Impacts of fire and prospects for recovery in a tropical peat forest ecosystem.

Uncontrolled fires place considerable burdens on forest ecosystems, compromising our ability to meet conservation and restoration goals. A poor understanding of the impacts of fire on ecosystems and their biodiversity exacerbates this challenge, particularly in tropical regions where few studies have applied consistent analytical techniques to examine a broad range of ecological impacts over multiyear time frames. We compiled 16 y of data on ecosystem properties (17 variables) and biodiversity (21 variables) from a tropical peatland in Indonesia to assess fire impacts and infer the potential for recovery. Burned forest experienced altered structural and microclimatic conditions, resulting in a proliferation of nonforest vegetation and erosion of forest ecosystem properties and biodiversity. Compared to unburned forest, habitat structure, tree density, and canopy cover deteriorated by 58 to 98%, while declines in species diversity and abundance were most pronounced for trees, damselflies, and butterflies, particularly for forest specialist species. Tracking ecosystem property and biodiversity datasets over time revealed most to be sensitive to recurrent high-intensity fires within the wider landscape. These megafires immediately compromised water quality and tree reproductive phenology, crashing commercially valuable fish populations within 3 mo and driving a gradual decline in threatened vertebrates over 9 mo. Burned forest remained structurally compromised long after a burn event, but vegetation showed some signs of recovery over a 12-y period. Our findings demonstrate that, if left uncontrolled, fire may be a pervasive threat to the ecological functioning of tropical forests, underscoring the importance of fire prevention and long-term restoration efforts, as exemplified in Indonesia.

Sociality predicts orangutan vocal phenotype.

In humans, individuals' social setting determines which and how language is acquired. Social seclusion experiments show that sociality also guides vocal development in songbirds and marmoset monkeys, but absence of similar great ape data has been interpreted as support to saltational notions for language origin, even if such laboratorial protocols are unethical with great apes. Here we characterize the repertoire entropy of orangutan individuals and show that in the wild, different degrees of sociality across populations are associated with different 'vocal personalities' in the form of distinct regimes of alarm call variants. In high-density populations, individuals are vocally more original and acoustically unpredictable but new call variants are short lived, whereas individuals in low-density populations are more conformative and acoustically consistent but also exhibit more complex call repertoires. Findings provide non-invasive evidence that sociality predicts vocal phenotype in a wild great ape. They prove false hypotheses that discredit great apes as having hardwired vocal development programmes and non-plastic vocal behaviour. Social settings mould vocal output in hominids besides humans.

Genetic characterization of nodular worm infections in Asian Apes.

Parasitic nematodes of Oesophagostomum spp., commonly known, as 'nodular worms' are emerging as the most widely distributed and prevalent zoonotic nematodes. Oesophagostomum infections are well documented in African non-human primates; however, the taxonomy, distribution and transmission of Oesophagostomum in Asian non-human primates are not adequately studied. To better understand which Oesophagostomum species infect Asian non-human primates and determine their phylogeny we analysed 55 faecal samples from 50 orangutan and 5 gibbon individuals from Borneo and Sumatra. Both microscopy and molecular results revealed that semi-wild animals had higher Oesophagostomum infection prevalence than free ranging animals. Based on sequence genotyping analysis targeting the Internal transcribed spacer 2 of rDNA, we report for the first time the presence of O. aculeatum in Sumatran apes. Population genetic analysis shows that there is significant genetic differentiation between Bornean and Sumatran O. aculeatum populations. Our results clearly reveal that O. aculeatum in free-ranging animals have a higher genetic variation than those in semi-wild animals, demonstrating that O. aculeatum is circulating naturally in wildlife and zoonotic transmission is possible. Further studies should be conducted to better understand the epidemiology and dynamics of Oesophagostomum transmission between humans, non-human primates and other wild species and livestock in Southeast Asia.

Entamoeba histolytica infections in wild and semi-wild orangutans in Sumatra and Kalimantan.

Key to the success of orangutan conservation management practices is the prevention of the introduction of infectious diseases to the remaining populations. Previous reports of Entamoeba spp. positive orangutans are of concern as Entamoeba spp. infection has been linked to morbidity and mortality in primates. It remains to be determined if the Entamoeba species infecting orangutans is the pathogenic Entamoeba histolytica. Orangutan fecal samples have been collected from orangutans from sites in Sumatra (Bukit Lawang, Ketambe, and Suaq, 241 samples from 64 individuals), and two sites in Kalimantan (Sebangau and Tuanan, 129 samples from 39 individuals). All samples were from wild orangutans except for a proportion from Sumatra which were from semi-wild (108 samples, 10 individuals). E. histolytica-specific nested PCR assays were carried out on the fecal samples. A total of 36 samples from 17 individuals tested positive for E. histolytica. When compared with published sequences using NCBI BLAST the E. histolytica positive samples showed a 98-99% concordance. The majority (76%, n = 36) of the positive isolates came from semi-wild orangutans in Bukit Lawang. This study supports the growing body of evidence that contact with humans is an important risk factor for infection of wild primates with E. histolytica.

The slow ape: High infant survival and long interbirth intervals in wild orangutans.

Orangutans (Pongo spp.) are reported to have extremely slow life histories, including the longest average interbirth intervals of all mammals. Such slow life history can be viable only when unavoidable mortality is kept low. Thus, orangutans' survivorship under natural conditions is expected to be extremely high. Previous estimates of orangutan life history were based on captive individuals living under very different circumstances or on small samples from wild populations. Here, we combine birth data from seven field sites, each with demographic data collection for at least 10 years (range 12-43 years) on wild orangutans to better document their life history. Using strict criteria for data inclusion, we calculated infant survival, interbirth intervals and female age at first reproduction, across species, subspecies and islands. We found an average closed interbirth interval of 7.6 years, as well as consistently very high pre-weaning survival for males and females. Female survival of 94% until age at first birth (at around age 15 years) was higher than reported for any other mammal species under natural conditions. Similarly, annual survival among parous females is very high, but longevity remains to be estimated. Current data suggest no major life history differences between Sumatran and Bornean orangutans. The high offspring survival is remarkable, noting that modern human populations seem to have reached the same level of survival only in the 20th century. The orangutans' slow life history illustrates what can be achieved if a hominoid bauplan is exposed to low unavoidable mortality. Their high survival is likely due to their arboreal and non-gregarious lifestyle, and has allowed them to maintain viable populations, despite living in low-productivity habitats. However, their slow life history also implies that orangutans are highly vulnerable to a catastrophic population crash in the face of drastic habitat change.

An ecophysiologically informed model of seed dispersal by orangutans: linking animal movement with gut passage across time and space.

Fauna-mediated ecosystem service provision (e.g. seed dispersal) can be difficult to quantify and predict because it is underpinned by the shifting niches of multiple interacting organisms. Such interactions are especially complex in tropical ecosystems, including endangered peat forests of Central Borneo, a biodiversity hot spot and home to the critically endangered orangutan (Pongo pygmaeus wurmbii). We combined studies of the digestive physiology of captive orangutans in Australia with detailed field studies of wild orangutans in the Natural Laboratory of Peat-Swamp Forest of Sabangau, Central Kalimantan, Indonesia. By measuring the gut transit time (TT) of indigestible seed mimics (beads) in captivity and applying this as a temporal constraint to movement data of wild orangutans, we developed a mechanistic, time-explicit spatial model to project the seed dispersal patterns by these large-bodied, arboreal frugivores. We followed seven orangutans and established home range kernels using Time Local Convex Hull (T-LoCoH) modelling. This allowed us to model individual orangutan movements and to adjust these models according to gut transit times to estimate seed dispersal kernels. Female movements were conservative (core ranges of 55 and 52 ha in the wet and dry seasons, respectively) and revisitation rates to the same location of n = 4 in each 24-h block. Male movements were more unpredictable, yielding fragmented core ranges and revisitation rates to the same location of only 1.2 times each 24 h; males also demonstrated large disjunctions where they moved rapidly over long distances and were frequently lost from view. Seed dispersal kernels were nested predictably within the core ranges of females, but not males. We used the T-LoCoH approach to analyse movement ecology, which offered a powerful tool to predict the primary deposition of seeds by orangutans, thereby providing a reliable method for making a priori predictions of seed dispersal dynamics by other frugivores in novel ecosystems.

Acoustic Characteristics of Long Calls Produced by Male Orang-Utans (Pongo pygmaeus wurmbii): Advertising Individual Identity, Context, and Travel Direction.

Acoustic characteristics and context of the long-distance call of male orang-utans (Pongo pygmaeus wurmbii) were examined in a population of orang-utans from Central Kalimantan, Borneo. Male orang-utans produced long calls under different circumstances, including calls made spontaneously, in response to conspecifics, when accompanied by a snag crash and when travelling with a female. It was shown by acoustic analyses that there was individual discrimination between the male's calls, discrimination between the calls made under different contexts, and between calls from one individual from different years, which coincided with a change in his dominance status. We also confirm that flanged male orang-utans advertise their intended travel route, by long calling in the direction of their travel. If other orang-utans (males and females) within ear shot of the caller can identify the caller from their long call, and even obtain information about the context and status of the individual, they can then therefore choose whether to approach or avoid them. Thus, males seem to be using their long call to announce their presence, allowing them to orient themselves spatially to other orang-utans, and, potentially, to co-ordinate a network of loose associations between both males and females in the area.

Prevalence of Cryptosporidium spp., Enterocytozoon bieneusi, Encephalitozoon spp. and Giardia intestinalis in Wild, Semi-Wild and Captive Orangutans (Pongo abelii and Pongo pygmaeus) on Sumatra and Borneo, Indonesia.

BACKGROUND: Orangutans are critically endangered primarily due to loss and fragmentation of their natural habitat. This could bring them into closer contact with humans and increase the risk of zoonotic pathogen transmission. AIMS: To describe the prevalence and diversity of Cryptosporidium spp., microsporidia and Giardia intestinalis in orangutans at seven sites on Sumatra and Kalimantan, and to evaluate the impact of orangutans' habituation and location on the occurrence of these zoonotic protists. RESULT: The overall prevalence of parasites in 298 examined animals was 11.1%. The most prevalent microsporidia was Encephalitozoon cuniculi genotype II, found in 21 animals (7.0%). Enterocytozoon bieneusi genotype D (n = 5) and novel genotype Pongo 2 were detected only in six individuals (2.0%). To the best of our knowledge, this is the first report of these parasites in orangutans. Eight animals were positive for Cryptosporidium spp. (2.7%), including C. parvum (n = 2) and C. muris (n = 6). Giardia intestinalis assemblage B, subtype MB6, was identified in a single individual. While no significant differences between the different human contact level groups (p = 0.479-0.670) or between the different islands (p = 0.992) were reported in case of E. bieneusi or E. cuniculi, Cryptosporidium spp. was significantly less frequently detected in wild individuals (p < 2×10-16) and was significantly more prevalent in orangutans on Kalimantan than on Sumatra (p < 2×10-16). CONCLUSION: Our results revealed that wild orangutans are significantly less frequently infected by Cryptosporidium spp. than captive and semi-wild animals. In addition, this parasite was more frequently detected at localities on Kalimantan. In contrast, we did not detect any significant difference in the prevalence of microsporidia between the studied groups of animals. The sources and transmission modes of infections were not determined, as this would require repeated sampling of individuals, examination of water sources, and sampling of humans and animals sharing the habitat with orangutans.

Nutritional Differences between Two Orangutan Habitats: Implications for Population Density.

Bottom-up regulatory factors have been proposed to exert a strong influence on mammalian population density. Studies relating habitat quality to population density have typically made comparisons among distant species or communities without considering variation in food quality among localities. We compared dietary nutritional quality of two Bornean orangutan populations with differing population densities in peatland habitats, Tuanan and Sabangau, separated by 63 km. We hypothesized that because Tuanan is alluvial, the plant species included in the orangutan diet would be of higher nutritional quality compared to Sabangau, resulting in higher daily caloric intake in Tuanan. We also predicted that forest productivity would be greater in Tuanan compared to Sabangau. In support of these hypotheses, the overall quality of the diet and the quality of matched dietary items were higher in Tuanan, resulting in higher daily caloric intake compared to Sabangau. These differences in dietary nutritional quality may provide insights into why orangutan population density is almost two times greater in Tuanan compared to Sabangau, in agreement with a potentially important influence of diet quality on primate population density.

Meat-eating by a wild Bornean orang-utan (Pongo pygmaeus).

We present the first evidence for consumption of meat by a wild Bornean orang-utan (Pongo pygmaeus). Meat-eating has been reported in Sumatran orang-utans, specifically the hunting and consumption of slow lorises (Nycticebus coucang), but loris-hunting behaviour has not been observed in the Bornean species and meat of any species is essentially absent from their diet, with only two anecdotal reports of vertebrate meat consumption prior to this current finding in over 40 years of study. In August 2012 an unhabituated adult flanged male orang-utan was observed eating an adult horse-tailed squirrel (Sundasciurus hippurus) carcass in the Sabangau peat-swamp forest, Central Kalimantan. We suspect this to be a case of scavenging, never reported previously in a Bornean orang-utan.

Fine-scale habitat use by orang-utans in a disturbed peat swamp forest, central Kalimantan, and implications for conservation management.

This study was conducted to see how orang-utans (Pongo pygmaeus wurmbii) were coping with fine-scale habitat disturbance in a selectively logged peat swamp forest in Central Kalimantan, Borneo. Seven habitat classes were defined, and orang-utans were found to use all of these, but were selective in their preference for certain classes over others. Overall, the tall forest classes (≥20 m) were preferred. They were preferred for feeding, irrespective of canopy connectivity, whereas classes with a connected canopy (canopy cover ≥75%), irrespective of canopy height, were preferred for resting and nesting, suggesting that tall trees are preferred for feeding and connected canopy for security and protection. The smaller forest classes (≤10 m high) were least preferred and were used mainly for travelling from patch to patch. Thus, selective logging is demonstrated here to be compatible with orang-utan survival as long as large food trees and patches of primary forest remain. Logged forest, therefore, should not automatically be designated as 'degraded'. These findings have important implications for forest management, forest classification and the designation of protected areas for orang-utan conservation.

Interactions between a wild Bornean orang-utan and a Philippine slow loris in a peat-swamp forest.

All documented orang-utan-loris interactions have been from Sumatra, where lorises were opportunistically preyed upon by orang-utans. In this paper, we describe two accounts of the Bornean orang-utan (Pongo pygmaeus wurmbii) interacting with the Philippine slow loris (Nycticebus menagensis). The interactions were by two adolescent female orang-utans. No attempts to catch the loris were observed on either occasion. Neither interaction was hostile. During the second observation, which was more detailed, we considered the behaviour to be play rather than aggression or attempted predation. Based upon the lack of interest from the adult females during these rare encounters, we propose that the behaviour represents play or non-aggressive exploration rather than predation.

The risk of disease to great apes: simulating disease spread in orang-utan (Pongo pygmaeus wurmbii) and chimpanzee (Pan troglodytes schweinfurthii) association networks.

All great ape species are endangered, and infectious diseases are thought to pose a particular threat to their survival. As great ape species vary substantially in social organisation and gregariousness, there are likely to be differences in susceptibility to disease types and spread. Understanding the relation between social variables and disease is therefore crucial for implementing effective conservation measures. Here, we simulate the transmission of a range of diseases in a population of orang-utans in Sabangau Forest (Central Kalimantan) and a community of chimpanzees in Budongo Forest (Uganda), by systematically varying transmission likelihood and probability of subsequent recovery. Both species have fission-fusion social systems, but differ considerably in their level of gregariousness. We used long-term behavioural data to create networks of association patterns on which the spread of different diseases was simulated. We found that chimpanzees were generally far more susceptible to the spread of diseases than orang-utans. When simulating different diseases that varied widely in their probability of transmission and recovery, it was found that the chimpanzee community was widely and strongly affected, while in orang-utans even highly infectious diseases had limited spread. Furthermore, when comparing the observed association network with a mean-field network (equal contact probability between group members), we found no major difference in simulated disease spread, suggesting that patterns of social bonding in orang-utans are not an important determinant of susceptibility to disease. In chimpanzees, the predicted size of the epidemic was smaller on the actual association network than on the mean-field network, indicating that patterns of social bonding have important effects on susceptibility to disease. We conclude that social networks are a potentially powerful tool to model the risk of disease transmission in great apes, and that chimpanzees are particularly threatened by infectious disease outbreaks as a result of their social structure.

Predicting the vulnerability of great apes to disease: the role of superspreaders and their potential vaccination.

Disease is a major concern for the conservation of great apes, and one that is likely to become increasingly relevant as deforestation and the rise of ecotourism bring humans and apes into ever closer proximity. Consequently, it is imperative that preventative measures are explored to ensure that future epidemics do not wipe out the remaining populations of these animals. In this paper, social network analysis was used to investigate vulnerability to disease in a population of wild orang-utans and a community of wild chimpanzees. Potential 'superspreaders' of disease--individuals with disproportionately central positions in the community or population--were identified, and the efficacy of vaccinating these individuals assessed using simulations. Three resident female orang-utans were identified as potential superspreaders, and females and unflanged males were predicted to be more influential in disease spread than flanged males. By contrast, no superspreaders were identified in the chimpanzee network, although males were significantly more central than females. In both species, simulating the vaccination of the most central individuals in the network caused a greater reduction in potential disease pathways than removing random individuals, but this effect was considerably more pronounced for orang-utans. This suggests that targeted vaccinations would have a greater impact on reducing disease spread among orang-utans than chimpanzees. Overall, these results have important implications for orang-utan and chimpanzee conservation and highlight the role that certain individuals may play in the spread of disease and its prevention by vaccination.

Call cultures in orang-utans?

BACKGROUND: Several studies suggested great ape cultures, arguing that human cumulative culture presumably evolved from such a foundation. These focused on conspicuous behaviours, and showed rich geographic variation, which could not be attributed to known ecological or genetic differences. Although geographic variation within call types (accents) has previously been reported for orang-utans and other primate species, we examine geographic variation in the presence/absence of discrete call types (dialects). Because orang-utans have been shown to have geographic variation that is not completely explicable by genetic or ecological factors we hypothesized that this will be similar in the call domain and predict that discrete call type variation between populations will be found. METHODOLOGY/PRINCIPAL FINDINGS: We examined long-term behavioural data from five orang-utan populations and collected fecal samples for genetic analyses. We show that there is geographic variation in the presence of discrete types of calls. In exactly the same behavioural context (nest building and infant retrieval), individuals in different wild populations customarily emit either qualitatively different calls or calls in some but not in others. By comparing patterns in call-type and genetic similarity, we suggest that the observed variation is not likely to be explained by genetic or ecological differences. CONCLUSION/SIGNIFICANCE: These results are consistent with the potential presence of 'call cultures' and suggest that wild orang-utans possess the ability to invent arbitrary calls, which spread through social learning. These findings differ substantially from those that have been reported for primates before. First, the results reported here are on dialect and not on accent. Second, this study presents cases of production learning whereas most primate studies on vocal learning were cases of contextual learning. We conclude with speculating on how these findings might assist in bridging the gap between vocal communication in non-human primates and human speech.

Evolutionary optimization of material properties of a tropical seed.

Here, we show how the mechanical properties of a thick-shelled tropical seed are adapted to permit them to germinate while preventing their predation. The seed has evolved a complex heterogeneous microstructure resulting in hardness, stiffness and fracture toughness values that place the structure at the intersection of these competing selective constraints. Analyses of different damage mechanisms inflicted by beetles, squirrels and orangutans illustrate that cellular shapes and orientations ensure damage resistance to predation forces imposed across a broad range of length scales. This resistance is shown to be around the upper limit that allows cracking the shell via internal turgor pressure (i.e. germination). Thus, the seed appears to strike an exquisitely delicate adaptive balance between multiple selection pressures.

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.

Effects of Pleistocene glaciations and rivers on the population structure of Bornean orangutans (Pongo pygmaeus).

Sundaland, a tropical hotspot of biodiversity comprising Borneo and Sumatra among other islands, the Malay Peninsula, and a shallow sea, has been subject to dramatic environmental processes. Thus, it presents an ideal opportunity to investigate the role of environmental mechanisms in shaping species distribution and diversity. We investigated the population structure and underlying mechanisms of an insular endemic, the Bornean orangutan (Pongo pygmaeus). Phylogenetic reconstructions based on mtDNA sequences from 211 wild orangutans covering the entire range of the species indicate an unexpectedly recent common ancestor of Bornean orangutans 176 ka (95% highest posterior density, 72-322 ka), pointing to a Pleistocene refugium. High mtDNA differentiation among populations and rare haplotype sharing is consistent with a pattern of strong female philopatry. This is corroborated by isolation by distance tests, which show a significant correlation between mtDNA divergence and distance and a strong effect of rivers as barriers for female movement. Both frequency-based and Bayesian clustering analyses using as many as 25 nuclear microsatellite loci revealed a significant separation among all populations, as well as a small degree of male-mediated gene flow. This study highlights the unique effects of environmental and biological features on the evolutionary history of Bornean orangutans, a highly endangered species particularly vulnerable to future climate and anthropogenic change as an insular endemic.

Methods for calculating activity budgets compared: a case study using orangutans.

The results of comparisons of behavioral data between individuals, age-sex classes, seasons, sites and possibly even species may depend on sample size and the computational method used. To establish whether these are valid concerns, we compared results for percentage time spent feeding on major food types (fruit, leaves, flowers, invertebrates, bark, pith and other) for two orangutan populations in Sabangau (24 months) and Tuanan (29 months), Indonesian Borneo. Both the minimum follow limit included in analyses and the computational method used produced small, but statistically significant, differences in the results obtained, and the differences were more common for food types eaten less frequently. In addition, using different computational methods produced more significant differences than did including different minimum follow lengths in analyses. The computational method used also influenced the results of tests for differences in diet composition between age-sex classes. Thus, the method used can influence the results obtained and, hence, it is important to state explicitly the minimum follow limit included and computational method used to compile averages, and to ensure standardization in methods when comparing data between age-sex classes, time periods, field sites or species.