Development In Chimpanzees Research Articles

Effects of infant age and sex, and maternal parity on the interaction of lactation with infant feeding development in chimpanzees.

The interaction between infant feeding and maternal lactational physiology influences female inter-birth intervals and mediates maternal reproductive trade-offs. We investigated variation in feeding development in 72 immature wild chimpanzees (Pan troglodytes schweinfurthii) at Ngogo, Kibale National Park, Uganda, and made inferences about maternal lactation over the course of infancy. We compared the percentage (%) of time that mothers nursed infants as a function of infant age and assessed how hourly rates and bout durations of nursing and foraging varied in association with differences in offspring age, sex, and maternal parity. Nursing % times, rates and durations were highest for infants ≤ 6 months old but did not change significantly from 6 months to 5 years old. Nursing continued at a decreasing rate for some 5- to 7-year-olds. Infants ≤ 6 months old foraged little. Foraging rates did not change after 1 year old, but foraging durations and the % time devoted to foraging increased with age. Independent foraging probably became a dietary requirement for infants at 1 year old, when their energy needs may have surpassed the available milk energy. Infants spent as much time foraging by the time they were 4 to 5 years old as adults did. No sex effect on infant nursing or foraging was apparent, but infants of primiparous females had higher foraging rates and spent more time foraging than the infants of multiparous females did. Although no data on milk composition were collected, these findings are consistent with a working hypothesis that like other hominoids, chimpanzee mothers maintained a fixed level of lactation effort over several years as infants increasingly supplemented their growing energy, micronutrient and hydration needs via independent foraging. Plateauing lactation may be a more widespread adaptation that allows hominoid infants time to attain the physiology and skills necessary for independent feeding, while also providing them with a steady dietary base on which they could rely consistently through infancy, and enabling mothers to maintain a fixed, predictable level of lactation effort.

Quantifying maxillary development in chimpanzees and humans: An analysis of prognathism and orthognathism at the morphological and microscopic scales

Facial orientation (projection and degree of prognathism) and form in hominins is highly variable, likely related to evolutionary modifications of the microscopic process of bone modeling (the simultaneous cellular activities of bone formation and resorption) during ontogeny. However, in anteriorly projected faces such as those of early hominins, little is known about the link between bone modeling and facial developmental patterns. Similarly, these aspects have been infrequently investigated in extant great apes. In this study, quantitative methods were applied to a cross-sectional ontogenetic sample of 33 chimpanzees (Pan troglodytes verus) and 59 modern humans (Homo sapiens) to compare the development of maxillary prognathism to orthognathism at both microscopic and macroscopic (or morphological) scales using surface histology and geometric morphometric techniques. Chimpanzees express on average lower amounts of bone resorption than humans on the maxillary periosteum throughout ontogeny; however, the premaxilla is consistently resorbed from early stages on. The presence of bone resorption in the chimpanzee premaxilla, such as that seen in some early hominins, suggests a more ape-like pattern of maxillary bone modeling in these specimens. However, this shows that similarities in bone modeling patterns can lead to variations in shape, suggesting that other aspects of facial growth (such as modifications of rates and timings of development, as well as sutural growth) also played a crucial role in facial evolution.

The development of communication in alarm contexts in wild chimpanzees

Animals have evolved a range of communicative behaviours in the presence of danger. Although the mechanisms and functions of some of these behaviours have been relatively well researched, comparatively little is known about their ontogeny, including how animals learn to inform social partners about impending danger. In adult chimpanzees, behaviours in response to dangers involve several channels, particularly alarm calls and simultaneous gaze alternations with nearby recipients. Gaze alternations may allow inexperienced individuals to learn from more experienced ones by assessing their reactions to unfamiliar objects or events, but they may also provide the basis for more advanced social referencing. Here, we were interested in the development of these two common behaviours, alarm calling and gaze alternations, in wild chimpanzees (Pan troglodytes schweinfurthii) confronted with a threat. Using a cross-sectional design, we investigated those in 8 infant and 8 juveniles by experimentally exposing them to an unfamiliar but potentially dangerous object, a large, remotely controlled, moving spider model. For alarm calling, we found a positive relation with age, starting at around 28 months, although alarm calls were not consistently emitted until after 80 months. For gaze alternations, we found no age effect, with some of the youngest infants already showing the behaviour. Although its function remains unclear in infant and juvenile chimpanzees, gaze alternations emerge early in chimpanzee development. Alarm calling may require more advanced developmental stages, such as greater perceptual abilities, categorical capacities or more sophisticated social cognition, i.e. an understanding that danger is a collective experience that requires communication.Significance statementAlarm calling and other anti-predatory behaviours have been the topic of much research but their ontogenies are still poorly described and understood. Recent studies on the behaviour of wild chimpanzees in threatening contexts have suggested sophisticated social cognitive abilities in adults. How do these behaviours develop in ontogeny? We addressed this question using a field experiment with 8 infants and 8 juveniles exposed to a novel and potentially threatening object in their natural habitat. We found that gaze alternations are present in some of the youngest individuals, potentially revealing early social awareness in chimpanzees. Age did not have an effect on the presence of gaze alternation. We also found that alarm calling was more common in older individuals, suggesting that call production and context of usage must be learnt. We discuss our results in light of developmental theories of social cognition and the role of social learning in the primate lineage.

Epiphyseal fusion and dental development in Pan paniscus with comparisons with Pan troglodytes.

Compared with frequent studies of skeletal development in chimpanzees, relatively little is known about bonobo skeletal development. This study seeks to explore the relationship between skeletal and dental development in both species of Pan. New data are presented for fusion sites not previously observed in bonobos. In a sample of 34 Pan paniscus and 168 Pan troglodytes subadults, state of fusion was recorded for 30 epiphyseal fusion sites using a three-stage system of unfused, midfusion, and complete fusion based on Wintheiser, Clauser, and Tappen. Stage of dental development for permanent mandibular dentition was assessed using the Demrijian, Goldstein, and Tanner method. These data allowed for comparisons of both species of Pan and the two subspecies of P. troglodytes. The sequence of fusion events was generally consistent between the two species, but some exceptions may exist for the knee and ankle. The number of fusion events that occurred after complete dental mineralization was similar in both species. No statistically significant differences were found in the fusion timing for the subspecies of P. troglodytes. Bolter and Zihlman suggested that fusion at the acetabulum occurs earlier in Pan paniscus, while fusion of epiphyses at the knee are delayed, compared with P. troglodytes. Our data do not indicate earlier fusion of the acetabulum, but fusion events at the knee may complete later relative to dental mineralization in Pan pansicus. Compared with Homo sapiens, both P. troglodytes and Pan paniscus demonstrate later completion of epiphyseal fusion relative to dental mineralization.

大型類人猿の母子の絆:チンパンジーとオランウータンにおける母子関係と認知発達

大型類人猿の母子の絆:チンパンジーとオランウータンにおける母子関係と認知発達

Analysis of correlations between measures of skeletal development and dental mineralization in Pan troglodytes.

This study seeks to assess the relationship between dental mineralization and skeletal development in chimpanzees (Pan troglodytes) and to evaluate the effect that differing numbers of ordinal and continuous variables have on correlation statistics, particularly in comparison with prior human studies. This study evaluated epiphyseal fusion, dental mineralization, and growth in length of long bones using 145 juvenile chimpanzee skeletons housed in osteological collections at the Powell-Cotton Museum, the Museum of Central Africa, and the Adolph Schultz Collection. Correlations between multiple epiphyseal fusion sites and dental maturity scores for crown and root mineralization were produced using Pearson's r, Spearman's ρ, and Kendall's τ. Correlation statistics were produced using different subgroups of epiphyseal fusion sites and long bone lengths, and both summary and individual tooth development scores. Methodological considerations were discussed as differences in sample, measurement scale, and statistical technique had an effect on the outcome of correlations obtained. These results suggest that sampling and methodological differences between studies may affect the interpretation and comparison of correlation results, and that correlation strength differences between extant species must be considered before applying such results to questions in human biology and palaeoanthropology. Even after consideration of such factors, the correlation coefficient values for chimpanzees obtained in this study were generally stronger than those previously published in human studies, and may reflect differences in skeletal and dental developmental patterns between species. Am J Phys Anthropol 158:279-287, 2015. © 2015 Wiley Periodicals, Inc.

Developmental patterns of chimpanzee cerebral tissues provide important clues for understanding the remarkable enlargement of the human brain

Developmental prolongation is thought to contribute to the remarkable brain enlargement observed in modern humans (Homo sapiens). However, the developmental trajectories of cerebral tissues have not been explored in chimpanzees (Pan troglodytes), even though they are our closest living relatives. To address this lack of information, the development of cerebral tissues was tracked in growing chimpanzees during infancy and the juvenile stage, using three-dimensional magnetic resonance imaging and compared with that of humans and rhesus macaques (Macaca mulatta). Overall, cerebral development in chimpanzees demonstrated less maturity and a more protracted course during prepuberty, as observed in humans but not in macaques. However, the rapid increase in cerebral total volume and proportional dynamic change in the cerebral tissue in humans during early infancy, when white matter volume increases dramatically, did not occur in chimpanzees. A dynamic reorganization of cerebral tissues of the brain during early infancy, driven mainly by enhancement of neuronal connectivity, is likely to have emerged in the human lineage after the split between humans and chimpanzees and to have promoted the increase in brain volume in humans. Our findings may lead to powerful insights into the ontogenetic mechanism underlying human brain enlargement.

First molar eruption, weaning, and life history in living wild chimpanzees

Understanding dental development in chimpanzees, our closest living relatives, is of fundamental importance for reconstructing the evolution of human development. Most early hominin species are believed to show rapid ape-like patterns of development, implying that a prolonged modern human childhood evolved quite recently. However, chimpanzee developmental standards are uncertain because they have never been based on living wild individuals. Furthermore, although it is well established that first molar tooth emergence (movement into the mouth) is correlated with the scheduling of growth and reproduction across primates broadly, its precise relation to solid food consumption, nursing behavior, or maternal life history is unknown. To address these concerns we conducted a photographic study of subadult chimpanzees (Pan troglodytes schweinfurthii) in Kanyawara, Kibale National Park, Uganda. Five healthy infants emerged their lower first molars (M1s) by or before 3.3 y of age, nearly identical to captive chimpanzee mean ages (∼3.2 y, n = 53). First molar emergence in these chimpanzees does not directly or consistently predict the introduction of solid foods, resumption of maternal estrous cycling, cessation of nursing, or maternal interbirth intervals. Kanyawara chimpanzees showed adult patterns of solid food consumption by the time M1 reached functional occlusion, spent a greater amount of time on the nipple while M1 was erupting than in the preceding year, and continued to suckle during the following year. Estimates of M1 emergence age in australopiths are remarkably similar to the Kanyawara chimpanzees, and recent reconstructions of their life histories should be reconsidered in light of these findings.

Fetal brain development in chimpanzees versus humans

Summary It is argued that the extraordinary brain enlargement observed in humans is due to not only the human-specific pattern of postnatal brain development, but also to that of prenatal brain development [1,2]. However, the prenatal trajectory of brain development has not been explored in chimpanzees ( Pan troglodytes ), even though they are our closest living relatives. To address this lack of information, we tracked fetal development of the chimpanzee brain from approximately 14 to 34 weeks of gestation (just before birth) in utero using three-dimensional ultrasound imaging. The results were compared with those obtained for the human brain during approximately the same period. We found that the brain volume of chimpanzee fetuses was only half that of human fetuses at 16 weeks of gestation. Moreover, although the growth velocity of brain volume increased until approximately 22 weeks of gestation in both chimpanzees and humans, chimpanzee fetuses did not show the same accelerated increase in brain volume as human fetuses after that time. This suggests that maintenance of fast development of the human brain during intrauterine life has contributed to the remarkable brain enlargement observed in humans.

Skeletal development inPan paniscuswith comparisons toPan troglodytes

Fusion of skeletal elements provides markers for timing of growth and is one component of a chimpanzee's physical development. Epiphyseal closure defines bone growth and signals a mature skeleton. Most of what we know about timing of development in chimpanzees derives from dental studies on Pan troglodytes. Much less is known about the sister species, Pan paniscus, with few in captivity and a wild range restricted to central Africa. Here, we report on the timing of skeletal fusion for female captive P. paniscus (n = 5) whose known ages range from 0.83 to age 11.68 years. Observations on the skeletons were made after the individuals were dissected and bones cleaned. Comparisons with 10 female captive P. troglodytes confirm a generally uniform pattern in the sequence of skeletal fusion in the two captive species. We also compared the P. paniscus to a sample of three unknown-aged female wild P. paniscus, and 10 female wild P. troglodytes of known age from the Taï National Park, Côte d'Ivoire. The sequence of teeth emergence to bone fusion is generally consistent between the two species, with slight variations in late juvenile and subadult stages. The direct-age comparisons show that skeletal growth in captive P. paniscus is accelerated compared with both captive and wild P. troglodytes populations. The skeletal data combined with dental stages have implications for estimating the life stage of immature skeletal materials of wild P. paniscus and for more broadly comparing the skeletal growth rates among captive and wild chimpanzees (Pan), Homo sapiens, and fossil hominins.

Differential Prefrontal White Matter Development in Chimpanzees and Humans

Differential Prefrontal White Matter Development in Chimpanzees and Humans

Differential Prefrontal White Matter Development in Chimpanzees and Humans

A comparison of developmental patterns of white matter (WM) within the prefrontal region between humans and nonhuman primates is key to understanding human brain evolution. WM mediates complex cognitive processes and has reciprocal connections with posterior processing regions [1, 2]. Although the developmental pattern of prefrontal WM in macaques differs markedly from that in humans [3], this has not been explored in our closest evolutionary relative, the chimpanzee. The present longitudinal study of magnetic resonance imaging scans demonstrated that the prefrontal WM volume in chimpanzees was immature and had not reached the adult value during prepuberty, as observed in humans but not in macaques. However, the rate of prefrontal WM volume increase during infancy was slower in chimpanzees than in humans. These results suggest that a less mature and more protracted elaboration of neuronal connections in the prefrontal portion of the developing brain existed in the last common ancestor of chimpanzees and humans, and that this served to enhance the impact of postnatal experiences on neuronal connectivity. Furthermore, the rapid development of the human prefrontal WM during infancy may help the development of complex social interactions, as well as the acquisition of experience-dependent knowledge and skills to shape neuronal connectivity.

Brief communication: Dental development timing in captivePan paniscuswith comparisons toPan troglodytes

Dental eruption provides markers of growth and is one component of a chimpanzee's physical development. Dental markers help characterize transitions between life stages, e.g., infant to juvenile. Most of what we know about the timing of development in chimpanzees derives from Pan troglodytes. Much less is known about the sister species, Pan paniscus, with few in captivity and a restricted wild range in central Africa. Here we report on the dental eruption timing for female captive P. paniscus (n = 5) from the Milwaukee and San Diego Zoos whose ages are known and range from birth to age 8.54 years. Some observations were recorded in zoo records on the gingiva during life; others were made at death on the gingiva and on the skeleton. At birth, P. paniscus infants have no teeth emerged. By 0.83 years, all but the deciduous second molars (dm(2) ) (when both upper and lower dentitions are referenced collectively, no super or subscript notation is used) and canines (dc) are emerged. For permanent teeth, results show a sequence polymorphism for an early P4 eruption, not previously described for P. paniscus. Comparisons between P. paniscus and P. troglodytes document absolute timing differences of emergence in upper second incisors (I(2) ), and upper and lower canines (C) and third molars (M3). The genus Pan encompasses variability in growth not previously recognized. These preliminary data suggest that physical growth in captive P. paniscus may be accelerated, a general pattern found in captive P. troglodytes.

Cognitive development in chimpanzees: A trade-off between memory and abstraction?

Cognitive development in chimpanzees: A trade-off between memory and abstraction?

Cognitive development in chimpanzees and humans assessed by object manipulation

Cognitive development in chimpanzees and humans assessed by object manipulation

Book review: Cognitive Development in Chimpanzees

Book review: Cognitive Development in Chimpanzees

Skeletal and dental growth and development in chimpanzees of the Taï National Park, Côte D'Ivoire

AbstractAn extraordinary collection of 22 immature skeletons from Taï National Park, Côte d'Ivoire, has provided a rare opportunity to establish the timing of dental eruption and its correlation with skeletal fusion and morphometrics in wild chimpanzees of known chronological ages. Comparison of the immature Taï chimpanzeesPan troglodytes veruswith adults from the same population show that sex differences in skeletal maturation apparently appear during the Juvenile II stage, about age 8. A few skeletons from other chimpanzee field sites conform to the dental and skeletal growth in Taï chimpanzees. The tempo of wild chimpanzee growth contrasts sharply with the rate demonstrated for captive individuals. Captive chimpanzees may mature as much as 3 years earlier. The ability to link physical development with field observations of immature chimpanzees increases our understanding of their life‐history stages. These data provide an improved dataset for comparing the rates of growth among chimpanzees,Homo sapiensand fossil hominids.

T. Matsuzawa, M. Tomonaga, M. Tanaka (eds): Cognitive Development in Chimpanzees

T. Matsuzawa, M. Tomonaga, M. Tanaka (eds): Cognitive Development in Chimpanzees

Tetsuro Matsuzawa, Masaki Tomonaga, Masayuki Tanaka (eds): Cognitive development in Chimpanzees

Tetsuro Matsuzawa, Masaki Tomonaga, Masayuki Tanaka (eds): Cognitive development in Chimpanzees

A Faithful Record of Stressful Life Events Recorded in the Dental Developmental Record of a Juvenile Gorilla

The pattern and rate of dental development are critical components of the life history of primates. Much recent research has focused on dental development in chimpanzees and other hominoids, but comparatively little is known about dental development in Gorilla. To date, dental chronologies for Gorilla are based on a sample of 1 and information about variations in the time and timing of crown initiation and completion is lacking. We provide data on dental development in 1 captive, juvenile, female, western lowland Gorilla gorilla gorilla of known age, sex, life events, and date of death (carefully documented as part of zoo records) that experienced various physical insults during her first year of life. The perfect natural experiment allowed us to test the association of the timing of accentuated stress lines in teeth with significant physiological and psychological events during ontogeny of this juvenile gorilla. We analyzed histological sections from 14 permanent teeth (maxillary and mandibular I1-M2) and assessed crown initiation (CI) and crown formation times (CFT) using short- and long-period incremental lines in both enamel and dentine; they are advanced for all teeth compared to previously published chronology. The data suggest a relatively accelerated pace of dental development in gorillas compared to chimpanzees and fit an emerging pattern of an accelerated life history schedule in gorillas. Data on the timing of major accentuated lines in the developing dentition are tightly associated with exact dates of surgical procedures and follow-up hospital visits as recorded on zoo medical records. Our data highlight the importance of captive individuals with well-documented medical records for studying life history.