Orangutan males make increased use of social learning opportunities, when resource availability is high.

Humans' colonization of diverse habitats relied on our ancestors' abilities to innovate and share innovations with others. While ecological impacts on innovations are well studied, their effect on social learning remains poorly understood. We examined how food availability affects social learning in migrant orangutan unflanged males, who may learn from local orangutans through peering (i.e., observational social learning). We analyzed 1,384 dyadic associations, including 360 peering events, among 46 wild Sumatran orangutan and 25 Bornean orangutan males, collected over 18 years. Migrants' peering rates significantly increased with higher food availability and time spent in proximity to others. Furthermore, migrants in the more sociable Sumatran population exhibited significantly higher peering rates compared to the Borneans, suggesting intrinsic and/or developmental effects of food availability on social learning. These findings emphasize the importance of investigating ecological effects on social learning on the immediate, developmental, and intrinsic levels for our understanding of cultural evolution.

Analysis of differences and commonalities in wildlife hunting across the Africa-Europe South-North gradient.

Hunting and its impacts on wildlife are typically studied regionally, with a particular focus on the Global South. Hunting can, however, also undermine rewilding efforts or threaten wildlife in the Global North. Little is known about how hunting manifests under varying socioeconomic and ecological contexts across the Global South and North. Herein, we examined differences and commonalities in hunting characteristics across an exemplary Global South-North gradient approximated by the Human Development Index (HDI) using face-to-face interviews with 114 protected area (PA) managers in 25 African and European countries. Generally, we observed that hunting ranges from the illegal, economically motivated, and unsustainable hunting of herbivores in the South to the legal, socially and ecologically motivated hunting of ungulates within parks and the illegal hunting of mainly predators outside parks in the North. Commonalities across this Africa-Europe South-North gradient included increased conflict-related killings in human-dominated landscapes and decreased illegal hunting with beneficial community conditions, such as mutual trust resulting from community involvement in PA management. Nevertheless, local conditions cannot outweigh the strong effect of the HDI on unsustainable hunting. Our findings highlight regional challenges that require collaborative, integrative efforts in wildlife conservation across actors, while identified commonalities may outline universal mechanisms for achieving this goal.

Temporal dynamics and fitness consequences of coalition formation in male primates.

Coalition formation is one of the most striking forms of cooperation found in animals. Yet, there is substantial variation between taxa regarding the mechanisms by which coalitions can result in fitness consequences. Here, we investigate the influence of coalitions on dominance rank trajectories and subsequently on reproductive success in wild male crested macaques (Macaca nigra) at Tangkoko Nature Reserve (Sulawesi, Indonesia). We observed 128 coalition events involving 28 males and tested how a variety of coalition properties and factors related to the social environment influenced future male rank. We further used genetic paternity analysis of 19 infants conceived during the study to assess male reproductive success. Our results show that males participating in coalitions achieved higher-than-expected future ranks, while coalition targets had lower-than-expected future ranks. Additionally, all-up coalitions had stronger effects on rank than all-down and bridging coalitions, and these were modulated by the relative strength of coalition partners versus targets. Finally, higher ranking males were more likely to sire infants than lower ranking males. These results provide important insights regarding the mechanisms underlying coalition formation and support the idea that one major path by which coalitions can affect fitness is through influencing male dominance trajectories.

Towards an understanding of multimodal traits of female reproduction in chimpanzees.

Although primates have long been regarded as microsmatic, recent studies indicate that olfaction is an important sensory mode of primate communication, e.g., in the context of reproduction. However, large gaps remain in our understanding of primate olfactory traits, especially in the great apes. Female chimpanzees (Pan troglodytes) possess an exaggerated sexual swelling, which is an imprecise signal of fertility that is thought to serve to confuse paternity. However, some high-ranking males that copulate most frequently on the days when females are most fertile seem to have more precise information on the timing of ovulation, which suggests the existence of an olfactory fertility trait. In order to examine, and provide evidence for, fertility-related chemical information in female chimpanzees, we used gas chromatography-mass spectrometry to analyze the chemical composition of female body odor collected across the menstrual cycle during various stages of sexual swelling (97 samples of six females). The chemical composition was significantly affected by swelling stage, and eight substances were detected that were strongly related to the latter. The existence of an additional, olfactory, fertility trait may help males to fine-tune their sexual behavior or allow females to strengthen concealment of the exact timing of ovulation, and needs to be further investigated in follow-up studies. The results of our study provide much-needed evidence for the existence of an olfactory cue related to reproduction in chimpanzees, and form a basis for future studies on the interplay between visual and olfactory information on female fertility.

An Online Unsupervised Dynamic Window Method to Track Repeating Patterns From Sensor Data.

Short bursts of repeating patterns [intervals of recurrence (IoR)] manifest themselves in many applications, such as in the time-series data captured from an athlete's movements using a wearable sensor while performing exercises. We present an efficient, online, one-pass, and real-time algorithm for finding and tracking IoR in a time-series data stream. We provide a detailed theoretical analysis of the behavior of any IoR and derive fundamental properties that can be used on real-world data streams. We show that why our method, unlike current state-of-the-art techniques, is robust to variations in repeats of the same pattern adjacent to each other. To evaluate our algorithm, we build a wearable device that runs our algorithm to conduct a user study. Our results show that our algorithm can detect intervals of repeating activities on edge devices with high accuracy (over 70% F1 -Score) and in a real-time environment with only a 1.5-s lag. Our experimental results from real-world datasets demonstrate that our approach outperforms state-of-the-art algorithms in both accuracy and robustness to variations of the signal of recurrence.

Occupancy of wild southern pig-tailed macaques in intact and degraded forests in Peninsular Malaysia.

Deforestation is a major threat to terrestrial tropical ecosystems, particularly in Southeast Asia where human activities have dramatic consequences for the survival of many species. However, responses of species to anthropogenic impact are highly variable. In order to establish effective conservation strategies, it is critical to determine a species' ability to persist in degraded habitats. Here, we used camera trapping data to provide the first insights into the temporal and spatial distribution of southern pig-tailed macaques (Macaca nemestrina, listed as 'Vulnerable' by the IUCN) across intact and degraded forest habitats in Peninsular Malaysia, with a particular focus on the effects of clear-cutting and selective logging on macaque occupancy. Specifically, we found a 10% decline in macaque site occupancy in the highly degraded Pasoh Forest Reserve from 2013 to 2017. This may be strongly linked to the macaques' sensitivity to intensive disturbance through clear-cutting, which significantly increased the probability that M. nemestrina became locally extinct at a previously occupied site. However, we found no clear relationship between moderate disturbance, i.e., selective logging, and the macaques' local extinction probability or site occupancy in the Pasoh Forest Reserve and Belum-Temengor Forest Complex. Further, an identical age and sex structure of macaques in selectively logged and completely undisturbed habitat types within the Belum-Temengor Forest Complex indicated that the macaques did not show increased mortality or declining birth rates when exposed to selective logging. Overall, this suggests that low to moderately disturbed forests may still constitute valuable habitats that support viable populations of M. nemestrina, and thus need to be protected against further degradation. Our results emphasize the significance of population monitoring through camera trapping for understanding the ability of threatened species to cope with anthropogenic disturbance. This can inform species management plans and facilitate the development of effective conservation measures to protect biodiversity.

Environmental variability supports chimpanzee behavioural diversity.

Large brains and behavioural innovation are positively correlated, species-specific traits, associated with the behavioural flexibility animals need for adapting to seasonal and unpredictable habitats. Similar ecological challenges would have been important drivers throughout human evolution. However, studies examining the influence of environmental variability on within-species behavioural diversity are lacking despite the critical assumption that population diversification precedes genetic divergence and speciation. Here, using a dataset of 144 wild chimpanzee (Pan troglodytes) communities, we show that chimpanzees exhibit greater behavioural diversity in environments with more variability - in both recent and historical timescales. Notably, distance from Pleistocene forest refugia is associated with the presence of a larger number of behavioural traits, including both tool and non-tool use behaviours. Since more than half of the behaviours investigated are also likely to be cultural, we suggest that environmental variability was a critical evolutionary force promoting the behavioural, as well as cultural diversification of great apes.

Group-specific archaeological signatures of stone tool use in wild macaques.

Stone tools in the prehistoric record are the most abundant source of evidence for understanding early hominin technological and cultural variation. The field of primate archaeology is well placed to improve our scientific knowledge by using the tool behaviours of living primates as models to test hypotheses related to the adoption of tools by early stone-age hominins. Previously we have shown that diversity in stone tool behaviour between neighbouring groups of long-tailed macaques (Macaca-fascicularis) could be explained by ecological and environmental circumstances (Luncz et al., 2017b). Here however, we report archaeological evidence, which shows that the selection and reuse of tools cannot entirely be explained by ecological diversity. These results suggest that tool-use may develop differently within species of old-world monkeys, and that the evidence of material culture can differ within the same timeframe at local geographic scales and in spite of shared environmental and ecological settings.

Human impact erodes chimpanzee behavioral diversity.

Chimpanzees possess a large number of behavioral and cultural traits among nonhuman species. The "disturbance hypothesis" predicts that human impact depletes resources and disrupts social learning processes necessary for behavioral and cultural transmission. We used a dataset of 144 chimpanzee communities, with information on 31 behaviors, to show that chimpanzees inhabiting areas with high human impact have a mean probability of occurrence reduced by 88%, across all behaviors, compared to low-impact areas. This behavioral diversity loss was evident irrespective of the grouping or categorization of behaviors. Therefore, human impact may not only be associated with the loss of populations and genetic diversity, but also affects how animals behave. Our results support the view that "culturally significant units" should be integrated into wildlife conservation.

Which male and female characteristics influence the probability of extragroup paternities in rhesus macaques, Macaca mulatta?

Extragroup paternity (EGP) is found across a wide range of species and may entail reproductive benefits, but may also entail costs to both sexes. While population and group parameters affecting the degree of EGPs are relatively well established, less is known about the individual characteristics that make males and females engage in alternative reproductive tactics such as EGP. Applying a combination of long-term demographic and genetic data from the rhesus macaque population of Cayo Santiago (Puerto Rico, U.S.A.), we investigate which male and female characteristics influence the probability of EGP to better understand the circumstances that shape the distribution and occurrence of EGP. Our results show that, against our expectations, higher-ranking females were more likely to produce EGP offspring than lower- ranking females. The probability of producing extragroup offspring was not significantly related to female or male age, male tenure or previous reproductive success. Furthermore, genetic relatedness between the parents did not affect the production of extragroup offspring, but extragroup offspring were more frequently produced early rather than late in a given mating season. Altogether, our analysis suggests that individual attributes and seasonal aspects create different opportunities and preferences for engaging in EGP as an alternative reproductive tactic. The observed patterns of EGP in rhesus macaques appear to be consistent with female mate choice for genetic benefits, which needs to be confirmed in future studies.

Parent-offspring facial resemblance increases with age in rhesus macaques.

Kin recognition is a key ability which facilitates the acquisition of inclusive fitness benefits and enables optimal outbreeding. In primates, phenotype matching is considered particularly important for the recognition of patrilineal relatives, as information on paternity is unlikely to be available via social familiarity. Phenotypic cues to both paternal and maternal relatedness exist in the facial features of humans and other primates. However, theoretical models suggest that in systems with uncertainty parentage it may be adaptive for offspring to conceal such cues when young, in order to avoid potential costs of being discriminated against by unrelated adults. Using experienced human raters, we demonstrate in a computer-based task that detection of parent-offspring resemblances in the faces of rhesus macaques (Macaca mulatta) increases significantly with offspring age. Moreover, this effect is specific to information about kinship, as raters were extremely successful at discriminating individuals even among the youngest animals. To our knowledge, this is the first evidence in non-humans for the age-dependent expression of visual cues used in kin recognition.

Chemical composition of axillary odorants reflects social and individual attributes in rhesus macaques.

ABSTRACT: Scents play an important role in the life of most terrestrial mammals and may transmit valuable information about conspecifics. Olfaction was long considered of low importance in Old World monkeys due to their relative reduction of olfactory structures and low incidence of scent-marking behavior but has been increasingly recognized for mediating social relationships in recent years. Yet, studies investigating the composition of their chemical cues remain scarce. In the present study, we analyzed the potential information content of chemicals present on the skin of rhesus macaques (Macaca mulatta). We collected axillary secretions from 60 animals of the semifree-ranging population on Cayo Santiago (Puerto Rico, USA) with precleaned cotton swabs from which the secretions were subsequently extracted and analyzed by gas chromatography-mass spectrometry. Rhesus macaque axillary odorants varied in their overall similarity and composition. This variation was attributable to differences in sex, group membership, and kinship and further appeared to reflect age and rank in parts of our sample. The compounds most strongly associated with this variation primarily comprised larger molecular weight aldehydes and steroids. Such compounds are considered to be perceivable by the primate olfactory system through close-range interactions or through breakdown into smaller molecules by bacterial fermentation. Overall, our results provide additional evidence that odors of Old World monkeys reflect a wealth of potential information about their carrier, which provides the basis for chemical communication via body odors; however, its use by conspecifics needs to be confirmed in bioassays. SIGNIFICANCE STATEMENT: One prerequisite for olfactory communication is the presence of systematic variation in animal odors that is related to attributes such as age, sex, or kinship. The composition of odors has been examined in numerous mammals but, with the exception of humans, remains poorly understood in Old World monkeys and apes, taxonomic groups in which most species do not show scent-marking behavior. In the present study, we show that the composition of axillary secretions of an Old World monkey, the rhesus macaque, reflects sex, group membership, relatedness, and possibly also age and rank. This variation thus provides a basis for olfactory communication in Old World monkeys.

Resource depletion through primate stone technology.

Tool use has allowed humans to become one of the most successful species. However, tool-assisted foraging has also pushed many of our prey species to extinction or endangerment, a technology-driven process thought to be uniquely human. Here, we demonstrate that tool-assisted foraging on shellfish by long-tailed macaques (Macaca fascicularis) in Khao Sam Roi Yot National Park, Thailand, reduces prey size and prey abundance, with more pronounced effects where the macaque population size is larger. We compared availability, sizes and maturation stages of shellfish between two adjacent islands inhabited by different-sized macaque populations and demonstrate potential effects on the prey reproductive biology. We provide evidence that once technological macaques reach a large enough group size, they enter a feedback loop - driving shellfish prey size down with attendant changes in the tool sizes used by the monkeys. If this pattern continues, prey populations could be reduced to a point where tool-assisted foraging is no longer beneficial to the macaques, which in return may lessen or extinguish the remarkable foraging technology employed by these primates.

Long-term analysis on the variance of extra-group paternities in rhesus macaques.

ABSTRACT: Extra-group paternity (EGP) has been described in various mammalian species; however, little is known about which factors contribute to the variation in EGP, as the majority of studies were restricted in time and the number of groups considered. Using longitudinal demographic and genetic data, we aim to investigate which factors predict rates of EGP in the free-ranging rhesus macaque population of Cayo Santiago, Puerto Rico (USA). Of the 1649 infants considered which were born into six social groups over 9 years, we identified an average of 16% of infants resulting from EGPs. We tested the influence of group size, breeding group sex ratio, female reproductive synchrony, and group instability on the occurrence of EGPs. Our results suggest a tendency for EGPs to increase as the proportion of females increased in larger groups, but no such effect in smaller groups. Furthermore, as group instability and female reproductive synchrony decreased, the number of EGPs tended to increase. Our results support the hypothesis that group structure affects the occurrence of EGPs, which might be mediated by male mating opportunities, male monopolization potential, and/or female choice. SIGNIFICANCE STATEMENT: In several species, both sexes seek alternative reproductive strategies to enhance their reproductive success. For instance, females may pursue EGPs to potentially increase genetic compatibility with males, or males may seek EGPs to improve their mating opportunities. Our longitudinal analysis, including demographic and genetic data over 9 years of six social groups of rhesus macaques, revealed high variation in the occurrence of EGPs across groups and years, and this variation tended to depend on group characteristics such as breeding group size, sex ratio, female synchrony, and group instability. The data suggest that group structure affects the number of EGPs in this group-living primate. Our results show that EGPs can affect the distribution of paternity within social groups and should be taken into account when assessing reproductive success.

Automated face detection for occurrence and occupancy estimation in chimpanzees.

Surveying endangered species is necessary to evaluate conservation effectiveness. Camera trapping and biometric computer vision are recent technological advances. They have impacted on the methods applicable to field surveys and these methods have gained significant momentum over the last decade. Yet, most researchers inspect footage manually and few studies have used automated semantic processing of video trap data from the field. The particular aim of this study is to evaluate methods that incorporate automated face detection technology as an aid to estimate site use of two chimpanzee communities based on camera trapping. As a comparative baseline we employ traditional manual inspection of footage. Our analysis focuses specifically on the basic parameter of occurrence where we assess the performance and practical value of chimpanzee face detection software. We found that the semi-automated data processing required only 2-4% of the time compared to the purely manual analysis. This is a non-negligible increase in efficiency that is critical when assessing the feasibility of camera trap occupancy surveys. Our evaluations suggest that our methodology estimates the proportion of sites used relatively reliably. Chimpanzees are mostly detected when they are present and when videos are filmed in high-resolution: the highest recall rate was 77%, for a false alarm rate of 2.8% for videos containing only chimpanzee frontal face views. Certainly, our study is only a first step for transferring face detection software from the lab into field application. Our results are promising and indicate that the current limitation of detecting chimpanzees in camera trap footage due to lack of suitable face views can be easily overcome on the level of field data collection, that is, by the combined placement of multiple high-resolution cameras facing reverse directions. This will enable to routinely conduct chimpanzee occupancy surveys based on camera trapping and semi-automated processing of footage. RESEARCH HIGHLIGHTS: Using semi-automated ape face detection technology for processing camera trap footage requires only 2-4% of the time compared to manual analysis and allows to estimate site use by chimpanzees relatively reliably.

Low incidence of inbreeding in a long-lived primate population isolated for 75 years.

ABSTRACT: When close relatives mate, offspring are expected to suffer fitness consequences due to inbreeding depression. Inbreeding has previously been quantified in two ways: using a sufficiently large panel of markers or deep and complete pedigrees over several generations. However, the application of both approaches is still limited by the challenge of compiling such data for species with long generation times, such as primates. Here, we assess inbreeding in rhesus macaques living on Cayo Santiago (Puerto Rico), a population genetically isolated since 1938, but descendant of a large set of presumably unrelated founders. Using comprehensive genetic data, we calculated inbreeding coefficients (F) for 2669 individuals with complete three generation pedigrees and 609 individuals with complete four generation pedigrees. We found that 0.79 and 7.39% of individuals had an F > 0 when using data from three and four generation pedigrees, respectively. No evidence of an increase in inbreeding over the study period (up to 23 years) was found. Furthermore, the observed mean relatedness of breeding pairs differed significantly from the distribution of parental relatedness expected as simulated based on previous reproductive data, suggesting that kin generally avoid breeding with each other. Finally, inbreeding was not a predictor of early mortality measured as survival until weaning and sexual maturation, respectively. Our results remain consistent with three estimators of inbreeding (standardized heterozygosity, internal relatedness, and homozygosity by loci) using up to 42 highly polymorphic microsatellites for the same set of individuals. Together, our results demonstrate that close inbreeding may not be prevalent even in populations isolated over long periods when mechanisms of inbreeding avoidance can operate. SIGNIFICANCE STATEMENT: When close relatives mate, offspring may suffer from such inbreeding, e.g., via lower survival and/or fertility. Using (i) a large panel of genetic markers and (ii) complete three or four generation pedigrees, respectively, we show that incidences of inbreeding in a long-lived primate population are rare, even after genetic isolation for 75 years. Moreover, our simulations suggest that kin in our population generally avoid breeding with each other. Finally, the few inbred individuals detected in our large sample did not suffer from lower survival. Given that many animal species face dramatic habitat loss combined with critical population declines, our study provides important implications for conservation biology in general and for population management in particular.

Distance-decay effect in stone tool transport by wild chimpanzees.

Stone tool transport leaves long-lasting behavioural evidence in the landscape. However, it remains unknown how large-scale patterns of stone distribution emerge through undirected, short-term transport behaviours. One of the longest studied groups of stone-tool-using primates are the chimpanzees of the Taï National Park in Ivory Coast, West Africa. Using hammerstones left behind at chimpanzee Panda nut-cracking sites, we tested for a distance-decay effect, in which the weight of material decreases with increasing distance from raw material sources. We found that this effect exists over a range of more than 2 km, despite the fact that observed, short-term tool transport does not appear to involve deliberate movements away from raw material sources. Tools from the millennia-old Noulo site in the Taï forest fit the same pattern. The fact that chimpanzees show both complex short-term behavioural planning, and yet produce a landscape-wide pattern over the long term, raises the question of whether similar processes operate within other stone-tool-using primates, including hominins. Where hominin landscapes have discrete material sources, a distance-decay effect, and increasing use of stone materials away from sources, the Taï chimpanzees provide a relevant analogy for understanding the formation of those landscapes.

Individual dispersal decisions affect fitness via maternal rank effects in male rhesus macaques.

Natal dispersal may have considerable social, ecological and evolutionary consequences. While species-specific dispersal strategies have received much attention, individual variation in dispersal decisions and its fitness consequences remain poorly understood. We investigated causes and consequences of natal dispersal age in rhesus macaques (Macaca mulatta), a species with male dispersal. Using long-term demographic and genetic data from a semi-free ranging population on Cayo Santiago, Puerto Rico, we analysed how the social environment such as maternal family, group and population characteristics affected the age at which males leave their natal group. While natal dispersal age was unrelated to most measures of group or population structure, our study confirmed earlier findings that sons of high-ranking mothers dispersed later than sons of low-ranking ones. Natal dispersal age did not affect males' subsequent survival, but males dispersing later were more likely to reproduce. Late dispersers were likely to start reproducing while still residing in their natal group, frequently produced extra-group offspring before natal dispersal and subsequently dispersed to the group in which they had fathered offspring more likely than expected. Hence, the timing of natal dispersal was affected by maternal rank and influenced male reproduction, which, in turn affected which group males dispersed to.