Vocal convergence in a multi-level primate society: insights into the evolution of vocal learning.

The extent to which nonhuman primate vocalizations are amenable to modification through experience is relevant for understanding the substrate from which human speech evolved. We examined the vocal behaviour of Guinea baboons, Papio papio, ranging in the Niokolo Koba National Park in Senegal. Guinea baboons live in a multi-level society, with units nested within parties nested within gangs. We investigated whether the acoustic structure of grunts of 27 male baboons of two gangs varied with party/gang membership and genetic relatedness. Males in this species are philopatric, resulting in increased male relatedness within gangs and parties. Grunts of males that were members of the same social levels were more similar than those of males in different social levels (N = 351 dyads for comparison within and between gangs, and N = 169 dyads within and between parties), but the effect sizes were small. Yet, acoustic similarity did not correlate with genetic relatedness, suggesting that higher amounts of social interactions rather than genetic relatedness promote the observed vocal convergence. We consider this convergence a result of sensory-motor integration and suggest this to be an implicit form of vocal learning shared with humans, in contrast to the goal-directed and intentional explicit form of vocal learning unique to human speech acquisition.

Baboons (Papio papio) Process a Context-Free but Not a Context-Sensitive Grammar.

Language processing involves the ability to master supra-regular grammars, that go beyond the level of complexity of regular grammars. This ability has been hypothesized to be a uniquely human capacity. Our study probed baboons' capacity to learn two supra-regular grammars of different levels of complexity: a context-free grammar generating sequences following a mirror structure (e.g., AB | BA, ABC | CBA) and a context-sensitive grammar generating sequences following a repeat structure (e.g., AB | AB, ABC | ABC), the latter requiring greater computational power to be processed. Fourteen baboons were tested in a prediction task, requiring them to track a moving target on a touchscreen. In distinct experiments, sequences of target locations followed one of the above two grammars, with rare violations. Baboons showed slower response times when violations occurred in mirror sequences, but did not react to violations in repeat sequences, suggesting that they learned the context-free (mirror) but not the context-sensitive (repeat) grammar. By contrast, humans tested with the same task learned both grammars. These data suggest a difference in sensitivity in baboons between a context-free and a context-sensitive grammar.

The effect of individual and food characteristics on food retrieval and food sharing in captive Guinea baboons (Papio papio).

Access to food is of major importance to the fitness and survival of every individual, particularly in group-living animals, in which individual characteristics and food distribution can affect food intake. Additionally, several species of primates are known to share food under certain conditions. Such unresisted transfer of food from one individual to another appears to be adaptive, for instance as a tool to maintain and reinforce social bonds. In this study, we aimed to test how food retrieval and food sharing varies depending on the social relationship between individuals, and on the characteristics of the food. In six different test conditions, we provided a captive group of Guinea baboons (Papio papio, N = 23) with multiple food items, differing in quality, quantity, density, monopolizability, and effort required to obtain it. We further used behavioral observations to assess individual relationships and possible variations in grooming exchanges linked to food sharing events. Out of 424 events in which food items were retrieved by the subjects, we detected no instances of active food sharing and only 17 of passive food sharing. The way food was retrieved was affected by individual and food characteristics (i.e., quantity, quality, and monopolizability of food): Males and central individuals (i.e., those connected to many partners, and/or having partners with many connections in the social network) were more likely to retrieve food during test conditions. In particular, events of passive food sharing mostly happened when the quality of food was low, and between individuals belonging to the same community (i.e., having close relationships). No other food characteristics affected the probability to share food, and the occurrence of food sharing had no immediate effect on grooming exchanges. Overall, our findings suggest that food sharing is relatively rare in Guinea baboons unless the food has a low quality and individuals form close social bonds.

Are baboons learning "orthographic" representations? Probably not.

The ability of Baboons (papio papio) to distinguish between English words and nonwords has been modeled using a deep learning convolutional network model that simulates a ventral pathway in which lexical representations of different granularity develop. However, given that pigeons (columba livia), whose brain morphology is drastically different, can also be trained to distinguish between English words and nonwords, it appears that a less species-specific learning algorithm may be required to explain this behavior. Accordingly, we examined whether the learning model of Rescorla and Wagner, which has proved to be amazingly fruitful in understanding animal and human learning could account for these data. We show that a discrimination learning network using gradient orientation features as input units and word and nonword units as outputs succeeds in predicting baboon lexical decision behavior-including key lexical similarity effects and the ups and downs in accuracy as learning unfolds-with surprising precision. The models performance, in which words are not explicitly represented, is remarkable because it is usually assumed that lexicality decisions, including the decisions made by baboons and pigeons, are mediated by explicit lexical representations. By contrast, our results suggest that in learning to perform lexical decision tasks, baboons and pigeons do not construct a hierarchy of lexical units. Rather, they make optimal use of low-level information obtained through the massively parallel processing of gradient orientation features. Accordingly, we suggest that reading in humans first involves initially learning a high-level system building on letter representations acquired from explicit instruction in literacy, which is then integrated into a conventionalized oral communication system, and that like the latter, fluent reading involves the massively parallel processing of the low-level features encoding semantic contrasts.

Charting the neglected West: The social system of Guinea baboons.

OBJECTIVES: Primate social systems are remarkably diverse, and thus play a central role in understanding social evolution, including the biological origin of human societies. Although baboons have been prominently featured in this context, historically little was known about the westernmost member of the genus, the Guinea baboon (Papio papio). MATERIAL AND METHODS: Here, we summarize the findings from the first years of observations at the field site CRP Simenti in the Niokolo Koba National Park in Senegal. RESULTS: Guinea baboons reveal a nested multi-level social organization, with reproductive units comprising one "primary" male, one to several females, young, and occasionally "secondary" males at the base of the society. Three to five units form "parties," which team up with other parties to form a "gang." Different gangs have largely overlapping home ranges and agonistic interactions between different parties or gangs are rare. Some but not all strongly socially bonded males are highly related, and population genetic and behavioral evidence indicate female-biased dispersal. Females play an important role in intersexual bond formation and maintenance, and female tenure length varies between a few weeks to several years. DISCUSSION: While the social organization resembles that of hamadryas baboons (P. hamadryas), the social structure differs considerably, specifically in terms of low male aggressiveness and female freedom. Despite substantial differences in social organization and social structure, the acoustic structure of Guinea baboon vocalizations does not differ substantially from that of other baboon taxa. With its multi-level organization, stable bonds between males and females, as well as a high-degree of male-male cooperation and tolerance, Guinea baboons constitute an intriguing model for reconstructing human social evolution.

Behavioral assessment of combinatorial semantics in baboons (Papio papio).

Combinatorial semantics is a core property of human language whose mechanisms remain poorly known. This study used computerized tasks with touch screens to investigate whether baboons (Papio papio) can understand the combination of shape and color labels in order to designate their corresponding colored shape. The baboons were trained either directly with label-pairs (Experiment 1) or with individual shape and color labels (Experiment 2), before being tested with novel compound labels from which they had to identify the referent. Compound labels understanding was found in one out of seven baboons tested in Experiment 1. Quite surprisingly, none of the 11 baboons showed this capacity in Experiment 2. We discuss several aspects of our protocols which could explain this difference between our two experiments, as well as the significance of our findings for language studies in animals and children.

Social behavior and patterns of testosterone and glucocorticoid levels differ between male chacma and Guinea baboons.

In multi-male, multi-female groups of mammals, males usually compete aggressively over access to females. However, species vary in the intensity of male contest competition, which has been linked to differences in testosterone and glucocorticoid profiles. Chacma (Papio ursinus) and Guinea (P. papio) baboons constitute an intriguing model to examine variation in male competition and male endocrine correlates, because of the differences in their social systems. Chacma baboons live in stable female-bonded groups with linear male dominance hierarchies and a high male mating skew, whereas Guinea baboons live in male-bonded, multi-level societies. We recorded male behavior and assayed testosterone (fT) and glucocorticoid metabolite (fGC) levels from fecal samples in one population of each species. Male chacma baboons were more frequently involved in agonistic interactions, and dominance relationships were more consistent than in Guinea baboons, where we could not detect linear hierarchies. Notably, male chacma baboons were also more aggressive towards females, indicating an overall higher aggressiveness in this species. In contrast, male Guinea baboons showed higher levels of affiliative interactions and spatial tolerance. High-ranking and consorting male chacma baboons showed elevated fGC levels and also tended to show elevated fT levels, but there was no effect of consortship in Guinea baboons. Agonism was not related to hormone levels in either species. Thus, predictors of fT and fGC levels in Guinea baboons seem to differ from chacma baboons. Our results support the view that different social systems create differential selection pressures for male aggression, reflected by different hormone profiles.

Population genetic insights into the social organization of Guinea baboons (Papio papio): Evidence for female-biased dispersal.

Sex differences in philopatry and dispersal have important consequences on the genetic structure of populations, social groups, and social relationships within groups. Among mammals, male dispersal and female philopatry are most common and closely related taxa typically exhibit similar dispersal patterns. However, among four well-studied species of baboons, only hamadryas baboons exhibit female dispersal, thus differing from their congenerics, which show female philopatry and close-knit female social relationships. Until recently, knowledge of the Guinea baboon social system and dispersal pattern remained sparse. Previous observations suggested that the high degree of tolerance observed among male Guinea baboons could be due to kinship. This led us to hypothesize that this species exhibits male philopatry and female dispersal, conforming to the hamadryas pattern. We genotyped 165 individuals from five localities in the Niokolo-Koba National Park, Senegal, at 14 autosomal microsatellite loci and sequenced a fragment of the mitochondrial hypervariable region I (HVRI) of 55 individuals. We found evidence for higher population structuring in males than in females, as expected if males are the more philopatric sex. A comparison of relatedness between male-male and female-female dyads within and among communities did not yield conclusive results. HVRI diversity within communities was high and did not differ between the sexes, also suggesting female gene flow. Our study is the first comprehensive analysis of the genetic population structure in Guinea baboons and provides evidence for female-biased dispersal in this species. In conjunction with their multilevel social organization, this finding parallels the observations for human hunter-gatherers and strengthens baboons as an intriguing model to elucidate the processes that shaped the highly cooperative societies of Homo.

Orangutans (Pongo spp.) have deeper, more efficient sleep than baboons (Papio papio) in captivity.

The nightly construction of arboreal sleeping platforms or "nests" has been observed among every great ape population studied to date. However, this behavior has never been reported in any other nonhuman primate and comparisons between ape and monkey sleep illuminate the link between sleeping substrates, positional behavior, and sleep efficiency. Here, we compare sleep depth and efficiency and night-time positional behavior between a large-bodied cercopithecoid (Papio papio) and a large-bodied hominoid (Pongo spp.) at the Indianapolis Zoo. We used infrared videography to assess nightly sleep and awake behavioral states, gross body movements, and postures in baboons (N = 45 nights) and orangutans (N = 128 nights). We calculated the total waking time, total sleep time, sleep fragmentation (the number of brief awakenings ≥2 min/h), sleep motor activity (number of motor activity bouts per hour), sleep efficiency (sleep duration/time in bed), and percentage of time spent in each posture. By every measure, orangutans experienced overall deeper, more efficient sleep. Baboons were more likely to sleep in guarded, upright positions (weight bearing on their ischial callosities) and never opted to use additional materials to augment sleep environments, whereas orangutans slept in insouciant, relaxed positions on constructed sleeping materials. Our results suggest that relaxed sleeping postures may have been enabled by sleeping platforms as a behavioral facilitator to sleep, which could have allowed for greater sleep depth and next-day cognitive capacities in both great apes and hominins.

Cultural evolution of systematically structured behaviour in a non-human primate.

Culture pervades human life and is at the origin of the success of our species. A wide range of other animals have culture too, but often in a limited form that does not complexify through the gradual accumulation of innovations. We developed a new paradigm to study cultural evolution in primates in order to better evaluate our closest relatives' cultural capacities. Previous studies using transmission chain experimental paradigms, in which the behavioural output of one individual becomes the target behaviour for the next individual in the chain, show that cultural transmission can lead to the progressive emergence of systematically structured behaviours in humans. Inspired by this work, we combined a pattern reproduction task on touch screens with an iterated learning procedure to develop transmission chains of baboons (Papio papio). Using this procedure, we show that baboons can exhibit three fundamental aspects of human cultural evolution: a progressive increase in performance, the emergence of systematic structure and the presence of lineage specificity. Our results shed new light on human uniqueness: we share with our closest relatives essential capacities to produce human-like cultural evolution.

Effects of freely accessible computerized test systems on the spontaneous behaviors and stress level of Guinea baboons (Papio papio).

Fagot and Paleressompoulle [Fagot and Paleressompoulle (2009) Behav Res Methods 41: 396-404] described a new automated learning device for monkeys (ALDM) to test the cognitive functions of nonhuman primates within their social groups. However, the impact of the ALDM procedure on animal well-being needs to be investigated. The present study assessed the consequences of ALDM testing on the behavioral repertoire of Guinea baboons (Papio papio) and their stress levels as inferred from measurements of saliva cortisol. Accessibility to ALDM test computers reduced the number of resting periods as well as the number of stereotypies. Lower cortisol levels were also found during ALDM testing. These findings and others demonstrate that ALDM testing has a positive impact on animal well-being and can be considered as a means for behavioral enrichment in captive primates.

Age-dependent behavioral strategies in a visual search task in baboons (Papio papio) and their relation to inhibitory control.

A computerized visual search task was presented to 18 guinea baboons (Papio papio) ranging from 2.7 to 14.3 years of age. The task, inspired from Hick's (1952) task, required detection of a target among a variable number of distractors equidistant to a start button. The reaction times (RTs) and movement times both increased with the number of distractors expressed in bits of information. However, the slope of RT per bit function correlated positively with age, whereas a negative correlation was found for the movement time slopes. In Experiment 2, the same baboons were required to inhibit an ongoing manual pointing toward a target stimulus, to reengage in a new point as a consequence of a change in target location. Results revealed a more accurate performance in the adults, suggesting that differences in behavioral strategies in Experiment 1 can be accounted for by a greater inhibitory control of the adult participants. Implications of these results are discussed regarding the relation between attention, inhibitory control, and behavioral strategies in monkeys, and the general significance of RT slopes in visual search tasks.

A comparative study of working memory: immediate serial spatial recall in baboons (Papio papio) and humans.

Two experiments assessed if non-human primates can be meaningfully compared to humans in a non-verbal test of serial recall. A procedure was used that was derived from variations of the Corsi test, designed to test the effects of sequence structure and movement path length in humans. Two baboons were tested in Experiment 1. The monkeys showed several attributes of human serial recall. These included an easier recall of sequences with a shorter number of items and of sequences characterized by a shorter path length when the number of items was kept constant. However, the accuracy and speed of processing did not indicate that the monkeys were able to benefit from the spatiotemporal structure of sequences. Humans tested in Experiment 2 showed a quantitatively longer memory span, and, in contrast with monkeys, benefitted from sequence structure. The results are discussed in relation to differences in how human and non-human primates segment complex visual patterns.

Executive control of perceptual features and abstract relations by baboons (Papio papio).

Studies of executive control often reveal significant limitations in nonhuman primate performance relative to that of humans. In the present study, 24 socially housed baboons were tested on a computerized version of the Wisconsin Card Sorting Task (WCST) to assess individual differences in executive control. In a second experiment, the same baboons completed a version of the WCST with paired-relational stimuli rather than those that varied on a single dimension to evaluate their set-shifting abilities with abstract relations (same/different). All baboons completed the required shifts on the traditional WCST, but only 12 baboons succeeded in making relational shifts. Age was found to be a significant factor in the level of success on both tasks with younger baboons (mean age 4 years) outperforming older, albeit not aged, baboons (mean age 11.5 years). These results implicate an earlier decline in executive control processes for nonhuman primates with more pronounced effects for cognitive flexibility of abstract relations.

Discrimination of contour-deleted images in baboons (Papio papio) and chimpanzees (Pan troglodytes).

Humans readily group component elements into a coherent perceptual whole and perceive the global form of visual patterns in priority over local features, which stands in contrast to at least some data from the animal literature, suggesting possible species differences in perceptual processes. In this study, chimpanzees and baboons were required to match intact and partially contour-deleted line-drawings in a computerized task in order to further explore the ability of nonhuman primates to group component elements into a coherent perceptual whole and to determine to what extent they use the global form or the local features. Experiment 1 showed that the baboons and chimpanzees matched intact continuous line-drawings (intact-intact) more easily than partially contour-deleted line-drawings (deleted-deleted). Both species could also match partially deleted line-drawings with their intact version (deleted-intact), but at a lower performance level. Experiment 2 further showed that subjects from the two species could match partially deleted coherent line-drawings (deleted-deleted) more easily than their scrambled incoherent versions (scrambled-scrambled). They could however match the coherent deleted forms with their scrambled version (deleted-scrambled). It is suggested that solutions of these tasks rely on the processing of both global and local cues, with no clear-cut species difference in that ability. Overall, the results show that contour completion of line-drawings was not easy. Implications on the processing of human-made two-dimensional representations such as line-drawings are discussed.

Patterns of gastro-intestinal parasites and commensals as an index of population and ecosystem health: the case of sympatric western chimpanzees (Pan troglodytes verus) and guinea baboons (Papio hamadryas papio) at Fongoli, Senegal.

The exponential decline of great apes over the past 50 years has resulted in an urgent need for data to inform population viability assessment and conservation strategies. Health monitoring of remaining ape populations is an important component of this process. In support of this effort, we examined endoparasitic and commensal prevalence and richness as proxies of population health for western chimpanzees (Pan troglodytes verus) and sympatric guinea baboons (Papio hamadryas papio) at Fongoli, Senegal, a site dominated by woodland-savanna at the northwestern extent of chimpanzees' geographic range. The small population size and extreme environmental pressures experienced by Fongoli chimpanzees make them particularly sensitive to the potential impact of pathogens. One hundred thirty-two chimpanzee and seventeen baboon fecal samples were processed using sodium nitrate floatation and fecal sedimentation to isolate helminth eggs, larvae, and protozoal cysts. Six nematodes (Physaloptera sp., Ascaris sp., Stronglyloides fuelleborni, Trichuris sp., an unidentified hookworm, and an unidentified larvated nematode), one cestode (Bertiella sp.), and five protozoans (Iodamoeba buetschlii, Entamoeba coli, Troglodytella abrassarti, Troglocorys cava, and an unidentified ciliate) were detected in chimpanzee fecal samples. Four nematodes (Necator sp., S. fuelleborni, Trichuris sp., and an unidentified hookworm sp.), two trematodes (Shistosoma mansoni and an unidentified fluke), and six protozoans (Entamoeba histolytica/dispar, E. coli, Chilomastix mesnili, Balantidium coli, T. abrassarti, and T. cava) were detected in baboon fecal samples. The low prevalence of pathogenic parasite species and high prevalence of symbiotic protozoa in Fongoli chimpanzees are indicative of good overall population health. However, the high prevalence of pathogenic parasites in baboons, who may serve as transport hosts, highlight the need for ongoing pathogen surveillance of the Fongoli chimpanzee population and point to the need for further research into the epidemiology and cross-species transmission ecology of zoonotic pathogens at this site.

Relational matching in baboons (Papio papio) with reduced grouping requirements.

Analogical reasoning is a corner stone of human cognition, but the phylogenetic origins of this skill are still unknown. Recent animal studies have suggested that only apes can solve the 2- by 2-item relational matching (RMTS) analogy problem, with potential benefits of language- (Premack, 1983) or token-training procedures (Thompson, Oden, & Boysen, 1997). In this study, 6 baboons were initially trained in an RMTS task in which the same and different relations were exemplified by compound stimuli made of 2 adjacent patches of colors. Learning occurred in this task with a first set of colors and transferred to probe trials with new colors (Experiment 1). Manipulation of the size of the sample or comparison stimuli (Experiment 2) showed that the performance was not merely controlled by the surface of the color patches, suggesting cognitive flexibility. Performance collapsed to chance level when a gap was introduced between the 2 elemental features composing the same or different displays (Experiment 3). Nevertheless, this effect of gap size was abolished by training (Experiment 4). It is suggested that monkeys share the ability to judge relations between relations with humans and apes, even in the absence of language or token training. However, this ability has been previously masked by a local mode of processing that hinders the processing of the stimuli as pairs rather than as independent objects.

Study of the development of fetal baboon brain using magnetic resonance imaging at 3 Tesla.

Direct observational data on the development of the brains of human and nonhuman primates is on remarkably scant, and most of our understanding of primate brain development is extrapolated from findings in rodent models. Magnetic resonance imaging (MRI) is a promising tool for the noninvasive, longitudinal study of the developing primate brain. We devised a protocol to scan pregnant baboons serially at 3 T for up to 3 h per session. Seven baboons were scanned 1-6 times, beginning as early as 56 days post-conceptional age, and as late as 185 days (term approximately 185 days). Successful scanning of the fetal baboon required careful animal preparation and anesthesia, in addition to optimization of the scanning protocol. We successfully acquired maps of relaxation times (T(1) and T(2)) and high-resolution anatomical images of the brains of fetal baboons at multiple time points during the course of gestation. These images demonstrated the convergence of gray and white matter contrast near term, and furthermore demonstrated that the loss of contrast at that age is a consequence of the continuous change in relaxation times during fetal brain development. These data furthermore demonstrate that maps of relaxation times have clear advantages over the relaxation time weighted images for the tracking of the changes in brain structure during fetal development. This protocol for in utero MRI of fetal baboon brains will help to advance the use of nonhuman primate models to study fetal brain development longitudinally.

One-male harems and female social dynamics in Guinea baboons.

Little is known about the mating system and social organization of Guinea baboons. This study investigated whether Guinea baboons have a harem-based mating system similar to that of hamadryas and gelada baboons and whether one-male mating units also correspond to social units. Ten adult females in a captive multi-male multi-female group of Guinea baboons were focally observed 2 h per week for 12 weeks, and all observed copulations within the group were recorded. Some males copulated with a single female while others had harems of 2-4 females. All females copulated with a single male except 1 female that switched harems early in the study. The focal females had higher rates of social interaction with their harem members, especially their harem male, than with individuals outside the harem. Females appeared to be subordinate to the harem male but little or no physical aggression or herding behavior from the male was observed. Variation in female social interactions within the harem was not accounted for by their sexual interactions with the male or their genetic relatedness with the females. Females, however, appeared to maintain social relationships with their female relatives in other harems. Taken together, the results of this study show that both mating and affiliative interactions in Guinea baboons are concentrated within one-male units and that the social dynamics within and between these units share some similarities as well as differences with those of hamadryas and gelada baboons.

Amodal completion by baboons (Papio papio): contribution of background depth cues.

Four baboons (Papio papio) were tested in a computerized two-alternative forced choice task in which partially occluded graphic stimuli were shown either on linear perspective backgrounds depicting a corridor or on uniformly black backgrounds. The results indicated that baboons complete partly occluded stimuli and that amodal completion is facilitated by the display of pictorial background depth cues. Inter-individual differences emerged in the ability to extrapolate three-dimensional information from two-dimensional visual information.