Lethal combats in the forest among wild western gorillas.

Lethal intergroup encounters occur in many species because of sexual selection. While documented in mountain gorillas, they are absent in western gorillas as, instead, it is predicted by their higher feeding (frugivory) and mate competition (single-vs. multi-male groups). We investigate whether the injuries on three dead silverbacks and one adult female from four groups of western gorillas in the Central African Republic, resulted from interactions with gorillas or leopards. We identified two distinct injury patterns caused by gorillas (isolated lacerations, round wounds) and leopards (punctures clustered on head/neck) by analyzing injuries caused by mountain gorillas and leopards to gorillas and non-gorilla species, respectively. The western gorilla injury pattern is similar to that of mountain gorillas suggesting that lethal encounters occur, albeit infrequently, as predicted by sexual selection in a one-male society. While sexual dimorphism and polygynous sociality favored the evolution of violent encounters, multiple males in groups may influence their frequency.

High urinary oxidative DNA damage in wild chimpanzees ranging in proximity of agricultural fields in Sebitoli area, Uganda.

Agriculture expansion is a major cause of habitat loss and exposure to phytochemical pollution for non-human primates. In addition to endocrine disruption, exposure to pesticides may have other sublethal physiological consequences for animals, such as generation of oxidative damage to macromolecules. In this study, we analyzed the pesticides contained in the river water across the home range of wild chimpanzees (Pan troglodytes) in Sebitoli area located on the Northern part of Kibale National Park (Uganda). We tested whether levels of three urinary markers of oxidative damage vary among individuals in relation to their ranging patterns, as a proxy for pesticide exposure intensity. To better characterize the foraging habitat use, the trophic level, and the energetic status of study individuals, we also quantified urinary levels of carbon and nitrogen stable isotope signatures and of C-peptide. Among the 511 pesticides screened, 18 compounds including herbicides, insecticides, and fungicides were found in the water sampled in the Western part of the home range of chimpanzees. In this area, chimpanzees used to feed on maize crops. By contrast, in the Eastern part where crop feeding was never observed, we found only seven pesticides. According to their ranging patterns and thus crop feeding frequency, the 139 urine samples collected from 43 Sebitoli chimpanzees were categorized as belonging to low, medium, and high exposure level. Chimpanzees from the high exposure zone had higher oxidative DNA damage (8-OHdG) than chimpanzees from both the low and medium exposure groups, who had similar levels of oxidative DNA damage. In addition, individuals with higher C-peptide tended to have significantly higher oxidative DNA damage and lipid peroxides. The three exposure groups had similar levels of urinary 8-isoprostanes and of urinary lipid peroxides. These results were robust for any potential confounding effect of other variables because neither age category nor sex or isotope levels were significantly associated with markers of oxidative damage. Our study points to genotoxic effects as one potential sublethal consequence of ranging in proximity of agricultural fields owing to exposure to pesticides or other unidentified sources of stress. Given our phylogenetic proximity, this information is relevant for the conservation of this species which is endangered and also sentinel for human health.

Feeling a bit peckish: Seasonal and opportunistic insectivory for wild gorillas.

OBJECTIVES: Insectivory likely contributed to survival of early humans in diverse conditions and influenced human cognitive evolution through the need to develop harvesting tools. In living primates, insectivory is a widespread behavior and frequently seasonal, although previous studies do not always agree on reasons behind this. Since western gorillas (Gorilla gorilla) diet is largely affected by seasonal variation in fruit availability, we aimed to test three non-mutually exclusive hypotheses (habitat use, frugivory and rainfall) to explain seasonality in termite feeding across age/sex classes in three habituated groups (Nindividuals = 27) in Central Africa. MATERIALS AND METHODS: We used 4 years of ranging, scan and continuous focal sampling records of gorillas (Nranging days = 883, Nscans = 12,384; Nhours = 891) in addition to 116 transects recording vegetation and termite mound distribution. RESULTS: Depending on the age/sex classes, we found support for all three hypotheses. Time spent in termite-rich vegetation positively impacted termite consumption in all age/sex classes, but subadults. Lengthier travels increased termite feeding in females but decreased it in subadults. Frugivory decreased termite consumption in adults. Daily rainfall had a positive effect on termite feeding and foraging in silverbacks and juveniles, but a negative effect in subadults. For females, rainfall had a positive effect on termite feeding, but a negative effect for termite foraging. DISCUSSION: In great apes, seasonal insectivory seems to be multifactorial and primarily opportunistic with important differences among age/sex classes. While insectivory has potentials to be traditional, it likely played a crucial role during primate evolution (including ours), allowing diet flexibility in changing environments.

Free hand hitting of stone-like objects in wild gorillas.

The earliest stone tool types, sharp flakes knapped from stone cores, are assumed to have played a crucial role in human cognitive evolution. Flaked stone tools have been observed to be accidentally produced when wild monkeys use handheld stones as tools. Holding a stone core in hand and hitting it with another in the absence of flaking, free hand hitting, has been considered a requirement for producing sharp stone flakes by hitting stone on stone, free hand percussion. We report on five observations of free hand hitting behavior in two wild western gorillas, using stone-like objects (pieces of termite mound). Gorillas are therefore the second non-human lineage primate showing free-hand hitting behavior in the wild, and ours is the first report for free hand hitting behavior in wild apes. This study helps to shed light on the morphofunctional and cognitive requirements for the emergence of stone tool production as it shows that a prerequisite for free hand percussion (namely, free hand hitting) is part of the spontaneous behavioral repertoire of one of humans' closest relatives (gorillas). However, the ability to combine free hand hitting with the force, precision, and accuracy needed to facilitate conchoidal fracture in free hand percussion may still have been a critical watershed for hominin evolution.

Group differences in feeding and diet composition of wild western gorillas.

The ecological-constraints model posits that living in larger groups is associated to higher travel costs and reduced nutritional intake due to within-group feeding competition setting upper group size limits. While this is critical for frugivorous mammals, the model is less ubiquitous for folivores who feed on more abundant and evenly distributed food. The seasonally frugivorous diet of western gorillas (Gorilla gorilla) provides the opportunity to study the ecological-constraints model in the largest primate species. We investigated how two groups of western gorillas of differing sizes (N = 9, N = 15) in Central African Republic, responded to seasonal variation in fruit availability in terms of activity and diet. We used continuous focal animal sampling during periods of high (July-August 2011) and low (October 2011-January 2012) fruit availability, measured by monthly phenological scores. While diet diversity, resting and moving time did not differ between groups, overall the smaller group spent more time feeding than the larger group although this became less evident when fruit was more available. The smaller group was more frugivorous than the larger group. However, the larger group increased more steeply fruit consumption when fruit was more available, and incorporated more insects, young leaves and bark when fruit was less available, when compared to the smaller group. Up to a certain limit, the flexibility of large, seasonal frugivores to survive on a more folivorous diet may buffer the upper limit group size, suggesting deviation from the ecological-constraints model as in some folivores.

The complex Y-chromosomal history of gorillas.

Studies of the evolutionary relationships among gorilla populations using autosomal and mitochondrial sequences suggest that male-mediated gene flow may have been important in the past, but data on the Y-chromosomal relationships among the gorilla subspecies are limited. Here, we genotyped blood and noninvasively collected fecal samples from 12 captives and 257 wild male gorillas of known origin representing all four subspecies (Gorilla gorilla gorilla, G. g. diehli, G. beringei beringei, and G. b. graueri) at 10 Y-linked microsatellite loci resulting in 102 unique Y-haplotypes for 224 individuals. We found that western lowland gorilla (G. g. gorilla) haplotypes were consistently more diverse than any other subspecies for all measures of diversity and comprised several genetically distinct groups. However, these did not correspond to geographical proximity and some closely related haplotypes were found several hundred kilometers apart. Similarly, our broad sampling of eastern gorillas revealed that mountain (G. b. beringei) and Grauer's (G. b. graueri) gorilla Y-chromosomal haplotypes did not form distinct clusters. These observations suggest structure in the ancestral population with subsequent mixing of differentiated haplotypes by male dispersal for western lowland gorillas, and postisolation migration or incomplete lineage sorting due to short divergence times for eastern gorillas.

Do primates flexibly use spatio-temporal cues when foraging?

Foraging in seasonal environments can be cognitively demanding. Comparative studies have associated large brain size with a frugivorous diet. We investigated the ability of three semi-free-ranging primate species with different degrees of frugivory (Ntrials: Macaca tonkeana = 419, Macaca fascicularis = 197, Sapajus apella = 346) in developing a mental representation of the spatio-temporal distribution of food using foraging experiments. Forty-two boxes were fixed on trees, and each week ("season"), some of them were filled with fruits which were either highly preferred, or less preferred. Spatial (geometrical panels) and temporal (peel skin of the available fruit) cues were present at each season to indicate where (food location), what (which food) was available, and when. To test the flexible use of the cues in primate foraging behaviour, we first removed the spatial and temporal cues one at a time, and then, we manipulated the "seasonal" order of the available fruit. We compared the foraging performances in the absence and the presence of the cues and during the usual and unusual seasonal order. The average proportion of baited boxes chosen by the subjects in presence of both cues was high (between 73% and 98%) for all species. The primates seemed to remember the spatio-temporal food availability (or used other cues) because no difference was found between trials with or without our spatial and temporal cues. When the usual seasonal pattern was changed, they flexibly adjusted the feeding choice by using the provided temporal cues. We discuss these results also in view of a possible experimental bias.

Foraging efficiency in temporally predictable environments: is a long-term temporal memory really advantageous?

Cognitive abilities enabling animals that feed on ephemeral but yearly renewable resources to infer when resources are available may have been favoured by natural selection, but the magnitude of the benefits brought by these abilities remains poorly known. Using computer simulations, we compared the efficiencies of three main types of foragers with different abilities to process temporal information, in spatially and/or temporally homogeneous or heterogeneous environments. One was endowed with a sampling memory, which stores recent experience about the availability of the different food types. The other two were endowed with a chronological or associative memory, which stores long-term temporal information about absolute times of these availabilities or delays between them, respectively. To determine the range of possible efficiencies, we also simulated a forager without temporal cognition but which simply targeted the closest and possibly empty food sources, and a perfectly prescient forager, able to know at any time which food source was effectively providing food. The sampling, associative and chronological foragers were far more efficient than the forager without temporal cognition in temporally predictable environments, and interestingly, their efficiencies increased with the level of temporal heterogeneity. The use of a long-term temporal memory results in a foraging efficiency up to 1.16 times better (chronological memory) or 1.14 times worse (associative memory) than the use of a simple sampling memory. Our results thus show that, for everyday foraging, a long-term temporal memory did not provide a clear benefit over a simple short-term memory that keeps track of the current resource availability. Long-term temporal memories may therefore have emerged in contexts where short-term temporal cognition is useless, i.e. when the anticipation of future environmental changes is strongly needed.

No evidence for female kin association, indications for extragroup paternity, and sex-biased dispersal patterns in wild western gorillas.

Characterizing animal dispersal patterns and the rational behind individuals' transfer choices is a long-standing question of interest in evolutionary biology. In wild western gorillas (Gorilla gorilla), a one-male polygynous species, previous genetic findings suggested that, when dispersing, females might favor groups with female kin to promote cooperation, resulting in higher-than-expected within-group female relatedness. The extent of male dispersal remains unclear with studies showing conflicting results. To investigate male and female dispersal patterns and extragroup paternity, we analyzed long-term field observations, including female spatial proximity data, together with genetic data (10 autosomal microsatellites) on individuals from a unique set of four habituated western gorilla groups, and four additional extragroup males (49 individuals in total). The majority of offspring (25 of 27) were sired by the group male. For two offspring, evidence for extragroup paternity was found. Contrarily to previous findings, adult females were not significantly more related within groups than across groups. Consistently, adult female relatedness within groups did not correlate with their spatial proximity inferred from behavioral data. Adult females were similarly related to adult males from their group than from other groups. Using R ST statistics, we found significant genetic structure and a pattern of isolation by distance, indicating limited dispersal in this species. Comparing relatedness among females and among males revealed that males disperse farer than females, as expected in a polygamous species. Our study on habituated western gorillas shed light on the dispersal dynamics and reproductive behavior of this polygynous species and challenge some of the previous results based on unhabituated groups.

Mind the food: rapid changes in antioxidant content of diet affect oxidative status of chimpanzees.

The link between dietary antioxidants and oxidative status has been studied extensively in humans. Surprisingly, comparative data are not available from closely related species, such as chimpanzees, which evolved in environments characterized by strong fluctuations in the availability and quality of vegetable food sources. We tested the hypothesis that an abrupt decrease in dietary antioxidants would increase oxidative damages in captive chimpanzees (Pan troglodytes), while a rapid increase in antioxidant intake would decrease oxidative damages accrued while on the low-antioxidant diet. An abrupt decline of dietary antioxidants increased urinary levels of lipid peroxides and of oxidative DNA damage but not of 8-isoprostanes. In contrast, an increased intake of dietary antioxidants did not affect the oxidative status. Chimpanzees that were both older and with a higher dominance rank had lower urinary levels of lipid peroxides and of DNA damage as compared with younger chimpanzees. Neither individual sex nor proportion of time being groomed explained any variation in all three markers of oxidative status. Finally, we found significant within-individual repeatability of all markers of oxidative status over the course of the experiment, suggesting a significant contribution of individual history to molding oxidative status. Our results show that antioxidant intake plays a nonnegligible role in the regulation of oxidative status homeostasis in our closest relatives, the chimpanzees. Our work also suggests that rapid short-term increases in antioxidant intake might not have the desired immediate impact on oxidative status, such as in the case of clinical interventions or training programs.

Reaction to allospecific death and to an unanimated gorilla infant in wild western gorillas: insights into death recognition and prolonged maternal carrying.

It is still unclear to what extent animals possess knowledge of death. Primates display a large variety and often contradictory behaviors toward conspecific corpses, particularly those of infants (e.g., prolonged carrying and care). This study reports on reactions in a wild, habituated western gorilla group (Gorilla gorilla, 11-13 individuals) in the Central African Republic to an unanimated conspecific infant, and to an allospecific corpse. Individuals' reactions were compared to their usual behavior using both continuous focal animal sampling and 10-min instantaneous scan sampling. In the first observation, an infant gorilla fell out of a tree and looked dead. The mother retrieved it and remained unusually close to another adult female, until the infant started to move again, almost 1 h later. Cases of infants regaining consciousness after almost-fatal accidents may act as positive reinforcement for continued carrying by mothers, which might be socially learned. In the second case, three immature gorillas reacted to a dead red river hog. For 20 min they stared at the corpse from tree branches above, while chest beating, defecating, and urinating several times. They showed fear and did not approach the corpse. These observations show that non-predatory species, such as gorillas, may be able to acquire and develop some knowledge about death even though they do not kill other vertebrates.

Prolonged care and cannibalism of infant corpse by relatives in semi-free-ranging capuchin monkeys.

Cannibalism is a quite common behaviour in animals that can have survival value when food is scarce or in the case of overpopulation. Conversely, cannibalism can also increase pathogen transmission and reduce fitness. In primates, some cases of cannibalism are associated with infanticide or are performed by mothers after their newborn has died (filial cannibalism). We report here the first observation of cannibalism, specifically infant cannibalism, in a semi-free-ranging group of brown capuchin monkeys (Sapajus apella). The baby was likely stillborn, as parts of the cranial bones were missing and no fresh injuries were visible. After half a day of taking care of the dead infant, the mother ate part of the corpse's skin and the highly nutritional viscera, possibly thereby compensating for the physiological costs of pregnancy. After attentively watching his mother's behaviour, the older brother of the dead newborn similarly ate parts of the corpse. Although we cannot rule out idiosyncrasy and vertical social transmission, it is possible that cannibalism is a normal-albeit rare-part of the behavioural repertoire of capuchin monkeys.

Where and what? Frugivory is associated with more efficient foraging in three semi-free ranging primate species.

Foraging in seasonal environments can be cognitively challenging. Comparative studies have associated brain size with a frugivorous diet. We investigated how fruit distribution (where) and preference (what) affect foraging decisions in three semi-free ranging primate species with different degrees of frugivory: Macaca tonkeana (N indiv = 5; N trials = 430), M. fascicularis (N indiv = 3; N trials = 168) and Sapajus apella (N indiv = 6; N trials = 288). We used 36 boxes fixed on trees and filled with highly and less preferred fruits with different (weekly) spatio-temporal distributions. Individuals were tested in two conditions: (1) same fruit provided concurrently in the same quantity but in a scattered and in a clumped distribution, (2) highly preferred fruit was scattered while the less preferred was clumped. Generally, primates preferred feeding first on the boxes of the clumped distribution in both conditions, with the more frugivorous species at a higher degree than the less frugivorous species in condition (1), but not (2). Therefore, what fruit was available changed the foraging decisions of the more frugivorous species who also engaged more in goal-directed travel. When feeding on preferred fruit, primates probably maximized foraging efficiency regardless of their degree of frugivory. Our findings emphasize that the food type and distribution may be a preponderant driver in cognitive evolution.

Mammal extinctions and the increasing isolation of humans on the tree of life.

A sixth great mass extinction is ongoing due to the direct and indirect effects of human pressures. However, not all lineages are affected equally. From an anthropocentric perspective, it is often purported that humans hold a unique place on Earth. Here, we show that our current impacts on the natural world risk realizing that expectation. We simulated species loss on the mammalian phylogenetic tree, informed by species current extinction risks. We explored how Homo sapiens could become isolated in the tree if species currently threatened with extinction disappeared. We analyzed correlates of mammal extinctions risks that may drive this isolation pattern. We show that, within mammals, and more particularly within primates, extinction risks increase with the number of known threat types, and decrease with geographic range size. Extinctions increase with species body mass, trophic level, and the median longitudinal extent of each species range in mammals but not within primates. The risks of extinction are frequently high among H. sapiens close relatives. Pruning threatened primates, including apes (Hominidae, Hylobatidae), from the tree of life will lead to our species being among those with the fewest close relatives. If no action is taken, we will thus not only lose crucial biodiversity for the preservation of Earth ecosystems, but also a key living reference to what makes us human.

What, where and when: spatial foraging decisions in primates.

When exploiting the environment, animals have to discriminate, track, and integrate salient spatial cues to navigate and identify goal sites. Actually, they have to know what can be found (e.g. what fruit), where (e.g. on which tree) and when (in what season or moment of the year). This is very relevant for primate species as they often live in seasonal and relatively unpredictable environments such as tropical forests. Here, we review and compare different approaches used to investigate primate spatial foraging strategies: from direct observations of wild primates to predictions from statistical simulations, including experimental approaches on both captive and wild primates, and experiments in captivity using virtual reality technology. Within this framework, most of these studies converge to show that many primate species can (i) remember the location of most of food resources well, and (ii) often seem to have a goal-oriented path towards spatially permanent resources. Overall, primates likely use mental maps to plan different foraging strategies to enhance their fitness. The majority of studies suggest that they may organise spatial information on food resources into topological maps: they use landmarks to navigate and encode local spatial information with regard to direction and distance. Even though these studies were able to show that primates can remember food quality (what) and its location (where), still very little is known on how they incorporate the temporal knowledge of available food (when). Future studies should attempt to increase our understanding of the potential of primates to learn temporal patterns and how both socio-ecological differences among species and their cognitive abilities influence such behavioural strategies.

Dialium seed coprophagy in wild western gorillas: Multiple nutritional benefits and toxicity reduction hypotheses.

Unraveling the relationship between the unusual feeding behaviors and the nutritional intake of endangered species may provide crucial information for understanding species response to habitat unpredictable changes. Primates occasionally re-ingest fruit seeds alongside ingestion of feces, a behavior called coprophagy. The nutritional benefit is one of the several non-mutual exclusive hypotheses proposed to explain this behavior. We investigated the ecological correlates of coprophagy in wild western gorillas. We tested whether coprophagy occurred during periods of lower fruit availability and whether it led to higher nutrient intake in comparison to the other food. Data integrated phenological, fecal and nutritional analyses of gorilla food with behavioral observations collected at two sites in Central Africa (Mbeli Bai: ad libitum observations on 15 groups/solitary males, October 2002-November 2005; Bai Hokou: 5-min scan on a habituated group, December 2004-December 2005). Coprophagy occurred at the end of the high-fruiting season in association of two Dialium species. Coprophagy correlated positively with the occurrence of Dialium spp. fruit in gorilla feces and in the feeding scans, and showed a positive trend with Dialium availability but not with total fruit availability. Nutritional comparison of Dialium seeds with other important gorilla food showed higher fat and mineral content, particularly of Mg, but also of phenols and tannins in Dialium seeds. We discuss how the effect of gut processing and gut heat via coprophagy may act as cooking-like effect: increasing the ability to maximize nutrient intake by concurrently softening fibers and decreasing the toxic effect of antifeedants, like in human traditional cooking. Our results support both the multiple nutritional benefit hypothesis and the toxicity reduction hypothesis. Since Dialium is precious timber, the importance of this tree for the critically endangered western gorillas should be taken with high consideration when planning controlled logging of degraded forests or in face of habitat changes.

Handedness in gestural and manipulative actions in male hunter-gatherer Aka pygmies from Central African Republic.

OBJECTIVES: All human populations display a right-biased handedness. Nonetheless, if studies on western populations are plenty, investigations of traditional populations living at subsistence levels are rare. Yet, understanding the geographical variation of phenotypes of handedness is crucial for testing evolutionary hypotheses. We aimed to provide a preliminary investigation of factors affecting handedness in 25 Aka pygmies from Central African Republic when spontaneously gesturing or manipulating food/tools (Nactions = 593). MATERIALS AND METHODS: We recorded spontaneous behaviors and characterized individuals' hand preference using GLMM with descriptive variables as target position, task complexity (unimanual/bimanual), task nature (food/tool manipulation, gesture), and task physical/cognitive constraints (precision or power for manipulative actions and informative content for gestures). RESULTS: Individuals were lateralized to the right (93%, N = 15) when manipulating food/tools but not when gesturing. Hand preference was affected by target position but not by task complexity. While nonexplicitly informative gestures were more biased to the right compared to explicitly informative ones, no differences were found within food/tool manipulation (power or precision vs. none). DISCUSSION: Although we do not intend to assume generalizable results due to our reduced sample, our observations provide additional information on handedness in a contemporary traditional society. Especially, the study mainly evidenced considerable cultural effects in gestures while also supporting theories considering active tool manipulation as one of the overriding factor in human handedness evolution.

Reading wild minds: A computational assay of Theory of Mind sophistication across seven primate species.

Theory of Mind (ToM), i.e. the ability to understand others' mental states, endows humans with highly adaptive social skills such as teaching or deceiving. Candidate evolutionary explanations have been proposed for the unique sophistication of human ToM among primates. For example, the Machiavellian intelligence hypothesis states that the increasing complexity of social networks may have induced a demand for sophisticated ToM. This type of scenario ignores neurocognitive constraints that may eventually be crucial limiting factors for ToM evolution. In contradistinction, the cognitive scaffolding hypothesis asserts that a species' opportunity to develop sophisticated ToM is mostly determined by its general cognitive capacity (on which ToM is scaffolded). However, the actual relationships between ToM sophistication and either brain volume (a proxy for general cognitive capacity) or social group size (a proxy for social network complexity) are unclear. Here, we let 39 individuals sampled from seven non-human primate species (lemurs, macaques, mangabeys, orangutans, gorillas and chimpanzees) engage in simple dyadic games against artificial ToM players (via a familiar human caregiver). Using computational analyses of primates' choice sequences, we found that the probability of exhibiting a ToM-compatible learning style is mainly driven by species' brain volume (rather than by social group size). Moreover, primates' social cognitive sophistication culminates in a precursor form of ToM, which still falls short of human fully-developed ToM abilities.

Primate energy input and the evolutionary transition to energy-dense diets in humans.

Humans and other large-brained hominins have been proposed to increase energy turnover during their evolutionary history. Such increased energy turnover is plausible, given the evolution of energy-rich diets, but requires empirical confirmation. Framing human energetics in a phylogenetic context, our meta-analysis of 17 wild non-human primate species shows that daily metabolizable energy input follows an allometric relationship with body mass where the allometric exponent for mass is 0.75 ± 0.04, close to that reported for daily energy expenditure measured with doubly labelled water in primates. Human populations at subsistence level (n = 6) largely fall within the variation of primate species in the scaling of energy intake and therefore do not consume significantly more energy than predicted for a non-human primate of equivalent mass. By contrast, humans ingest a conspicuously lower mass of food (-64 ± 6%) compared with primates and maintain their energy intake relatively more constantly across the year. We conclude that our hominin hunter-gatherer ancestors did not increase their energy turnover beyond the allometric relationship characterizing all primate species. The reduction in digestive costs due to consumption of a lower mass of high-quality food, as well as stabilization of energy supply, may have been important evolutionary steps enabling encephalization in the absence of significantly raised energy intakes.