Growth and sexual dimorphism in orangutan crania: a three-dimensional approach

New insights may be gleaned by taking an ontogenetic approach to investigations of adult dimorphism. Previous work in this area relied on traditional, caliper-based, morphometric methods, and produced conflicting results. This study uses a three-dimensional (3-D) approach for both local and global form comparisons of sex-specific growth and growth patterns. 3-D coordinate data were collected for 20 landmarks on 94 orangutan crania divided into five developmental stages. Data were analyzed using Euclidean distance matrix analysis (EDMA). Results indicate that differences in growth patterns between male and female orangutans exist in the youngest age intervals. Dimorphic patterns are strongest in the face and basicranium at the youngest age intervals, and in the face and neurocranium during adult stages. Females grow substantially more in the cranial base and face during the youngest age groups, while males grow more than females in all anatomical regions later in development. Growth in the palate was similar between sexes. Sexual dimorphism may be produced through the continued growth of one sex relative to the other, representing differences in timing, or growth duration. Dimophism may also result from different growth rates between sexes, where one sex develops faster than the other sex in the same time interval. Orangutan males and females differ in both the rate and duration of their craniofacial development. The data analysis technique used here, EDMA, was integral in identifying dynamic growth processes rather than just the static end results of each developmental stage.     

Aspects of dental development in the orangutan prior to eruption of the permanent dentition

In spite of a resurgence of interest in the interpretation of the sequences of dental development and eruption in various Plio-Pleistocene hominoids as being either “modern human” or “ape-like,” the body of comparative material on the extant hominoids remains deficient in critical areas. In concert with recent attempts to rectify this situation, we present the results of our studies on dental morphogenesis in the orangutan. We have focused on the growth and eruption of the deciduous dentition as well as early stages of permanent tooth formation and have found that 1) many permanent teeth develop earlier than was thought, 2) differences exist between development in the upper and in the lower jaw, and 3) states of tooth formation can vary significantly among individuals of similar chronological age or tooth eruption status.     

Review of medical literature of great apes in the 1980s

The medical problems of great apes including gorillas (Gorilla gorilla), orangutans (Pongo pymaeus), and chimpanzees (Pan sp.) published during the last decade are reviewed. Anesthetic techniques, diseases or organ systems, neoplasia, infectious diseases, and reproductive problems are reviewed. Gonadal tumors and atherosclerosis in great apes appear frequently in the literature. Diseases with suspected viral etiology include papillomas in chimpanzees, retrovirus-associated lymphomas in gorillas, and various herpesvirus disease. Technology developed for human medicine has expanded the diagnostic opportunities for clinicians working with great apes.     

A possible case of hantavirus infection in a Borneo orangutan and its conservation implication

Background Natural infection of hantavirus in orangutans has never been reported. Methods Enzyme‐linked immunosorbent assays (ELISA), Indirect immunofluorescence assay (IFA), and RT‐PCR were used to diagnosis a suspected case in a pet orangutan in southern Taiwan. Results Although the RT‐PCR result was negative, the high IgG titer in the beginning and its dramatic drop after treatments suggested a recent Seoul‐type hantavirus infection. Conclusions Hantavirus transmission and its potential damage to wild orangutans should not be overlooked.     

Developmental changes in the facial morphology of the Borneo orangutan (Pongo pygmaeus): possible signals in visual communication

Orangutans display remarkable developmental changes and sexual differences in facial morphology, such as the flanges or cheek-pads that develop only on the face of dominant adult males. These changes suggest that facial morphology is an important factor in visual communication. However, developmental changes in facial morphology have not been examined in detail. We studied developmental changes in the facial morphology of the Borneo orangutan (Pongo pygmaeus) by observing 79 individuals of various ages living in the Sepilok Orangutan Rehabilitation Centre (SORC) in Malaysia and in Japanese zoos. We also analyzed photographs of one captive male that were taken over a period of more than 16 years. There were clear morphological changes that occurred with growth, and we identified previously unreported sexual and developmental differences in facial morphology. Light-colored skin around the eyes and mouth is most prominent in animals younger than 3 years, and rapidly decreases in area through the age of approximately 7 years. At the same time, the scattered, erect hairs on the head (infant hair) become thick, dense hairs lying on the head (adult hair) in both sexes. The results suggest that these features are infant signals, and that adult signals may include darkened face color, adult hair, whiskers, and a beard, which begin to develop after the age of approximately 7 years in both sexes. In females, the eyelids remain white even after 10 years, and turn black at around the age of 20; in males, the eyelids turn black before the age of 10. The whiskers and beards of adults are thicker in males than in females, and are fully developed before the age of 10 in males, while they begin to develop in females only after approximately 20 years. White eyelids and undeveloped whiskers and beards may be visual signals that are indicative of young adult females. Our results also show that the facial morphology of the unflanged male is similar to that of the adult female, although it has also been pointed out that unflanged males resemble younger individuals.     

Estimated number of snake species that can be managed by Species Survival Plans in North America

A survey designed to estimate the number of snake enclosures available for Species Survival Plan (SSP) programs was distributed to all North American zoos containing 100 or more reptile and amphibian specimens. Of the 52 zoos surveyed, 44 (84.6%) responded, indicating that 790 (26.3%) of the 3,012 snake enclosures were available for SSP programs. Available enclosures were classified by size and existing themes to help define limitations of the potential SSP space. This spatial information was then used in conjunction with existing population genetics models to estimate that up to 16 snake species can be accommodated by SSP programs in these zoos collectively. Values used in the models were estimates of those for an average snake species with a generation time of 15 years, lambda of 1.15, with 26 effective founders, and an n_e/n ratio of 0.3. It was further assumed that 90% of the genetic variation would be maintained in each species for a period of 100 years. Tactics to increase the number of species that SSP programs can accommodate include: increase reserve space, devote more space for SSP snakes, lengthen generation time, promote gene exchange with wild populations, goal SSP programs for less than 200 years, invest in short-term programs, involve the private sector, build new enclosures, increase the number of snakes per enclosure, and encourage participation of non-North American institutions. To maximize biological diversity in relation to captive carrying capacity, it is recommended that SSP programs represent both infraorders of living snakes and as many families within those infraorders as possible. Although not all 16 families of snakes are likely to be represented due to exhibit value, obtainability, and husbandry success, it may be possible to represent as many as nine families in 16 SSP programs. © 1993 Wiley-Liss, Inc.     

Body mass of wild bornean orangutans living in human‐dominated landscapes: Implications for understanding their ecology and conservation

Body mass is a key determinant of a species' ecology, including locomotion, foraging strategies, and energetics. Accurate information on the body mass of wild primates allows us to develop explanatory models for relationships among body size, ecology, and behavior and is crucial for reconstructing the ecology and behavior of fossil primates and hominins. Information on body mass can also provide indirect information on health and can be an important tool for conservation in the context of increasingly widespread habitat disturbance. This study reports body mass data recorded for wild Northeast Bornean orangutans (Pongo pygmaeus morio) during relocation efforts in forestry and oil palm plantations in East Kalimantan, Indonesia. The average mass of flanged adult males (n = 12, 74 ± 9.78 kg) and adult females (n = 7, 35.29 ± 7.32 kg) from this study were 13.6% and 9% lower, respectively, than the only other published wild Bornean orangutan body mass measurements, but the range of weights for both males and females was larger for this study. This pattern could be due to sampling error, data collection differences, or the influence of habitat disturbance, specifically a lack of access to resources, on individual health. When necessary relocations present the opportunity, we encourage researchers to prioritize the collection of body size data for the purposes of understanding ecology but also as an indirect means of monitoring population viability. As primate habitat becomes increasingly fragmented and altered by humans such data will become critical to our ability to make informed conservation decisions. Am J Phys Anthropol 157:339–346, 2015. © 2015 Wiley Periodicals, Inc.     

Evidence for African origins of founders of the asiatic lion species survival plan

The Asiatic lion (Panthera leo persica) exists in the wild as a single relict population of approximately 250 individuals in the protected Gir Forest Sanctuary in western India. In 1981, a species survival plan (SSP) for the Asiatic lion was established by the American Association of Zoological Parks and Aquariums to manage the 200 + descendants of Asiatic lions in captivity in western zoological facilities. This captive population was derived from seven founders. In order to compare the genetic structure of the Gir Forest population with that of the captive SSP population, a genetic survey of 46 electrophoretic allozyme systems resolved from extracts of lion blood was undertaken by using 29 SSP Asiatic lions and 28 wild-caught or captive-bred lions maintained at the Sakkarbaug Zoo in India but originally derived from the Gir Forest. The Gir lion population was found to be genetically monomorphic at each of 46 allozyme loci. This was in contrast to several African lion (Panthera leo leo) populations, which show moderate levels of allozyme variation at the same loci. The SSP lion population was polymorphic at three allozyme loci (IDHI, TF, and PTI) for alleles that were previously found only in African lion populations. Pedigree analysis of the genetic transmission of these three biochemical loci demonstrated that two of the five primary founder animals of the SSP Asiatic lion population (a breeding pair originally imported from the Trivandrum Zoo in southern India) were descendants of the African subspecies. Three other founder animals were pure Asian. A retrospective SSP pedigree analysis of two morphologic characters (prominent abdominal fold and pairing of infraorbital foramen) that are partially diagnostic for persica vs leo was consistent with this conclusion as well. The implications for the management of small captive populations of threatened species and of the Asiatic lion SSP population are discussed.     

Development of the orangutan permanent dentition: Assessing patterns and variation in tooth development

This study examines dental formation and alveolar emergence in a large cross-sectional sample composed primarily of wild-reared orangutans (N = 89) in order to provide information on the development of the permanent dentition in this hominoid and to address questions of variation in individual tooth formation, between teeth and between individuals. All specimens have been radiographed in lateral aspect and stages of crown and root formation recorded for all teeth. The ranges of crown and root formation of I¹₁, C¹₁, P⁴₄, and M³₃ have been calculated relative to the stage of M₁¹ development within a specific tooth quadrant. Then, for each specimen, BMDP scatterplot and nonparametric statistics have been used to graph changes in stages of these teeth relative to M¹₁ stages and to examine relationships between pairs of upper and lower dental counterparts and between teeth of each jaw. Results indicate 1) high correlations between upper and lower tooth pairs and between many of the permanent teeth within individuals, 2) a relatively large range of variability in individual tooth development (multistage ranges relative to M¹₁), 3) greater variation in root development at emergence than earlier reports, and 4) evidence of variability within the sequence emergence pattern of the orangutan. © 1996 Wiley-Liss, Inc.     

Appearance of ossification centers of the lower arm,wrist, lower leg,and ankle in immature orangutans and chimpanzees with an assessment of the relationship of ossification to dental development

This study examines the appearance of the secondary ossification centers in the lower arms, wrists, lower legs, and ankles of a cross-sectional sample of 20 infant orangutans and chimpanzees (15 of known age). The number of tarsal and carpal centers is analyzed relative to the degree of M₁ development and the weight of individual animals. Variation in the appearance of these ossification centers is discussed relative to these variables and others. In addition, a sequence of appearance is established for the carpal and tarsal ossification centers in the orangutan and data is presented on the status of these centers in a fetal and newborn gorilla. Study results indicate that 1) there is variation in the number of secondary epiphyses present in animals of similar ages; 2) tarsal ossification is completed prior to carpal ossification in the orangutan; 3) there are indications of a relationship between weight and the number of ossification centers present in animals of similar age; and 4) there appears to be no evidence of specific relationships between carpal and tarsal development and M₁ development. © 1996 Wiley-Liss, Inc.     

Infectious disease surveillance in captive and free-living cheetahs: An integral part of the species survival plan

During the formulative stages of developing the Species Survival Plan (SSP) for the cheetah, the impact of infectious disease upon its survival in captivity was of prime consideration, together with genetics, nutrition, physiology, and behavior. This paper summarizes the results of an infectious disease surveillance program, initially designed to monitor the infectious agents associated with clinically normal and clinically ill cheetahs in captivity, but subsequently supplemented with data from free-living cheetahs. The focus was on two viral infections, feline infectious peritonitis (FIP) and feline rhinotracheitis virus. Results indicated that between 1989 and 1991, there was an increase in the seroprevalence (number antibody-positive animals) of cheetahs to feline coronavirus from 41% to 64% in captivity. During this same time period, there were only two documented cases of FIP in cheetahs in the United States. The results suggest that feline coronavirus (feline enteric coronavirus--feline infectious peritonitis group) or a closely related coronavirus of cheetahs is becoming endemic in the captive cheetah population. Further serologic results from 39 free-living cheetahs demonstrated that there was a high seroprevalence (61%) to feline coronavirus, although serum antibody titers were considerably lower than those encountered in captive cheetahs. The observation of a high percentage of free-living cheetahs, which were seropositive to feline herpesvirus (44%), was unexpected, since it has been generally regarded that this infection is primarily associated with cheetahs in captivity. © 1993 Wiley-Liss, Inc.     

Captive and wild orangutan (Pongo sp.) survivorship: a comparison and the influence of management

For managers of captive populations it is important to know whether their management provides a species with the physical and social environment that maximizes its survivorship. To determine this, survivorship comparisons with wild populations and long‐term evaluations of captive populations are important. Here we provide both for orangutans. We show that survivorship has increased during the past 60 years for captive orangutan populations in zoos. In addition, we show that survivorship of captive orangutans in the past used to be lower than for wild orangutans, but that for recently born (1986–2005) orangutans survivorship is not significantly different from the wild. This indicates that captive management in the past was suboptimal for orangutan survivorship, but that modern management of captive orangutans has increased their survivorship. We discuss the possible factors of modern management that could have influenced this. Am. J. Primatol. 71:680–686, 2009. © 2009 Wiley‐Liss, Inc.     

Genetic diversity in the North American captive African elephant collection

One hundred and eight mitochondrial DNA (mtDNA) sequences were used in combination with multilocus genotypes generated from 19 nuclear microsatellite loci to assess the genetic diversity in the North American captive African elephant collection. The analysis of 4488 bp of mitochondrial nicotinamide adenine dinucleotide hydrogenenase subunit 4-cytochrome b (ND4-cyt b ) sequence revealed the existence of three distinct mtDNA lineages (Haplogroups I–III). The genetic distance between Haplogroups I/II and Haplogroup III was determined to be 0.046. The nucleotide diversity for the elephant mtDNA ND4-cyt b was <0.004. Analysis of multilocus genotypes indicated an average observed heterozygosity of 0.53 compared with the expected heterozygosity of 0.64. No subdivision in the data was detected including data partitioned by mtDNA haplogroup. Relatedness among the 108 individuals did not differ from that expected in random mating populations.     

Use of space and activity budgets in relation to age and social status in a captive herd of American bison,Bison bison

A stable herd of 11 captive American bison (Bison bison) of known ages and social rank was studied between June 18 and August 6, 1979 at the Jardin zoologique du Québec, Charlesbourg, Quebec. During the 8-week study, the first author collected scan data of predefined behaviors and locations on all individuals of the herd. Space use analysis revealed extensive occupation of (and preference for) the barn and sand mound by higher-ranking animals and calves, and the tendency for lower-ranked individuals to use alternate, lower-quality sites. Overall, the herd spent an average of 40% of the daytime resting, 25% standing, 23% feeding, and 12% walking/running and group exploring. High-ranking individuals spent significantly more time standing and walking, and less time foraging than average. Most low-ranking individuals spent significantly less time lying, and more time feeding than average. Calves spent significantly more time lying than average. The extra feeding time of low-ranking individuals occurred mostly in early morning and mid-day, when the high-ranking individuals were mostly inactive. Our results suggest differential space and time use in relation to age and social status. The effects of resource limitations caused by captivity conditions, as compared with natural conditions, are discussed in regard to the activity and movement coordination of individuals in this particular captive herd. © 1993 Wiley-Liss, Inc.     

Breeding program for the lesser kudu (Tragelaphus imberbis) in North America

The lesser kudu (Tragelaphus imberbis) has been kept in North American zoological parks since 1930 but has never been a common species in collections. In 1987 this population totaled 28 animals: 15 males and 13 females. A pedigree evaluation in 1987 of the existing population indicated that eight effective founders and one potential founder were represented in the North American herd. Three new potential founders from European captive populations were added to the population in 1987 to increase the number of existing founder lines to 12 animals. As this species is not endangered or threatened in its native habitat, it is not a high priority to qualify for designation as an SSP species. Because of this, the institutions holding lesser kudu in North America decided to join informally and draft a breeding program to better manage this small captive population. This program was designed to minimize inbreeding and equalize genetic representation of founder animals to maximize genetic diversity. It requires a shift in management philosophy to establish stable groups of breeding females at participating institutions while rotating appropriate breeder males through these herds in a controlled manner to ensure minimization of inbreeding and maximization of genetic diversity. It is hoped that this program can serve as a model for the management of other small captive populations of non-SSP species.