Systematic mapping of developmental milestones in wild chimpanzees

Postnatal development is protracted relative to lifespan in many primates, including modern humans (Homo sapiens), facilitating the acquisition of key motor, communication and social skills that can maximize fitness later in life. Nevertheless, it remains unclear what evolutionary drivers led to extended immature periods. While the developmental milestone literature is well established in humans, insight we can gain from one‐species models is limited. By comparing the timing of relatable developmental milestones in a closely related species, the chimpanzee (Pan troglodytes), we can gain further understanding of the evolution of such an extended developmental phase. To date, few studies have specifically attempted to estimate developmental milestones in a manner comparable to the human literature, and existing studies lack sufficient sample sizes to estimate which milestones are more plastic with higher inter‐individual variation in the timing of their emergence. Here, we describe the emergence of gross motor, fine motor, social interaction and communication traits from a longitudinal sample of 19 wild chimpanzee infants (8 females and 11 males), Taï National Park, Côte d’Ivoire. Gross motor traits emerged at a mean of 4 months, communication traits at 12 months, social interaction traits at 14 months and fine motor traits at 15 months, with later emerging milestones demonstrating greater inter‐individual variation in the timing of the emergence. This pattern of milestone emergence is broadly comparable to observations in humans, suggesting selection for a prolonged infantile phase and that sustained skills development has a deep evolutionary history, with implications for theories on primate brain development.     

The development of a greeting signal in wild chimpanzees

Adult chimpanzees produce a unique vocal signal, the pant-grunt, when encountering higher-ranking group members. The behaviour is typically directed to a specific receiver and has thus been interpreted as a 'greeting' signal. The alpha male obtains a large share of these calls, followed by the other adult males of the group. In this study, we describe the development of pant-grunting behaviour from the first grunt-like calls of newborn babies to the fully developed pant-grunts in adults. Although babies produce grunts from very early on, they are not directed to others until about 2 months of age. Subsequently, socially directed grunting steadily increases in frequency to peak around 7 months of age, but then decreases again to reach a nadir in older infants and juveniles, while the specificity in use increases. During adolescence, grunt production increases again with grunts given most frequently to socially relevant individuals. As young chimpanzees are closely affiliated to their mothers for the first decade of their lives, we also compared the grunting patterns of mothers and their offspring, which revealed some influences in pant-grunt production. In conclusion, the acquisition of pant-grunting behaviour in chimpanzees is a long-lasting process with distinct developmental phases in which social influences by the mother and other group members are likely to play a role.     

Lessons learned: challenges in applying current constraints on research on chimpanzees to other animals

The Institute of Medicine (IOM) Committee on the Necessity of the Use of Chimpanzees in Biomedical and Behavioral Research made a series of recommendations that, as of an announcement on June 26, 2013, the National Institutes of Health (NIH) is turning into implemented guidelines. Many advocates, including some researchers and scholars, have suggested that the Committee’s recommendations could be applied successfully to other animal species. This article examines, from my perspective as the IOM Committee’s chair, some of the most important features of the Committee’s work, addresses whether chimpanzees represent a special or unique case for the purpose of research policy, and suggests an approach for evaluating the applicability of the Committee’s recommendations for other animal species used in research. I first present my perspective on the features of the Committee’s work that influenced its approach and conclusions. I then argue that despite the fact that chimpanzees represent a somewhat unique case for restricted research use, their case still offers important lessons for policy regarding the use of other species. Finally, I offer some observations regarding the recommendations and implications of the report from the NIH Working Group charged with crafting guidelines for implementing the IOM Committee’s recommendations.     

The ontogeny of intentional communication in chimpanzees in the wild

The onset of intentional communication in children's first year of life represents a major milestone in human cognitive development. Similarly, it is well established that our closest living relatives, the great apes, communicate with signals characterized by at least first‐order intentionality. Despite the well‐documented influence of developmental experiences on socio‐cognitive abilities in apes, the developmental trajectory of intentional signal use as well as effects of social exposure remain poorly understood under naturalistic conditions. Here, we addressed these issues by studying the ontogeny of intentional communication in chimpanzee infants of two subspecies (Pan troglodytes schweinfurthii/verus) and communities living in their natural environments. Overall, we found that gestures and bimodal signal combinations were most commonly accompanied by markers of intentional communication: audience checking, persistence to the goal, and sensitivity to recipient’s attentional state. Within individuals, the proportion of communicative behaviours associated with goal persistence and sensitivity to attention increased with age. Cross‐sectional comparisons between infants revealed an age effect on the use of audience checking. Context, interaction partner and site affiliation affected the production of specific markers irrespective of infants' age. The present study provided hitherto undocumented evidence for the development of three important markers of intentional communication in great apes. Moreover, our results suggest that social exposure impacts early intentional signal use.     

The repertoire and intentionality of gestural communication in wild chimpanzees

A growing body of evidence suggests that human language may have emerged primarily in the gestural rather than vocal domain, and that studying gestural communication in great apes is crucial to understanding language evolution. Although manual and bodily gestures are considered distinct at a neural level, there has been very limited consideration of potential differences at a behavioural level. In this study, we conducted naturalistic observations of adult wild East African chimpanzees (Pan troglodytes schweinfurthii) in order to establish a repertoire of gestures, and examine intentionality of gesture production, use and comprehension, comparing across manual and bodily gestures. At the population level, 120 distinct gesture types were identified, consisting of 65 manual gestures and 55 bodily gestures. Both bodily and manual gestures were used intentionally and effectively to attain specific goals, by signallers who were sensitive to recipient attention. However, manual gestures differed from bodily gestures in terms of communicative persistence, indicating a qualitatively different form of behavioural flexibility in achieving goals. Both repertoire size and frequency of manual gesturing were more affiliative than bodily gestures, while bodily gestures were more antagonistic. These results indicate that manual gestures may have played a significant role in the emergence of increased flexibility in great ape communication and social bonding.     

Communicative intentions in wild chimpanzees: persistence and elaboration in gestural signalling

We examine evidence for communicative intent during conspecific interactions in wild chimpanzees (Budongo Forest, Uganda), focusing on persistence in gestural communication. Previous research indicates that great apes have large gestural repertoires and produce gestural communication in a flexible and intentional manner, including the production of gesture sequences. Although there is a lack of consensus on the form and function of sequences, there is some evidence that sequences are produced when signallers fail to receive any response from a recipient. Here, we provide first systematic evidence for communicative persistence in wild chimpanzees. Rather than examining only the presence or absence of a response, we used the most commonly observed response to assign meanings to gestures and examined sequence production in relation to response congruency. Chimpanzees ceased communication if successful, but persevered when unsuccessful. Chimpanzees repeated gestures when a response partially matched their goal but substituted the original gesture when a response was incongruent. Persistence was also mediated by recipient intent to respond, with more sequences produced within competitive than affiliative contexts. Gestures within sequences were homogenous in semantic meaning and signallers continued until the response matched the assigned meaning of the initial gesture. Gestural sequence production was not primarily affective; gesture intensity (in terms of modality) did not increase within sequences. Chimpanzee gestural sequences emerged to achieve specific outcomes; given variability in recipient behaviour following initial gestures, signallers were flexible in their persistence towards these goals.     

A machine learning approach to infant distress calls and maternal behaviour of wild chimpanzees

Animal Cognition - Distress calls are an acoustically variable group of vocalizations ubiquitous in mammals and other animals. Their presumed function is to recruit help, but there has been much...     

Locus of habituation in the human newborn

There is some controversy concerning the youngest age at which an infant will habituate to a visual stimulus or will prefer a novel to a familiar pattern. One suggestion has been that apparently successful reports of habituation and dishabituation in the newborn baby are attributable to retinal adaptation. This interpretation was tested in two experiments. In both experiments monocular conditions of viewing were used: newborns were habituated with one eye as the 'seeing' eye, and posthabituation novelty preferences investigated with the other eye. Significant preferences were found both for a novel colour (experiment 1) and for a novel shape (experiment 2), which implies that a retinal-adaptation model can be ruled out. It is suggested that the habituation effects and the subsequent novelty preferences found in the experiments are most reasonably interpreted as a function of memory formation, and evidence is presented for the storage of visual experience from birth. The results also demonstrate some form of binocular interaction in the newborn.     

Socially induced renal pathology of captive wild rats (Rattus villosissimus)

Long-haired rats, Rattus villosissimus, were studied in large cages. Groups of adult rats (each of 3 males, or 1 male and 2 females) were observed during intermittent encounters with a male intruder for up to 9 days. Two further groups, each of 8 males and 8 females, were maintained for 70 days without introduction of intruders. Controls were kept in small cages in which intolerant behavior was rare. Behavior during attack resembled that of male R. norvegicus, but social relationships were less stable. Only observations on males are described in detail. Some rats collapsed under attack, though unwounded, and died when not removed. Collapse occurred sometimes after a few hours, but sometimes after many days of exposure. Exposure to attack was accompanied by a decline in body weight and by some adrenal hypertrophy. Two kinds of renal pathology are described: focal glomerular hypercellularity (FGH), probably due to glomerulonephritis, and dilated distal convoluted tubules. Neither condition occurred in the controls. FGH occurred in 3 of 12 rats (25%) that remained apparently healthy during the 9 days of continuous exposure, in 21 of 23 intruders (91%) that were exposed to intermittent attack over 9 days or less without becoming debilitated, and in 8 of 11 such rats (73%) that collapsed. All rats examined from 70-day colonies had FGH, whether collapsed or not. Dilated tubules occurred in 6 of 32 intruders (19%) exposed to intermittent attack, and in 2 of 6 animals that collapsed during 70 days of exposure. Renal pathology, especially glomerulonephritis, was therefore a correlate of social intolerance; but there was no evidence that it was a significant cause of death.     

Socially learned preferences for differentially rewarded tokens in the brown capuchin monkey (Cebus apella)

Social learning is assumed to underlie traditions, yet evidence indicating social learning in capuchin monkeys (Cebus apella), which exhibit traditions, is sparse. The authors tested capuchins for their ability to learn the value of novel tokens using a previously familiar token-exchange economy. Capuchins change their preferences in favor of a token worth a high-value food reward after watching a conspecific model exchange 2 differentially rewarded tokens, yet they fail to develop a similar preference after watching tokens paired with foods in the absence of a conspecific model. They also fail to learn that the value of familiar tokens has changed. Information about token value is available in all situations, but capuchins seem to pay more attention in a social situation involving novel tokens.     

Sex-dependent habituation to novelty in rats

Male and female rats were familiarized with one-half of an exploration box for 30 or 60 minutes. When later tested, females showed higher preferences for the other novel half than males. Females also showed higher levels of rearing and ambulation. No sex differences were evident for grooming, freezing or defecation. The results were interpreted as females having habituated to the forced-exposure novelty of the familiar half of the apparatus more rapidly than males when the familiarization period was relatively short. With a longer period, males would have had more time to reach a similar level of habituation to that attained by females familiarized for 30 minutes. Relationships between novelty preferences and both rearing and ambulation as indices of exploration were also discussed in the light of significant correlations for males only.     

Serial gesturing by wild chimpanzees: its nature and function for communication

Chimpanzees at Budongo, Uganda, regularly gesture in series, including ‘bouts’ of gesturing that include response waiting and ‘sequences’ of rapid-fire gesturing without pauses. We examined the distribution and correlates of 723 sequences and 504 bouts for clues to the function of multigesture series. Gesturing by older chimpanzees was more likely to be successful, but the success rate of any particular gesture did not vary with signaller age. Rather, older individuals were more likely to choose successful gestures, and these highly successful gestures were more often used singly. These patterns explain why bouts were recorded most in younger animals, whereas older chimpanzees relied more on single gestures: bouts are best interpreted as a consequence of persistence in the face of failure. When at least one gesture of a successful type occurred in a sequence, that sequence was more likely to be successful; overall, however, sequences were less successful than single gestures. We suggest that young chimpanzees use sequences as a ‘fail-safe’ strategy: because they have the innate potential to produce a large and redundant repertoire of gestures but lack knowledge of which of them would be most efficient. Using sequences increases the chance of giving one effective gesture and also allows users to learn the most effective types. As they do so, they need to use sequences less; sequences may remain important for subtle interpersonal adjustment, especially in play. This ‘Repertoire Tuning’ hypothesis explains a number of results previously reported from chimpanzee gesturing.     

Sex-dependent habituation to novelty in rats

Male and female rats were familiarized with one-half of an exploration box for 30 or 60 minutes. When later tested, females showed higher preferences for the other novel half than males. Females also showed higher levels of rearing and ambulation. No sex differences were evident for grooming, freezing or defecation. The results were interpreted as females having habituated to the forced-exposure novelty of the familiar half of the apparatus more rapidly than males when the familiarization period was relatively short. With a longer period, males would have had more time to reach a similar level of habituation to that attained by females familiarized for 30 minutes. Relationships between novelty preferences and both rearing and ambulation as indices of exploration were also discussed in the light of significant correlations for males only.     

Lateral differences in habituation of ipsilateral head-turning to repeated tactile stimulation in the human newborn

Lateral differences in habituation of ipsilateral head-turning to repeated tactile perioral stimulation following midline head restriction was studied in 44 full-term neonates. Left-sided stimulation had a significantly greater and faster decremental effect than right-sided stimulation. Even in the absence of tactile stimulation (Control Group), head-turning to the left decreased systematically whereas head-turning to the right did not. The transient efficacy of prior midline head restriction for the elimination of lateral differences in both spontaneous head movements and responsiveness to tactile input suggests that behavioral asymmetry is already well-established in the newborn.     

Slow development of vocal sequences through ontogeny in wild chimpanzees (Pan troglodytes verus)

The development of the unique, hierarchical, and endless combinatorial capacity in a human language requires neural maturation and learning through childhood. Compared with most non-human primates, where combinatorial capacity seems limited, chimpanzees present a complex vocal system comprising hundreds of vocal sequences. We investigated how such a complex vocal system develops and the processes involved. We recorded 10,929 vocal utterances of 98 wild chimpanzees aged 0–55 years, from Taï National Park, Ivory Coast. We developed customized Generalized non-Linear Models to estimate the ontogenetic trajectory of four structural components of vocal complexity: utterance length, diversity, probability of panting (requiring phonation across inhalation and exhalation), and probability of producing two adjacent panted units. We found chimpanzees need 10 years to reach adult levels of vocal complexity. In three variables, the steepest increase coincided with the age of first non-kin social interactions (2–5 years), and plateaued in sub-adults (8–10 years), as individuals integrate into adult social life. Producing two adjacent panted units may require more neuromuscular coordination of the articulators, as its emergence and steepest increase appear later in development. These results suggest prolonged maturational processes beyond those hitherto thought likely in species that do not learn their vocal repertoire. Our results suggest that multifaceted ontogenetic processes drive increases in vocal structural complexity in chimpanzees, particularly increases in social complexity and neuro-muscular maturation. As humans live in a complex social world, empirical support for the “social complexity hypothesis” may have relevance for theories of language evolution.

Research Highlights

• Chimpanzees need around 10 years to develop the vocal structural complexity present in the adult repertoire, way beyond the age of emergence of every single vocal unit.
• Multifaceted ontogenetic processes may drive increases in vocal structural complexity in chimpanzees, particularly increases in social complexity and neuro-muscular maturation.
• Non-linear increases in vocal complexity coincide with social developmental milestones.
• Vocal sequences requiring rapid articulatory change emerge later than other vocal sequences, suggesting neuro-muscular maturational processes continue through the juvenile years.

     

Overlooked evidence for semantic compositionality and signal reduction in wild chimpanzees (Pan troglodytes)

Animal Cognition - Recent discoveries of semantic compositionality in Japanese tits have enlivened the discussions on the presence of this phenomenon in wild animal communication. Data on semantic...     

Visual habituation in human infants: development and rearing circumstances

Summary Habituation is a type of learning that reflects changing responsiveness to repeated information. In two longitudinal studies, we examined individual differences, stability, and developmental change in the ontogeny of visual habituation in human infants across the middle of the first year of life. To study this phenomenon in breadth, we tested infants from two social classes within the same culture and infants from two different cultures. Infants demonstrated significant, but comparable, individual differences in habituation across socioeconomic and cultural variations in rearing circumstances; they showed significant, if moderate, stability in habituation; and they habituated significantly more quickly with age. These results are interpreted in terms of developing human beings' increasing efficiency in processing visual information near the beginning of extrauterine life.     

Cultural innovation and transmission of tool use in wild chimpanzees: evidence from field experiments

Chimpanzees (Pan troglodytes) are the most proficient and versatile users of tools in the wild. How such skills become integrated into the behavioural repertoire of wild chimpanzee communities is investigated here by drawing together evidence from three complementary approaches in a group of oil-palm nut- (Elaeis guineensis) cracking chimpanzees at Bossou, Guinea. First, extensive surveys of communities adjacent to Bossou have shown that population-specific details of tool use, such as the selection of species of nuts as targets for cracking, cannot be explained purely on the basis of ecological differences. Second, a 16-year longitudinal record tracing the development of nut-cracking in individual chimpanzees has highlighted the importance of a critical period for learning (3–5 years of age), while the similar learning contexts experienced by siblings have been found to result in near-perfect (13 out of 14 dyads) inter-sibling correspondence in laterality. Third, novel data from field experiments involving the introduction of unfamiliar species of nuts to the Bossou group illuminates key aspects of both cultural innovation and transmission. We show that responses of individuals toward the novel items differ markedly with age, with juveniles being the most likely to explore. Furthermore, subjects are highly specific in their selection of conspecifics as models for observation, attending to the nut-cracking activities of individuals in the same age group or older, but not younger than themselves. Together with the phenomenon of inter-community migration, these results demonstrate a mechanism for the emergence of culture in wild chimpanzees.     

Disposition to recognize goals in infant chimpanzees

Do nonhuman primates attribute goals to others? Traditional studies with chimpanzees provide equivocal evidence for “mind reading” in nonhuman primates. Here we adopt looking time, a methodology commonly used with human infants to test infant chimpanzees. In this experiment, four infant chimpanzees saw computer-generated stimuli that mimicked a goal-directed behavior. The baby chimps performed as well as human infants, namely, they were sensitive to the trajectories of the objects, thus suggesting that chimpanzees may be endowed with a disposition to understand goal-directed behaviors. The theoretical implications of these results are discussed.