Improved method for artificial insemination in the great apes

Artificial insemination in the great apes has not achieved its potential as a tool in maintenance of the endangered captive population. Three factors can influence the success rate of artificial insemination: sperm preparation, site of insemination, and timing of insemination. We have tried to optimize methods regarding these three steps. A modified method for insemination is described which has resulted in a 21% success rate (six term pregnancies from 29 inseminations) in the chimpanzee and which has successfully initiated a pregnancy in a gorilla.     

Physical Mapping of Human 7q and 14q Subtelomeric DNA Sequences in the Great Apes

Phylogenetic divergence of the members of the Pongidae familyhas been based on genetic evidence. The terminal repeat array(T₂AG₃) has lately been considered as an additional basis toanalyze genomes of highly related species. The recent isolationof subtelomeric DNA probes specific for human (HSA) chromosomes7q and 14q has prompted us to cross-hybridize them to the chromosomesof the chimpanzee (PTR), gorilla (GGO) and orangutan (PPY) tosearch for its equivalent locations in the great ape species.Both probes hybridized to the equivalent telomeric sites ofthe long (q) arms of all three great ape species. Hybridizationsignals to the 7q subtelomeric DNA sequence probe were observedat the telomeres of HSA 7q, PTR 6q, GGO 6q and PPY 10q, whilehybridization signals to the 14q subtelomeric DNA sequence probewere observed at the telomeres of HSA 14q, PTR 15q, GGO 18qand PPY 15q. No hybridization signals to the chromosome 7-specificalpha satellite DNA probe on the centromeric regions of theape chromosomes were observed. Our observations demonstratesequence homology of the subtelomeric repeat families D7S427and D14S308 in the ape chromosomes. An analogous number of subtelomericrepeat units exists in these chromosomes and has been preservedthrough the course of differentiation of the hominoid species.Our investigation also suggests a difference in the number ofalpha satellite DNA repeat units in the equivalent ape chromosomes,possibly derived from interchromosomal transfers and subsequentamplification of ancestral alpha satellite sequences.     

Ontogeny of mirror behavior in two species of great apes

Mirror image reactions of two infant apes, a female chimpanzee (Pan troglodytes) and a male orangutan (Pongo pygmaeus), born at the Zoo de Vincennes and the Jardin des Plantes of Paris, France, respectively, were studied and compared with those of children. Self-recognition was also tested following 46.5 hours of mirror exposure by application of red marks on parts of the body invisible to the animal without the aid of the mirror. Results indicated that the behavior of the two young apes followed a developmental trend similar to that of human babies. At the end of the study, the female chimpanzee (11 months of age) expressed social behavior, searched for the image behind the mirror, and showed interest in imaged movement. The orangutan (2 years and 5 months old) had begun to test movement synchronism and to display self-directed behaviors. The tests of self-recognition yielded negative results in both animals.     

Onset and early use of gestural communication in nonhuman great apes

The early gesturing of six bonobos, eight chimpanzees, three gorillas, and eight orangutans was systematically documented using focal animal sampling. Apes' were observed during their first 20 months of life in an effort to investigate: (i) the onset of gesturing; (ii) the order in which signals of different sensory modalities appear; (iii) the extent to which infants make use of these modalities in their early signaling; and (iv) the behavioral contexts where signals are employed. Orangutans differed in important gestural characteristics to African ape species. Most notably, they showed the latest gestural onset and were more likely to use their early signals in food-related interactions. Tactile and visual signals appeared similarly early across all four species. In African apes, however, visual signaling gained prominence over time while tactile signaling decreased. These findings suggest that motor ability, which encourages independence from caregivers, is an important antecedent, among others, in gestural onset and development, a finding which warrants further investigation.     

Regional localization of human M-BCR gene to chromosome 23 band q11 in the great apes

We hybridized a human M-BCR DNA probe to the chromosomes of chimpanzee (Pan troglodytes), gorilla (Gorilla gorilld) and orangutan (Pongo pygmaeus) by FISH-technique. The human M-BCR gene was localized to chromosome 23 band q11 (23q11), which is equivalent to the human chromosome 22 band q11 in all three species. The conservation of M-BCR gene in higher primates at the corresponding human chromosome locus provides phylogenetic clues concerning the evolution of genes.     

Comparative mapping of human alphoid satellite DNA repeat sequences in the great apes

Heterochromatic regions of chromosomes contain highly repetitive, tandemly arranged DNA sequences that undergo very rapid variation compared to unique DNA sequences that are predominantly conserved. In this study the chromosomal basis of speciation has been looked at in terms of repeat sequences. We have hybridized twenty-one chromosome-specific human alphoid satellite DNA probes to metaphase spreads of the chimpanzee (Pan troglodytes), gorilla (Gorilla gorilla), and orangutan (Pongo pygmaeus) to investigate the evolutionary relationship of heterochromatic regions among such hominoid species. The majority of the probes did not hybridize to their corresponding equivalent chromosome but presented hybridization signals on non-corresponding chromosomes. Such observations suggest that rapid changes may have occurred in the ancestral alphoid satellite DNA sequence, resulting in divergence among the great ape species. This revised version was published online in July 2006 with corrections to the Cover Date.     

Sexual dimorphism in canine shape among extant great apes

There have been numerous attempts to sex fossil specimens using the canine dentition. Whether focused on canine size or canine shape, most of these efforts share two deficiencies: lack of quantification of male-female differences in the adopted criteria and a failure to adequately explore among extant species the discriminatory power of these criteria. Here, canine shape indices relating to relative canine height, upper canine root/crown proportionality, and relative length of the lower canine mesial ridge were calculated for males and females of all species and subspecies of extant great apes and two species of gibbons. The accuracy of these indices for identifying the sex of the extant ape specimens was investigated through discriminant analysis and the use of bivariate plots of the two upper and two lower canine indices. The indices were found to be highly accurate in identifying the sex of great ape individuals, not only in single-species and subspecies samples but in mixed-species samples as well; assignment error rates were mostly between 0 and 4%. Accuracy was lowest in Pan (error rates as high as 15%) and highest in Pongo (one error). In most cases, error rates were lower in the upper canines. The effectiveness of these shape indices for sexing might be related to the degree of absolute canine size dimorphism; the indices did not effectively segregate males and females among minimally canine-dimorphic gibbons. The mixed-species results reveal that same-sex index values are remarkably concordant across great ape species, as are the patterns of spatial segregation of males and females in the bivariate plots. Results suggest that, while the indices can be used with some confidence to sex individual fossil specimens, their greatest utility will be for identifying the sex of groups of canines united by size and morphology. © 1995 Wiley-Liss, Inc.     

Brief communication: Testing the usefulness of the basilar suture as a means to determine age in great ape skeletons

A fused/closed basilar suture is usually treated as an indication of old age in great apes. A sample, drawn from a variety of sources, of known-aged captive great ape skeletons was analyzed to test the usefulness of using the basilar suture to categorize adult skeletons as either "adult" or "old adult". The state of closure of the basilar suture was examined in 30 chimpanzees, 19 gorillas, and 15 orangutans, all of known age. The results show that the basilar suture demonstrates a high level of uniformity in rate of closure and is closed at an early age in virtually all known-aged individuals. Thus, an old adult category most likely includes individuals who are, in fact, relatively young. This indicates that using the basilar suture as a means to classify individual skeletons as adult or old adult is very imprecise. The homogenous nature of basilar suture closure appears to prevent meaningful application of suture status for categorizing adult ape skeletons by age groups.     

A unique genomic sequence in the Wolf-Hirschhorn syndrome [WHS] region of humans is conserved in the great apes

The Wolf-Hirschhorn syndrome (WHS) is caused by a partial deletion in the short arm of chromosome 4 band 16.3 (4p16.3). A unique-sequence human DNA probe (39 kb) localized within this region has been used to search for sequence homology in the apes' equivalent chromosome 3 by FISH-technique. The WHS loci are conserved in higher primates at the expected position. Nevertheless, a control probe, which detects alphoid sequences of the pericentromeric region of humans, is diverged in chimpanzee, gorilla, and orangutan. The conservation of WHS loci and divergence of DNA alphoid sequences have further added to the controversy concerning human descent.     

Airsacculitis in fourteen juvenile southern Bornean orangutans (Pongo pygmaeus wurmbii)

BACKGROUND: Airsacculitis is a clinical condition which has been reported in a range of primates species, including orangutans. METHODS: This report describes the occurence and management of airsacculitis in fourteen juvenile Southern Bornean orangutans (Pongo pygmaeus wurmbii) that presented beween January 1st 1999 and January 31st 2001 at the Orangutan Care Center and Quarantine (OCC&Q), Kalimantan Tengah, Indonesia (S 2 degrees 43' 49.2"; E 111 degrees 38' 54.2"). Details of the signalment, clinical history, presenting clinical signs, clinicopathological findings and bacterial isolates in each case were reviewed. RESULTS: Cough, halitosis and nasal discharge were the most frequently observed clinical signs. A range of Gram-negative bacteria were isolated from infected air sacs, including Pseudomonas sp., Enterobacter sp. and Klebsiella pneumoniae. A simple drainage and lavage technique was used in cases where surgical intervention was indicated, in combination with local and systemic antibiotic therapy. CONCLUSIONS: The importance of early diagnosis, prompt management and antibiotic selection, based on bacterial culture and sensitivity profiles, is outlined.     

Brief communication: Comparative mapping of the human estrogen receptor (ESR) and the Kallmann (KAL) regions to the chromosomes of the great apes

Human and great ape chromosomes display significant concordance by molecular and cytogenetic techniques, which may reflect their common origin. Nevertheless, chromosomal banding techniques did not reflect the syntenic homology at the DNA level, which created controversy and debate. The recent availability of the unique sequence loci-specific human estrogen receptor (ESR) (bq25.1) region and Kallmann (KAL) (Xp22.3) DNA probes have prompted us to search the degree of DNA sequence synteny among chimpanzee, gorilla, and orangutan by the FISH technique. The conservation of the ESR and Kallmann regions at the corresponding equivalent loci of the great ape chromosomes (5q25 and Xp22, respectively) has provided insights into genome evolution and facilitated assignment of map locations for human unique DNA sequences. These findings are aimed toward developing an augmented framework to determine with greater certainty the pathway of human descent at the single gene level. Am J Phys Anthropol 103:561–563, 1997. © 1997 Wiley-Liss, Inc.     

Morphology and DNA quantitation of human and great ape spermatozoa

A comparative study of human and great ape spermatozoa was carried out with the purpose of looking at spermatozoal morphology and DNA content in man's closest living relatives. This study showed that man and the gorilla are unique among mammals in normally exhibiting a remarkable morphological pleiomorphism in the ejaculate. The modal cell types in the ejaculates of these two species were morphologically identical. The less frequent cell types, defined as morphologically abnormal spermatozoa, were also very similar, and occurred in similar proportions. Thus, it was impossible to distinguish between man and the gorilla by a simple examination of the ejaculate, although it is possible to distinguish between man and the chimpanzees, between the gorilla and the chimpanzees or between the orangutan and man. Both species of chimpanzees produced identical spermatozoa. DNA estimations showed that man and the gorilla produce a similarly low proportion of diploid spermatozoa. Morphological pleiomorphism in man was not positively correlated with a higher variation of DNA content than that observed in the chimpanzees and the organutan. In the gorilla, however, a significantly higher variability in DNA content was observed.     

North American orangutan species survival plan: Current status and progress in the 1980s

The SSP program for orangutan (Pongo pygmaeus ssp.) was initiated in 1982. Since that time, the Propagation Group has dealt with issues related to improving captive management of the species. Prior to 1982, most orangutans in North America were managed as a single species, though a number of institutions did house their Bornean and Sumatran specimens separately. However, the determination of race at that time was made largely on the basis of physical appearance, a method subsequently proven imprecise. A major achievement of the SSP has been the refinement of orangutan subspecies determination; SSP-sponsored karotyping has determined, on a chromosomal level, the true subspecies of virtually every orangutan managed by the SSP. The validity of these results has been confirmed by recent fieldwork, also completed under the auspices of the SSP. Since 1985, as a result of these captive and field data, the SSP has held to the policy that subspecific hybrid orangutans should not be produced; to that end, there is a moratorium on the breeding of hybrid animals. Another significant step taken by the SSP group is the completion of the sophisticated demographic and genetic analyses, leading to the development of a Masterplan for this species and its captive management. Goals for the near future include refinement of the Masterplan analyses and publication of a new international studbook for the species.     

Pan-African sanctuary alliance: status and range of activities for great ape conservation

While wild populations continue to decrease, the number of orphaned primates, sanctuaries, and attempts to reintroduce primates back to the natural environment are increasing. An umbrella organization called the Pan-African Sanctuary Alliance (PASA) was formed in 2000 and recently the IUCN Reintroduction Specialist Group developed a set of specific policy guidelines for primates (2002). Data presented in this report are based upon questionnaire responses by managers from 17 African facilities that have become members of PASA (membership in PASA is defined by attendance at an annual PASA workshop). These PASA facilities house over 500 great apes. (There may be other facilities not represented here simply because their managers did not attend a PASA workshop.) The majority of the apes arrived at the sanctuaries when they were less than 4 years old and half were confiscated. Over 40% were found awaiting sale, and 30% had been previously kept as pets. Common ailments upon arrival included internal parasites, behavioral abnormalities, and malnutrition; 20% of the total sanctuary population died prematurely. Most sanctuaries use a combination of enclosures surrounded by electric fencing and cages to accommodate the apes. Sanctuaries actively participate in conservation education, habitat protection, tourism, scientific data collection, local development, and reintroduction. The median total facility operating cost was 65,000 US dollars per annum. The median facility cost per ape was 2,222 US dollars per annum. Most funding comes from overseas nongovernmental agencies. Discussion focuses on evaluating the present status of sanctuaries, the problems facing them, and their potential role in African conservation issues.     

Hypothesis for the causes and periodicity of repetitive linear enamel hypoplasia in large, wild African (Pan troglodytes and Gorilla gorilla) and Asian (Pongo pygmaeus) apes

Repetitive linear enamel hypoplasia (rLEH) is often observed in recent large-bodied apes from Africa and Asia as well as Mid- to Late Miocene sites from Spain to China. The ubiquity and periodicity of rLEH are not understood. Its potential as an ontogenetic marker of developmental stress in threatened species (as well as their ancient relatives) makes rLEH an important if enigmatic problem. We report research designed to show the periodicity of rLEH among West African Pan troglodytes (12 male, 32 female), Gorilla gorilla (10 male, 10 female), and Bornean and Sumatran Pongo pygmaeus (11 male, 9 female, 9 unknown) from collections in Europe. Two methods were employed. In the common chimpanzees and gorillas, the space between adjacent, macroscopically visible LEH grooves on teeth with two or more episodes was expressed as an absolute measure and as a ratio of complete unworn crown height. In the orangutans, the number of perikymata between episode onsets, as well as duration of rLEH, was determined from scanning electron micrographs of casts of incisors and canines. We conclude that stress in the form of LEH commences as early as 2.5 years of age in all taxa and lasts for several years, and even longer in orangutans; the stress is not chronic but episodic; the stressor has a strong tendency to occur in pulses of two occurrences each; and large apes from both land masses exhibit rLEH with an average periodicity of 6 months (or multiples thereof; Sumatran orangutans seem to show only annual stress), but this needs further research. This is supported by evidence of spacing between rLEH as well as perikymata counts. Duration of stress in orangutans averages about 6 weeks. Finally, the semiannual stressor transcends geographic and temporal boundaries, and is attributed to regular moisture cycles associated with the intertropical convergence zone modified by the monsoon. While seasonal cycles can influence both disease and nutritional stress, it is likely the combination of seasonal variation in fruiting cycles with specific stressors (malaria and/or intestinal parasites, especially hookworm) that results in this widespread phenomenon. This seasonal stress is sufficiently common and of long duration (6 weeks on average in orangutans) that we think rLEH may reflect significant stress in recent and, inferentially, fossil apes. Increasing seasonality may have impinged negatively on later Miocene apes, especially if they lacked a clear birth peak or seasonality in their reproductive cycles.     

The behavior of a zoo-housed infant orangutan after the death of its mother

The behavior of an infant female orangutan at Dublin Zoo before and after the death of her mother was recorded using scan sampling and compared. Social interactions and associations of the infant with the other individuals in the group were also compared before and after the death of her mother. Increases in climbing and object manipulation were observed, and a decrease in resting occurred. The infant orangutan significantly increased the amount of time she spent in close contact with another related adult female in the group after her mother's death. This case study describes an example of a zoo‐housed infant orangutan being successfully fostered by a related female without human intervention. It also provides a quantification of the behavior of an infant orangutan before and after being orphaned. Zoo Biol 30:205–211, 2011. © 2010 Wiley‐Liss, Inc.     

Ontogenetic allometry, heterochrony, and interspecific differences in the skull of African apes, using tridimensional Procrustes analysis

Ontogenetic studies of African ape skulls lead to an analysis of morphological differences in terms of allometry, heterochrony, and sexual dimorphism. The use of geometric morphometrics allows us 1) to define size and shape variations as independent factors (an essential but seldom respected condition for heterochrony), and 2) to calculate in percentage of shape changes and to graphically represent the parts of shape variation which are related to various biological phenomena: common allometry, intraspecific allometry, and allometric and nonallometric shape discrimination. Three tridimensional Procrustes analyses and the calculation of multivariate allometries, discriminant functions, and statistical tests are used to compare the skulls of 50 Pan troglodytes, and 50 Gorilla gorilla of different dental stages. The results both complement and modify classical results obtained from similar material but with different methods. Size and Scaling in Primate Morphology, New York: Plenum, p. 175-205). As previously described by Shea, the common growth allometric pattern is very important (64% of total shape variation). It corresponds to a larger increase of facial volume than of neurocranial volume, a more obliquely oriented foramen magnum, and a noticeable reshaping of the nuchal region (higher inion). However, the heterochronic interpretation based on common allometry is rather different from Shea. Gorillas differ from chimpanzees not only with a larger magnitude of allometric change (rate peramorphosis), as is classically said, but also grow more in size than in shape (size acceleration). In other words, for a similar stage of growth, gorillas have the size and shape corresponding to older chimpanzees, and for a similar shape, gorillas have a larger size than chimpanzees. In contrast, sexual dimorphism actually corresponds to allometric changes only, as classically demonstrated (time hypermorphosis). Sexual dimorphism is here significant in adult gorillas alone, and solely in terms of allometry (size-related shape and size, given that sagittal and nuchal crests are not taken into account). The study also permits us to differentiate two different shape variations that are classically confused in ontogenetic studies: a very small part of allometric shape change which is specific to each species (1% of the total shape variation), and nonallometric species-specific traits independent of growth (8% of total shape change). When calculated in terms of intraspecific allometries (including common allometry and noncommon allometry), shape changes are more extensive in gorillas (36% of total shape change) than in chimpanzees (29% of total shape change). The allometric differences mainly concern the inion, which becomes higher; the position of the foramen magnum, more dorsally oriented; and the palate, more tilted in adult gorillas than in adult chimpanzees. In contrast, nonallometric species-specific traits in gorillas are the long and flat vault characterized by a prominent occipital region, the higher and displaced backward glabella, and the protrusive nose. Biomechanical schemes built from shape partition suggest that the increased out-of-plumb position of the head during growth is partially compensated in gorillas by a powerful nuchal musculature due to the peculiar shape of the occipital region.