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The development of the unique, hierarchical, and endless combinatorial capacity in a human language requires neural maturation and learning through childhood. Compared with most non-human primates, where combinatorial capacity seems limited, chimpanzees present a complex vocal system comprising hundreds of vocal sequences. We investigated how such a complex vocal system develops and the processes involved. We recorded 10,929 vocal utterances of 98 wild chimpanzees aged 0-55 years, from Taï National Park, Ivory Coast. We developed customized Generalized non-Linear Models to estimate the ontogenetic trajectory of four structural components of vocal complexity: utterance length, diversity, probability of panting (requiring phonation across inhalation and exhalation), and probability of producing two adjacent panted units. We found chimpanzees need 10 years to reach adult levels of vocal complexity. In three variables, the steepest increase coincided with the age of first non-kin social interactions (2-5 years), and plateaued in sub-adults (8-10 years), as individuals integrate into adult social life. Producing two adjacent panted units may require more neuromuscular coordination of the articulators, as its emergence and steepest increase appear later in development. These results suggest prolonged maturational processes beyond those hitherto thought likely in species that do not learn their vocal repertoire. Our results suggest that multifaceted ontogenetic processes drive increases in vocal structural complexity in chimpanzees, particularly increases in social complexity and neuro-muscular maturation. As humans live in a complex social world, empirical support for the "social complexity hypothesis" may have relevance for theories of language evolution. RESEARCH HIGHLIGHTS: Chimpanzees need around 10 years to develop the vocal structural complexity present in the adult repertoire, way beyond the age of emergence of every single vocal unit. Multifaceted ontogenetic processes may drive increases in vocal structural complexity in chimpanzees, particularly increases in social complexity and neuro-muscular maturation. Non-linear increases in vocal complexity coincide with social developmental milestones. Vocal sequences requiring rapid articulatory change emerge later than other vocal sequences, suggesting neuro-muscular maturational processes continue through the juvenile years.

International audience; The causes and consequences of being in a particular dominance position have been illuminated in various animal species, and new methods to assess dominance relationships and to describe the structure of dominance hierarchies have been developed in recent years. Most research has focused on same-sex relationships, however, so that intersexual dominance relationships and hierarchies including both sexes have remained much less studied. In particular, different methods continue to be employed to rank males and females along a dominance hierarchy, and sex biases in dominance are still widely regarded as simple byproducts of sexual size dimorphism. However, males and females regularly compete over similar resources when living in the same group, and sexual conflict takes a variety of forms across Frontiers in Ecology and Evolution 01 frontiersin.org Kappeler et al. 10.3389/fevo.2022.918773 societies. These processes affect the fitness of both sexes, and are mitigated by intersexual hierarchies. In this study, we draw on data from free-ranging populations of nine species of mammals that vary in the degree to which members of one sex dominate members of the other sex to explore the consequences of using different criteria and procedures for describing intraand intersexual dominance relationships in these societies. Our analyses confirmed a continuum in patterns of intersexual dominance, from strictly male-dominated species to strictly female-dominated species. All indices of the degree of female dominance were well correlated with each other. The rank order among same-sex individuals was highly correlated between the intra-and intersexual hierarchies, and such correlation was not affected by the degree of female dominance. The relative prevalence of aggression and submission was sensitive to variation in the degree of female dominance across species, with more submissive signals and fewer aggressive acts being used in societies where female dominance prevails. Thus, this study provides important insights and key methodological tools to study intersexual dominance relationships in mammals.

In mammals, allogrooming is prominent in forming and maintaining social and cooperative relationships. Yet an animal's social time is constrained, which may limit its access to a large number of partners. Dunbar (1993, Behavioral and Brain Sciences, 16 (4), 681–694) proposed that human polyadic conversations, which allow access to several social partners simultaneously, evolved as a form of social grooming to circumvent this time constraint. In nonhuman primates, polyadic grooming (PG), in contrast to dyadic grooming, may similarly be a time-efficient way to maintain weak social relationships with many partners which can be important for group level cooperation. It remains unknown whether PG is used to fulfil specific cooperative needs by accessing numerous weakly bonded partners and increasing the number of partners accessed per unit of time. We compared the use and effect of PG between chimpanzees, Pan troglodytes, which are highly territorial and collaborative (especially males), and bonobos, Pan paniscus, which are less territorial and collaborative and in which females are the main co-operators. We carried out focal grooming observations in one bonobo and two chimpanzee communities in the wild. As predicted, chimpanzees engaged in more PG than bonobos. Surprisingly, males engaged in PG more than females in both species. While chimpanzees accessed more partners per minute of grooming than bonobos via dyadic grooming, PG increased the number of partners accessed per minute only in bonobos. Finally, chimpanzees primarily used PG with individuals who were close in rank and frequent grooming partners, whereas bonobos used PG with individuals who were distant in rank, close party associates and frequent grooming partners. We suggest that bonobo males use PG to enhance conspecific social tolerance and mate choice. The overall higher rate of PG in chimpanzees suggests that between-group competition may promote polyadic affiliation, which possibly reinforces group cohesion and coordination. © 2020 The Authors

The origins of human speech are obscure; it is still unclear what aspects are unique to our species or shared with our evolutionary cousins, in part due to a lack of a common framework for comparison. We asked what chimpanzee and human vocal production acoustics have in common. We examined visible supra-laryngeal articulators of four major chimpanzee vocalizations (hoos, grunts, barks, screams) and their associated acoustic structures, using techniques from human phonetic and animal communication analysis. Data were collected from wild adult chimpanzees, Taï National Park, Ivory Coast. Both discriminant and principal component classification procedures revealed classification of call types. Discriminating acoustic features include voice quality and formant structure, mirroring phonetic features in human speech. Chimpanzee lip and jaw articulation variables also offered similar discrimination of call types. Formant maps distinguished call types with different vowel-like sounds. Comparing our results with published primate data, humans show less F1–F2 correlation and further expansion of the vowel space, particularly for [i] sounds. Unlike recent studies suggesting monkeys achieve human vowel space, we conclude from our results that supra-laryngeal articulatory capacities show moderate evolutionary change, with vowel space expansion continuing through hominoid evolution. Studies on more primate species will be required to substantiate this.This article is part of the theme issue ‘Voice modulation: from origin and mechanism to social impact (Part II)’.

An analysis of the structural complexity of vocal sequences in chimpanzees in the Tai National Park reveal that single vocal units are combined into numerous structured sequences with adjacency dependencies between units.The origins of human language remains a major question in evolutionary science. Unique to human language is the capacity to flexibly recombine a limited sound set into words and hierarchical sequences, generating endlessly new sentences. In contrast, sequence production of other animals appears limited, stunting meaning generation potential. However, studies have rarely quantified flexibility and structure of vocal sequence production across the whole repertoire. Here, we used such an approach to examine the structure of vocal sequences in chimpanzees, known to combine calls used singly into longer sequences. Focusing on the structure of vocal sequences, we analysed 4826 recordings of 46 wild adult chimpanzees from Tai National Park. Chimpanzees produced 390 unique vocal sequences. Most vocal units emitted singly were also emitted in two-unit sequences (bigrams), which in turn were embedded into three-unit sequences (trigrams). Bigrams showed positional and transitional regularities within trigrams with certain bigrams predictably occurring in either head or tail positions in trigrams, and predictably co-occurring with specific other units. From a purely structural perspective, the capacity to organize single units into structured sequences offers a versatile system potentially suitable for expansive meaning generation. Further research must show to what extent these structural sequences signal predictable meanings.

Glucocorticoids, such as cortisol, mediate homeostatic processes, allowing individuals to adjust to fluctuating environments. The regulation of circadian cortisol responses, a key homeostatic function, has been shown to be heritable. However, to understand better the role of parental care in shaping physiological functioning in long-lived mammals with protracted parental care, there is a need to disentangle genetic and non-genetic parental contributions to variation in glucocorticoid phenotypes. We used a dataset of 6,123 cortisol measures from urine samples from 170 wild chimpanzees spanning 18 years of data collection. We found consistent inter-individual differences in circadian cortisol phenotypes, with differences most apparent when considering average cortisol levels given the effect of time of day. Maternal effects explained around 10% (2-18%) variation in these average cortisol levels, while variation attributable to genetic factors was not distinguishable from zero. Our results indicate, relative to genetic effects, a qualitatively stronger influence of mothers, whether via epigenetic processes or via behavioral priming for coping with stressors, in shaping cortisol phenotypes in this species. This provides novel insight into the vital role of mothers in the developmental plasticity of long-lived mammals and, more generally, the selective pressures shaping physiological plasticity.

The biological embedding model (BEM) suggests that fitness costs of maternal loss arise when early-life experience embeds long-term alterations to hypothalamic-pituitary-adrenal (HPA) axis activity. Alternatively, the adaptive calibration model (ACM) regards physiological changes during ontogeny as short-term adaptations. Both models have been tested in humans but rarely in wild, long-lived animals. We assessed whether, as in humans, maternal loss had short- and long-term impacts on orphan wild chimpanzee urinary cortisol levels and diurnal urinary cortisol slopes, both indicative of HPA axis functioning. Immature chimpanzees recently orphaned and/or orphaned early in life had diurnal cortisol slopes reflecting heightened activation of the HPA axis. However, these effects appeared short-term, with no consistent differences between orphan and non-orphan cortisol profiles in mature males, suggesting stronger support for the ACM than the BEM in wild chimpanzees. Compensatory mechanisms, such as adoption, may buffer against certain physiological effects of maternal loss in this species.

Socioecological theories predict that, in mammals, feeding and mating competitions affect male and female energetic conditions differently but energetic studies investigating both sexes simultaneously are rare. We investigated the effect of socioecological factors on the energetic conditions of male and female western chimpanzees, a long-lived species with high degrees of male-male competition. We used behavioural data collected on one chimpanzee community in the Taï National Park over 12 months, phenological data and urinary c-peptide (UCP) measures, a marker of energy balance. We found a positive effect of food availability on UCP levels in both sexes. Dominance rank also affected chimpanzee UCP levels. High-ranking females had higher UCP levels than low-ranking ones but only in periods when no oestrus females were present in the community. In contrast, high-ranking males had higher UCP levels than low-ranking males in the presence of oestrus females but lower UCP levels in their absence. Our results suggest that oestrus female presence lessened the competitive advantages of high-ranking females in feeding competition and that low-ranking males bore higher energetic costs related to mating competition than high-ranking ones. Yet caution should apply in interpreting these results since the statistical model was only close to significance. High-ranking male and female chimpanzees spent significantly less energy. Furthermore, all chimpanzees significantly spent less time feeding and spent more energy when food availability was high. Finally, our behavioural measure of energy intake and expenditure did not correlate with UCP levels highlighting the value of non-invasive hormonal markers for field studies.Significance statementGeneral socioecological theories hypothesize that the social grouping dynamic and energetics of females are highly influenced by food competition, whereas in males, competition for sexual partners is more influential for these factors. Recent studies in the non-invasive physiological assessment of energy balance in primates have begun to test the implied relationship between chimpanzee socioecology and individual energetic condition, with inconsistent results. However, only a few studies have investigated this relationship concurrently for both sexes. Here, using non-invasive measures of energy balance in wild western chimpanzees, we found that the energetics of both males and females are related to ecological factors, such as food availability. However, female energy balance appears also to be related to increased male mating competition, as this can result in increased aggression directed from males to females, with apparent energetic costs for females.

In mammals, early life adversity negatively affects survival and reproductive success. A key causal mechanism is proposed by the biological embedding model which posits that adversity experienced early in life has deleterious consequences on individual physiology across the lifespan. In particular, early life adversity is expected to be a severe stressor leading to long-term alteration of the hypothalamic pituitary adrenal (HPA) axis activity. Here we tested this idea by assessing whether, as in humans, maternal loss had short and long-term impacts on orphan chimpanzee urinary cortisol levels and diurnal urinary cortisol slopes, as an indicator of the HPA axis functioning. We used 18 years of data on 50 immature and 28 mature male wild chimpanzees belonging to four communities in Taï National Park, Ivory Coast. Immature orphans who experienced early maternal loss had diurnal cortisol slopes characterised by higher early morning and late afternoon cortisol levels indicative of high activation of the HPA axis. Recently orphaned immatures had higher cortisol levels than other immatures, possibly reflecting social and nutritional stress. However, unlike in humans, we did not find significantly different cortisol profiles in orphan and non-orphan adult male chimpanzees. Our study highlights that long-term alteration of stress physiology related to early life adversity may not be viable in some wild animal populations and/or that chimpanzees, as humans, may have access to mechanisms that buffer this physiological stress, such as adoption. Our results suggest that biological embedding of altered HPA axis function is unlikely to be a mechanism contributing to the demonstrated long-term fitness consequences of maternal loss, such as reduced reproductive success, in wild long-lived mammals.

Compared with most mammals, postnatal development in great apes is protracted, presenting both an extended period of phenotypic plasticity to environmental conditions and the potential for sustained mother-offspring and/or sibling conflict over resources. Comparisons of cortisol levels during ontogeny can reveal physiological plasticity to species or population specific socioecological factors and in turn how these factors might ameliorate or exaggerate mother-offspring and sibling conflict. Here, we examine developmental patterns of cortisol levels in two wild chimpanzee populations (Budongo and Taï), with two and three communities each, and one wild bonobo population (LuiKotale), with two communities. Both species have similar juvenile life histories. Nonetheless, we predicted that key differences in socioecological factors, such as feeding competition, would lead to interspecific variation in mother-offspring and sibling conflict and thus variation in ontogenetic cortisol patterns. We measured urinary cortisol levels in 1394 samples collected from 37 bonobos and 100 chimpanzees aged up to 12 years. The significant differences in age-related variation in cortisol levels appeared population specific rather than species specific. Both bonobos and Taï chimpanzees had comparatively stable and gradually increasing cortisol levels throughout development; Budongo chimpanzees experienced declining cortisol levels before increases in later ontogeny. These age-related population differences in cortisol patterns were not explained by mother-offspring or sibling conflict specifically; instead, the comparatively stable cortisol patterns of bonobos and Taï chimpanzees likely reflect a consistency in experience of competition and the social environment compared with Budongo chimpanzees, where mothers may adopt more variable strategies related to infanticide risk and resource availability. The clear population-level differences within chimpanzees highlight potential intraspecific flexibility in developmental processes in apes, suggesting the flexibility and diversity in rearing strategies seen in humans may have a deep evolutionary history. Publisher PDF

ECOLOGICAL AND REPRODUCTIVE CORRELATES OF ENERGY BALANCE IN WILD MOOR MACAQUES (MACACA MAURA) USING C-PEPTIDE MEASUREMENTS Lavinia Germani a, Cédric Girard-Buttoz b, Michael Heistermann c, Putu Oka Ngakan d, Monica Carosi a aDepartment of Sciences, Roma Tre University, Rome, Italy; bDepartment of Primatology, Max Planck Institute for Evolutionary Anthropology, Leipzig, Germany; cEndocrinology Laboratory, German Primate Centre, Leibniz Institute for Primate Research, Göttingen, Germany, dFaculty of Forestry, Hasanuddin University, Makassar, Indonesia Energy is a key factor for wild animal survival. Reproduction and energy balance might be affected by seasonal variation in food availability and reproductive costs in both sexes. This is relatively well established for seasonally breeding primates living in highly predictable environments and showing intense male competition, yet little is known about factors affecting energy balance in species with weaker ecological and reproductive seasonality. Here, we investigated the ecological and reproductive correlates of energy balance in adult individuals of the moderately seasonal, polygynandrous and tolerant moor macaques, Macaca maura. We studied one social group living in the karst forests of south Sulawesi (Indonesia), which provide relatively stable food supply. Urine samples (n=120; 11 males, 13 females) were collected for 11 months across 2 field seasons (each covering both dry and wet season) and analysed for urinary C-peptide (UCP), a biomarker of energy balance. We tested the effect of fruit availability on the energy balance of males and females of different reproductive states (each likely related to different energetic costs). We also tested male UCP in response to the presence of potentially fertile females. Both male and female UCP levels positively responded to fruit availability increase, and the strength of this relationship was similar in males and in cycling and lactating females. Pregnant females, however, responded more strongly than other groups, suggesting that they are more sensitive to ecological variation. Finally, the presence of potentially fertile females did not influence male UCP levels. Although based on a small sample size, these results challenge the applicability of classical socio-ecological theories to tolerant primates inhabiting a relatively steady environment since, in these species, competition for access to food resources might be as important in males as in females and male energetic investment in mating competition might be relatively low.

Regulation of energy allocation and metabolic rate plays an important role in determining behavior and fitness in wild animals, calling for the validation of non-invasive markers of energetic condition. Recently, the thyroid hormone triiodothyronine (T3) has emerged as a promising marker as concentrations decrease to lower the metabolic rate during energetically challenging periods. However, it remains largely unclear whether T3 merely represents an alternative or provides additional information compared to other compounds involved in the regulation of energy acquisition and allocation, like cortisol and C-peptide, as few joint measurements have been conducted to date in non-invasively collected samples. We aimed to validate the non-invasive measurement of immunoreactive urinary total T3 (uTT3), in comparison to urinary cortisol (uCort) and urinary C-peptide (uCP), as a marker of metabolic response to variation in food intake in macaques, and to address a number of issues regarding the collection, storage and processing of samples which are important for application of uTT3 measurements under field conditions. We used daily samples and body mass measures from a prior food restriction-refeeding experiment over 4 weeks with six captive macaques and analyzed concentrations of uTT3 and uCort in samples collected prior to (fasting) and after morning feeding (non-fasting). Concentrations of uTT3 decreased in response to restriction in food supply and were also lower during weeks of food restriction compared to weeks of refeeding. Variation in uTT3 also correlated positively with variation in body mass and concentrations of uCP. As expected, uCort showed the reverse pattern, increasing during food restriction and decreasing following refeeding, but was not associated with variation in body mass. Generally, compared to fasting samples, concentrations were higher in post-morning feeding, i.e. non-fasting, samples for uTT3 but not uCort. Contamination of urine samples with fecal matter, but not soil, and exposure to UV light led to a decrease in uTT3. uTT3 was largely unaffected by repeated freeze–thaw cycles and by refrigeration for medium-term storage (2 days) but degraded substantially when stored at ambient temperature for the same period. In conclusion, uTT3 measurements inform on the effect of food intake and its associated metabolic response to variation in energetic status. Since uTT3 is reasonably robust to many issues associated with collection and storage of urine samples under field conditions, it is a promising biomarker for studies of energetic condition and basal metabolic rate in wild macaques.

M.S. thanks the Leaky Foundation, the Wenner Gren Foundation, the National Geographic Society, Basler Stiftung fuer Biologische Forschung and the SNF. B.F. and G.H. thank the DFG, DAAD, National Geographic Society, Leakey Foundation, Volkswagen Foundation and Ludwig Maximilians Universitaet Muenchen for funding this research. K.E.L. thanks the Leakey Foundation for funding. K.Z. acknowledges the Royal Zoological Society of Scotland for providing core funding to the Budongo Conservation Field Station, and the European Research Council (grant PRILANG 283871) for providing core funding for the research. M.S., C.B., C.G.-B., C.C., R.M.W. and G.H. thank the Max Planck Society for funding. In several group-living species, individuals’ social preferences are thought to be influenced by cooperation. For some societies with fission-fusion dynamics, sex-specific association patterns reflect sex differences in cooperation in within- and betweengroup contexts. In our study, we investigated this hypothesis further by comparing sex-specific association patterns in two closely related species, chimpanzees and bonobos, which differ in the level of between-group competition and in the degree to which sex and kinship influence dyadic cooperation. Here, we used long-term party composition data collected on five chimpanzee and two bonobo communities and assessed, for each individual of 10 years and older, the sex of its top associate and of all conspecifics with whom it associated more frequently than expected by chance. We found clear speciesdifferences in association patterns. While in all chimpanzee communities males and females associated more with same-sex partners, in bonobos males and females tended to associate preferentially with females, but the female association preference for other females is lower than in chimpanzees. Our results also show that, for bonobos (but not for chimpanzees), association patterns were predominantly driven by mother-offspring relationships. These species differences in association patterns reflect the high levels of male-male cooperation in chimpanzees and of mother- son cooperation in bonobos. Finally, female chimpanzees showed intense association with a few other females, and male chimpanzees showed more uniform association across males. In bonobos, the most differentiated associations were from males towards females. Chimpanzee male association patterns mirror fundamental human male social traits and, as in humans, may have evolved as a response to strong between-group competition. The lack of such a pattern in a closely related species with a lower degree of between-group competition further supports this notion. Publisher PDF

Male primates living in multimale groups tend to direct mate and mate-guarding choices toward females of high reproductive value, i.e., high-ranking, parous females, or females with which they share strong bonds. Little is known, however, about the constraints that may limit male mate-guarding choices (the costs of this behavior) and the influence of the females' quality on male investment in mate-guarding. We aimed to study the effects of female rank, parity status, and male-female social bond strength on the costs of and investment in mate-guarding by males. We carried out our study during two reproductive seasons on three groups of wild long-tailed macaques in Indonesia. We combined behavioral observations on male locomotion and activity with noninvasive measurements of fecal glucocorticoids (fGC). Males spent less time feeding when mate-guarding nulliparous females than when mate-guarding parous females and tended to have higher fGC levels when mate-guarding low-ranking nulliparous females than when mate-guarding high-ranking nulliparous ones. Evolution should thus favor male choice for high-ranking parous females because such a decision brings benefits at proximate (reduced costs of mate-guarding) and ultimate (higher reproductive value) levels. Further, male investment in mate-guarding was flexible and contingent on female reproductive and social value. Males were more vigilant and more aggressive toward other males when mate-guarding females to which they were strongly bonded and/or high-ranking ones than when mate-guarding other females. Our findings bring a new dimension to the study of mate choice by showing that males not only mate preferentially with high-quality females but may also aim to secure paternity with these females through optimized monopolization. peerReviewed

Coalitions among males during within group conflicts have a strong influence on the competitive and social environment within social groups. To evaluate possible variation in the occurrence of such coalitions in our closest relatives, chimpanzees and bonobos, we compared male aggression and coalitionary behavior in two natural communities, one of each species, with a similar size and composition. Furthermore we compared affiliative behavior that might be related to coalition formation among males. We found higher frequencies of aggression and a greater likelihood to form coalitions during within-group conflicts among wild male chimpanzees at Taï compared to wild male bonobos at LuiKotale. The species differed in the predominant sex of the male coalition partners, with male bonobos forming coalitions more often with females, while male chimpanzees formed coalitions more often with other males. Compared to male bonobos, male chimpanzees showed higher rates of grooming and tended to reconcile more conflicts with other males. Overall our results showed lower frequencies of reconciliation among bonobos than those described in captivity and at artificial feeding sites. These findings add to the evidence that male cooperation and conflict resolution are potentially very different in bonobos and chimpanzees, despite the fact that these two species are closely related, live in multi-male, multi-female communities with a high degree of fission-fusion dynamics and have female-biased migration patterns. Given the correlation between aggressive, cooperative and some affiliative patterns within the species in our study, we hypothesize that the fitness benefits of male relationships are greater in chimpanzees compared to bonobos.

The challenge hypothesis (Wingfield et al., 1990) has been broadly utilised as a conceptual framework to study male androgen correlates of reproductive challenges in mammals. These studies mainly assessed male androgen responsiveness to a general degree of challenge over extended periods of time. Short term co-variation between the socio-sexual challenging context and androgen levels remains, however, largely understudied. We thus aim at providing a multi-level test of the challenge hypothesis by investigating the inter- and intra-individual variations in faecal androgen excretion associated to 1) breeding seasonality, 2) dominance rank, 3) mate-guarding activity and 4) value of the guarded female. We studied long-tailed macaques, a species in which males engage in highly challenging monopolisation of females over discreet periods of time. This particularity allows testing specifically the predicted increase from level B to level C in the challenge hypothesis. The study was carried out during two reproductive seasons on three groups of wild long-tailed macaques. We combined behavioural observations and non-invasive measurements of faecal androgen metabolite (fAM) levels. We found that, as predicted by the challenge hypothesis, male long-tailed macaques respond not only to seasonal but also to short term reproductive challenges by adapting their androgen levels. First, males exhibited a seasonal rise in fAM levels during the mating period which may be triggered by fruit availability as shown by our phenological data. Second, males had increased androgen levels when mate-guarding females and, across mate-guarding periods, males had higher fAM levels when monopolising high-ranking parous females than when monopolising low-ranking ones. Finally, high-ranking males had higher fAM levels than low-ranking males year round. Our study confirms that, in species with a high degree of female monopolisability, androgen may be an important physiological fitness enhancing tool for males by increasing female monopolisation efficiency (in particular with highly valuable females) and helping males to respond to rank take-over challenges.

Coalitions among males during within group conflicts have a strong influence on the competitive and social environment within social groups. To evaluate possible variation in the occurrence of such coalitions in our closest relatives, chimpanzees and bonobos, we compared male aggression and coalitionary behavior in two natural communities, one of each species, with a similar size and composition. Furthermore we compared affiliative behavior that might be related to coalition formation among males. We found higher frequencies of aggression and a greater likelihood to form coalitions during within-group conflicts among wild male chimpanzees at Tai compared to wild male bonobos at LuiKotale. The species differed in the predominant sex of the male coalition partners, with male bonobos forming coalitions more often with females, while male chimpanzees formed coalitions more often with other males. Compared to male bonobos, male chimpanzees showed higher rates of grooming and tended to reconcile more conflicts with other males. Overall our results showed lower frequencies of reconciliation among bonobos than those described in captivity and at artificial feeding sites. These findings add to the evidence that male cooperation and conflict resolution are potentially very different in bonobos and chimpanzees, despite the fact that these two species are closely related, live in multi-male, multi-female communities with a high degree of fission-fusion dynamics and have female-biased migration patterns. Given the correlation between aggressive, cooperative and some affiliative patterns within the species in our study, we hypothesize that the fitness benefits of male relationships are greater in chimpanzees compared to bonobos.

Mate-guarding is an important determinant of male reproductive success in a number of species. However, it is known to potentially incur costs. The aim of the present study was to assess the effect of mate-guarding on male physiological stress and aggression in long-tailed macaques, a species in which males mate-guard females to a lesser extent than predicted by the Priority of Access model (PoA). The study was carried out during two mating periods on three groups of wild long-tailed macaques in Indonesia by combining behavioral observations with non-invasive measurements of fecal glucocorticoid (fGC) levels. Mate-guarding was associated with a general rise in male stress hormone levels but, from a certain threshold of mate-guarding onwards, increased vigilance time was associated with a decrease in stress hormone output. Mate-guarding also increased male-male aggression rate and male vigilance time. Overall, alpha males were more physiologically stressed than other males independently of mating competition. Increased glucocorticoid levels during mate-guarding are most likely adaptive since it may help males to mobilize extra-energy required for mate-guarding and ultimately maintain a balanced energetic status. However, repeated exposure to high levels of stress over an extended period is potentially deleterious to the immune system and thus may carry costs. This potential physiological cost together with the cost of increased aggression mate-guarding male face may limit the male's ability to mate-guard females, explaining the deviance from the PoA model observed in long-tailed macaques. Comparing our results to previous findings we discuss how ecological factors, reproductive seasonality and rank achievement may modulate the extent to which costs of mate-guarding limit male monopolization abilities. peerReviewed

Chez les primates, au sein des groupes multimâles, les mâles généralement copulent avec, et monopolisent préférentiellement, les femelles à fort potentiel reproducteur (i.e. femelles de rangs supérieurs) ou celles avec lesquelles ils partagent de forts liens sociaux. Les contraintes qui pèsent sur ces décisions et peuvent in-fine limiter la capacité des males à monopoliser les femelles (e.g. les coûts de cette monopolisation), ainsi que l’influence de la qualité des femelles sur la minutie avec laquelle les mâles les monopolisent, restent néanmoins très peu connues. L’objectif de cette étude était donc d’analyser l’effet de la position hiérarchique des femelles, de la parité reproductive et du lien social entre mâle et femelle sur le coût de la monopolisation pour le mâle et sur son investissement dans ce comportement. Pour cette étude, trois groupes de macaques crabiers (Macaca fascicularis) sauvages ont été suivis pendant deux saisons de reproduction en Indonésie. Nous avons combiné des observations comportementales sur l’activité des mâles avec des mesures hormonales non-invasives de glucocorticoïdes fécaux (fGC). Les mâles consacraient moins de temps à s’alimenter lorsqu’ils monopolisaient des femelles nullipares et leurs niveaux de fGC étaient plus élevés lorsqu’ils monopolisaient des femelles nullipares et de rangs inférieurs. L’évolution devrait donc favoriser les décisions reproductrices des mâles vers la monopolisation de femelles pares et de rangs supérieurs puisque de telles décisions apportent un double bénéfice au niveau proximal (réduction des coûts de la monopolisation) et ultime (meilleure valeur reproductive des femelles). Notre étude met également en évidence que la minutie avec laquelle le mâle monopolise différentes femelles peut-être flexible et dépend de la valeur sociale et reproductive de la femelle. Les mâles étaient plus vigilants et plus agressifs envers les autres mâles lorsqu’ils monopolisaient des femelles de rangs élevés ou celles avec qui ils partageaient de forts liens sociaux. Nos résultats offrent une nouvelle dimension à l’étude des décisions reproductives en montrant que les mâles non seulement préfèrent copuler avec des femelles de qualité supérieure mais tendent également à accroitre leurs chances d’assurer leur paternité avec ces femelles par le biais d’une monopolisation optimale.

Mate-guarding is an important determinant of male reproductive success in a number of species. Little is known however about the constraints of this behaviour, e.g. the associated energetic costs. We investigated these costs in long-tailed macaques where alpha males mate guard females to a lesser extent than predicted by the priority of access model. The study was carried out during two mating periods on three wild groups living in the Gunung Leuser National Park, Indonesia. We combined behavioural observations on males’ locomotion and feeding activity, GPS records of distance travelled and non-invasive measurements of urinary C-peptide (UCP), a physiological indicator of male energetic status. Mate-guarding led to a decrease in feeding time and fruit consumption suggesting a reduced intake of energy. At the same time, vertical locomotion was reduced, which potentially saved energy. These findings, together with the fact that we did not find an effect of mate-guarding on UCP levels, suggest that energy intake and expenditure was balanced during mate-guarding in our study males. Mate-guarding thus seems to not be energetically costly under all circumstances. Given that in strictly seasonal rhesus macaques, high-ranking males lose physical condition over the mating period, we hypothesise that the energetic costs of mate-guarding vary inter-specifically depending on the degree of seasonality and that males of non-strictly seasonal species might be better adapted to maintain balanced energetic condition year-round. Finally, our results illustrate the importance of combining behavioural assessments of both energy intake and expenditure with physiological measures when investigating energetic costs of behavioural strategies.

Studies of the nutritional status of wild animals are important in a wide range of research areas such as ecology, behavioural ecology and reproductive biology. However, they have so far been strongly limited by the indirect nature of the available non-invasive tools for the measurement of individual energetic status. The measurement of urinary C-peptide (UCP), which in humans and great apes shows a close link to individual nutritional status, may be a more direct, non-invasive tool for such studies in other primates as well and possibly even in non-primate mammals. Here, we test the suitability of UCPs as markers of nutritional status in non-hominid primates, investigating relationships between UCPs and body-mass-index (BMI), skinfold fatness, and plasma C-peptide levels in captive and free-ranging macaques. We also conducted a food reduction experiment, with daily monitoring of body weight and UCP levels. UCP levels showed significant positive correlations with BMI and skinfold fatness in both captive and free-ranging animals and with plasma C-peptide levels in captive ones. In the feeding experiment, UCP levels were positively correlated with changes in body mass and were significantly lower during food reduction than during re-feeding and the pre-experimental control condition. We conclude that UCPs may be used as reliable biomarkers of body condition and nutritional status in studies of free-ranging catarrhines. Our results open exciting opportunities for energetic studies on free-ranging primates and possibly also other mammals. peerReviewed

Whereas it is well known that in strictly seasonal breeding primates (income breeders), alike other vertebrates, males show pronounced changes in testicular and adrenal hormone levels concurrent with reproductive activity, hormonal patterns in males of non-strictly seasonal breeding primate species (capital breeders) and their relation to seasonal and social correlates remain largely unknown. In the present study, we examined the annual pattern of fecal androgen and glucocorticoid excretion and their relationship to environmental (rainfall, temperature) and social factors (number of cycling females, male aggression and copulation rates, male dominance rank) in a group of wild long-tailed macaques (Macaca fascicularis), a species with a moderate degree of reproductive seasonality and classified as capital breeder. The study was carried out in the Gunung Leuser National Park, North Sumatra, Indonesia over a period of ten months encompassing the conception and the birth season. Our results show that male long-tailed macaques exhibit a distinct annual variation in both androgen and glucocorticoid levels. Androgen (but not glucocorticoid) levels were significantly elevated during the conception period in association with elevated rates of male-male aggression and copulatory activity, both strongly related to the number of cycling females in the group. Neither glucocorticoid nor androgen levels were related to male dominance rank or to the environmental parameters investigated. Interestingly, levels of both hormones started to increase in the late birth season and thus 1-2 months prior to the mating season, suggesting that male long-tailed macaques go through pre-breeding hormonal changes in preparation for prospective challenges. Our data thus provide the first evidence that males of a non-strictly seasonal breeding species/capital breeder show endocrine patterns generally similar to those found in strictly seasonal/income breeders.

Mate-guarding is an important determinant of male reproductive success in a number of species. Little is known however about the constraints of this behaviour, e.g. the associated energetic costs. We investigated these costs in long-tailed macaques where alpha males mate guard females to a lesser extent than predicted by the priority of access model. The study was carried out during two mating periods on three wild groups living in the Gunung Leuser National Park, Indonesia. We combined behavioural observations on males’ locomotion and feeding activity, GPS records of distance travelled and non-invasive measurements of urinary C-peptide (UCP), a physiological indicator of male energetic status. Mate-guarding led to a decrease in feeding time and fruit consumption suggesting a reduced intake of energy. At the same time, vertical locomotion was reduced, which potentially saved energy. These findings, together with the fact that we did not find an effect of mate-guarding on UCP levels, suggest that energy intake and expenditure was balanced during mate-guarding in our study males. Mate-guarding thus seems to not be energetically costly under all circumstances. Given that in strictly seasonal rhesus macaques, high-ranking males lose physical condition over the mating period, we hypothesise that the energetic costs of mate-guarding vary inter-specifically depending on the degree of seasonality and that males of non-strictly seasonal species might be better adapted to maintain balanced energetic condition year-round. Finally, our results illustrate the importance of combining behavioural assessments of both energy intake and expenditure with physiological measures when investigating energetic costs of behavioural strategies.

Nutritional status is a critical element of many aspects of animal ecology, but has proven difficult to measure non-invasively in studies of free-ranging animals. Urinary C-peptide of insulin (UCP), a small polypeptide cleaved in an equimolar ratio from proinsulin when the body converts it to insulin, offers great promise in this regard, and recent studies of several non-human primate species have utilized it with encouraging results. Despite this, there are a number of unresolved issues related to the collection, processing, storage and transport of samples. These include: contamination of samples on collection (most commonly by dirt or faeces), short-term storage before returning to a field station, differences in processing and long-term storage methods (blotting onto filter paper, freezing, lyophilizing), and for frozen samples, transportation while keeping samples frozen. Such issues have been investigated for urine samples in particular with respect to their effects on steroid hormone metabolites, but there has been little investigation of their effects on UCP measurement. We collected samples from captive macaques, and undertook a series of experiments where we systematically manipulated samples and tested the effects on subsequent UCP measurements. We show that contamination of urine samples by faeces led to a decrease in UCP levels by .90%, but that contamination with dirt did not have substantial effects. Short-term storage (up to 12 hours) of samples on ice did not affect UCP levels significantly, but medium-term storage (up to 78 hours) did. Freezing and lyophilization for long-term storage did not affect UCP levels, but blotting onto filter paper did. A transportation simulation showed that transporting frozen samples packed in ice and insulated should be acceptable, but only if it can be completed within a period of a few days and if freeze-thaw can be avoided. We use our data to make practical recommendations for fieldworkers. peerReviewed