Speciation and intrasubspecific variation of Bornean orangutans, Pongo pygmaeus pygmaeus

Mitochondrial DNA control region sequences of orangutans (Pongo pygmaeus) from six different populations on the island of Borneo were determined and analyzed for evidence of regional diversity and were compared separately with orangutans from the island of Sumatra. Within the Bornean population, four distinct subpopulations were identified. Furthermore, the results of this study revealed marked divergence, supportive evidence of speciation between Sumatran and Bornean orangutans. This study demonstrates that, as an entire population, Bornean orangutans have not experienced a serious genetic bottleneck, which has been suggested as the cause of low diversity in humans and east African chimpanzees. Based on these new data, it is estimated that Bornean and Sumatran orangutans diverged approximately 1.1 MYA and that the four distinct Bornean populations diverged 860,000 years ago. These findings have important implications for management, breeding, and reintroduction practices in orangutan conservation efforts.     

Glucose regulation in captive Pongo pygmaeus abeli,P. p. pygmaeus,andP. p. abeli x P. p. pygmaeus orangutans

Intravenous glucose tolerance tests (IVGTT) were performed on 30 anesthetized, captive Sumatran (Pongo pygmaeus abeli), Bornean (P. p. pygmaeus), and hybrid (P. p. ablie x P. p. pygmaeus) orangutans, and fasted blood samples were taken from two additional juvenile orangutans in 11 U.S. zoos from 1989 to 1997. The age range of animals was 3.5 to 40.5 years. Plasma and serum samples were assayed for glucose and insulin concentrations. Glucose disappearance rate (K_G), an index of glucose tolerance, was calculated, as were the early (acute) and second phase insulin responses to administered glucose. The mean ± SE (and median) fasting glucose and insulin concentrations were 113 ± 16 mg/dL (90 mg/dL) and 45 ± 7 μU/mL (27 μU/mL), respectively. Two animals previously suspected to be diabetic were easily identified by their markedly elevated fasting glucose concentrations (380 and 562 mg/dL) and relatively low fasted insulin concentrations (21 and 14 μU/mL); their insulin responses during the IVGTTs were also low or non‐detectable. Without these diabetics, the mean ± SE (median) fasting glucose concentration was 92 ± 18 mg/dL (89 mg/dL). Two animals, ages 18 and 40, were identified as potentially pre‐diabetic based on age, adiposity, elevated fasted glucose (116 and 137 mg/dL, respectively), and elevated fasted insulin concentrations (114 and 217 μU/mL, respectively). In addition, nearly half of the animals of varying ages, all sub‐species and both sexes exhibited delayed or attenuated acute insulin responses during the IVGTTs, resulting in lower K_G (P < 0.04) and suggesting propensity for glucose intolerance in captive orangutans. Glucose and insulin concentrations and insulin responses to glucose did not differ between females on hormonal contraception regimes and those not receiving treatment. Zoo Biol 19:193–208, 2000. © 2000 Wiley‐Liss, Inc.     

Health evaluation of free-ranging and semi-captive orangutans (Pongo pygmaeus pygmaeus) in Sabah,Malaysia

Baseline data on health of free-ranging wildlife is essential to evaluate impacts of habitat transformation and wildlife translocation, rehabilitation, and reintroduction programs. Health information on many species, especially great apes, is extremely limited. Between 1996 and 1998, 84 free-ranging orangutans captured for translocation, underwent a complete health evaluation. Analogous data were gathered from 60 semi-captive orangutans in Malaysia. Baseline hematology and serology; vitamin, mineral and pesticide levels; and results of health evaluations, including physical examination, provide a baseline for future monitoring. Free-ranging and semi-captive orangutans shared exposure to 11 of 47 viruses. The semi-captive orangutans had significantly higher prevalence of antibodies to adenovirus (P < 0.0005) and rota (SA 11) virus (P < 0.008). More free-ranging than semi-captive animals had antibodies to Japanese encephalitis virus (P < 0.08) and foamy virus (P = 0.05). Exposure to parainfluenza and langat viruses was detected exclusively in semi-captive animals and exposure to sinbis virus was only found in free-ranging orangutans. There was evidence of exposure to respiratory syncytial virus, coxsackie virus, dengue virus, and zika virus in both groups. Ebstein-Barr virus was ubiquitous in both groups. Prevalence of antibodies against mumps virus changed from 0% in 1996 to 45% in 1998. No antibodies were detected to many important zoonotic viral pathogens, including herpesvirus and hepatitis virus. Prevalence of Balantidium coli and Plasmodium pitheci infections and exposure to mycobacterium was higher in the semi-captive animals. Differences in exposure to pathogens between the groups may be due to environmental factors including differences in exposures to other species, habitat quality, nutritional status, and other potential stressors. Differences in health parameters between captive and free-ranging orangutans need to be considered when planning conservation areas, translocation procedures, and rehabilitation protocols. Because survival of the orangutan is linked to animal and ecosystem health, results of this study will assist wildlife conservation programs by providing baseline health information.     

Meat-eating behaviour in wild orang utans,Pongo pygmaeus

Meat-eating was observed for the first time among a population of wild orang utans at Gunung Leuser National Park, Sumatra. An adult female who was consorting with an adult male consumed a gibbon (Hylobates lar) carcass. There was no food sharing between the consort pair. The absence of food sharing is interpreted as indicative of the anti-social attitude of adult orang utans.     

Removal,early hand rearing,and successful reintroduction of an orangutan (Pongo pygmaeus pygmaeus/x abelii) to her mother

A newborn orangutan was removed from her mother 55 h after birth because no nursing had been observed. She was hand reared in a nursery for 3 d and then successfully reintroduced to her mother. Several factors that may have contributed to the successful reintroduction are discussed.     

Evidence of Cannibalism in Macrolophus pygmaeus, a Natural Enemy of Whiteflies

Cannibalism and the effects of host plant, sex, time and food resources on its expression were studied for the zoophagous mirid Macrolophus pygmaeus Wagner (Hemiptera: Miridae). Cannibalistic behaviour was studied by offering 5 conspecific larvae (first instar) to newly emerging adults. Four treatments were studied: without water, with water only, with a host plant (tobacco) and with both a host plant and prey (eggs of Ephestia kuehniella). Cannibalism was observed in all treatments. In the “host plant + eggs of E. kuehniella” treatment, very few individuals displayed cannibalistic behaviour. The proportion of cannibalism was only reduced when eggs of E. kuehniella were offered. Water (free or via a host plant) was very important for both survival and feeding. The cannibalistic behaviour of M. pygmaeus should be taken into account when planning a release strategy in the context of biological control.     

Orangutans (Pongo pygmaeus) Remember Old Acquaintances

Many social animals can discriminate between familiar and unfamiliar faces. Orangutans, however, lead a semi-solitary life and spend much of the day alone. As such, they may be less adept at recognizing conspecifics and are a good model for determining how social structure influences the evolution of social cognition such as facial recognition. The present study is the first report of whether orangutans can distinguish among individual faces. We adopted a preferential looking method and found that orangutans used facial discrimination to identify known conspecifics. This suggests that frequent and intense social interaction is not necessary for facial discrimination, although our findings were limited by the small number of stimuli and the unequal numbers of male and female orangutans depicted in the stimuli.     

A note on the labial swelling of a pregnant orang-utan,Pongo pygmaeus abelii

Labial swellings following copulation were recorded during each of seven pregnancies for an adult female Sumatran orang-utan (Pongo pygmaeus abelii). These swellings persisted throughout pregnancy and disappeared within a short time after the termination of pregnancy. Labial swellings may be a useful tool in diagnosing pregnancy in orang-utans.     

Alkaptonuria in an orangutan (Pongo pygmaeus)

Alkaptonuria has been diagnosed in a laboratory born, five year old, female orangutan. In man, this relatively rare amino acid metabolic disorder is characterized by arthritis, pigmentation of cartilage, and darkening of the urine upon standing. The color change is due to oxidation of homogentisic acid not normally found in the urine. The condition in man is a simple Mendelian recessive trait characterized by the absence of homogentisic acid oxidase activity. At two years of age, the affected orangutan was noted to void urine of normal color, which upon standing turned a very dark maroon color. Clinically the animal appeared normal; and the results of a urinalysis, hemogram, and survey radiographs confirmed this evaluation. Nonspecific laboratory determinations used to diagnose alkaptonuria in man were positive. Homogentisic acid in the urine was confirmed by paper chromatography, and a quantitative evaluation was made by a commercial laboratory. The orangutan has shown no clinical change or evidence of ochronosis during the past three years, and quarterly survey radiographs show no evidence of osteoarthropathy. The affected orangutan has half brothers and sisters in the colony but no full sibling. Both parents are young, however, and are being paired in an attempt to produce siblings. It is hoped that additional animals with this metabolic defect will become available for use as potential models for studying this inborn error of metabolism.     

The ontogeny of sexual dimorphism in the cranium of Bornean orang-utans (Pongo pygmaeus pygmaeus): I. Univariate analyses

Based on a homogeneous sample of 212 individuals spanning all postnatal age periods, we examine the ontogeny of cranial sexual dimorphism in Bornean orang-utans (Pongo pygmaeus pygmaeus) by means of univariate statistics. A distinct pattern emerges at the early juvenile stage and continues at all subsequent stages with males tending to exceed females in all cranial dimensions. In conjunction, starting at mid-juvenile stage, there is a strong tendency for an increase in number and strength of significant cranial sex differences, all of them in favor of males. Significant sex differences in the viscerocranium, reflecting stronger prognathism in males, emerge prior to those in the neurocranium. The total ontogenetic pattern of cranial sexual dimorphism in orang-utans is remarkably similar to that of gorillas, except that there is no evidence of a sex difference in timing of the adolescent growth spurt in the orang-utan. As for other catarrhine species (Wood 1976), male variance of cranial dimensions tends to be greater than that of females, thus lending support to Leutenegger & Cheverud's (1982, 1985) model on the evolution of character dimorphism by means of variance dimorphism.     

The ontogeny of sexual dimorphism in the cranium of Bornean orang-utans (Pongo pygmaeus pygmaeus) as detected by principal-components analysis

The ontogeny of cranial sexual dimorphism in the Bornean orang-utan (Pongo pygmaeus pygmaeus) is examined by means of principal-components analysis (PCA). Normalized first components are called allometry vectors or vectors of relative growth and show that sexual dimorphism is present at all stages of growth. Two patterns of sexual dimorphism are present: (1) sexual differences at age groups 2 and 3 are the result primarily of differences in principal component II scores, reflecting mainly shape-related differences, and (2) age groups 5, 6, and 7 show a trend of stronger size-related shape differences with increasing age in the allometry vector along with decreasing differences in principal component II scores, reflecting an increase in size-related shape differences between the sexes. Age group 4 shows a combination of both patterns. Our results support Shea's hypothesis (1985a) that when using multigroup PCAs in closely related taxa, the allometry vector will generally estimate the shape variation resulting from the extension of common growth allometry patterns (ontogenetic scaling). The second and subsequent components summarize shape variation from slope and intercept differences between the groups, provided that ontogenetic scaling is not solely responsible for all the shape differences present. Subanalyses of those dimensions previously found to show ontogenetic scaling and acceleration follow this pattern well. The total sample provides a pattern whereby ontogenetically scaled dimensions possess a stronger influence over accelerated dimensions but still generally follow Shea's hypothesis. Finally, variously derived coefficients provided several interesting findings: (1) strong evidence was found against multivariate isometry for both the pooled and the separate samples, (2) multivariate allometric coefficients for both sexes follow the general growth pattern of negative scaling in neurocranial dimensions and positive scaling in the viscerocranium, and (3) multivariate slopes have a very high correlation with bivariate slopes relative to the same independent X variable, thereby lending further support to Jolicoeur's (1963a, b) allometry generalization.     

Selecting nest-sites of sumatran organ-utans,Pongo pygmaeus abelii in the Gunung Leuser National Park,Indonesia

In the Gunung Leuser National Park of Indonesia a population of orang-utans has been observed. The location of 172 night-nest sites has been examined with respect to their position in relation to the last food tree visited during the preceding day and with respect to their height above the ground. There were significant differences between the sex-age classes in the distribution of distances between nest-sites and the last visited food tree. The more vulnerable animals nested at greater distances and also tended to nest at greater height. These aspects of nest-sites selection have been interpreted in terms of an anti-predator strategy: the more vulnerable animals avoid nesting in fruit trees; instead they prefer more cryptic, unpredictable and inaccessible sites.     

Hand preferences in captive orangutans (Pongo pygmaeus)

The strength of the evidence for population-level handedness in the great apes is a topic of considerable debate, yet there have been few studies of handedness in orangutans. We conducted a study of manual lateralization in a captive group of eight orangutans (Pongo pygmaeus) ranking the degrees of manual preference according to a defined framework. We analyzed five behavioral patterns: eat (one- and two-handed), make/modify tool, oral tool-use, and manual tool-use. Although some individuals showed significant manual preferences for one or more tasks, at the group-level both one-handed and two-handed eating, oral tool-use, and make/modify tool were ranked at level 1 (unlateralized). Manual tool-use was ranked at level 2, with four subjects demonstrating significant hand preferences, but no group-level bias to the right or left. Four subjects also showed hand specialization to the right or left across several tasks. These results are consistent with most previous studies of manual preference in orangutans. The emergence of manual lateralization in orangutans may relate to more complex manipulative tasks. We hypothesize that more challenging manual tasks elicit stronger hand preferences.     

Patterns of Gazing in Orangutans (Pongo pygmaeus)

Eyes play an important role in communication amongst humans and animals. However, relatively little is known about specific differences in eye morphology amongst primates and how these features might be associated with social structure and direction of gaze. We present a detailed study of gazing and eye morphology—exposed sclera and surrounding features—in orangutans. We measured gazing in rehabilitating orangutans in two contexts: interspecific viewing of the experimenter (with video camera) and intraspecific gazing (between subjects). Our findings show that direct staring is avoided and social looking is limited to certain age/social categories: juveniles engage in more looking at other orangutans than do adults or infants. While orangutans use eye movements in social communication, they avoid the more prolonged mutual gaze that is characteristic of humans, and also apparent in chimpanzees and gorillas. Detailed frame-by-frame analysis of videotapes from field and zoo studies of orangutans revealed that they pay visual attention to both human observers and conspecifics by glancing sideways, with the head turned at an angle away from the subject being observed. Mutual gaze was extremely rare, and we have observed only two incidences of gaze following. Orangutans in captivity appear to use a more restricted pattern of gazes compared to free-living, rehabilitating ones, possibly suggesting the presence of a pathological condition (such as depression) in the captive subjects. Our findings have implications for further investigations of social communication and cognition in orangutans.     

Genetic Divergence of Orangutan Subspecies (Pongo pygmaeus)

Microsatellites and mitochondrial DNA sequences were studied for the two subspecies of orangutans (Pongo pygmaeus), which are located in Borneo (P. p. pygmaeus) and Sumatra (P. p. abelii), respectively. Both subspecies possess marked genetic diversity. Genetic subdivision was identified within the Sumatran orangutans. The genetic differentiation between the two subspecies is highly significant for ND5 region but not significant for 16s rRNA or microsatellite data by exact tests, although F _ST estimates are highly significant for these markers. Divergence time between the two subspecies is approximately 2.3 ± 0.5 million years ago (MYA) estimated from our data, much earlier than the isolation of their geological distribution. Neither subspecies underwent a recent bottleneck, though the Sumatran subspecies might have experienced expansion approximately 82,000 years ago. The estimated effective population sizes for both subspecies are on the order of 10⁴. Our results contribute additional information that may be interpreted in the context of orangutan conservation efforts. Received: 13 June 2000 / Accepted: 30 January 2000     

Large body size in the pygmy swordtail Xiphophorus pygmaeus

Fishes in the genus Xiphophorus (swordtails and platyfishes) are well known for the influence of the pituitary ( P ) locus on variation of male size at maturity both within and among species. We report the discovery of large male size (>29 mm SL) in several populations of the swordtail X. pygmaeus , a species previously thought to consist of only small males (<29 mm SL). Large size is geographically restricted, and average male size varies significantly by site and year sampled in a pattern suggesting a recent origin and slow spreading of the large male phenotype. However, large male size is not strongly paternally inherited in this species, as it is in its two closest relatives, X. nigrensis and X. multilineatus , showing that large size does not result from the same genetic ( P locus) mechanism. Large X. pygmaeus males do not court, can exhibit the gold morph, do not possess swords and have slender body shape. In these traits they resemble small conspecific males and small males of X. nigrensis and X. multilineatus rather than large males of these latter two species. This shows that correlations between morphological and behavioural traits that occur in X. nigrensis and X. multilineatus are absent in X. pygmaeus.     

The ontogeny of sexual dimorphism in the cranium of Bornean orang-utans (Pongo pygmaeus pygmaeus): II. Allometry and heterochrony

Based on a homogeneous sample of 212 individuals spanning all postnatal periods, we examine the ontogeny of cranial sexual dimorphism in Bornean orang-utans (Pongo pygmaeus pygmaeus) by means of allometric analysis and in terms of heterochrony. The bivariate growth allometries of 20 cranial dimensions against basicranial length yield two major patterns. Confirming the null hypothesis, strong ontogenetic scaling, where growth regressions of both sexes fall along a single ontogenetic continuum, and where shape differences between adult males and females result from the extension of relative growth in the smaller females to larger size in males, is found in 10 cases. Ontogenetic scaling is particularly strong in proportions of (1) the neurocranium directly associated with brain size, (2) the orbital region, and (3) the dental arcade. In terms of heterochrony such a pattern most likely is the result of a process termed "time hypermorphosis", i.e. an extension of the growth period in time in males. The second major pattern seen in the remaining 10 cases shows a departure from ontogenetic scaling, with males exhibiting a significantly steeper slope than females. Departures from ontogenetic scaling, where size and shape are dissociated with adult males being disproportionately larger than adult females, are found in proportions of cranial regions directly associated with secondary sexual character development: prognathism, canine size, and cheek pad area. In terms of heterochrony such a pattern most likely is the result of a process termed "acceleration", i.e. the rate of shape change is increased in males.