Variation in brain size and ecology in Pongo

Numerous hypotheses have been advanced to explain relative increases in brain size in primates and other mammals. However, notably less attention has been directed towards addressing the biological limits to increasing brain size. Here we explore variation in brain size in orangutans. We evaluated both raw and size-adjusted cranial capacity (CC) in adult Pongo pygmaeus pygmaeus (n=147), P. p. wurmbii (n=24), P. p. morio (n=14), and P. abelii (n=36). Results demonstrate significant variation in CC among orangutan taxa. Population differences in raw CC are significant for females (p=0.014) but not males. Post-hoc pairwise comparisons among females further reveal that raw CC is significantly smaller in P. p. morio compared to both P. abelii and P. p. pygmaeus. When evaluated for proportionality, geometric equivalence in CC is not maintained in orangutans, as P. p. morio has a significantly smaller CC when compared to one or more other orangutan groups. Even after statistically partitioning size and size-correlated shape, P. p. morio has a significantly smaller CC compared to most other orangutan groups. These observed differences in relative brain size are consistent with known variation in resource quality and life history amongst orangutan populations. Specifically, P. p. morio is characterized by the least productive habitat, the lowest energy intake during extended lean periods, and the shortest interbirth intervals. Our results, therefore, provide conditional support for the hypothesis that decreased brain size is related to prolonged episodes of food scarcity, and suggest a correlation between brain size, diet quality, and life history at the lowest macroevolutionary level. The association of a relatively small brain and poor diet quality in Pongo further suggests that ecological factors may plausibly account for such a reduction in brain size as observed in the recently recovered Homo floresiensis from Indonesia.     

The mitochondrial DNA molecule of sumatran orangutan and a molecular proposal for two (Bornean and Sumatran) species of orangutan

The complete mitochondrial DNA (mtDNA) molecule of Sumatran orangutan, plus the complete mitochondrial control region of another Sumatran specimen and the control regions and five protein-coding genes of two specimens of Bornean orangutan were sequenced and compared with a previously reported complete mtDNA of Bornean orangutan. The two orangutans are presently separated at the subspecies level. Comparison with five different species pairs—namely, harbor seal/grey seal, horse/donkey, fin whale/blue whale, common chimpanzee/pygmy chimpanzee, and Homo/common chimpanzee—showed that the molecular difference between Sumatran and Bornean orangutan is much greater than that between the seals, and greater than that between the two chimpanzees, but similar to that between the horse and the donkey and the fin and blue whales. Considering their limited morphological distinction the comparison revealed unexpectedly great molecular difference between the two orangutans. The nucleotide difference between the orangutans is about 75% of that between Homo and the common chimpanzee, whereas the amino acid difference exceeds that between Homo and the common chimpanzee. On the basis of their molecular distinction we propose that the two orangutans should be recognized as different species, Pongo pygmaeus, Bornean orangutan, and P. abelii, Sumatran orangutan. Received: 15 May 1996 / Accepted: 21 June 1996     

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.     

Evolution of immunoglobulin allotypes and phylogeny of apes

Serum samples from 72 Pan troglodytes, 5 Pan paniscus, 22 Gorilla gorilla, 23 Pongo pygmaeus abelii, 5 Pongo pygmaeus pygmaeus, 2 hybrids P.p. abelii X P.p. pygmaeus and 13 Hylobates lar were tested for Gm(1, 2, 3, 5, 6, 10, 11, 13, 14, 15, 16, 17, 21, 24, 28), Km(1) and Bm(1, 2, 3, 4, 5, 6, 7, 8) immunoglobulin allotypes by the classical hemagglutination inhibition method. The distribution of the various alleles and phenotypes makes it possible to distinguish each species or subspecies. Common chimpanzees have the richest polymorphism. Pygmy chimpanzees share common phenotypes with gorillas. Bornean and Sumatran orangutans have their own patterns of polymorphism, as do gibbons. Our principal component plot and dendrogram are compatible with the traditional classification of Hominoidea [e.g. Simpson, Bull. Am. Mus. nat. Hist. 85: 1-350, 1945] in 3 families: Hominidae, Pongidae and Hylobatidae.     

Sex-biased dispersal and volcanic activities shaped phylogeographic patterns of extant Orangutans (genus: Pongo)

The Southeast Asian Sunda archipelago harbors a rich biodiversity with a substantial proportion of endemic species. The evolutionary history of these species has been drastically influenced by environmental forces, such as fluctuating sea levels, climatic changes, and severe volcanic activities. Orangutans (genus: Pongo), the only Asian great apes, are well suited to study the relative impact of these forces due to their well-documented behavioral ecology, strict habitat requirements, and exceptionally slow life history. We investigated the phylogeographic patterns and evolutionary history of orangutans in the light of the complex geological and climatic history of the Sunda archipelago. Our study is based on the most extensive genetic sampling to date, covering the entire range of extant orangutan populations. Using data from three mitochondrial DNA (mtDNA) genes from 112 wild orangutans, we show that Sumatran orangutans, Pongo abelii, are paraphyletic with respect to Bornean orangutans (P. pygmaeus), the only other currently recognized species within this genus. The deepest split in the mtDNA phylogeny of orangutans occurs across the Toba caldera in northern Sumatra and, not as expected, between both islands. Until the recent past, the Toba region has experienced extensive volcanic activity, which has shaped the current phylogeographic patterns. Like their Bornean counterparts, Sumatran orangutans exhibit a strong, yet previously undocumented structuring into four geographical clusters. However, with 3.50 Ma, the Sumatran haplotypes have a much older coalescence than their Bornean counterparts (178 kya). In sharp contrast to the mtDNA data, 18 Y-chromosomal polymorphisms show a much more recent coalescence within Sumatra compared with Borneo. Moreover, the deep geographic structure evident in mtDNA is not reflected in the male population history, strongly suggesting male-biased dispersal. We conclude that volcanic activities have played an important role in the evolutionary history of orangutans and potentially of many other forest-dwelling Sundaland species. Furthermore, we demonstrate that a strong sex bias in dispersal can lead to conflicting patterns in uniparentally inherited markers even at a genus-wide scale, highlighting the need for a combined usage of maternally and paternally inherited marker systems in phylogenetic studies.     

Enamel thickness in Bornean and Sumatran orangutan dentitions

Dental enamel thickness has received considerable attention in ecological models of the adaptive significance of primate morphology. Several authors have theorized that the degree of enamel thickness may reflect selective pressures related to the consumption of fallback foods (dietary items that may require complex processing and/or have low nutritional value) during times of preferred food scarcity. Others have speculated that enamel thickness reflects selection during mastication of foods with particular material properties (i.e., toughness and hardness). Orangutans prefer ripe fruit when available, but show interspecific and sex differences in the consumption of fallback foods (bark, leaves, and figs) and other preferred foods (certain seeds). Bornean orangutans (Pongo pygmaeus) have also been reported to masticate more mechanically demanding foods than Sumatran orangutans (Pongo abelii). To test these ecological models, we assessed two-dimensional enamel thickness in orangutan full dentitions using established histological and virtual quantification methods. No significant differences in average enamel thickness (AET) were found between species. We found significant differences in the components of enamel thickness indices between sexes, with males showing greater enamel-dentine junction lengths and dentine core areas, and thus relatively thinner enamel than females. Comparisons of individuals of known sex and species revealed a dentition-wide trend for Bornean females to show greater AET than Sumatran females. Differences between small samples of males were less evident. These data provide only limited support for ecological explanations of enamel thickness patterns within great ape genera. Future studies of dietary ecology and enamel thickness should consider sex differences more systematically.     

Fertility and mortality patterns of captive Bornean and Sumatran orangutans: is there a species difference in life history?

Across broad taxonomic groups, life history models predict that increased ecological predictability will lead to conservative investment in reproductive effort. Within species, however, organisms are predicted to have increased reproductive rates under improved environmental conditions. It is not clear how these models apply to closely-related species. In this paper, we examine predictions from these models as applied to variability in reproductive rates between the two species of orangutans, Pongo pygmaeus (Bornean) and Pongo abelii (Sumatran). Orangutans exhibit characteristics of a "slow" life history strategy with large bodies, late age at maturity, low reproductive rates, and long lifespan. Recently, researchers proposed that Sumatran orangutans may have an even slower life history than Bornean orangutans as a result of ecological and genetic differences (Wich et al., 2004). We examined this hypothesis by studying important aspects of life history of both species under conditions of relative ecological stability, in captivity. In this large dataset, there were no significant species differences in age of first or last reproduction, completed fertility, perinatal and postnatal mortality, or female longevity. Bornean orangutans in captivity did have significantly longer interbirth intervals, and male Bornean orangutans had higher survival past maturity. Our results do not support the hypothesis that selection has led to decreased reproductive effort under conditions of increased habitat quality in Sumatra (Wich et al., 2004), and instead suggest that phenotypic flexibility may be particularly important in explaining differences between closely related species.     

Use of limestone karst forests by Bornean orangutans (Pongo pygmaeus morio) in the Sangkulirang peninsula, east Kalimantan, Indonesia

The Indonesian province of East Kalimantan is home to some of the largest remaining contiguous tracts of lowland Dipterocarp forest on the island of Borneo. Nest surveys recently conducted in these forests indicated the presence of a substantial population of Eastern Bornean orangutans (Pongo pygmaeus morio) in the Berau and East Kutai regencies in the northern half of the province. The Sangkulirang Peninsula contains extensive limestone karst forests in close proximity to the lowland Dipterocarp forests inhabited by orangutans in these regencies. Orangutans have been sighted in these limestone karst forests, but the importance of this forest type for orangutans has been unclear. Therefore, we conducted 49 km of nest surveys in limestone karst forest to obtain the first quantitative estimates of orangutan densities in this habitat, and walked 28 km of surveys in nearby lowland Dipterocarp forests for comparison. We also gathered basic ecological data along our transects in an attempt to identify correlates of orangutan abundance across these habitat types. Undisturbed limestone karst forests showed the lowest orangutan densities (147 nests/km(2), 0.82 indiv/km(2)), disturbed limestone forests had intermediate densities (301 nests/km(2), 1.40 indiv/km(2)), and undisturbed lowland Dipterocarp forests contained the highest density (987 nests/km(2), 5.25 indiv/km(2)), significantly more than the undisturbed limestone karst forests. This difference was not correlated with variation in liana abundance, fig stem density, or stump density (an index of forest disturbance). Therefore, other factors, such as the relatively low tree species diversity of limestone karst forests, may explain why orangutans appear to avoid these areas. We conclude that limestone karst forests are of low relevance for safeguarding the future of orangutans in East Kalimantan.     

Treatment of disseminated Strongyloides spp. infection in an infant Sumatran orangutan (Pongo abelii)

Strongyloides nematodes have been reported in all species of great apes with orangutans ≤5 years old most susceptible to severe clinical disease. This brief communication describes the first published case of antemortem diagnosis and treatment of disseminated strongyloidiasis in a clinically affected 5‐month‐old Sumatran orangutan (Pongo abelii).     

Molecular genetic divergence of orang utan (Pongo pygmaeus) subspecies based on isozyme and two-dimensional gel electrophoresis

The orang utan (Pongo pygmaeus), as currently recognized, includes two geographically separated subspecies: Pongo pygmaeus pygmaeus, which resides on Borneo, and P. p. abelii, which inhabits Sumatra. At present, there is no known route of gene flow between the two populations except through captive individuals which have been released back into the wild over the last several decades. The two subspecies are differentiated by morphological and behavioral characters, and they can be distinguished by a subspecies specific pericentric chromosomal inversion. Nei-genetic distances were estimated between orang utan subspecies, gorilla, chimpanzee and humans using 44 isozyme loci and using 458 soluble fibroblast proteins which were resolved by two-dimensional gel electrophoresis. Phenetic analysis of both data sets supports the following conclusions: the orang utan subspecies distances are approximately 10 times closer to each other than they are to the African apes, and the orang utan subspecies are approximately as divergent as are the two chimpanzee species. Comparison of the genetic distances to genetic distance estimates done in the same laboratory under identical conditions reveals that the distance between Bornean vs. Sumatran orang utans is 5-10 times the distance measured between several pairs of subspecies including lions, cheetahs, and tigers. Near species level molecular genetic distances between orang utan subspecies would support the separate management of Bornean and Sumatran orang utans as evolutionary significant units (Ryder 1987). Evolutionary topologies were constructed from the distance data using both cladistic and phenetic methods. The majority of resulting trees affirmed previous molecular evolutionary studies that indicated that man and chimpanzee diverged from a common ancestor subsequent to the divergence of gorilla from the common ancestor.     

The phylogeography of orangutan foamy viruses supports the theory of ancient repopulation of Sumatra

Phylogenetic analysis of foamy virus sequences obtained from Bornean and Sumatran orangutans showed a distinct clustering pattern. One subcluster was represented by both Bornean and Sumatran orangutan simian foamy viruses (SFV). Combined analysis of host mitochondrial DNA and SFV phylogeny provided evidence for the hypothesis of the repopulation of Sumatra by orangutans from Borneo.     

Chromosome studies in the orangutan (Pongo pygmaeus): Practical applications for breeding and conservation

The unequivocal identification of Bornean, Sumatran, and first-generation hybrid orangutans can be carried out by chromosome analysis, a procedure that is more reliable than any other so far used to distinguish between orangutan subspecies. Chromosome differences between subspecies have been compared with protein and DNA studies, and these have shown that Bornean and Sumatran orangutans are more different from each other than we originally thought. Chromosome studies in the orangutan have shown variant chromosome types that are not subspecies-specific. One of these variant types is a product of a complex double inversion rearrangement and is a polymorphic trait in both subspecies. In view of our findings, specific guidelines have been recommended for evaluating the fertility of hybrid specimens and maintaining purebred orangutan stocks.     

Inferring Pongo conservation units: a perspective based on microsatellite and mitochondrial DNA analyses

In order to define evolutionarily significant and management units (ESUs and MUs) among subpopulations of Sumatran (Pongo pygmaeus abelii) and Bornean (P. p. pygmaeus) orangutans we determined their genetic relationships. We analyzed partial sequences of four mitochondrial genes and nine autosomal microsatellite loci of 70 orangutans to test two hypotheses regarding the population structure within Borneo and the genetic distinction between Bornean and Sumatran orangutans. Our data show Bornean orangutans consist of two genetic clusters—the western and eastern clades. Each taxon exhibits relatively distinct mtDNA and nuclear genetic distributions that are likely attributable to genetic drift. These groups, however, do not warrant designations as separate conservation MUs because they demonstrate no demographic independence and only moderate genetic differentiation. Our findings also indicate relatively high levels of overall genetic diversity within Borneo, suggesting that observed habitat fragmentation and erosion during the last three decades had limited influence on genetic variability. Because the mtDNA of Bornean and Sumatran orangutans are not strictly reciprocally monophyletic, we recommend treating these populations as separate MUs and discontinuing inter-island translocation of animals unless absolutely necessary.     

Locomotor behavior of wild orangutans (Pongo pygmaeus wurmbii) in disturbed peat swamp forest, Sabangau, Central Kalimantan, Indonesia

This study examined the locomotor behavior of wild Bornean orangutans (P. p. wurmbii) in an area of disturbed peat swamp forest (Sabangau Catchment, Indonesia) in relation to the height in the canopy, age-sex class, behavior (feeding or traveling), and the number of supports used to bear body mass. Backward elimination log-linear modeling was employed to expose the main influences on orangutan locomotion. Our results showed that the most important distinctions with regard to locomotion were between suspensory and compressive, or, orthograde (vertical trunk) and pronograde (horizontal trunk) behavior. Whether orangutans were traveling or feeding had the most important influence on locomotion whereby compressive locomotion had a strong association with feeding, suspensory locomotion had a strong association with travel in the peripheral strata using multiple supports, whereas vertical climb/descent and oscillation showed a strong association with travel on single supports in the core stratum. In contrast to theoretical predictions on positional behavior and body size, age-sex category had a limited influence on locomotion. The study revealed that torso orthograde suspension dominates orangutan locomotion, concurring with previous studies in dipterocarp forest. But, orangutans in the Sabangau exhibited substantially higher frequencies of oscillatory locomotion than observed at other sites, suggesting this behavior confers particular benefits for traversing the highly compliant arboreal environment typical of disturbed peat swamp forest. In addition, torso pronograde suspensory locomotion was observed at much lower levels than in the Sumatran species. Together these results highlight the necessity for further examination of differences between species, which control for habitat.     

Parasites found from the feces of Bornean orangutans in Danum Valley, Sabah, Malaysia, with a redescription of Pongobius hugoti and the description of a new species of Pongobius (Nematoda: Oxyuridae)

In order to obtain basic data on parasitic infections of Bornean orangutans, Pongo pygmaeus morio (Owen, 1837), in Danum Valley, Sabah, Malaysia, fecal examinations were conducted. Based on a total of 73 fecal samples from 25 individuals, cysts of Entamoeba coli, Entamoeba spp., and Chilomastix mesnili, cysts and trophozoites of Balantidium coli, and eggs of Trichuris sp. or spp., unknown strongylid(s), Strongyloides fuelleborni, and an unknown oxyurid, plus a rhabditoid larva of Strongyloides sp., were found. Mature and immature worms of Pongobius hugoti Baru? et al., 2007 and Pongobius foitovae n. sp. (Oxyuridae: Enterobiinae) were recovered from fecal debris and described. Pongobius foitovae is readily distinguished from P. hugoti by having a much longer esophageal corpus, a longer and distally hooked spicule in males, and a more posteriorly positioned vulva in female. Presence of plural species of non- Enterobius pinworms is a remarkable feature of the orangutan-pinworm relationship, which may reflect speciation process of the orangutans, host switching, and coevolution by pinworms.     

Bornean orangutans on the brink of protein bankruptcy

Protein is a limiting resource that is essential to the growth, maintenance and reproduction of tropical frugivores, yet few studies have examined how wild animals maintain protein balance. During chronic periods of fruit scarcity, Bornean orangutans (Pongo pygmaeus) often catabolize their own fat reserves despite unusually low metabolic requirements. Such energy deficits suggest a marginal existence, and raise the possibility that orangutans also endure periods of negative protein balance. To test this hypothesis, we conducted the first study of protein cycling in a wild primate. Our five year analysis of urinary metabolites revealed evidence of protein recycling when fruit was scarce. During these periods, orangutans consumed more leaves and bark, proteinaceous but tough foods that yielded a mean daily intake of 1.4 g protein kg(-1) metabolic mass. Such an amount is inadequate for humans and one-tenth the intake of mountain gorillas, but sufficient to avert, perhaps narrowly, a severe protein deficit. Our findings highlight the functional and adaptive value of traits that maximize protein assimilation during periods of ecological exigency.     

Tool-use and tool-making by captive, group-living orangutans (Pongo pygmaeus abelii) at an artificial termite mound

The present study examined the use and making of tools to obtain foodstuffs in artificial-mound holes by five captive, group-living Sumatran orangutans (Pongo pygmaeus abelii). Three adult orangutans frequently stripped leaves and twigs from a branch provided (tool-making), and then inserted the tool into a hole to obtain foodstuffs (tool-using). A 5-year-old female juvenile usually used the tools that adult orangutans had previously used, but rarely made tools herself. A 2-year-old male infant did not use any tools. The adult orangutans tend to leave one to several leaves at the top of the branch than to leave many leaves on the branch or to strip all leaves. It seemed likely that tools with appropriate leaves are easier to insert into holes and obtain more foodstuffs, compared with branches with many leaves or sticks without any leaves. When the orangutans were unable to insert a tool into a hole, they usually modified the tool and/or changed their tool-using technique, such as changing how they grasped the tool. These findings are discussed from the perspectives of the orangutan's behavioral flexibility regarding tool-use skills and hierarchical organization in food-processing techniques.     

Forest Structure and Support Availability Influence Orangutan Locomotion in Sumatra and Borneo

The influence of habitat structure and support availability on support use is an important aspect of understanding locomotor behavior in arboreal primates. We compared habitat structure and support availability in three orangutan study sites—two on Sumatra (Pongo abelii) in the dry‐lowland forest of Ketambe and peat swamp forest of Suaq Balimbing, and one on Borneo (Pongo pygmaeus wurmbii) in the disturbed peat swamp forest of Sabangau—to better understand orangutan habitat use. Our analysis revealed vast differences in tree and liana density between the three sites. Sabangau had a much higher overall tree density, although both Sumatran sites had a higher density of larger trees. The two peat swamp forests were more similar to each other than to Ketambe, particularly with regard to support availability. Ketambe had a wider variety of supports of different sizes and types, and a higher density of larger lianas than the two peat swamps. Orangutans in all three sites did not differ substantially in terms of their preferred supports, although Sumatran orangutans had a strong tendency to use lianas, not observed in Sabangau. Differences in observed frequencies of locomotor behavior suggest the homogeneous structure of Sabangau limits the locomotor repertoire of orangutans, with high frequencies of fewer behaviors, whereas the wider range of supports in Ketambe appears to have facilitated a more varied locomotor repertoire. There were no differences among age‐sex classes in the use of arboreal pathways in Suaq Balimbing, where orangutans selected larger trees than were typically available. This was less apparent in Sabangau, where orangutans generally used trees in relation to their environmental abundance, reflecting the homogeneous nature of disturbed peat swamp forest. These results demonstrate that forest architecture has an important influence on orangutan locomotion, which may become increasingly important as the structure of orangutan habitat continues to be altered through human disturbance. Am. J. Primatol. 74:1128‐1142, 2012. © 2012 Wiley Periodicals, Inc.     

Food material properties and mandibular load resistance abilities in large-bodied hominoids

Numerous comparative studies have sought to demonstrate a functional link between feeding behavior, diet, and mandibular form in primates. In lieu of data on the material properties of foods ingested and masticated, many investigators have relied on qualitative dietary classifications such as "folivore" or "frugivore." Here we provide the first analysis of the relationship between jaw form, dietary profiles, and food material properties in large-bodied hominoids. We employed ratios of area moments of inertia and condylar area to estimate moments imposed on the mandible in order to evaluate and compare the relative ability to counter mandibular loads among central Bornean orangutans (Pongo pygmaeus wurmbii), Virunga mountain gorillas (Gorilla beringei beringei), and east African chimpanzees (Pan troglodytes schweinfurthii). We used data on elastic modulus (E) of fruit, fracture toughness (R) of fruit, leaves, and non-fruit, non-leaf vegetation, and derived fragmentation indices ( radicalR/E and radicalER), as proxies for bite force. We generated bending and twisting moments (forcexmoment arm) for various mandibular loading behaviors using food material properties to estimate minimally required bite forces. Based on E and R of foods ingested and masticated, we hypothesized improved resistance to mandibular loads in Pongo p. wurmbii compared to the African apes, and in G. b. beringei compared to Pan t. schweinfurthii. Results reveal that our predictions are borne out only when bite forces are estimated from maximum R of non-fruit, non-leaf vegetation. For all other tissues and material properties results were contrary to our predictions. Importantly, as food material properties change, the moments imposed on the mandible change; this, in turn, alters the entire ratio of relative load resistance to moment. The net effect is that species appear over- or under-designed for the moments imposed on the mandible. Our hypothesis, therefore, is supported only if we accept that maximum R of these vegetative tissues represents the relevant mechanical property influencing the magnitude of neuromuscular activity, food fragmentation, and mandibular morphology. A general implication is that reliable estimates of average and maximum bite forces from food material properties require that the full range of tissues masticated be tested. Synthesizing data on ingestive and masticatory behaviors, the number of chewing cycles associated with a given food, and food mechanical properties, should inform the broader question of which foods and feeding behaviors are most influential on the mandibular loading environment.