Abilities Of Nonhuman Primates Research Articles

Influence of food physical properties and environmental context on manipulative behaviors highlighted by new methodological approaches in zoo-housed bonobos (Pan paniscus).

Research on manipulative abilities in nonhuman primates, in the context of hominid evolution, has mostly focused on manual/pedal postures considered as static behaviors. While these behavioral repertoires highlighted the range of manipulative abilities in many species, manipulation is a dynamic process that mostly involves successive types of grips before reaching its goal. The present study aims to investigate the use of manual/pedal postures in zoo-housed bonobos in diverse dynamic food processing by using an innovative approach: the optimal matching analysis that compares sequences (i.e., succession of grasping postures) with each other. To characterize the manipulative techniques spontaneously employed by bonobos, we performed this sequential analysis of manual/pedal postures during 766 complete feeding sequences of 17 individuals. We analyzed the effectiveness with a score defined by a partial proxy of food intake (i.e., the number of mouthfuls) linked to a handling score measuring both the diversity and changes of manual postures during each sequence. We identified four techniques, used differently depending on the physical substrate on which the individual performed food manipulation and the food physical properties. Our results showed that manipulative techniques were more complex (i.e., higher handling score) for large foods and on substrates with lower stability. But the effectiveness score was not significantly lower for these items since manipulative complexity seemed to be compensated by a greater number of mouthfuls. It appeared that the techniques employed involved a trade-off between manipulative complexity and the amount of food ingested. This study allowed us to test and validate innovative analysis methods that are applicable to diverse ethological studies involving sequential events. Our results bring new data for a better understanding of the evolution of manual abilities in primates in association with different ecological contexts and both terrestrial and arboreal substrates and suggest that social and individual influences need to be explored further.

Anogenital distance as a measure of male competitive ability in Rwenzori Angolan colobus.

Anogenital distance (AGD) is positively correlated to fetal androgen exposure and developmental masculinization in mammals. Independent of overall body size, AGD shows a strong positive correlation with male fertility and in rodents, AGD is a good indicator of male competitive ability and is associated with female choice. We hypothesized that AGD will also predict male competitive ability in non-human primates. To test this, we measured AGD noninvasively with a parallel laser in a wild population of Angolan colobus monkeys (Colobus angolensis ruwenzorii) in Uganda and correlated to it to their social structure. C. angolensis ruwenzorii form a multilevel society with both one-male/multifemale units (OMUs) and multimale/multifemale units (MMUs). We compared AGD in males from five OMUs and six MMUs and related it to their fecal androgen metabolite concentrations, dominance rank and body size, and to the number of females in their unit. Males in OMUs had greater access to females, so were predicted to have longer AGDs, but this was not found. AGD also did not correlate overall with mean fecal androgen metabolites in MMUs. However, AGD was correlated with dominance rank in MMUs, demonstrating that higher-ranking males in these multimale units had longer AGDs. Body size did not show the same relationship with dominance rank, suggesting that male rank was not just a reflection of absolute male size. Our findings indicate that AGD predicts male competitive ability in this species and that it may be a useful correlate throughout the non-human primates. These results also support the idea that prenatal androgen exposure increases the likelihood of the expression of behaviors that maintain high dominance rank.

Interaction of music and emotional stimuli in modulating working memory in macaque monkeys.

Background music is one of the most frequently encountered contextual factors that affect cognitive and emotional functions in humans. However, it is still unclear whether music induces similar effects in nonhuman primates. Answering this question might bring insight to the long-lasting question regarding the ability of nonhuman primates in perceiving and dissociating music from other nonmusical acoustic information. In the present study, macaque monkeys were trained to perform a working memory task that required matching visual stimuli. These stimuli had different emotional content (neutral, negative, and positive). Monkeys performed the task within different background acoustic conditions (music, same-intensity noise, and silence). We hypothesized that the auditory stimuli might interact with emotional information of visual stimuli and modulate monkeys' performance. Furthermore, if the effects of music and noise on monkeys' behavioral measures differ it would mean that monkeys perceived and processed music differently. We found that, monkeys committed more errors and were slower when they encountered stimuli with negative or positive emotional content. In the presence of music, the influence of emotional stimuli on monkeys' performance significantly differed from those of the neutral stimuli, however, in the presence of noise, the effects of emotional stimuli on monkeys' performance were not distinguishable. The dissociable effects of music and noise on monkeys' performance show that the effects of emotional stimuli were dependent on the background acoustic conditions. Our findings indicate that background music and the same-intensity noise were differentially perceived by monkeys and influenced their cognitive functions.

Bipedal Steps in the Development of Rhythmic Behavior in Humans

We contrast two related hypotheses of the evolution of dance: H1: Maternal bipedal walking influenced the fetal experience of sound and associated movement patterns; H2: The human transition to bipedal gait produced more isochronous/predictable locomotion sound resulting in early music-like behavior associated with the acoustic advantages conferred by moving bipedally in pace. The cadence of walking is around 120 beats per minute, similar to the tempo of dance and music. Human walking displays long-term constancies. Dyads often subconsciously synchronize steps. The major amplitude component of the step is a distinctly produced beat. Human locomotion influences, and interacts with, emotions, and passive listening to music activates brain motor areas. Across dance-genres the footwork is most often performed in time to the musical beat. Brain development is largely shaped by early sensory experience, with hearing developed from week 18 of gestation. Newborns reacts to sounds, melodies, and rhythmic poems to which they have been exposed in utero. If the sound and vibrations produced by footfalls of a walking mother are transmitted to the fetus in coordination with the cadence of the motion, a connection between isochronous sound and rhythmical movement may be developed. Rhythmical sounds of the human mother locomotion differ substantially from that of nonhuman primates, while the maternal heartbeat heard is likely to have a similar isochronous character across primates, suggesting a relatively more influential role of footfall in the development of rhythmic/musical abilities in humans. Associations of gait, music, and dance are numerous. The apparent absence of musical and rhythmic abilities in nonhuman primates, which display little bipedal locomotion, corroborates that bipedal gait may be linked to the development of rhythmic abilities in humans. Bipedal stimuli in utero may primarily boost the ontogenetic development. The acoustical advantage hypothesis proposes a mechanism in the phylogenetic development.

Monkeys Spontaneously Discriminate Their Unfamiliar Paternal Kin under Natural Conditions Using Facial Cues

Kin recognition can enhance inclusive fitness via nepotism and optimal outbreeding. Mechanisms allowing recognition of patrilineal relatives are of particular interest in species in which females mate promiscuously, leading to paternity uncertainty. Humans are known to detect facial similarities between kin in the faces of third parties, and there is some evidence for continuity of this ability in nonhuman primates . However, no study has yet shown that this propensity translates into an ability to detect one's own relatives, one of the key prerequisites for gaining fitness benefits. Here we report a field experiment demonstrating that free-ranging rhesus macaques (Macaca mulatta) spontaneously discriminate between facial images of their paternal half-siblings and unrelated individuals, when both animals are unfamiliar to the tested individual. Specifically, subjects systematically biased their inspection time toward nonkin when the animals pictured were of their own sex (potential threats), relative to when they were of the opposite sex (potential mates). Our results provide strong evidence for visual phenotype matching and the first demonstration in any primate that individuals can spontaneously detect their own paternal relatives on the basis of facial cues under natural conditions.

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.

Social learning of vocal structure in a nonhuman primate?

BackgroundNon-human primate communication is thought to be fundamentally different from human speech, mainly due to vast differences in vocal control. The lack of these abilities in non-human primates is especially striking if compared to some marine mammals and bird species, which has generated somewhat of an evolutionary conundrum. What are the biological roots and underlying evolutionary pressures of the human ability to voluntarily control sound production and learn the vocal utterances of others? One hypothesis is that this capacity has evolved gradually in humans from an ancestral stage that resembled the vocal behavior of modern primates. Support for this has come from studies that have documented limited vocal flexibility and convergence in different primate species, typically in calls used during social interactions. The mechanisms underlying these patterns, however, are currently unknown. Specifically, it has been difficult to rule out explanations based on genetic relatedness, suggesting that such vocal flexibility may not be the result of social learning.ResultsTo address this point, we compared the degree of acoustic similarity of contact calls in free-ranging Campbell's monkeys as a function of their social bonds and genetic relatedness. We calculated three different indices to compare the similarities between the calls' frequency contours, the duration of grooming interactions and the microsatellite-based genetic relatedness between partners. We found a significantly positive relation between bond strength and acoustic similarity that was independent of genetic relatedness.ConclusionGenetic factors determine the general species-specific call repertoire of a primate species, while social factors can influence the fine structure of some the call types. The finding is in line with the more general hypothesis that human speech has evolved gradually from earlier primate-like vocal communication.

Concept of mind in non-human primates

Research concerning animal cognition explores the abilities and capacity of animals to perceive, think and conceive. As an extension of this, researchers have tried to ascertain the concept of animal minds. The field has been a matter of great debate as it has brought into question the uniqueness of the human mind. This dissertation will review the various areas of research that have contributed to our understanding of animal minds, with a specific focus on non-human primates. The term ‘theory of mind’ was originally proposed by Premack and Woodruff in 1978. The ability entails a recognition and understanding of another’s mental states. Recently, this term has included the cognition of seeing. Throughout this article, the important distinction between theory of mind capabilities and complex behavioural analysis is emphasized. It is important to consider how various primates represent entities in their environment, including their own image. In particular reference to this latter point, self-recognition could act as a first step towards understanding others. With this ability, other individuals may then be understood and manipulated through deception, imitation and teaching. In addition to deception, pretend play and external representation are proposed as another dimension of understanding false representations. Decisions about the evolutionary point at which theory of mind may have developed will depend on interpretations of the evidence for these abilities in non-human primates and whether indeed theory of mind is underlying them. Since the conception of the term ‘theory of mind’, the issue may have evolved beyond whether or not there is theory of mind in non-human primates to a more sophisticated appreciation that the concept of mind has many facets and some of these may exist in non-human primates while others may not.

Behavioural responses to photographs by pictorially naïve baboons (Papio anubis), gorillas (Gorilla gorilla) and chimpanzees (Pan troglodytes)

This study assessed how pictorially naïve nonhuman primates understand pictures. Fifty-five baboons with no prior exposure to pictures were trained to grasp a slice of banana presented against a pebble in a two alternative forced choice task. Post-training testing involved three stimulus pairs: (1) real banana slice vs. its picture, (2) the banana picture vs. a real pebble and (3) banana picture vs. a pebble picture which were presented twice. Preliminary data were also collected on naïve gorillas (n=4) and chimpanzees (n=7) using the same procedure. Baboons revealed a preference for the food picture in (2) and (3) and often ate this stimulus, but the food item and its picture were accurately discriminated in (1). These results suggest that baboons mistook the pictorial stimulus and its referent, but processed the banana pictures as poor exemplars of the real banana category. Among apes, only gorillas ate the banana pictures, suggesting that picture-object confusion may also occur in this species. Findings are discussed as pertaining to the general issue of representational abilities in nonhuman primates, and its evolution.

Measuring reward assessment in a semi-naturalistic context: The effects of selective amygdala, orbital frontal or hippocampal lesions

Studying the neural mechanisms underlying complex goal-directed behaviors, such as social behavior, reward seeking or punishment avoidance, has become increasingly tractable in humans, nonhuman primates and rodents. In most experiments, however, goal-directed behaviors are measured in a laboratory setting, which is vastly different from the context in which these behaviors naturally occur. This study adapted a reward assessment paradigm, previously conducted with rhesus monkeys (Macaca mulatta) in the controlled environment of a Wisconsin General Testing Apparatus (WGTA) [Machado CJ, Bachevalier J (2007) The effects of selective amygdala, orbital frontal cortex or hippocampal formation lesions on reward assessment in nonhuman primates. Eur J Neurosci 25:2885–2904], to a more naturalistic context. We used this new paradigm to examine the effects of bilateral amygdaloid, hippocampal or orbital frontal cortex lesions on established food and nonfood preferences. Behavioral modification following reinforcer devaluation was also measured. Consistent with our previous study, none of the lesions produced changes in preference for palatable foods relative to pre-surgery, but animals with amygdala lesions displayed heightened preference for unpalatable foods that control or other operated animals typically avoided. In contrast to several previous WGTA-based experiments, nonfood preference was not affected by any of the lesions. Finally, animals with orbital frontal cortex lesions continued to select preferred foods after satiation, but those with amygdala, hippocampal or sham lesions altered their foraging behavior appropriately and selected less of the sated food. These findings parallel food devaluation results obtained with these same animals when tested in the WGTA. Overall, this study stresses the importance of testing context when measuring decision-making abilities in nonhuman primates with selective brain lesions.

Current advances and challenges in HIV-1 vaccines

Recent advances in science, which have aided HIV-1 vaccine development, include an improved understanding of HIV-1 envelope structure and function, expansion of the pipeline with innovative vaccine strategies, promising multi-gene and multi-clade vaccines that elicit cellular immunity, conduct of clinical trials in a global network, and development of validated techniques that enable simultaneous measurement of multiple T cell vaccine-induced immune responses in humans. A common feature of several preventive vaccine strategies now in early clinical trials is their ability in nonhuman primates to attenuate clinical disease rather than completely prevent HIV-1 infection. One vaccine concept has been tested in large-scale clinical trials, two are currently in efficacy trials, and one more is poised to enter efficacy trial in the next few years. Simultaneously, expanded efforts continue to identify new designs that induce mucosal immunity as well as broadly neutralizing antibodies.

New Type of Puzzle-Task Finger Maze Learning in Macaca fascicularis

In order to easily estimate the global cognitive ability of nonhuman primates, we developed a 4-step noncorrection-method-type finger maze (4FM) based on the standard puzzle feeder. We tested 7 experimentally naive long-tailed macaques (Macaca fascicularis) to assess the validity of the apparatus and the testing procedure. The most notable difference between the 4FM and the standard puzzle feeder is the presence of an error box. There is a hole at both ends of each step. One hole of each step is connected to the lower step or feeding box. The other hole of each step is connected to an error box. The monkey had to move the reward into the feeding box without dropping it into the error box and to retrieve the reward from the feeding box. Task difficulties could be controlled by deciding on which step to place the food reward at the beginning of the trial. All the monkeys could complete the tasks without food/water deprivation and pretraining. The results suggest that the 4FM is a suitable device to assess the cognitive ability of the monkeys simply, easily, and objectively.

Théories des primates sur l'esprit des primates

Primate theories of primate minds : conceptual and methodological issues Casual observation of spontaneous behaviours in non-human primates (especially apes) reveals complex social behaviours that appear to be symptomatic of some Theory-of-mind abilities. However, when experimentally tested, their performance fails to convince experts of their having any real ability to understand mental states. In this paper I suggest reasons for this paradox : First, there might be some methodological inadequacies in the experimental procedures developed to assess tom functions with non-verbal procedures. Secondly, there is a conceptual confusion about what is meant by having a theory-of-mind in non-human primates and therefore what should count as evidence of mentalising abilities in non-human primates. I consider some possible avenues for future studies of non-human mentalism that are capable of overcoming these problems. I present some recent studies that avoid the pitfalls of extensive preliminary training and favour the spontaneous performance of apes. Secondly, I discuss the notion of having an implicit theory of mind as the proper level to conceptualise apes' mentalism and suggest some implications of these comparative studies for our understanding of human theories of mind.

Primate vocal communication as “a window of the mind”

Most studies about mental abilities in nonhuman primates have been held in laboratory conditions. Considering the highy developed social organization of the primate species, however, it is necessary to study about their mental abilities in free-ranging conditions. Numerous studies have been made on natural vocal communication of nonhuman primates. Results of the studies tell mental abilities of nonhuman primates as well as functional significance of vocalizations in their lfe. This paper reviews some studies about nonhuman primate vocal communication and shows examples of mental abilities emerged in these studies, which is recognition of other individuals, perception of quantity, understanding of causal reasoning, categorization, and ability of deception.

Social processes and mental abilities in non-human primates

Social processes and mental abilities in non-human primates

La coopération chez les primates

Summary : Cooperation among non-human primates. The behaviour of cooperative individuals appears to involve cognitive abilities specific to human beings. However, biologists have proposed mathematical models to investigate the dynamics of cooperation in an evolutionary framework ; cooperative behaviour is assumed to be transmitted genetically from one generation to another. These mathematical models calculate the costs and benefits of cooperative behaviour and predict the evolution of different behavioural strategies in animal populations. In this neo-darwinian perspective, the question of the existence of intentional cooperation in animals is not approached. From a cognitive-psychological perspective, the problem is to determine the criteria that allow us to define cooperation, to decide if cooperative behaviour exists in animais, and possibly, to explain how this behaviour is acquired. We propose a « cognitive » definition of cooperation and discuss the nature of this ability in non-human primates. Key words : cooperation, intentionality, communication, primates.

The anthropomorphic and the sceptical

From this list it is clear that at least one of the salient characteristics of the scientific study of primate communication is an interest in comparing the communicational abilities of nonhuman primates to the communicational abilities of Homo sapiens. In other words, primate communication specialists want to determine the extent to which what monkeys and apes do is like what we do and the extent to which monkeys and apes can be taught

The development of self-recognition: a review.

The development of self-recognition has been studied mainly by examining infants' responses to their reflections in mirrors. The definitive test is whether or not the infant is capable of using the reflection to notice and respond to a mark on the face or head by touching the mark. The mark should be inconspicuous to the infant not looking in a mirror. In general, studies agree that this response appears in some infants around 15 months of age and is shown by a majority of infants by 24 months of age. There is less agreement over the existence of a "withdrawal" component in the second year, or the presence of a "social" phase analogous to the reaction of many animals confronted with a mirror. Infants as young as 3 months are differentially responsive to a self-reflection and a live peer. Various "self-conscious" reactions and self-labelling may also indicate self-recognition in the second year, but their validity is not well established. Studies using videotapes of the self and others show that contingency of movement is a salient cue which is learned early, and that attempts to engage in contingent play and to imitate representations of oneself are useful measures of early self-recognition. The validity of the response of turning to look at an object first seen in a mirror as a sign of self-recognition is questioned. The age at which self-recognition in still pictures first appears is less clear. Verbal comprehension of self-relevant labels appears earlier than active self-labelling. A few studies have addressed the question of cognitive correlates of self-recognition, but a variety of behaviors that imply self-awareness and the corresponding ability to impute mental states to others remains to be studied in relation to self-recognition. Continued research into self-recognition and associated abilities in nonhuman primates enhances the overall understanding of the development of self-awareness.

FM detection by monkeys

The information‐bearing role of frequency modulation (FM) in human speech and other biological acoustic signals is well documented. Further, the sensory acuity for FM in man has been established [I. Nabelek and I. J. Hirsh, J. Acoust. Soc. Am. 45, 1510–1519 (1969); I. Pollack, J. Exp. Psych. 77, 535–541 (1968)], yet despite its confirmed role in nonhuman primate communication [e.g., S. Green, Z. Tierpsychol. 38, 304–314 (1975)] no information is available on the ability of nonhuman primates to resolve FM or other such complex “biologically relevant” signals. The experiment reported here sought to determine thresholds for FM in monkeys in and near the frequency range of their calls in an effort to better understand their perception of FM and its potential relation to their communication system. Subjects were three macaque monkeys trained by positive reinforcement behavioral procedures to discriminate FM stimuli from pure tones. The parameters of the computer‐synthesized FM linear upsweeps matched critical ...