Women's subsistence networks scaffold cultural transmission among BaYaka foragers in the Congo Basin.

In hunter-gatherer societies, women's subsistence activities are crucial for food provisioning and children's social learning but are understudied relative to men's activities. To understand the structure of women's foraging networks, we present 230 days of focal-follow data in a BaYaka community. To analyze these data, we develop a stochastic blockmodel for repeat observations with uneven sampling. We find that women's subsistence networks are characterized by cooperation between kin, gender homophily, and mixed age-group composition. During early childhood, individuals preferentially coforage with adult kin, but those in middle childhood and adolescence are likely to coforage with nonkin peers, providing opportunities for horizontal learning. By quantifying the probability of coforaging ties across age classes and relatedness levels, our findings provide insights into the scope for social learning during women's subsistence activities in a real-world foraging population and provide ground-truth values for key parameters used in formal models of cumulative culture.

Music production and its role in coalition signaling during foraging contexts in a hunter-gatherer society.

Music is a cultural activity universally present in all human societies. Several hypotheses have been formulated to understand the possible origins of music and the reasons for its emergence. Here, we test two hypotheses: (1) the coalition signaling hypothesis which posits that music could have emerged as a tool to signal cooperative intent and signal strength of alliances and (2) music as a strategy to deter potential predators. In addition, we further explore the link between tactile cues and the propensity of mothers to sing toward infants. For this, we investigated the singing behaviors of hunter-gatherer mothers during daily foraging trips among the Mbendjele BaYaka in the Republic of the Congo. Although singing is a significant component of their daily activities, such as when walking in the forest or collecting food sources, studies on human music production in hunter-gatherer societies are mostly conducted during their ritual ceremonies. In this study, we collected foraging and singing behavioral data of mothers by using focal follows of five BaYaka women during their foraging trips in the forest. In accordance with our predictions for the coalition signaling hypothesis, women were more likely to sing when present in large groups, especially when group members were less familiar. However, predictions of the predation deterrence hypothesis were not supported as the interaction between group size and distance from the village did not have a significant effect on the likelihood of singing. The latter may be due to limited variation in predation risk in the foraging areas, because of the intense bush meat trade, and hence, future studies should include foraging areas with higher densities of wild animals. Lastly, we found that mothers were more likely to sing when they were carrying infants compared to when infants were close, but carried by others, supporting the prediction that touch plays an important prerequisite role in musical interaction between the mother and child. Our study provides important insight into the role of music as a tool in displaying the intent between or within groups to strengthen potentially conflict-free alliances during joint foraging activities.

Girls in early childhood increase food returns of nursing women during subsistence activities of the BaYaka in the Republic of Congo.

Nursing mothers face an energetic trade-off between infant care and work. Under pooled energy budgets, this trade-off can be reduced by assistance in food acquisition and infant care tasks from non-maternal carers. Across cultures, children also often provide infant care. Yet the question of who helps nursing mothers during foraging has been understudied, especially the role of children. Using focal follow data from 140 subsistence expeditions by BaYaka women in the Republic of Congo, we investigated how potential support from carers increased mothers' foraging productivity. We found that the number of girls in early childhood (ages 4-7 years) in subsistence groups increased food returns of nursing women with infants (kcal collected per minute). This effect was stronger than that of other adult women, and older girls in middle childhood (ages 8-13 years) and adolescence (ages 14-19 years). Child helpers were not necessarily genetically related to nursing women. Our results suggest that it is young girls who provide infant care while nursing mothers are acquiring food-by holding, monitoring and playing with infants-and, thus, that they also contribute to the energy pool of the community during women's subsistence activities. Our study highlights the critical role of children as carers from early childhood.

Chimpanzees (Pan troglodytes) navigate to find hidden fruit in a virtual environment.

Almost all animals navigate their environment to find food, shelter, and mates. Spatial cognition of nonhuman primates in large-scale environments is notoriously difficult to study. Field research is ecologically valid, but controlling confounding variables can be difficult. Captive research enables experimental control, but space restrictions can limit generalizability. Virtual reality technology combines the best of both worlds by creating large-scale, controllable environments. We presented six chimpanzees with a seminaturalistic virtual environment, using a custom touch screen application. The chimpanzees exhibited signature behaviors reminiscent of real-life navigation: They learned to approach a landmark associated with the presence of fruit, improving efficiency over time; they located this landmark from novel starting locations and approached a different landmark when necessary. We conclude that virtual environments can allow for standardized testing with higher ecological validity than traditional tests in captivity and harbor great potential to contribute to longstanding questions in primate navigation, e.g., the use of landmarks, Euclidean maps, or spatial frames of reference.

Using natural travel paths to infer and compare primate cognition in the wild.

Within comparative psychology, the evolution of animal cognition is typically studied either by comparing indirect measures of cognitive abilities (e.g., relative brain size) across many species or by conducting batteries of decision-making experiments among (typically) a few captive species. Here, we propose a third, complementary approach: inferring and comparing cognitive abilities through observational field records of natural information gradients and the associated variation in decision-making outcomes, using the ranging behavior of wild animals. To demonstrate the feasibility of our proposal, we present the results of a global survey assessing the availability of long-term ranging data sets from wild primates and the willingness of primatologists to share such data. We explore three ways in which such ranging data, with or without the associated behavioral and ecological data often collected by primatologists, might be used to infer and compare spatial cognition. Finally, we suggest how ecological complexity may be best incorporated into comparative analyses.

Mandrills learn two-day time intervals in a naturalistic foraging situation.

Primates display high efficiency in finding food in complex environments. Knowledge that many plant species produce fruit simultaneously, can help primates to anticipate fruit finding at the start of fruiting seasons. Knowledge of elapsed time can help primates decide when to revisit food trees to find ripened fruit and to return before competitors find these fruits. To investigate whether mandrills are able to learn time intervals of recurring food, we recorded the foraging choices of captive mandrills in a group setting. We used a procedure with renewable food rewards that could be searched for: carrots and grapes, hidden underground in specific places with different renewal intervals (2 and 5 days, respectively). We monitored the first choice of location for individuals, if other individuals had not already searched at the same location, to exclude possible effects of individuals following others rather than relying on memory. Throughout the study, the mandrills became increasingly likely to first search at carrot locations on carrot days, while the probability of them searching at carrot locations decreased on days without carrot. Due to model instability, our results were inconclusive about an effect of grape days on the choice of the mandrills. Cues provided by conspecifics indicating the availability of simultaneously emerging food rewards did not affect the choice of the mandrills. We conclude that mandrills can take into account elapsed time in a foraging context. Thereby, this study indicates how mandrills can use temporal cognitive abilities to overcome temporal challenges of food-finding in a group setting.

Travel linearity and speed of human foragers and chimpanzees during their daily search for food in tropical rainforests.

To understand the evolutionary roots of human spatial cognition, researchers have compared spatial abilities of humans and one of our closest living relatives, the chimpanzee (Pan troglodytes). However, how humans and chimpanzees compare in solving spatial tasks during real-world foraging is unclear to date, as measuring such spatial abilities in natural habitats is challenging. Here we compared spatial movement patterns of the Mbendjele BaYaka people and the Taï chimpanzees during their daily search for food in rainforests. We measured linearity and speed during off-trail travels toward out-of-sight locations as proxies for spatial knowledge. We found similarly high levels of linearity in individuals of Mbendjele foragers and Taï chimpanzees. However, human foragers and chimpanzees clearly differed in their reactions to group size and familiarity with the foraging areas. Mbendjele foragers increased travel linearity with increasing familiarity and group size, without obvious changes in speed. This pattern was reversed in Taï chimpanzees. We suggest that these differences between Mbendjele foragers and Taï chimpanzees reflect their different ranging styles, such as life-time range size and trail use. This result highlights the impact of socio-ecological settings on comparing spatial movement patterns. Our study provides a first step toward comparing long-range spatial movement patterns of two closely-related species in their natural environments.

What animals do not do or fail to find: A novel observational approach for studying cognition in the wild.

To understand how our brain evolved and what it is for, we are in urgent need of knowledge about the cognitive skills of a large variety of animal species and individuals, and their relationships to rapidly disappearing social and ecological conditions. But how do we obtain this knowledge? Studying cognition in the wild is a challenge. Field researchers (and their study subjects) face many factors that can easily interfere with their variables of interest. Although field studies of cognition present unique challenges, they are still invaluable for understanding the evolutionary drivers of cognition. In this review, I discuss the advantages and urgency of field-based studies on animal cognition and introduce a novel observational approach for field research that is guided by three questions: (a) what do animals fail to find?, (b) what do they not do?, and (c) what do they only do when certain conditions are met? My goal is to provide guidance to future field researchers examining primate cognition.

Sun, age and test location affect spatial orientation in human foragers in rainforests.

The ability to know the direction of food sources is important for the foraging success of hunter-gatherers, especially in rainforests where dense vegetation limits visual detection distances. Besides sex and age, prior experience with the environment and the use of environmental cues are known to influence orientation abilities of humans. Among environmental cues, the position of the sun in the sky is important for orientation of diurnal animal species. However, whether or to what extent humans use the sun is largely unknown. Here, we investigated orientation abilities of the Mbendjele BaYaka people in the Republic of Congo, by conducting pointing tests (Nparticipants = 54, age: 6-76 years) in different locations in the rainforest. The Mbendjele were overall highly accurate at pointing to out-of-sight targets (median error: 6°). Pointing accuracy increased with age, but sex did not affect accuracy. Crucially, sun visibility increased pointing accuracy in young participants, especially when they were far from the camp. However, this effect became less apparent in older participants who exhibited high pointing accuracy, also when the sun was not visible. This study extends our understandings of orientation abilities of human foragers and provides the first behavioural evidence for sun compass use in humans.

Sooty mangabeys scavenge on nuts cracked by chimpanzees and red river hogs-An investigation of inter-specific interactions around tropical nut trees.

Carrion scavenging is a well-studied phenomenon, but virtually nothing is known about scavenging on plant material, especially on remnants of cracked nuts. Just like meat, the insides of hard-shelled nuts are high in energetic value, and both foods are difficult to acquire. In the Taï forest, chimpanzees (Pan troglodytes) and red river hogs (Potamochoerus porcus) crack nuts by using tools or strong jaws, respectively. In this study, previously collected non-invasive camera trap data were used to investigate scavenging by sooty mangabeys (Cercocebus atys), two species of Guinea fowl (Agelestres meleagrides; Guttera verreauxi), and squirrels (Scrunidae spp.) on the nut remnants cracked by chimpanzees and red river hogs. We investigated how scavengers located nut remnants, by analyzing their visiting behavior in relation to known nut-cracking events. Furthermore, since mangabeys are infrequently preyed upon by chimpanzees, we investigated whether they perceive an increase in predation risk when approaching nut remnants. In total, 190 nut-cracking events were observed in four different areas of Taï National Park, Ivory Coast. We could confirm that mangabeys scavenged on the nuts cracked by chimpanzees and hogs and that this enabled them to access food source that would not be accessible otherwise. We furthermore found that mangabeys, but not the other species, were more likely to visit nut-cracking sites after nut-cracking activities than before, and discuss the potential strategies that the monkeys could have used to locate nut remnants. In addition, mangabeys showed elevated levels of vigilance at the chimpanzee nut-cracking sites compared with other foraging sites, suggesting that they perceived elevated danger at these sites. Scavenging on remnants of cracked nuts is a hitherto understudied type of foraging behavior that could be widespread in nature and increases the complexity of community ecology in tropical rainforests.

Spatio-temporal complexity of chimpanzee food: How cognitive adaptations can counteract the ephemeral nature of ripe fruit.

Ecological complexity has been proposed to play a crucial role in primate brain-size evolution. However, detailed quantification of ecological complexity is still limited. Here we assess the spatio-temporal distribution of tropical fruits and young leaves, two primary chimpanzee (Pan troglodytes) foods, focusing on the predictability of their availability in individual trees. Using up to 20 years of information on monthly availability of young leaf, unripe and ripe fruit in plant species consumed by chimpanzees from tropical forests in East, Central, and West Africa, we estimated: (1) the forest-wide frequency of occurrence of each food type and (2) the predictability of finding ripe fruit-bearing trees, focusing on the timing, frequency, and amount of ripe fruit present. In all three forests, at least half of all encountered trees belonged to species that chimpanzees were known to feed on. However, the proportion of these trees bearing young leaves and fruit fluctuated widely between months. Ripe fruit was the most ephemeral food source, and trees that had more than half of their crown filled were at least nine times scarcer than other trees. In old growth forests only one large ripe fruit crop was on average encountered per 10 km. High levels of inter-individual variation in the number of months that fruit was present existed, and in some extreme cases individuals bore ripe fruit more than seven times as often as conspecifics. Some species showed substantially less variation in such ripe fruit production frequencies and fruit quantity than others. We hypothesize that chimpanzees employ a suite of cognitive mechanisms, including abilities to: (1) generalize or classify food trees; (2) remember the relative metrics of quantity and frequency of fruit production across years; and (3) flexibly plan return times to feeding trees to optimize high-energy food consumption in individual trees, and efficient travel between them. Am. J. Primatol. 78:626-645, 2016. © 2016 Wiley Periodicals, Inc.

Wild chimpanzees plan their breakfast time, type, and location.

Not all tropical fruits are equally desired by rainforest foragers and some fruit trees get depleted more quickly and carry fruit for shorter periods than others. We investigated whether a ripe-fruit specialist, the chimpanzee (Pan troglodytes verus), arrived earlier at breakfast sites with very ephemeral and highly sought-after fruit, like figs, than sites with less ephemeral fruit that can be more predictably obtained throughout the entire day. We recorded when and where five adult female chimpanzees spent the night and acquired food for a total of 275 full days during three fruit-scarce periods in a West African tropical rainforest. We found that chimpanzees left their sleeping nests earlier (often before sunrise when the forest is still dark) when breakfasting on very ephemeral fruits, especially when they were farther away. Moreover, the females positioned their sleeping nests more in the direction of the next day's breakfast sites with ephemeral fruit compared with breakfast sites with other fruit. By analyzing departure times and nest positioning as a function of fruit type and location, while controlling for more parsimonious explanations, such as temperature, we found evidence that wild chimpanzees flexibly plan their breakfast time, type, and location after weighing multiple disparate pieces of information. Our study reveals a cognitive mechanism by which large-brained primates can buffer the effects of seasonal declines in food availability and increased interspecific competition to facilitate first access to nutritious food. We discuss the implications for theories on hominoid brain-size evolution.

Taï chimpanzees anticipate revisiting high-valued fruit trees from further distances.

The use of spatio-temporal memory has been argued to increase food-finding efficiency in rainforest primates. However, the exact content of this memory is poorly known to date. This study investigated what specific information from previous feeding visits chimpanzees (Pan troglodytes verus), in Taï National Park, Côte d'Ivoire, take into account when they revisit the same feeding trees. By following five adult females for many consecutive days, we tested from what distance the females directed their travels towards previously visited feeding trees and how previous feeding experiences and fruit tree properties influenced this distance. To exclude the influence of sensory cues, the females' approach distance was measured from their last significant change in travel direction until the moment they entered the tree's maximum detection field. We found that chimpanzees travelled longer distances to trees at which they had previously made food grunts and had rejected fewer fruits compared to other trees. In addition, the results suggest that the chimpanzees were able to anticipate the amount of fruit that they would find in the trees. Overall, our findings are consistent with the hypothesis that chimpanzees act upon a retrieved memory of their last feeding experiences long before they revisit feeding trees, which would indicate a daily use of long-term prospective memory. Further, the results are consistent with the possibility that positive emotional experiences help to trigger prospective memory retrieval in forest areas that are further away and have fewer cues associated with revisited feeding trees.

Taï chimpanzees use botanical skills to discover fruit: what we can learn from their mistakes.

Fruit foragers are known to use spatial memory to relocate fruit, yet it is unclear how they manage to find fruit in the first place. In this study, we investigated whether chimpanzees (Pan troglodytes verus) in the Taï National Park make use of fruiting synchrony, the simultaneous emergence of fruit in trees of the same species, which can be used together with sensory cues, such as sight and smell, to discover fruit. We conducted observations of inspections, the visual checking of fruit availability in trees, and focused our analyses on inspections of empty trees, so to say "mistakes". Learning from their "mistakes", we found that chimpanzees had expectations of finding fruit days before feeding on it and significantly increased inspection activity after tasting the first fruit. Neither the duration of feeding nor density of fruit-bearing trees in the territory could account for the variation in inspection activity, which suggests chimpanzees did not simply develop a taste for specific fruit on which they had fed frequently. Instead, inspection activity was predicted by a botanical feature-the level of synchrony in fruit production of encountered trees. We conclude that chimpanzees make use of the synchronous emergence of rainforest fruits during daily foraging and base their expectations of finding fruit on a combination of botanical knowledge founded on the success rates of fruit discovery, and a categorization of fruit species. Our results provide new insights into the variety of food-finding strategies employed by primates and the adaptive value of categorization capacities.

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

We investigated long-term site fidelity of gray-cheeked mangabey (Lophocebus albigena) groups in Kibale National Park, Uganda. Concurrently, we monitored shifts in home range by individual females and subadult and adult males. We documented home range stability by calculating the area of overlap in successive years, and by recording the drift of each group's monthly centroid from its initial location. Home ranges remained stable for 3 of our 4 groups (overlap over 10 yr >60%). Core areas were more labile, but group centroids drifted an average of only 530 m over the entire decade. Deviations from site fidelity were associated with dispersal or group fission. During natal dispersal, subadult males expanded their home ranges over many months, settling

Primates take weather into account when searching for fruits.

Temperature and solar radiation are known to influence maturation of fruits and insect larvae inside them . We investigated whether gray-cheeked mangabeys (Lophocebus albigena johnstonii) of Kibale Forest, Uganda, take these weather variables into account when searching for ripe figs or unripe figs containing insect larvae. We predicted that monkeys would be more likely to revisit a tree with fruit after several days of warm and sunny weather compared to a cooler and more cloudy period. We preselected 80 target fig trees and monitored whether they contained ripe, unripe, or no fruit. We followed one habituated monkey group from dawn to dusk for three continuous observation periods totalling 210 days. Whenever the group came within a 100 m circle of a previously visited target tree for a second time, we noted whether or not individuals proceeded to the trunk, i.e., whether they "revisited" or simply "bypassed" the tree. We found that average daily maximum temperature was significantly higher for days preceding revisits than bypasses. The probability of a revisit was additionally influenced by solar radiation experienced on the day of reapproach. These effects were found only for trees that carried fruit at the previous visit but not for trees that had carried none. We concluded that these nonhuman primates were capable of taking into account past weather conditions when searching for food. We discuss the implication of these findings for theories of primate cognitive evolution.