concentrations in females when other females in their groups were at the peak of sexual swelling, and when immigrant males joined the group

Maternal Investment and Infant Survival in Gray-Cheeked Mangabeys (Lophocebus albigena)

International audienceDifferences among females in infant survival can contribute substantially to variance in fitness. Infant survival is a product of external risk factors and investment by kin, especially the mother, and is thus closely tied with the evolution of behavior and life history. Here we present a 9-yr study (2004–2012) of infant survival and sex ratio relative to age and dominance ranks of mothers and the presence of immigrant males in a free-ranging population of gray-cheeked mangabeys (Lophocebus albigena) in Kibale National Park, Uganda.We consider immigrant males because they are known to increase infant mortality in several other species.We found that infants of older mothers had higher survival than those of younger mothers but that high rank did not confer a significant benefit on infant survival. Female infants had higher survival than male infants. Young, low-ranking females had more male infants than young, high-ranking females, which had slightly more daughters, but this difference declined as females aged because low-ranking females had more daughters as they aged. With limited data, we found a significantrelationship between the presence of male immigrants and infant mortality (falls and unexplained disappearances) to 18 mo. Our results suggest that infant survival in graycheeked mangabeys is most precarious when mothers must allocate energy to their own growth as well as to their infants, that sons of young mothers are at greatest risk, and that immigrant males can negatively affect infant survival

Impact of joint interactions with humans and social interactions with conspecifics on the risk of zooanthroponotic outbreaks among wildlife populations.

Pandemics caused by pathogens that originate in wildlife highlight the importance of understanding the behavioral ecology of disease outbreaks at human-wildlife interfaces. Specifically, the relative effects of human-wildlife and wildlife-wildlife interactions on disease outbreaks among wildlife populations in urban and peri-urban environments remain unclear. We used social network analysis and epidemiological Susceptible-Infected-Recovered models to simulate zooanthroponotic outbreaks, through wild animals' joint propensities to co-interact with humans, and their social grooming of conspecifics. On 10 groups of macaques (Macaca spp.) in peri-urban environments in Asia, we collected behavioral data using event sampling of human-macaque interactions within the same time and space, and focal sampling of macaques' social interactions with conspecifics and overall anthropogenic exposure. Model-predicted outbreak sizes were related to structural features of macaques' networks. For all three species, and for both anthropogenic (co-interactions) and social (grooming) contexts, outbreak sizes were positively correlated to the network centrality of first-infected macaques. Across host species and contexts, the above effects were stronger through macaques' human co-interaction networks than through their grooming networks, particularly for rhesus and bonnet macaques. Long-tailed macaques appeared to show intraspecific variation in these effects. Our findings suggest that among wildlife in anthropogenically-impacted environments, the structure of their aggregations around anthropogenic factors makes them more vulnerable to zooanthroponotic outbreaks than their social structure. The global features of these networks that influence disease outbreaks, and their underlying socio-ecological covariates, need further investigation. Animals that consistently interact with both humans and their conspecifics are important targets for disease control