Laëtitia Maréchal

Recognition of faces of known individuals in two lemur species (Eulemur fulvus and E. macaco)

Three brown lemurs, Eulemur fulvus, and two black lemurs, Eulemur macaco, were trained to select consistently the photograph of the face of a known individual (KI: belonging to the same social group) when it was presented simultaneously with a photograph of the face of an unfamiliar individual (UI: belonging to another social group). After the learning phase, the subjects were presented with new pairs of photographs (KI versus UI: photographs that were not used in the learning phase), the same pairs presented in different associations, and finally pairs of photographs that were completely novel (50 different pairs). All the subjects selected the KI significantly more often than the UI under all conditions. Additional tests showed that the subjects preferentially selected photographs of a UI belonging to their own species versus a UI belonging to the other species. No preference was observed when the subjects were presented with two KI or with their own photograph associated with a UI. These results reveal that the face contains information allowing lemurs to discriminate familiar individuals from unfamiliar ones.

Assessing the Effects of Tourist Provisioning on the Health of Wild Barbary Macaques in Morocco

Feeding wildlife is a very popular tourist activity, largely because it facilitates the close observation of animals in their natural habitat. Such provisioning may benefit animals by improving their survival and reproductive success, especially during periods of natural food shortage. However, provisioning by tourists may also have negative impacts on the health of the animals involved; to date such impacts are poorly understood. Here, we investigated the effects of tourist provisioning on the health of wild adult Barbary macaques, Macaca sylvanus, in Morocco. We compared health measures between a heavily provisioned group and a group that received negligible food from tourists and, in the former group, we also assessed health measures in relation to the intensity of provisioning. We used a broad range of non-invasive health measures relating to birth rate and survival, disease and injury risk, body size and condition, and physiological stress. Our findings indicate that feeding by tourists may overall have negative impacts on the health of Barbary macaques, being linked in particular to larger body size, elevated stress levels and more alopecia. Finally, we propose a framework to help consider the potential costs and benefits of provisioning, which may facilitate future research and management decisions on whether—and how much—provisioning is acceptable.

Metabolic strategies in wild male Barbary macaques: evidence from faecal measurement of thyroid hormone

Selection is expected to favour the evolution of flexible metabolic strategies, in response to environmental conditions. Here, we use a non-invasive index of basal metabolic rate (BMR), faecal thyroid hormone (T3) levels, to explore metabolic flexibility in a wild mammal inhabiting a highly seasonal, challenging environment. T3 levels of adult male Barbary macaques in the Atlas Mountains, Morocco, varied markedly over the year; temporal patterns of variation differed between a wild-feeding and a provisioned group. Overall, T3 levels were related to temperature, foraging time (linked to food availability) and intensity of mating activity, and were higher in the provisioned than in the wild-feeding group. In both groups, T3 levels began to increase markedly one month before the start of the mating season, peaking four to six weeks into this period, and at a higher level in the wild-feeding group. Our results suggest that while both groups demonstrate marked metabolic flexibility, responding similarly to ecological and social challenges, such flexibility is affected by food availability. This study provides new insights into the way Barbary macaques respond to the multiple demands of their environment.

Out of Asia: The Singular Case of the Barbary Macaque

The Barbary macaque (Macaca sylvanus) is the only species of the genus Macaca living outside Asia. Currently, two disjointed and highly fragmented populations of this species exist in the wild, in Morocco and Algeria. The Barbary macaque is listed as endangered in the IUCN 2010 Red List of Threatened Species and the total population size in the wild is estimated at between 5,000 and 6,000 individuals. Outside Africa, a free-ranging population of macaques inhabits the Rock of Gibraltar. The Barbary macaque can be considered a flagship species of the cedar and oak forests of Morocco and Algeria. Despite this, little is known about the population structure, ecology and behaviour of wild Barbary macaques. Scarce data exist on the effect of human activity on the conservation and behaviour of this species. In this chapter, we review the literature on wild Barbary macaques to describe their ecology and behaviour. We discuss the factors threatening the survival of this species, and the history of human-macaque interactions in Morocco and Algeria, as well as in Gibraltar. Moreover, we analyse the effect of tourist pressure on the behaviour of the Barbary macaque at our field site in the Middle Atlas Mountains of Morocco, as a case study of human-macaque interactions.

Between-group competition elicits within-group cooperation in children

Aggressive interactions between groups are frequent in human societies and can bear significant fitness costs and benefits (e.g. death or access to resources). During between-group competitive interactions, more cohesive groups (i.e. groups formed by individuals who cooperate in group defence) should out-perform less cohesive groups, other factors being equal (e.g. group size). The cost/benefit of between-group competition are thought to have driven correlated evolution of traits that favour between-group aggression and within-group cooperation (e.g. parochial altruism). Our aim was to analyse whether the proximate relationship between between-group competition and within-group cooperation is found in 3–10 years old children and the developmental trajectory of such a relationship. We used a large cohort of children (n = 120) and tested whether simulated between-group competition increased within-group cooperation (i.e. how much of a resource children were giving to their group companions) in two experiments. We found greater within-group cooperation when groups of four children were competing with other groups then in the control condition (no between-group competition). Within-group cooperation increased with age. Our study suggests that parochial altruism and in-group/out-group biases emerge early during the course of human development.

Primates' behavioural responses to tourists: evidence for a trade-off between potential risks and benefits.

The presence of, and interactions with tourists can be both risky and beneficial for wild animals. In wildlife tourism settings, animals often experience elevated rates of aggression from conspecifics, and they may also be threatened or physically aggressed by the tourists themselves. However, tourist provisioning of wild animals provides them with highly desirable foods. In situations of conflicting motivations such as this, animals would be expected to respond using behavioural coping mechanisms. In the present study, we investigated how animals respond to tourist pressure, using wild adult Barbary macaques in the Middle Atlas Mountains, Morocco, as a case study. We found evidence that these animals use a range of different behavioural coping mechanisms–physical avoidance, social support, affiliative, aggressive and displacement behaviours–to cope with the stress associated with tourists. The pattern of use of such behaviours appears to depend on a trade-off between perceived risks and potential benefits. We propose a framework to describe how animals respond to conflicting motivational situations, such as the presence of tourists, that present simultaneously risks and benefits.

Experience-based human perception of facial expressions in Barbary macaques (Macaca sylvanus)

Background Facial expressions convey key cues of human emotions, and may also be important for interspecies interactions. The universality hypothesis suggests that six basic emotions (anger, disgust, fear, happiness, sadness, and surprise) should be expressed by similar facial expressions in close phylogenetic species such as humans and nonhuman primates. However, some facial expressions have been shown to differ in meaning between humans and nonhuman primates like macaques. This ambiguity in signalling emotion can lead to an increased risk of aggression and injuries for both humans and animals. This raises serious concerns for activities such as wildlife tourism where humans closely interact with wild animals. Understanding what factors (i.e., experience and type of emotion) affect ability to recognise emotional state of nonhuman primates, based on their facial expressions, can enable us to test the validity of the universality hypothesis, as well as reduce the risk of aggression and potential injuries in wildlife tourism. Methods The present study investigated whether different levels of experience of Barbary macaques, Macaca sylvanus, affect the ability to correctly assess different facial expressions related to aggressive, distressed, friendly or neutral states, using an online questionnaire. Participants’ level of experience was defined as either: (1) naïve: never worked with nonhuman primates and never or rarely encountered live Barbary macaques; (2) exposed: shown pictures of the different Barbary macaques’ facial expressions along with the description and the corresponding emotion prior to undertaking the questionnaire; (3) expert: worked with Barbary macaques for at least two months. Results Experience with Barbary macaques was associated with better performance in judging their emotional state. Simple exposure to pictures of macaques’ facial expressions improved the ability of inexperienced participants to better discriminate neutral and distressed faces, and a trend was found for aggressive faces. However, these participants, even when previously exposed to pictures, had difficulties in recognising aggressive, distressed and friendly faces above chance level. Discussion These results do not support the universality hypothesis as exposed and naïve participants had difficulties in correctly identifying aggressive, distressed and friendly faces. Exposure to facial expressions improved their correct recognition. In addition, the findings suggest that providing simple exposure to 2D pictures (for example, information signs explaining animals’ facial signalling in zoos or animal parks) is not a sufficient educational tool to reduce tourists’ misinterpretations of macaque emotion. Additional measures, such as keeping a safe distance between tourists and wild animals, as well as reinforcing learning via videos or supervised visits led by expert guides, could reduce such issues and improve both animal welfare and tourist experience.

Correlates of androgens in wild male Barbary macaques: Testing the challenge hypothesis

Investigating causes and consequences of variation in hormonal expression is a key focus in behavioral ecology. Many studies have explored patterns of secretion of the androgen testosterone in male vertebrates, using the challenge hypothesis (Wingfield, Hegner, Dufty, & Ball, 1990; The American Naturalist, 136(6), 829–846) as a theoretical framework. Rather than the classic association of testosterone with male sexual behavior, this hypothesis predicts that high levels of testosterone are associated with male–male reproductive competition but also inhibit paternal care. The hypothesis was originally developed for birds, and subsequently tested in other vertebrate taxa, including primates. Such studies have explored the link between testosterone and reproductive aggression as well as other measures of mating competition, or between testosterone and aspects of male behavior related to the presence of infants. Very few studies have simultaneously investigated the links between testosterone and male aggression, other aspects of mating competition and infant‐related behavior. We tested predictions derived from the challenge hypothesis in wild male Barbary macaques (Macaca sylvanus), a species with marked breeding seasonality and high levels of male‐infant affiliation, providing a powerful test of this theoretical framework. Over 11 months, 251 hr of behavioral observations and 296 fecal samples were collected from seven adult males in the Middle Atlas Mountains, Morocco. Fecal androgen levels rose before the onset of the mating season, during a period of rank instability, and were positively related to group mating activity across the mating season. Androgen levels were unrelated to rates of male–male aggression in any period, but higher ranked males had higher levels in both the mating season and in the period of rank instability. Lower androgen levels were associated with increased rates of male‐infant grooming during the mating and unstable periods. Our results generally support the challenge hypothesis and highlight the importance of considering individual species’ behavioral ecology when testing this framework.

Measuring Cortisol in the Classroom with School-Aged Children—A Systematic Review and Recommendations

The collection of salivary cortisol has been chosen as one of the least intrusive, easiest to collect, analyze, and store methods of obtaining information on physiological changes. It is, however, not clear what the best practice is when collecting salivary cortisol from children within the school setting. The aim of this systematic review is to evaluate the feasibility of cortisol collection in schools for future research and to make recommendations for best practice. The review included 25 peer-reviewed articles from seven databases. The hypotheses of the included studies vary, but they all use cortisol as a diurnal, baseline, or acute measure, or to measure the effect of an intervention. Two methods of salivary cortisol collection were preferred by most of the research, i.e., passive drool or cotton Salivettes. The review has concluded that cortisol is a physiological marker that can be successfully measured in school-based research. However, there are discrepancies across studies when evaluating the collection guidelines, protocols, and instructions to participants as well as transparency of the success rate of obtaining all samples. Recommendations are made for future research to address and avoid such discrepancies and improve cross-study comparisons by implementing standard protocol guidelines.

Implications of Tourist–Macaque Interactions for Disease Transmission

During wildlife tourism, proximity or actual contact between people and animals may lead to a significant risk of anthropozoonotic disease transmission. In this paper, we use social network analysis, disease simulation modelling and data on animal health and behaviour to investigate such risks at a site in Morocco, where tourists come to see wild Barbary macaques (Macaca sylvanus). Measures of individual macaques’ network centrality—an index of the strength and distribution of their social relationships and thus potentially their ability to spread disease—did not show clear and consistent relationships with their time spent in close proximity to, or rate of interacting with, tourists. Disease simulation modelling indicated that while higher-ranked animals had a significantly greater ability to spread disease within the group, in absolute terms there was little difference in the size of outbreaks that different individuals were predicted to cause. We observed a high rate of physical contact and close proximity between humans and macaques, including during three periods when the macaques were coughing and sneezing heavily, highlighting the potential risk of disease transmission. We recommend that general disease prevention strategies, such as those aimed at reducing opportunities for contact between tourists and macaques, should be adopted.