Great Ape Species Research Articles

Object permanence in rooks (Corvus frugilegus): Individual differences and behavioral considerations.

Piagetian object permanence (OP) refers to the ability to know that an object continues to exist when out of sight: In humans, it develops in six stages. Species of great apes, other mammals, and birds (parrots, corvids, and pigeons) have been shown to possess partial or full OP, which is a prerequisite for more complex physical cognition abilities they may possess. In birds, the greatest variation is in Stage 6 (invisible displacements) and in "A-not-B" errors-incorrectly persevering in searching an empty location rewarded previously. Caching abilities have been invoked as holding explanatory power over results in corvids, for which this error is sometimes completely absent. The rook (Corvus frugilegus), a cognitively advanced, social, caching corvid, has not yet been studied for OP. This study applies tasks of one OP scale commonly adapted for nonhuman animals, Uzgiris and Hunt's Scale 1, as well as later-conceived tasks 16 and S, to a sample of adult, captive rooks. One rook demonstrated full OP (Stage 6b, multiple invisible displacements), whereas other individuals varied, attaining between Stages 5a (single visible displacements) and 6a (single invisible displacements). Like some corvids, a few made transient "A-not-B" errors. Behavioral considerations potentially underlying observed individual variation in results in rooks, including dominance, neophobia, past experiences, and individual idiosyncrasies, are examined. Rooks, like other corvids, possess well-developed OP abilities, and these results support the idea that exertion of executive control is required to avoid "A-not-B" errors, rather than caching abilities or developmental age, as previously suggested.

The uniqueness of human vulnerability to brain aging in great ape evolution.

Aging is associated with progressive gray matter loss in the brain. This spatially specific, morphological change over the life span in humans is also found in chimpanzees, and the comparison between these great ape species provides a unique evolutionary perspective on human brain aging. Here, we present a data-driven, comparative framework to explore the relationship between gray matter atrophy with age and recent cerebral expansion in the phylogeny of chimpanzees and humans. In humans, we show a positive relationship between cerebral aging and cortical expansion, whereas no such relationship was found in chimpanzees. This human-specific association between strong aging effects and large relative cortical expansion is particularly present in higher-order cognitive regions of the ventral prefrontal cortex and supports the "last-in-first-out" hypothesis for brain maturation in recent evolutionary development of human faculties.

The origin of great ape gestural forms.

Two views claim to account for the origins of great ape gestural forms. On the Leipzig view, gestural forms are ontogenetically ritualised from action sequences between pairs of individuals. On the St Andrews view, gestures are the product of natural selection for shared gestural forms. The Leipzig view predicts within- and between-group differences between gestural forms that arise as a product of learning in ontogeny. The St Andrews view predicts universal gestural forms comprehensible within and between species that arise because gestural forms were a target of natural selection. We reject both accounts and propose an alternative "recruitment view" of the origins of great ape gestures. According to the recruitment view, great ape gestures recruit features of their existing behavioural repertoire for communicative purposes. Their gestures inherit their communicative functions from visual (and sometimes tactile) presentations of familiar and easily recognisable action schemas and states and parts of the body. To the extent that great ape species possess similar bodies, this predicts mutual comprehensibility within and between species - but without supposing that gestural forms were themselves targets of natural selection. Additionally, we locate great ape gestural communication within a pragmatic framework that is continuous with human communication, and make testable predications for adjudicating between the three alternative views. We propose that the recruitment view best explains existing data, and does so within a mechanistic framework that emphasises continuity between human and non-human great ape communication.

Human lncRNAs harbor conserved modules embedded in different sequence contexts

We analyzed the structure of human long non-coding RNA (lncRNAs) genes to investigate whether the non-coding transcriptome is organized in modular domains, as is the case for protein-coding genes. To this aim, we compared all known human lncRNA exons and identified 340 pairs of exons with high sequence and/or secondary structure similarity but embedded in a dissimilar sequence context. We grouped these pairs in 106 clusters based on their reciprocal similarities. These shared modules are highly conserved between humans and the four great ape species, display evidence of purifying selection and likely arose as a result of recent segmental duplications. Our analysis contributes to the understanding of the mechanisms driving the evolution of the non-coding genome and suggests additional strategies towards deciphering the functional complexity of this class of molecules.

Phylogenetic differences in the morphology and shape of the central sulcus in great apes and humans: implications for the evolution of motor functions.

The central sulcus divides the primary motor and somatosensory cortices in many anthropoid primate brains. Differences exist in the surface area and depth of the central sulcus along the dorso-ventral plane in great apes and humans compared to other primate species. Within hominid species, there are variations in the depth and aspect of their hand motor area, or knob, within the precentral gyrus. In this study, we used post-image analyses on magnetic resonance images to characterize the central sulcus shape of humans, chimpanzees (Pan troglodytes), gorillas (Gorilla gorilla), and orangutans (Pongo pygmaeus and Pongo abelii). Using these data, we examined the morphological variability of central sulcus in hominids, focusing on the hand region, a significant change in human evolution. We show that the central sulcus shape differs between great ape species, but all show similar variations in the location of their hand knob. However, the prevalence of the knob location along the dorso-ventral plane and lateralization differs between species and the presence of a second ventral motor knob seems to be unique to humans. Humans and orangutans exhibit the most similar and complex central sulcus shapes. However, their similarities may reflect divergent evolutionary processes related to selection for different positional and habitual locomotor functions.

Ape recognition of familiar human faces changed by time and COVID-19 face masks

Reports of primates being able to recognise familiar humans are rare in the literature and tend to be regarded as anecdotal. The COVID-19 pandemic created two unique conditions facilitating the observation of spontaneous face recognition in zoo apes: i) lengthy gaps in contact with human visitors due to lockdowns and zoo closures, and ii) the wearing of face masks obscuring at least half the face of familiar individuals. Here, I report on the historical context of the familiarity between a primatologist and individual apes of two species, how those apes consistently showed recognition of this particular human over a time span of up to thirty years, how facial recognition was extended to family members, and how recognition persisted even when a significant portion of the face was obscured by a mask. This constitutes, to my knowledge, the first documented cases of recognition of familiar human faces changed by time and COVID-19 face masks in two great ape species. Although based on just two individuals, the documentation of this ability is important because it arose in a more naturalistic and spontaneous context compared to typical face processing research in which primates are tested with experimental stimuli in a laboratory setting. Implications for face processing theory and applications for the therapeutic utility of faces are discussed. These observations provide insight into the evolutionary origins of face recognition and, sitting at the interface of science and society, are of interest to a wide audience.

Applying best practice to feasibility assessment and strategic planning for great ape translocation: A case study of Grauer's gorilla (Gorilla beringei graueri)

We outline the feasibility and risk assessments that are essential prerequisites to conservation translocation of great apes, while upholding the precautionary principle to avoid harms to conspecifics, sympatric taxa and ecosystems. As part of a strategic planning process, we addressed key questions on the costs and benefits of a translocation of Grauer's gorillas in Democratic Republic of Congo. We reviewed published and gray literature to compile data on Grauer's gorilla ecology and potential release sites in the subspecies' geographic range. Taking into account ecological dimensions of the habitats, impacts on conspecifics, sympatric great apes and other wildlife, and existing threats, we formulated recommendations on whether and where translocation could benefit conservation of this taxon. We concluded that one site assessed is compatible with key IUCN criteria. At Mt. Tshiaberimu in Virunga National Park, the resident Grauer's gorilla population is non-viable, no sympatric great ape species is present and the site is actively protected against poaching and habitat encroachment. Conservation translocations are widely used for species recovery; however, detailed accounts of the analyses and planning required to adhere to IUCN best practice are rare. Our approach enabled evidence-based determination of feasibility despite some initial information gaps. The process is widely applicable and could encourage improved compliance with IUCN guidelines when risks to wild conspecifics might be high, yet ecological knowledge of the target population is limited. The Grauer's Gorilla Conservation and Reinforcement Project is a partnership between the Gorilla Rehabilitation and Conservation Education Center, Virunga National Park and Re:wild.

Spontaneous playful teasing in four great ape species.

Joking draws on complex cognitive abilities: understanding social norms, theory of mind, anticipating others' responses and appreciating the violation of others' expectations. Playful teasing, which is present in preverbal infants, shares many of these cognitive features. There is some evidence that great apes can tease in structurally similar ways, but no systematic study exists. We developed a coding system to identify playful teasing and applied it to video of zoo-housed great apes. All four species engaged in intentionally provocative behaviour, frequently accompanied by characteristics of play. We found playful teasing to be characterized by attention-getting, one-sidedness, response looking, repetition and elaboration/escalation. It takes place mainly in relaxed contexts, has a wide variety of forms, and differs from play in several ways (e.g. asymmetry, low rates of play signals like the playface and absence of movement-final 'holds' characteristic of intentional gestures). As playful teasing is present in all extant great ape genera, it is likely that the cognitive prerequisites for joking evolved in the hominoid lineage at least 13 million years ago.

WILL THE GREAT PRIMATES BE RECOGNIZED AS NON-HUMAN PERSONS IN THE 21ST CENTURY?

Great primates have been an endangered species for more than fifty years. The continued pressure that humans make in the habitants and rainforests around the glove have pushed chimpanzees, bonobos, orangutans, and gorillas to the very limits of their well-being. Nowadays there exists a big international pressure, which aims to release primates from their captive environments in zoos, or to promote the development of laws that protect these animals from suffering, hunting, and captivity. In order to accomplish this pursuit, it would be a great movement ahead to recognize the four species of great apes (aside of humans) as non-human persons giving them rights under which the law would protect them from human activities in their natural habitats and the captive situation they live in many countries around the globe.

Understanding others' preferences: A comparison across primate species and human societies.

We investigated children's and non-human great apes' ability to anticipate others' choices from their evident food preferences-regardless of whether these preferences deviate or align with one's own. We assessed children from three culturally-diverse societies (Namibia, Germany, and Samoa; N = 71; age range = 5-11) and four non-human great ape species (chimpanzees (Pan troglodytes), bonobos (Pan paniscus), gorillas (Gorilla gorilla), and orangutans (Pongo abelii); N = 25; age range = 7-29) regarding their choices in a dyadic food-retrieval task. Across conditions, participants' preferences were either aligned (same preference condition) or opposed (opposite preference condition) to those of their competitors. Children across societies altered their choices based on their competitor's preferences, indicating a cross-culturally recurrent capacity to anticipate others' choices relying on preferences-based inferences. In contrast to human children, all non-human great apes chose according to their own preferences but independent of those of their competitors. In sum, these results suggest that the tendency to anticipate others' choices based on their food preferences is cross-culturally robust and, among the great apes, most likely specific to humans.

Pediatric Respiratory Pathogens Circulate in Children and Adults in Communities Near Susceptible Wild Great Ape Populations in Uganda

Respiratory infections are a leading cause of death in developing countries. Infants and young children are especially susceptible to disease because they lack immunity, whereas adults who have acquired immunity can be infected asymptomatically. Great ape species, all of which are endangered, are similarly susceptible to respiratory illnesses caused by human respiratory pathogens. We obtained 432 nasopharyngeal swab samples (127 from adults and 305 from children) in a cross‐sectional study that took place between February and October 2022 at four sites in Western Uganda (Budongo Central Forest Reserve, Bulindi Town Council, Bwindi Impenetrable National Park, and Kibale National Park) where the participants live in communities where interaction with apes is frequent. Prior research at Kibale has shown that locally circulating human respiratory pathogens have led to multiple lethal outbreaks in wild eastern chimpanzees (Pan troglodytes schweinfurthii). We used a multiplex PCR panel to characterize respiratory pathogens, with the goal of assessing whether respiratory illnesses in the chimpanzees of Budongo and Bulindi and the mountain gorillas (Gorilla beringei beringei) of Bwindi might have originated in local children and been introduced to the apes via asymptomatic adult carriers. The prevalence of respiratory pathogens was twice as high in Bwindi (44.0%) as it was in Budongo (24.0%) and Bulindi (20.8%), while the prevalence was intermediate at Kibale (34.4%). Rates of respiratory pathogen detection were higher but statistically indistinguishable in children compared to adults at Budongo and Bulindi, and children were 15.0 times more likely than adults to have positive detections at Kibale. At Bwindi, however, the pattern was reversed, with adults 2.6 times more likely than children to have positive detections. Rhinovirus, metapneumovirus, human parainfluenza virus 3, respiratory syncytial virus, and coronavirus OC43, all of which have been identified as causative agents of respiratory disease outbreaks in great ape populations across sub‐Saharan Africa, accounted for three quarters (73.6%) of detected pathogens. Our data support the idea that human respiratory pathogens that can infect great apes occur at high frequencies in human populations in Western Uganda that live close to and interact with wild apes that have suffered from lethal outbreaks caused by these same pathogens. Reducing respiratory infections in local children, thereby reducing both carriage of those infections into the forest by people and ape exposure to these pathogens when they enter human spaces, should decrease the risk of respiratory disease outbreaks in apes.

Evolutionary Insight into the Association between New Jersey Polyomavirus and Humans.

Advances in viral discovery techniques have led to the identification of numerous novel viruses in human samples. However, the low prevalence of certain viruses in humans raises doubts about their association with our species. To ascertain the authenticity of a virus as a genuine human-infecting agent, it can be useful to investigate the diversification of its lineage within hominines, the group encompassing humans and African great apes. Building upon this rationale, we examined the case of the New Jersey polyomavirus (NJPyV; Alphapolyomavirus terdecihominis), which has only been detected in a single patient thus far. In this study, we obtained and analyzed sequences from closely related viruses infecting all African great ape species. We show that NJPyV nests within the diversity of these viruses and that its lineage placement is compatible with an ancient origin in humans, despite its apparent rarity in human populations.

Transcript Isoform Diversity of Ampliconic Genes on the Y Chromosome of Great Apes.

Y chromosomal ampliconic genes (YAGs) are important for male fertility, as they encode proteins functioning in spermatogenesis. The variation in copy number and expression levels of these multicopy gene families has been studied in great apes; however, the diversity of splicing variants remains unexplored. Here, we deciphered the sequences of polyadenylated transcripts of all nine YAG families (BPY2, CDY, DAZ, HSFY, PRY, RBMY, TSPY, VCY, and XKRY) from testis samples of six great ape species (human, chimpanzee, bonobo, gorilla, Bornean orangutan, and Sumatran orangutan). To achieve this, we enriched YAG transcripts with capture probe hybridization and sequenced them with long (Pacific Biosciences) reads. Our analysis of this data set resulted in several findings. First, we observed evolutionarily conserved alternative splicing patterns for most YAG families except for BPY2 and PRY. Second, our results suggest that BPY2 transcripts and proteins originate from separate genomic regions in bonobo versus human, which is possibly facilitated by acquiring new promoters. Third, our analysis indicates that the PRY gene family, having the highest representation of noncoding transcripts, has been undergoing pseudogenization. Fourth, we have not detected signatures of selection in the five YAG families shared among great apes, even though we identified many species-specific protein-coding transcripts. Fifth, we predicted consensus disorder regions across most gene families and species, which could be used for future investigations of male infertility. Overall, our work illuminates the YAG isoform landscape and provides a genomic resource for future functional studies focusing on infertility phenotypes in humans and critically endangered great apes.

Regularized sequence-context mutational trees capture variation in mutation rates across the human genome.

Germline mutation is the mechanism by which genetic variation in a population is created. Inferences derived from mutation rate models are fundamental to many population genetics methods. Previous models have demonstrated that nucleotides flanking polymorphic sites-the local sequence context-explain variation in the probability that a site is polymorphic. However, limitations to these models exist as the size of the local sequence context window expands. These include a lack of robustness to data sparsity at typical sample sizes, lack of regularization to generate parsimonious models and lack of quantified uncertainty in estimated rates to facilitate comparison between models. To address these limitations, we developed Baymer, a regularized Bayesian hierarchical tree model that captures the heterogeneous effect of sequence contexts on polymorphism probabilities. Baymer implements an adaptive Metropolis-within-Gibbs Markov Chain Monte Carlo sampling scheme to estimate the posterior distributions of sequence-context based probabilities that a site is polymorphic. We show that Baymer accurately infers polymorphism probabilities and well-calibrated posterior distributions, robustly handles data sparsity, appropriately regularizes to return parsimonious models, and scales computationally at least up to 9-mer context windows. We demonstrate application of Baymer in three ways-first, identifying differences in polymorphism probabilities between continental populations in the 1000 Genomes Phase 3 dataset, second, in a sparse data setting to examine the use of polymorphism models as a proxy for de novo mutation probabilities as a function of variant age, sequence context window size, and demographic history, and third, comparing model concordance between different great ape species. We find a shared context-dependent mutation rate architecture underlying our models, enabling a transfer-learning inspired strategy for modeling germline mutations. In summary, Baymer is an accurate polymorphism probability estimation algorithm that automatically adapts to data sparsity at different sequence context levels, thereby making efficient use of the available data.

Revisiting the baby schema by a geometric morphometric analysis of infant facial characteristics across great apes

Infants across species are thought to exhibit specific facial features (termed the “baby schema”, such as a relatively bigger forehead and eyes, and protruding cheeks), with an adaptive function to induce caretaking behaviour from adults. There is abundant empirical evidence for this in humans, but, surprisingly, the existence of a baby schema in non-human animals has not been scientifically demonstrated. We investigated which facial characteristics are shared across infants in five species of great apes: humans, chimpanzees, bonobos, mountain gorillas, and Bornean orangutans. We analysed eight adult and infant faces for each species (80 images in total) using geometric morphometric analysis and machine learning. We found two principal components characterizing infant faces consistently observed across species. These included (1) relatively bigger eyes located lower in the face, (2) a rounder and vertically shorter face shape, and (3) an inverted triangular face shape. While these features are shared, human infant faces are unique in that the second characteristic (round face shape) is more pronounced, whereas the third (inverted triangular face shape) is less pronounced than other species. We also found some infantile features only found in some species. We discuss future directions to investigate the baby schema using an evolutionary approach.

Factors affecting nest height and ground nesting behaviour in Eastern chimpanzees (Pan troglodytes schweinfurthii) of the northern Democratic Republic of the Congo.

In order to achieve a better understanding of the factors that might have led our hominin ancestors to transition to a more terrestrial niche, including sleeping on the ground, we have conducted a study on the ground nesting behavior of chimpanzees (Pan troglodytes). Chimpanzees, like all other species of great apes, build nests in which to sleep each night, but little is known about regional differences in their nesting habits. Previously, nesting on the ground was considered typical of gorillas, but rare in most populations of chimpanzees. Using data acquired during our extensive chimpanzee nesting survey conducted between 2004 and 2013 across a > 50 000km2 region in northern Democratic Republic of the Congo, we report a distinctive ground nesting behaviour of eastern chimpanzees (P. t. schweinfurthii). We have mapped the geographical distribution of ground nesting and compared its frequency at 20 survey areas on both sides of a large river, the Uele. We found that ground nests made up more than 1% of total nests at 15 of the 20 survey regions. For a subset of 16 of these regions, we utilized statistical models to investigate whether forest type and structure, as well as the abundance of carnivores and large herbivores, and the activities of humans impacted the frequency of ground nesting and nest height. We predicted that higher encounter rates of human and dangerous animal signs would be associated with lower rates of ground nesting as well as increased nest height. Overall, 10.4% of the Bili-Uéré chimpanzee nests were terrestrial, but the frequency of ground nesting varied extensively between the survey areas (0-29% of nests). The occurrence of ground nests was positively associated with denser forests (p= 0.004), herb patches (p < 0.001), and light gaps (p < 0.001). Light gaps (p < 0.001), herb patches (p= 0.044), and vine tangles (p= 0.016) also had a strong negative effect on nest height. Hunting by humans had a negative effect on the probability of the occurrence of ground nests (p= 0.001) and a positive one on nest height (p= 0.013), with a similar but likely marginal effect of large herbivores on nest height (p= 0.023). In addition, the chimpanzees nested at significantly lower heights with increasing distance from roads and settlements (p< 0.001). Carnivore encounter rates, however, had no significant impact on ground nest frequency or nest height. Our results indicate that ground nesting can no longer be considered a rare and patchily-occurring phenomenon in Pan troglodytes, but is instead a major component of the chimpanzee behavioural repertoire across a considerable fraction of the range of the Eastern subspecies. Our study highlights that neither the large body size of gorillas nor the taming of fire are necessary conditions for hominids to sleep overnight on the ground, even in areas inhabited by multiple species of large carnivore. Human hunting, however, appears to reduce the probability of ground nesting, or eliminate the behavior altogether.

Primate origins of discourse-managing gestures: the case of hand fling

Abstract The last decades have seen major advances in the study of gestures both in humans and non-human primates. In this paper, we seriously examine the idea that there may be gestural form types that are shared across great ape species, including humans, which may underlie gestural universals, both in form and meaning. We focus on one case study, the hand fling gesture common to chimpanzees and humans, and provide a semantic analysis of this gesture.

Through the looking glass: how do marked dolphins use mirrors and what does it mean?

Mirror-guided self-inspection is seen as a cognitive hallmark purportedly indicating the existence of self-recognition. Only a few species of great apes have been reported to pass a standard mark test for mirror self-recognition in which animals attempt to touch a mark. In addition, evidence for passing the mark test was also reported for Asian elephants, two species of corvids, and a species of cleaner fish. Mirror self-recognition has also been claimed for bottlenose dolphins, using exposure of marked areas to a mirror as evidence. However, what counts as self-directed behaviour to see the mark and what does not has been debated. To avoid this problem, we marked the areas around both eyes of the animals at the same time, one with visible and the other with transparent dye to control for haptic cues. This allowed the animal to see the mark easily and us to investigate what side was exposed to the mirror as an indicator for mark observation. We found that the animals actively chose to inspect their visibly marked side while they did not show an increased interest in a marked conspecific in the pool. These results demonstrate that dolphins use the mirror to inspect their marks and, therefore, likely recognise a distinction between self and others.

Stable isotopic investigation of the feeding ecology of wild Bornean orangutans

AbstractObjectivesWe applied stable carbon and nitrogen isotope analyses to wild Bornean orangutans (Pongo pygmaeus morio) to investigate the feeding ecology of wild orangutans. Compared with African great ape species, orangutans are adapted to environments with chronic lower nutrition. But the usefulness of stable isotope analysis in the study of wild orangutan feeding ecology has not been fully explored.MethodsThe study site was a primary lowland dipterocarp forest in the Danum Valley, Sabah, Malaysia. A total of 164 plant and 94 fecal samples collected across 18 months were analyzed.ResultsCarbon and nitrogen stable isotope ratios of plant food samples do not systematically vary by plant parts (i.e., bark, fruits, and leaves). Elemental composition and stable isotope ratios of orangutan feces do not systematically vary by orangutans' sex and age classes, although fecal stable isotope ratios showed seasonal fluctuations. No isotopic contribution of breast milk was found in fecal samples collected from individuals at 2.7–6.5 years of age.ConclusionsThis study revealed key characteristics of the stable isotope ecology of wild orangutans living in a primary lowland forest. Although there was little isotopic variation among plant foods and orangutan individuals, seasonal fluctuations in baseline isotope ratios or orangutans' diet were found in Danum valley.

Hierarchical object combination and tool use in the great apes and human children

Object manipulation can be used as a comparative scale of cognitive development among primates, including humans. Combinatory object manipulation is a precursor of tool-using behavior that indicates material intelligence in primates. However, developmental data on it regarding the great apes other than chimpanzees is insufficient. We conducted a longitudinal investigation of humans and chimpanzees as well as a cross-sectional examination of other great-ape infants (two bonobos, three gorillas, and four orangutans) in captive settings by using two kinds of tasks that required either inserting or stacking combinatory action. The four species of great apes and humans demonstrated both types of combinatory object manipulation during infancy. However, the order of development in different types of combinatory object manipulations varied among the great apes. Furthermore, we applied a nesting-cup task to examine the hierarchical complexity in the combinatory strategies of human children and adult chimpanzees. Both of them exhibited highly hierarchical combinations in the nesting-cup task and employed the subassembly strategy, indicating that an action merge may exist not only in human children but also in adult chimpanzees. The results were discussed with reviews of the tool-use literature from the wild great apes. The early acquisition of an inserting action in the chimpanzees may explain the tool utilization commonality reported in wild chimpanzees. The combinatory object manipulation may have worked as an external enhancer to achieve an additional hierarchical complexity in cognition and behavior, eventually leading humans to develop a language system.