Factors determining tool-using ability in two captive chimpanzee (Pan troglodytes) colonies

The influence of several determinants of performance in a reaching tool task were studied: rearing history, object experience, and gender. Forty-five chimpanzees between the ages of 7 and 36 years served as subjects. They were chosen from two facilities, each group having different levels of tool experience. Each group was made up of individuals from three rearing conditions: wild born, captive mother reared, and captive nursery reared. Results indicated that wild-born subjects were better at the task than were both groups of captive-born subjects, who performed similarly. Previous experience with reaching tools was not a significant factor in the determination of tool-using ability. Gender differences were not apparent for either group, and the range of ages of chimpanzees tested was not related to tool-using ability.     

Characteristics of reproductive biology and proximate factors regulating seasonal breeding in captive golden-headed lion tamarins (Leontopithecus chrysomelas)

Reproduction is highly demanding in terms of energy expenditure, and the costs and benefits associated with postponing or investing in a reproductive effort are crucial determinants of an individual's fitness. Understanding the reproductive potential of a species under varying ecological conditions offers important insights into the dynamics of its social system. This study provides the first detailed analysis of the reproductive potential of wild- and captive-born golden-headed lion tamarins (Leontopithecus chrysomelas) under captive conditions, based on studbook data compiled during 1984-2000. Litters produced by wild-born females breeding in captivity are similar in size to litters observed in the wild, but smaller than litters of captive-born females. The more stringent ecological conditions experienced by wild-born females during maturation may result in a lifelong effect on litter size. However, interbirth intervals are shorter for wild-born than captive-born females. The relatively smaller burden of infant care that results from having smaller litters may allow wild-born females to sustain the next pregnancy sooner. Reproduction in the Brazilian captive population is highly seasonal for both wild-born females and females born in captivity in Brazil. Changes in photoperiod over a year provide a proximate explanation for changes in the proportion of conceptions and births per month. Outside Brazil, breeding occurs year-round, and no clear birth peak is apparent. Information from field reports that could be used to relate this finding to ecological factors, such as resource availability, is unavailable.     

Correlates of sexual and maternal competence in captive gorillas

The captive gorilla population may not be self-sustaining, in part because the overall birth rate is low and because many potential founders have failed to reproduce. We used questionnaires to collect standardized biographies of every gorilla held in North America. These biographies were searched for factors associated with reproductive success or failure. Captive-born gorillas are reproducing at least as well as wild-borns, when reproductive success is expressed as number of infants per year of reproductive opportunity. Mother-reared females are reproductively more successful than hand-reared females, but there is no difference in the reproductive success of mother-reared and hand-reared males. Social access to conspecifics in the 1st year is associated with higher reproductive success, at least for females. Reproductively successful and unsuccessful gorillas of both sexes have had equal access to potential mates, but unsuccessful animals are less likely than successful ones to exhibit normal sexual behavior. We conclude that many cases of reproductive failure are due to deficits in sexual behavior, which in turn may result from lack of early social experience with conspecifics. Some reproductive failure involves medical problems; interventive diagnostic techniques continue to be useful, if only to identify healthy individuals that can be managed intensively. The probability that a female will be a competent mother is not affected by her being wild-born or captive-born, or mother-reared or hand-reared.     

Life-History Inference in the Early Hominins Australopithecus and Paranthropus

The life histories of early hominins are commonly characterized as being like those of great apes. However, the life histories of the extant great apes differ considerably from one another. Moreover, the extent to which their life histories correlate with the two aspects of morphology used to infer the life histories of fossil species, brain size and dental development, has remained subject to debate. Increased knowledge of great ape life histories and, more recently, dental development —in particular ages at first molar emergence— now make it clearer that the latter is strongly associated with important life-history attributes, whereas brain size, as reflected by cranial capacity, is less informative. Here we estimate ages at M1 emergence in several infant/juvenile individuals of Australopithecus and Paranthropus based on previous estimates of ages at death, determined through dental histology. These are uniformly earlier than would be predicted either by adult cranial capacity or by comparison to ages at M1 emergence in free-living extant great apes. This suggests that either, 1) the life histories of the early hominins were faster than those of all extant great apes; 2) there was selection for rapid initial dental development and presumably early weaning, but that early hominin life histories were otherwise more prolonged and consistent with adult cranial capacities; or 3) the ages at death have been systematically underestimated, resulting in underestimates of the ages at M1 emergence. We investigate the implications of each of these alternatives and, where possible, explore evidence that might support one over the others.     

Hepatitis viruses in non-human primates

BACKGROUND: Previous epidemiological studies of rural human populations in Gabon reveal a high prevalence of human hepatitis A, B, C and D viruses. In order to investigate the prevalence of the blood-born hepatitis viruses in apes and monkeys living in the same area, we performed an epidemiological survey of HBV, HCV and HDV in wild-born non-human primates. METHODS: We tested 441 wild-born non-human primates from Gabon and Congo and 132 imported monkeys for the presence of serological markers of HBV, HCV and HDV infections. RESULTS: None of Cercopithecidae monkeys were reactive against HBV/HDV and HCV. In contrast, 29.2% of wild-born great apes (154 chimpanzees and 14 gorillas) were positive for HBV serological markers. Nine chimpanzees were in the replicative phase of HBV infection. None of these HBV infected chimpanzees exhibited symptoms or significant changes in serum clinical chemistry related to HBV infection. CONCLUSIONS: The negativity to HCV-related viruses and the negativity of the Cercopithecidae species tested against HBV/HDV do not allow us to definitively rule out the presence of an animal counterpart of human hepatitis viruses in non-human primates.     

Ontogenetic variation in the mandibular ramus of great apes and humans

Considerable variation exists in mandibular ramus form among primates, particularly great apes and humans. Recent analyses of adult ramal morphology have suggested that features on the ramus, especially the coronoid process and sigmoid notch, can be treated as phylogenetic characters that can be used to reconstruct relationships among great ape and fossil hominin taxa. Others have contended that ramal morphology is more influenced by function than phylogeny. In addition, it remains unclear how ontogeny of the ramus contributes to adult variation in great apes and humans. Specifically, it is unclear whether differences among adults appear early and are maintained throughout ontogeny, or if these differences appear, or are enhanced, during later development. To address these questions, the present study examined a broad ontogenetic sample of great apes and humans using two‐dimensional geometric morphometric analysis. Variation within and among species was summarized using principal component and thin plate spline analyses, and Procrustes distances and discriminant function analyses were used to statistically compare species and age classes. Results suggest that morphological differences among species in ramal morphology appear early in ontogeny and persist into adulthood. Morphological differences among adults are particularly pronounced in the height and angulation of the coronoid process, the depth and anteroposterior length of the sigmoid notch, and the inclination of the ramus. In all taxa, the ascending ramus of the youngest specimens is more posteriorly inclined in relation to the occlusal plane, shifting to become more upright in adults. These results suggest that, although there are likely functional influences over the form of the coronoid process and ramus, the morphology of this region can be profitably used to differentiate among great apes, modern humans, and fossil hominid taxa. J. Morphol. 275:661–677, 2014. © 2013 Wiley Periodicals, Inc.     

Birth Origin Differentially Affects Depressive-Like Behaviours: Are Captive-Born Cynomolgus Monkeys More Vulnerable to Depression than Their Wild-Born Counterparts?

Background

Adverse early-life experience might lead to the expression of abnormal behaviours in animals and the predisposition to psychiatric disorder (e.g. major depressive disorder) in Humans. Common breeding processes employ weaning and housing conditions different from what happens in the wild.

Methods

The present study, therefore, investigated whether birth origin impacts the possible existence of spontaneous atypical/abnormal behaviours displayed by 40 captive-born and 40 wild-born socially-housed cynomolgus macaques in farming conditions using an unbiased ethological scan-sampling analysis followed by multifactorial correspondence and hierarchical clustering analyses.

Results

We identified 10 distinct profiles (groups A to J) that significantly differed on several behaviours, body postures, body orientations, distances between individuals and locations in the cage. Data suggest that 4 captive-born and 1 wild-born animals (groups G and J) present depressive-like symptoms, unnatural early life events thereby increasing the risk of developing pathological symptoms. General differences were also highlighted between the captive- and wild-born populations, implying the expression of differential coping mechanisms in response to the same captive environment.

Conclusions

Birth origin thus impacts the development of atypical ethologically-defined behavioural profiles, reminiscent of certain depressive-like symptoms. The use of unbiased behavioural observations might allow the identification of animal models of human mental/behavioural disorders and their most appropriate control groups.     

Comparison of cranial ontogenetic trajectories among great apes and humans

Molecular data suggest that humans are more closely related to chimpanzees than either is to the gorillas, yet one finds the closest similarity in craniofacial morphology to be among the great apes to the exclusion of humans. To clarify how and when these differences arise in ontogeny, we studied ontogenetic trajectories for Homo sapiens, Pan paniscus, Pan troglodytes, Gorilla gorilla and Pongo pygmaeus. A total of 96 traditional three-dimensional landmarks and semilandmarks on the face and cranial base were collected on 268 adult and sub-adult crania for a geometric morphometric analysis. The ontogenetic trajectories are compared by various techniques, including a new method, relative warps in size-shape space. We find that adult Homo sapiens specimens are clearly separated from the great apes in shape space and size-shape space. Around birth, Homo sapiens infants are already markedly different from the great apes, which overlap at this age but diverge among themselves postnatally. The results suggest that the small genetic differences between Homo and Pan affect early human ontogeny to induce the distinct adult human craniofacial morphology. Pure heterochrony does not sufficiently explain the human craniofacial morphology nor the differences among the African apes.     

Higher rate of evolution of X chromosome alpha-repeat DNA in human than in the great apes.

The rate of introduction of neutral mutations is lower in man than in other primates, including the chimpanzee. This species is generally regarded as our closest relative among the great apes. We present here an analysis of sequences of X chromosomal alphoid repetitive DNA from man and the great apes, which supports the closer relationship between man and chimpanzee and indicates a considerably increased rate of recombination in the human repeat DNA. These results indicate that the 'molecular clock' is running more quickly in man.     

Does Sympathy Motivate Prosocial Behaviour in Great Apes?

Prosocial behaviours such as helping, comforting, or sharing are central to human social life. Because they emerge early in ontogeny, it has been proposed that humans are prosocial by nature and that from early on empathy and sympathy motivate such behaviours. The emerging question is whether humans share these abilities to feel with and for someone with our closest relatives, the great apes. Although several studies demonstrated that great apes help others, little is known about their underlying motivations. This study addresses this issue and investigates whether four species of great apes (Pongo pygmaeus, Gorilla gorilla, Pan troglodytes, Pan paniscus) help a conspecific more after observing the conspecific being harmed (a human experimenter steals the conspecific’s food) compared to a condition where no harming occurred. Results showed that in regard to the occurrence of prosocial behaviours, only orangutans, but not the African great apes, help others when help is needed, contrasting prior findings on chimpanzees. However, with the exception of one population of orangutans that helped significantly more after a conspecific was harmed than when no harm occurred, prosocial behaviour in great apes was not motivated by concern for others.     

The cross-sectional geometry of the hand and foot bones of the hominoidea and its relationship to locomotor behavior

Cheiridia are valuable indicators of positional behavior, as they directly contact the substrate, but systematic comparison of the structural properties of both metacarpals and metatarsals has never been carried out. Differences in locomotor behavior among the great apes (knuckle-walking vs. quadrumanous climbing) can produce biomechanical differences that may be elucidated by the parallel study of cross-sectional characteristics of metacarpals and metatarsals. The aim of this work is to study the cross-sectional geometric properties of these bones and their correlation with locomotor behavior in large-bodied hominoids. The comparisons between bending moments of metacarpals and metatarsals of the same ray furnished interesting results. Metacarpals III and especially IV of the knuckle-walking African apes were relatively stronger than those of humans and orangutans, and metatarsal V of humans was relatively stronger than those of the great apes. Interestingly, the relative robusticity of the metacarpal IV of the quadrumanous orangutan was between that of the African apes and that of humans. The main conclusions of the study are: 1) cross-sectional dimensions of metacarpals and metatarsals are influenced by locomotor modes in great apes and humans; 2) interlimb comparisons of cross-sectional properties of metacarpals and metatarsals are good indicators of locomotor modes in great apes and humans; and 3) the results of this study are in accord with those of previous analyses of plantar pressure and morphofunctional traits of the same bones, and with behavioral studies. These results provide a data base from which it will be possible to compare the morphology of the fossils in order to gain insight into the locomotor repertoires of extinct taxa.     

Lineage-Specific Changes in Biomarkers in Great Apes and Humans

Although human biomedical and physiological information is readily available, such information for great apes is limited. We analyzed clinical chemical biomarkers in serum samples from 277 wild- and captive-born great apes and from 312 healthy human volunteers as well as from 20 rhesus macaques. For each individual, we determined a maximum of 33 markers of heart, liver, kidney, thyroid and pancreas function, hemoglobin and lipid metabolism and one marker of inflammation. We identified biomarkers that show differences between humans and the great apes in their average level or activity. Using the rhesus macaques as an outgroup, we identified human-specific differences in the levels of bilirubin, cholinesterase and lactate dehydrogenase, and bonobo-specific differences in the level of apolipoprotein A-I. For the remaining twenty-nine biomarkers there was no evidence for lineage-specific differences. In fact, we find that many biomarkers show differences between individuals of the same species in different environments. Of the four lineage-specific biomarkers, only bilirubin showed no differences between wild- and captive-born great apes. We show that the major factor explaining the human-specific difference in bilirubin levels may be genetic. There are human-specific changes in the sequence of the promoter and the protein-coding sequence of uridine diphosphoglucuronosyltransferase 1 (UGT1A1), the enzyme that transforms bilirubin and toxic plant compounds into water-soluble, excretable metabolites. Experimental evidence that UGT1A1 is down-regulated in the human liver suggests that changes in the promoter may be responsible for the human-specific increase in bilirubin. We speculate that since cooking reduces toxic plant compounds, consumption of cooked foods, which is specific to humans, may have resulted in relaxed constraint on UGT1A1 which has in turn led to higher serum levels of bilirubin in humans.     

Great Apes Do Not Learn Novel Tool Use Easily: Conservatism,Functional Fixedness,or Cultural Influence?

Animal culture has been of interest for decades but the concept remains controversial. Many researchers feel that animal behavior should not be granted the label “culture” because the latter includes more than “simple” behavioral variation. In recent years, the study of animal culture has been concerned mainly with social learning mechanisms, often claimed to be human specific, which led to the uniqueness of human culture. In addition, failure to innovate novel cultural behavior as often as humans is usually explained by psychological mechanisms presented as more parsimonious, such as conservatism or functional fixedness. However, it is unclear how cognitively complex these mechanisms are in the first place. Here, I analyze recent data obtained with wild chimpanzees (Pan troglodytes schweinfurthii) and wild-born orangutans (Pongo abelii) using the honey-trap experiment, in which individuals must devise a solution to reach inaccessible honey. I compare behavior of apes that developed a tool-based solution in the task with those that did not, and test whether conservatism and functional fixedness can explain individual variation in ape behavior. I find evidence of conservatism, with apes relying on their existing knowledge, and evidence of functional fixedness, with this knowledge potentially preventing them from innovating. However, the apes showed large intraspecific variability. I discuss the two mechanisms through a representational perspective to tackle their cognitive complexity. Understanding how conservatism and functional fixedness interact with ape cultural knowledge to limit innovation of novel tool use appears necessary to understand the full extent of ape cultures and how they compare to human cultures.     

Development of the visual preference of chimpanzees (<Emphasis Type="Italic">Pan troglodytes</Emphasis>) for photographs of primates: effect of social experience

In a study by Tanaka (2003) five captive chimpanzees preferred photographs of humans to those of chimpanzees. All the subjects were raised by humans and lived in captivity for many years. This suggests their preference might have developed through social experience. In this study examined this hypothesis by using three young chimpanzees raised by their mothers in a captive chimpanzee community. The young chimpanzees were tested four times before six years of age. I also tested eight adult chimpanzees that had been in captivity for more than 20 years. Each subject was presented with digitized color photographs of different species of primates on a touch-sensitive screen. The subjects received a food reward when they touched a photograph, irrespective of which photograph they touched. All the adult chimpanzees touched photographs of humans more frequently than those of any other species of primate. Two of the young chimpanzees showed no species preference before reaching 5 years of age, when they started to show preference for humans. The remaining young chimpanzee consistently preferred chimpanzees. These results suggest that development of visual preference of chimpanzees is affected by social experience during infancy.     

Use of buckets as tools by Western lowland gorillas

While all great apes have been documented to use tools, gorillas are arguably the least proficient tool users. In 2009, a Western lowland gorilla (Gorilla gorilla gorilla) at the Buffalo Zoo was observed using a bucket, which had been provided as part of normal enrichment, as a tool to collect water. We conducted a brief, ad libitum investigation to confirm the validity of the initial observation. We then carried out a systematic investigation of the behavior in 2010. We collected 72 hr of videotaped data and tested the null hypothesis that the gorillas did not differ in their prevalence of engaging in bucket-use behaviors. We documented that all four adult gorillas in the group used buckets as drinking tools; however, there was significant individual variation in frequency and type of use of buckets. Four of the eight behaviors showed significant variation among individuals. The silverback male and the youngest adult female contacted and held the bucket significantly more than the remaining two adult females. The young female carried and drank from the bucket significantly more than any other individual. Furthermore, she was observed to fill the bucket with water four of the six times during which this behavior was observed. These data provide evidence of the ability of gorillas to utilize tools, given the appropriate environmental conditions. We continue to explore the abilities of gorillas to recognize the functionality of buckets as tools.     

Sex differences in play among western lowland gorilla (Gorilla gorilla gorilla) infants: implications for adult behavior and social structure

Mammalian play is believed to improve motor skills as well as facilitate the development of social relationships. Given the marked sexual dimorphism in gorilla body size and the role assumed by the male in protecting the group from conspecifics and predators, the motor-training hypothesis of play predicts that male infants should exhibit higher frequencies of social play than female infants, and that males should prefer to play with other males. Given that adult female gorillas are strongly attracted to adult breeding males and form only weak social bonds with unrelated adult females, the social-relationship hypothesis of play predicts that female infants should prefer to play with males. These hypotheses were tested in a 22-month study of 12 gorilla infants, aged between 0-5 years, living in three zoological parks in Chicago and Atlanta. Consistent with the hypotheses, male infants played more than female infants did, and both male and female infants preferred to play with males rather than with females. These findings suggest that sex differences in play in the great apes and other primates can be predicted by the characteristics of adult behavior and social structure above and beyond the patterns of sex-biased dispersal or coalition formation with same-sex kin.     

Asian small-clawed otter (Aonyx cinerea) urolithiasis prevalence in North America

The prevalence of urolithiasis in the North American Asian small-clawed otter (Aonyx cinerea) population was determined through a retrospective survey. A questionnaire regarding diet and radiographic or necropsy evidence of urolithiasis was sent to the 16 North American institutions or individuals listed in the Asian Small-Clawed Otter North American Regional Studbook. Completed forms were returned by 75% of questionnaire recipients. Individual surveys or necropsy reports were received for 79.8% of the living or dead animals listed as comprising the North American population. Renal calculi were detected in 66.1%, and cystic calculi in 23.2%, of the captive adult population that had been radiographed or necropsied. All otters with cystic calculi also had renal calculi. Bilateral renal calculi occurred in 83.8% of affected otters. Both males (61.2%) and females (72%) were frequently affected. The prevalence of urolithiasis in wild-born otters was 76.7%, and in adult (≥1 year) captive-born otters it was 53.8%. The higher prevalence in wild-born otters may be a reflection of the older mean age at which they were first evaluated. In the overwhelming majority of otters with renal calculi, the calculi were multiple and diffusely distributed throughout the renal parenchyma. Renal and cystic calculi analyzed were primarily composed of calcium oxalate or urates. Glucosuria was infrequently reported. Necropsies of dependent neonates (≤ 2 months old) that died revealed cystic calculi in one animal. Renal disease was the cause of, or a contributing factor in, the deaths of all older animals whose necropsy reports were reviewed. The captive diet may be a contributing factor to urolith formation and progression.     

Dispersal Patterns of Orang-utans (<Emphasis Type="BoldItalic">Pongo</Emphasis> spp.) in a Bornean Peat-swamp Forest

Knowledge regarding dispersal patterns in great apes may help in understanding the evolution of dispersal patterns and social grouping in early hominoids, as well as in our own species. However, the social structure and dispersal system of orang-utans (Pongo spp.) remains little understood despite past research. We addressed this question by conducting genetic analyses on a wild orang-utan (Pongo pygmaeus wurmbii) population from the Sabangau peat-swamp in Borneo. We estimated pairwise relatedness among 16 adult individuals using 19 polymorphic microsatellite markers. Mean relatedness among females was significantly higher than in males, irrespective of the relatedness estimator used, following the pattern predicted for male dispersal. Our results support field observations that average dispersal distance for females is less than for males, suggesting that female orang-utans are philopatric, whereas males disperse. This contrasts with previous findings from other sites where anthropogenic influences were present. Based on qualitative mitochondrial DNA analyses, it appears that unflanged adult males show some degree of site fidelity compared to flanged males. Thus, male orang-utans may disperse permanently from their natal range once they are fully flanged. Male-biased dispersal and female philopatry in orang-utans differ from those of extant African apes and are more similar to many Old World monkey species. Hence we hypothesize that this system may represent the ancestral state of early hominoids.     

Fecundity in the captive howler monkey,Alouatta caraya

Seven female Black howler monkeys, Alouatta caraya, from both wild- and captive-born origins have reproduced at Riverbanks Zoological Park. Three of the five wild-born females arrived as juveniles and grew to maturity; the other two were already mature upon arrival and reproduced shortly therafter. Two females which were born within the park's collection have since reached maturity and also reproduced. The interval between the first and second young of wild-born howlers is longer than between subsequent birth intervals. Subsequent young are also more precocious than their preceding siblings. In at least one case, a socially inferior female did not reproduce until placed within a different troop situation which elevated her social status. Females born in captivity conceived when 42 and 35 months old, the former situation being linked to low social status. Young born to females housed under both seasonal and regulated conditions of photoperiod demonstrated no difference in breeding intervals and seasonality of birth does not appear to be a factor in howler monkey reproduction.     

Sex differences in compatibility of pair-housed adult longtailed macaques

This research was designed to evaluate the effects of same-sex pair housing on the psychological well-being of adult wild-born longtailed macaques (Macaca fascicularis). We studied behavioral compatibility and stress as measured by urinary cortisol excretion in 15 pairs of each sex. Before they were housed together, the pairs were categorized by noncontact pairedpreference testing as preferred, nonpreferred, or randomly assigned partners. Every aspect of data analysis indicated that the success of pairing was strongly related to gender. Whereas 100% of female pairs were compatible, only eight of the 15 male pairs were still together after two weeks, and only five (33%) showed a degree of compatibility resembling that of females. The psychological well-being of virtually all females seemed to be improved during the physical contact paired-housing conditions; they spent more than one-third of the day engaged in social grooming. Paired adult males had much lower interaction rates than adult females. On average, males were initially somewhat stressed by the introduction to a cagemate as indicated by increased urinary cortisol excretion. The noncontact preference testing procedure was no more predictive of pair success than random assignment. For males, the presence of fighting combined with the absence of grooming during the first 90 min opportunity for physical contact (“introduction”) was associated with pair incompatibility, but not to a statistically significant extent. For research protocols permitting social grouping of this species, the social contact requirement of the USDA Animal Welfare Rules usually can be met for adult females by pair housing. For males, pairing with other adult males often is unsuccessful; by our estimates, at least 20% of males cannot be pair-housed with other males. These sex differences in response to same-sex adults are consistent with the known socioecology of macaques. Further research is necessary to determine whether adult males have a lower need for social contact than females, or whether their needs are better met by other types of social contact. © 1994 Wiley-Liss, Inc.