Humans (Homo sapiens) but not baboons (Papio papio) demonstrate crossmodal pitch-luminance correspondence.

Humans spontaneously and consistently map information coming from different sensory modalities. Surprisingly, the phylogenetic origin of such cross-modal correspondences has been under-investigated. A notable exception is the study of Ludwig et al. (Visuoauditory mappings between high luminance and high pitch are shared by chimpanzees [Pan troglodytes] and humans. Proceedings of the National Academy of Sciences, 108(51), 20661-20665) which reports that both humans and chimpanzees spontaneously map high-pitched sounds with bright objects and low-pitched sounds with dark objects. Our pre-registered study aimed to directly replicate this research on both humans and baboons (Papio papio), an old world monkey which is more phylogenetically distant from humans than chimpanzees. Following Ludwig et al. participants were presented with a visual classification task where they had to sort black and white square (low and high luminance), while background sounds (low or high-pitched tones) were playing. Whereas we replicated the finding that humans' performance on the visual task was affected by congruency between sound and luminance of the target, we did not find any of those effects on baboons' performance. These results question the presence of a shared cross-modal pitch-luminance mapping in other nonhuman primates.

Guinea baboons are strategic cooperators.

Humans are strategic cooperators; we make decisions on the basis of costs and benefits to maintain high levels of cooperation, and this is thought to have played a key role in human evolution. In comparison, monkeys and apes might lack the cognitive capacities necessary to develop flexible forms of cooperation. We show that Guinea baboons (Papio papio) can use direct reciprocity and partner choice to develop and maintain high levels of cooperation in a prosocial choice task. Our findings demonstrate that monkeys have the cognitive capacities to adjust their level of cooperation strategically using a combination of partner choice and partner control strategies. Such capacities were likely present in our common ancestor and would have provided the foundations for the evolution of typically human forms of cooperation.

Simple questions on simple associations: regularity extraction in non-human primates.

When human and non-human animals learn sequences, they manage to implicitly extract statistical regularities through associative learning mechanisms. In two experiments conducted with a non-human primate species (Guinea baboons, Papio papio), we addressed simple questions on the learning of simple AB associations appearing in longer noisy sequences. Using a serial reaction time task, we manipulated the position of AB within the sequence, such that it could be either fixed (by appearing always at the beginning, middle, or end of a four-element sequence; Experiment 1) or variable (Experiment 2). We also tested the effect of sequence length in Experiment 2 by comparing the performance on AB when it was presented at a variable position within a sequence of four or five elements. The slope of RTs from A to B was taken for each condition as a measurement of learning rate. While all conditions differed significantly from a no-regularity baseline, we found strong evidence that the learning rate did not differ between the conditions. These results indicate that regularity extraction is not impacted by the position of the regularity within a sequence and by the length of the sequence. These data provide novel general empirical constraints for modeling associative mechanisms in sequence learning.

The dynamics of chunking in humans (Homo sapiens) and Guinea baboons (Papio papio).

Chunking is an important cognitive process allowing the compression of information in short-term memory. The aim of this study is to compare the dynamics of chunking during the learning of a visuomotor sequence in humans (Homo sapiens) and Guinea baboons (Papio papio). We duplicated in humans an experimental paradigm that has been used previously in baboons. On each trial, human participants had to point to a moving target on a touch screen. The experiment involved the repetition of the same sequence of nine items over a 1,000 trials. To reproduce as much as possible the conditions under which baboons performed the task, human participants were tested at their own pace. Results revealed that baboons and humans shared similar chunking dynamics: In both species, the sequence was initially parsed into small chunks that became longer and fewer with practice through two reorganization mechanisms (recombinations and concatenations). Differences were also observed regarding the global decrease in response times that was faster and more pronounced in humans compared with baboons. Analyses of these similarities and differences provide new empirical evidence for understanding the general properties of chunking mechanisms in sequence learning and its evolution across species. (PsycInfo Database Record (c) 2023 APA, all rights reserved).

Simultaneous learning of directional and non-directional stimulus relations in baboons (Papio papio).

While humans exposed to a sequential stimulus pairing A-B are commonly assumed to form a bidirectional mental relation between A and B, evidence that non-human animals can do so is limited. Careful examination of the animal literature suggests possible improvements in the test procedures used to probe such effects, notably measuring transfer effects on the learning of B-A pairings, rather than direct recall of A upon cuing with B. We developed such an experimental design and tested 20 Guinea baboons (Papio papio). Two pairings of visual shapes were trained (A1-B1, A2-B2) and testing was conducted in a reversed order, either with conserved pairings (B1-A1, B2-A2) or broken ones (B1-A2, B2-A1). We found baboons' immediate test performance to be above chance level for conserved pairings and below chance level for broken ones. Moreover, baboons needed less trials to learn conserved pairings compared to broken ones. These effects were apparent for both pairings on average, and separately for the best learned pairing. Baboons' responding on B-A trials was thus influenced by their previous A-B training. Performance level at the onset of testing, however, suggests that baboons did not respond in full accordance with the hypothesis of bidirectionality. To account for these data, we suggest that two competing types of relations were concomitantly encoded: a directional relation between A and B, which retains the sequential order experienced, and a non-directional relation, which retains only the co-occurrence of events, not their temporal order.

On the role of interference in sequence learning in Guinea baboons (Papio papio).

It is well established that decay and interference are the two main causes of forgetting. In the present study, we specifically focus on the impact of interference on memory forgetting. To do so, we tested Guinea baboons (Papio papio) on a visuo-motor adaptation of the Serial Reaction Time task in which a target sequence is repeated, and a random sequence is interposed between repetitions, a similar situation as the one used in the Hebb repetition paradigm. In this task, one three-item sequence, the repeated sequence, was presented every second trial and interleaved with random sequences. Interference was implemented by using random sequences containing one item that was also part of the repeated sequence. In a first condition, the overlapping item was located at the same position as the repeated sequence. In a second condition, the overlapping item was located at one of the two other positions. In a third condition, there was no overlap between repeated and random sequences. Contrary to previous findings, our results reveal similar learning slopes across all three conditions, suggesting that interference did not affect sequence learning in the conditions tested. Findings are discussed in the light of previous research on sequence learning and current models of memory and statistical learning.

Impact of female contraception for population management on behavior and social interactions in a captive troop of Guinea baboons (Papio papio).

As part of a population management strategy for a troop of Guinea baboons (Papio papio) at Yorkshire Wildlife Park, adult females were given a Suprelorin contraceptive implant. There was no information on the effect of contraception on behavior in this species, so behavioral data were collected before and after implant placement to determine any impact on the troops' welfare. Social interactions, affiliative, agonistic, and self-directed displacement behaviors (SDBs) in all adults were monitored via focal sampling. Preimplant data were collected in August/September 2019 before Suprelorin placement on November 2019, and postimplant data were collected in August/September 2020, allowing for comparison while controlling for seasonal differences in behavior. We found a significant reduction of SDBs after intervention, suggesting that contraception has a positive impact on group welfare, as SDBs are key behavioral indicators of stress and anxiety in nonhuman primates. Additionally, the rate of substate change per hour (i.e., the number of times the baboon changed their behavior), duration of sentry behavior, and the frequency of agonistic bouts were significantly lower postimplant, further suggesting improvements in welfare. There were also no significant decreases in the duration of positive social interactions, such as allogrooming and play. The results show that Suprelorin did not have a detrimental impact on the behavior of adults in the troop and may have even improved welfare. The use of Suprelorin in females could be considered as an effective population management strategy for primates existing in similar social systems.

Evidence for compositionality in baboons (Papio papio) through the test case of negation.

Can non-human animals combine abstract representations much like humans do with language? In particular, can they entertain a compositional representation such as 'not blue'? Across two experiments, we demonstrate that baboons (Papio papio) show a capacity for compositionality. Experiment 1 showed that baboons can entertain negative, compositional, representations: they can learn to associate a cue with iconically related referents (e.g., a blue patch referring to all blue objects), but also to the complement set associated with it (e.g., a blue patch referring to all non-blue objects). Strikingly, Experiment 2 showed that baboons not only learn to associate a cue with iconically related referents, but can learn to associate complex cues (composed of the same cue and an additional visual element) with the complement object set. Thus, they can learn an operation, instantiated by this additional visual element, that can be compositionally combined with previously learned cues. These results significantly reduce any claim that would make the manipulation and combination of abstract representations a solely human privilege.

Gastrointestinal parasites of baboons (Papio papio) in Niokolo-Koba National Park, Senegal.

Background: Primates can harbor parasites that could be pathogenic or not for humans and primates themselves. It is necessary to know the parasitological situation of the primates that are under surveillance in the park. Aim: To estimate the prevalence and diversity of gastrointestinal parasites, including zoonotic potential parasites, in baboons in the Niokolo-Koba National Park located in Senegal. Method: Fecal samples (n = 50) from two groups of baboons (A and B) were collected in October 2019. The samples were processed using the flotation technique and the modified Ritchie method. Slides were examined microscopically and the parasite identification was based on morphology, color, and parasite content. Results: A total of seven nematodes (Strongyloides sp., Trichirus sp., Ancylostoma sp., Mammo monogamus, Enterobius sp., Strongyloides stercoralis, Strongyle digestif), one cestode (Bertiella sp.), and one trematode (Fasciolopsis sp.) were identified. The overall prevalence was 78%, while the prevalence of poly-infected samples was 49%. The parasite with zoonotic potential, S. stercoralis, was identified in group B samples. Trichuris sp., which is common and pathogenic to humans and primates, was present with prevalence of 52% and of 32% in groups A and B, respectively. Conclusion: These results suggest that baboons are infested with zoonotic parasites and this situation could expose people working in this park to infection. Contact between humans and these baboons or their feces could expose them to infection with zoonotic parasites.

Age effect in expert cognitive flexibility in Guinea baboons (Papio papio).

Cognitive flexibility in non-human primates is traditionally measured with the conceptual set shifting task (CSST). In our laboratory, Guinea baboons (N = 24) were continuously tested with a CSST task during approximately 10 years. Our task involved the presentation of three stimuli on a touch screen all made from 3 possible colours and 3 shapes. The subjects had to touch the stimulus containing the stimulus dimension (e.g., green) that was constantly rewarded until the stimulus dimension changed. Analysis of perseveration responses, scores and response times collected during the last two years of testing (approximately 1.6 million trials) indicate (1) that the baboons have developed an "expert" form of cognitive flexibility and (2) that their performance was age-dependent, it was at a developing stage in juveniles, optimal in adults, declining in middle-aged, and strongly impaired in the oldest age group. A direct comparison with the data collected by Bonté , Flemming & Fagot (2011) on some of the same baboons and same task as in the current study indicates that (3) the performance of all age groups has improved after 10 years of training, even for the now old individuals. All these data validate the use of non-human primates as models of human cognitive flexibility and suggest that cognitive flexibility in humans has a long evolutionary history.

Are monkeys sensitive to informativeness: An experimental study with baboons (Papio papio).

Informativeness (defined as reduction of uncertainty) is central in human communication. In the present study, we investigate baboons' sensitivity to informativeness by manipulating the informativity of a cue relative to a response display and by allowing participants to anticipate their answers or to wait for a revealed answer (with variable delays). Our hypotheses were that anticipations would increase with informativity, while response times to revealed trials would decrease with informativity. These predictions were verified in Experiment 1. In Experiments 2 and 3, we manipulated rewards (rewarding anticipation responses at 70% only) to see whether reward tracking alone could account for the results in Experiment 1. We observed that the link between anticipations and informativeness disappeared, but not the link between informativeness and decreased RTs for revealed trials. Additionally, in all three experiments, the number of correct answers in revealed trials with fast reaction times (< 250ms) increased with informativeness. We conclude that baboons are sensitive to informativeness as an ecologically sound means to tracking reward.

Categorization of vocal and nonvocal stimuli in Guinea baboons (Papio papio).

Categorization of vocal sounds apart from other sounds is one of the key abilities in human voice processing, but whether this ability is present in other animals, particularly nonhuman primates, remains unclear. In the present study, 25 socially housed Guinea baboons (Papio papio) were tested on a vocal/nonvocal categorization task using Go/Nogo paradigm implemented on freely accessible automated learning devices. Three individuals from the group successfully learned to sort Grunt vocalizations from nonvocal sounds, and they generalized to new stimuli from the two categories, indicating that some baboons have the ability to develop open-ended categories in the auditory domain. Contrary to our hypothesis based on the human literature, these monkeys learned the nonvocal category faster than the Grunt category. Moreover, they failed to generalize their classification to new classes of conspecific vocalizations (wahoo, bark, yak, and copulation calls), and they categorized human vocalizations in the nonvocal category, suggesting that they had failed to represent the task as a vocal versus nonvocal categorization problem. Thus, our results do not confirm the existence of a separate perceptual category for conspecific vocalizations in baboons. Interestingly, the three successful baboons are the youngest of the group, with less training in visual tasks, which supports previous reports of age and learning history as crucial factors in auditory laboratory experiments.

Male-male social bonding, coalitionary support and reproductive success in wild Guinea baboons.

Male-male bonds may confer substantial fitness benefits. The adaptive value of these relationships is often attributed to coalitionary support, which aids in rank ascension and female defence, ultimately resulting in greater reproductive success. We investigated the link between male-male sociality and both coalitionary support and reproductive success in wild Guinea baboons. This species lives in a tolerant multi-level society with reproductive units comprising a male and 1-6 females at the core. Males are philopatric, form differentiated, stable and equitable affiliative relationships (strong bonds) with other males, and lack a clear rank hierarchy. Here, we analysed behavioural and paternity data for 30 males and 50 infants collected over 4 years in the Niokolo-Koba National Park, Senegal. Strongly bonded males supported each other more frequently during conflicts, but strong bonds did not promote reproductive success. Instead, males that spent less time socializing with other males were associated with a higher number of females and sired more offspring. Notably, reproductively active males still maintained bonds with other males, but adjusted their social investment in relation to life-history stage. Long-term data will be needed to test if the adaptive value of male bonding lies in longer male tenure and/or in promoting group cohesion.

Learning Higher-Order Transitional Probabilities in Nonhuman Primates.

The extraction of cooccurrences between two events, A and B, is a central learning mechanism shared by all species capable of associative learning. Formally, the cooccurrence of events A and B appearing in a sequence is measured by the transitional probability (TP) between these events, and it corresponds to the probability of the second stimulus given the first (i.e., p(B|A)). In the present study, nonhuman primates (Guinea baboons, Papio papio) were exposed to a serial version of the XOR (i.e., exclusive-OR), in which they had to process sequences of three stimuli: A, B, and C. In this manipulation, first-order TPs (i.e., AB and BC) were uninformative due to their transitional probabilities being equal to .5 (i.e., p(B|A) = p(C|B) = .5), while second-order TPs were fully predictive of the upcoming stimulus (i.e., p(C|AB) = 1). In Experiment 1, we found that baboons were able to learn second-order TPs, while no learning occurred on first-order TPs. In Experiment 2, this pattern of results was replicated, and a final test ruled out an alternative interpretation in terms of proximity to the reward. These results indicate that a nonhuman primate species can learn a nonlinearly separable problem such as the XOR. They also provide fine-grained empirical data to test models of statistical learning on the interaction between the learning of different orders of TPs. Recent bioinspired models of associative learning are also introduced as promising alternatives to the modeling of statistical learning mechanisms.

Understanding Imitation in Papio papio: The Role of Experience and the Presence of a Conspecific Demonstrator.

What factors affect imitation performance? Varying theories of imitation stress the role of experience, but few studies have explicitly tested its role in imitative learning in non-human primates. We tested several predictions regarding the role of experience, conspecific presence, and action compatibility using a stimulus-response compatibility protocol. Nineteen baboons separated into two experimental groups learned to respond by targeting on a touch screen the same stimulus as their neighbor (compatible) or the opposite stimulus (incompatible). They first performed the task with a conspecific demonstrator (social phase) and then a computer demonstrator (ghost phase). After reaching a predetermined success threshold, they were then tested in an opposite compatibility condition (i.e., reversal learning conditions). Seven baboons performed at least two reversals during the social phase, and we found no significant difference between the compatible and incompatible conditions, although we noticed slightly faster response times (RTs) in the compatible condition that disappeared after the first reversal. During the ghost phase, monkeys showed difficulties in learning the incompatible condition, and the compatible condition RTs tended to be slower than during the social phase. Together, these results suggest that (a) there is no strong movement compatibility effect in our task and that (b) the presence of a demonstrator plays a role in eliciting correct responses but is not essential as has been previously shown in human studies.

The experimental emergence of convention in a non-human primate.

Conventions form an essential part of human social and cultural behaviour and may also be important to other animal societies. Yet, despite the wealth of evidence that has accumulated for culture in non-human animals, we know surprisingly little about non-human conventions beyond a few rare examples. We follow the literature in behavioural ecology and evolution and define conventions as systematic behaviours that solve a coordination problem in which two or more individuals need to display complementary behaviour to obtain a mutually beneficial outcome. We start by discussing the literature on conventions in non-human primates from this perspective and conclude that all the ingredients for conventions to emerge are present and therefore that they ought to be more frequently observed. We then probe the emergence of conventions by using a unique novel experimental system in which pairs of Guinea baboons (Papio papio) can voluntarily participate together in touchscreen-based cognitive testing and we show that conventions readily emerge in our experimental set-up and that they share three fundamental properties of human conventions (arbitrariness, stability and efficiency). These results question the idea that observational learning, and imitation in particular, is necessary to establish conventions; they suggest that positive reinforcement is enough. This article is part of a discussion meeting issue 'The emergence of collective knowledge and cumulative culture in animals, humans and machines'.

Computerized assessment of dominance hierarchy in baboons (Papio papio).

Dominance hierarchies are an important aspect of Primate social life, and there is an increasing need to develop new systems to collect social information automatically. The main goal of this research was to explore the possibility to infer the dominance hierarchy of a group of Guinea baboons (Papio papio) from the analysis of their spontaneous interactions with freely accessible automated learning devices for monkeys (ALDM, Fagot & Bonté Behavior Research Methods, 42, 507-516, 2010). Experiment 1 compared the dominance hierarchy obtained from conventional observations of agonistic behaviours to the one inferred from the analysis of automatically recorded supplanting behaviours within the ALDM workstations. The comparison, applied to three different datasets, shows that the dominance hierarchies obtained with the two methods are highly congruent (all rs ≥ 0.75). Experiment 2 investigated the experimental potential of inferring dominance hierarchy from ALDM testing. ALDM data previously published in Goujon and Fagot (Behavioural Brain Research, 247, 101-109, 2013) were re-analysed for that purpose. Results indicate that supplanting events within the workstations lead to a transient improvement of cognitive performance for the baboon supplanting its partners and that this improvement depends on the difference in rank between the two baboons. This study therefore opens new perspectives for cognitive studies conducted in a social context.

Comparative analysis of ACE2 protein expression in rodent, non-human primate, and human respiratory tract at baseline and after injury: A conundrum for COVID-19 pathogenesis.

Angiotensin converting enzyme 2 (ACE2) is the putative functional receptor for severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2). Current literature on the abundance and distribution of ACE2 protein in the human respiratory tract is controversial. We examined the effect of age and lung injury on ACE2 protein expression in rodent and non-human primate (NHP) models. We also examined ACE2 expression in human tissues with and without coronavirus disease 19 (COVID-19). ACE2 expression was detected at very low levels in preterm, but was absent in full-term and adult NHP lung homogenates. This pattern of ACE2 expression contrasted with that of transmembrane protease serine type 2 (TMPRSS2), which was significantly increased in full-term newborn and adult NHP lungs compared to preterm NHP lungs. ACE2 expression was not detected in NHP lungs with cigarette smoke-induced airway disease or bronchopulmonary dysplasia. Murine lungs lacked basal ACE2 immunoreactivity, but responded to hyperoxia, bacterial infection, and allergen exposure with new ACE2 expression in bronchial epithelial cells. In human specimens, robust ACE2 immunoreactivity was detected in ciliated epithelial cells in paranasal sinus specimens, while ACE2 expression was detected only in rare type 2 alveolar epithelial cells in control lungs. In autopsy specimens from patients with COVID-19 pneumonia, ACE2 was detected in rare ciliated epithelial and endothelial cells in the trachea, but not in the lung. There was robust expression of ACE2 expression in F344/N rat nasal mucosa and lung specimens, which authentically recapitulated the ACE2 expression pattern in human paranasal sinus specimens. Thus, ACE2 protein expression demonstrates a significant gradient between upper and lower respiratory tract in humans and is scarce in the lung. This pattern of ACE2 expression supports the notion of sinonasal epithelium being the main entry site for SARS-CoV-2 but raises further questions on the pathogenesis and cellular targets of SARS-CoV-2 in COVID-19 pneumonia.

Extraction of structural regularities by baboons (Papio Papio): Adjacent and nonadjacent repetition patterns differ in learnability.

Several animal species can discriminate between different sequential patterns based on repetitions of items (e.g., ABB vs. ABA), and generalize their performance to sequences made of novel elements but following the same underlying structure. This achievement suggests that these species possess the ability to abstract the sequences structures beyond exemplars. Developmental studies in humans suggest however that adjacent repetition patterns (e.g., ABB) are easier to extract than patterns based on a nonadjacent (e.g., ABA) repetitions. This study addressed this effect of adjacency from a comparative perspective. Seventeen Guinea baboons (Papio papio) were tested with an adaptation of the serial response time task. Results show that baboons successfully learned and generalized both adjacent and nonadjacent repetition patterns after extensive exposure to each pattern in 2 successive experimental phases (Experiment 1). However, when these patterns were presented interleaved within the same experimental phase and at equal frequencies (Experiment 2), or presented successively as in Experiment 1 but with less exposure trials (Experiment 3), baboons showed evidence of learning of the adjacent repetition pattern only. Overall, these data suggest that baboons are more sensitive to adjacent than nonadjacent repetitions. We argue that a strategy based on sole detection of the presence/absence of an adjacent repetition is therefore likely to be adopted by the tested animals in pattern learning studies contrasting adjacent versus nonadjacent repetition patterns, and that future studies may need to avoid this contrast to prevent the use of this strategy. (PsycInfo Database Record (c) 2021 APA, all rights reserved).

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.