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Morphological adaptations related to food processing generally reflect those elements of the diet that represent the greatest biomechanical challenge or that numerically dominate the diet. However, in periods of the annual cycle when the availability of such foods is low, items to which a species has low apparent morphological adaptation may be included in the diet. Here we test the responses of a diet-specialist primate to limitations in the supply of the resource it is specialized to exploit. Uacaris are primarily predators of immature seeds, in seasonally flooded forests in Amazonian Brazil, and have dental specializations to open hard-shelled fruits. We investigated the importance of arthropods in the diet of golden-backed uacaris (Cacajao melanocephalus ouakary), examining their seasonal importance in the uacari diet, and the ways C. m. ouakary used to access them. Using scan and ad libitum sampling of feeding and phenology from botanical study plots to assess fruit availability, we conducted an 18-mo study in Jaú National Park, Amazonas State, Brazil. We recorded arthropod predation 298 times, with Cacajao melanocephalus ouakary feeding on 26 invertebrate taxa in ≥11 families and 9 different orders. Uacaris extracted wood-boring beetles dentally from rotting wood and smaller larvae from twigs, stems, and petioles, but this food class did not predominate. This food class (encapsulated foods) constituted 23.4 % of the arthropod records. The majority of arthropod food items were either manually removed from substrates (ants, beetle larvae, caterpillars, fulgorid bugs, grasshoppers, mayflies, spiders, termites, wasps, and a whip-scorpion) or plucked from the air (volant Lepidoptera). Uacaris appeared to avoid toxic caterpillars. Insectivory was most frequent when fruit and seeds were least available. Arthropods seem to be seasonally important to this primate, supplementing or making up for shortfalls in the hard fruits and immature seeds for which uacaris have hig

A female mammal's reproductive function and output are limited by the energy she is able to extract from her environment. Previous studies of the interrelationships between energetic circumstances and reproductive function in a variety of mammal species have produced varied results, which do not all support the common assumption that higher female reproductive hormone levels, specifically progesterone, indicate better ovarian function and greater reproductive potential, and are associated with lower energetic stress. In the present study faecal progesterone and glucocorticoid levels were assessed in two troops of olive baboons (Papio anubis) in the same population. They face similar ecological challenges, except that one troop crop-raids, potentially affecting its energetic intake and stress levels. The energy intake of individual females was assessed by combining detailed feeding observations with nutritional analysis of food samples. The crop-raiding troop experienced 50% higher energy intake rates and 50% lower glucocorticoid levels compared to the non-crop-raiding troop alongside substantially lower progesterone levels. This suggests that energetic stress is associated with elevated progesterone levels and may be the cause of the non-crop-raiding troop’s lower reproductive output. By comparing groups which differ little, except in terms of food access, and also by directly assessing energy intake, our study addresses some of the design limitations of previous research investigating variation in progesterone levels and energetic stress. It therefore has the potential to contribute to greater understanding of the factors affecting differences in reproductive and stress hormone levels and reproductive function in mammals experiencing different energetic circumstances.

Measuring rates of self-scratching provides a powerful index of anxiety in non-human primates, and investigating the relationship between self-scratching and dominance rank can shed light on the 'emotional costs' of holding different positions in the hierarchy. Here we explored the relationship between self-scratching rates and rank in wild adult female Barbary macaques (Macaca sylvanus) in Morocco. We found a significant correlation between rank and females' mean self-scratching rates over the study period, with subordinates showing higher rates of self-scratching. Analysis of temporal variation in females' self-scratching rates indicated that while these rates were related to measures of both grooming and aggression, the relationship between rank and self-scratching remained significant even after controlling for these effects. Our data suggest that lower ranked female Barbary macaques suffer higher levels of anxiety than more dominant individuals, and hence that there is an emotional cost associated with having low social status in this species.

Behavioural syndromes are a well-established phenomenon in human and non-human animal behavioural ecology. However, the mechanisms that lead to correlations among behaviours and individual consistency in their expression at the apparent expense of behavioural plasticity remain unclear. The ‘state-dependent’ hypothesis posits that inter-individual variation in behaviour arises from inter-individual variation in state and that the relative stability of these states within an individual leads to consistency of behaviour. The endocrine stress response, in part mediated by glucocorticoids (GCs), is a proposed behavioural syndrome-associated state as GC levels are linked to an individual’s behavioural responses to stressors. In this study, in wild Barbary macaques (Macaca sylvanus), consistent inter-individual differences were observed in both sexes for GC activity (faecal glucocorticoid, fGC concentrations), but not GC variation (coefficient of variation in fGC concentrations). The expression of the behavioural syndrome ‘Excitability’ (characterized by the frequencies of brief affiliation or aggressive interactions) was related to GC activity in males but not in females; more ‘excitable’ males had lower GC activity. There was no relationship in females between any of the behavioural syndromes and GC activity, nor in either sex with GC variation. The negative relationship between GC activity and Excitability in males provides some support for GC expression as a behavioural syndromegenerating state under the state-dependent framework.

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.

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 genera

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.

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.

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.

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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

Measuring rates of self-scratching provides a powerful index of anxiety in non-human primates, and investigating the relationship between self-scratching and dominance rank can shed light on the ‘emotional costs’ of holding different positions in the hierarchy. Here we explored the relationship between self-scratching rates and rank in wild adult female Barbary macaques (Macaca sylvanus) in Morocco.We found a significant correlation between rank and females’ mean self-scratching rates over the study period, with subordinates showing higher rates of self-scratching. Analysis of temporal variation in females’ self-scratching rates indicated that while these rates were related to measures of both grooming and aggression, the relationship between rank and self-scratching remained significant even after controlling for these effects. Our data suggest that lower ranked female Barbary macaques suffer higher levels of anxiety than more dominant individuals, and hence that there is an emotional cost associated with having low social status in this species.

Wildlife tourism is a burgeoning global industry with the potential to make a significant contribution to the conservation of endangered species. However, a number of studies have provided evidence that tourists’ presence and behaviour may impact negatively on the animals involved, with potentially harmful consequences for their health, reproduction and population viability. Here, we investigate impacts of tourism on wild male Barbary macaques (Macaca sylvanus) in Morocco, quantifying a behavioural index of animals’ anxiety (self-scratching) and a measure of their physiological stress levels (faecal glucocorticoid concentrations – FGCs). Four measures of tourist presence, number or proximity were explored: maximum number, percentage of time present, mean number while present, and closest proximity to the macaques. In addition, rates of three types of interactions between tourists and macaques – neutral (e.g. photographing), feeding and aggressive – were quantified. Males’ rates of self-scratching were positively related to the mean number of tourists present and to rates of all three human-macaque interactions, but were unrelated to the other three measures of tourist pressure. FGCs were positively related to rates of aggressive interactions between humans and macaques, but unrelated to any of the other six measures of tourist pressure. These findings suggest that while tourist presence and interactions (even apparently innocuous ones) with the macaques elevate the study animals’ anxiety levels, only aggressive interactions are sufficient to elicit a detectable increase in our measure of physiological stress. These results can be used to inform management of tourism both at this site, and at other locations where tourists view and can interact with wild primates.