Barriers to chimpanzee gene flow at the south-east edge of their distribution.

Populations on the edge of a species' distribution may represent an important source of adaptive diversity, yet these populations tend to be more fragmented and are more likely to be geographically isolated. Lack of genetic exchanges between such populations, due to barriers to animal movement, can not only compromise adaptive potential but also lead to the fixation of deleterious alleles. The south-eastern edge of chimpanzee distribution is particularly fragmented, and conflicting hypotheses have been proposed about population connectivity and viability. To address this uncertainty, we generated both mitochondrial and MiSeq-based microsatellite genotypes for 290 individuals ranging across western Tanzania. While shared mitochondrial haplotypes confirmed historical gene flow, our microsatellite analyses revealed two distinct clusters, suggesting two populations currently isolated from one another. However, we found evidence of high levels of gene flow maintained within each of these clusters, one of which covers an 18,000 km2 ecosystem. Landscape genetic analyses confirmed the presence of barriers to gene flow with rivers and bare habitats highly restricting chimpanzee movement. Our study demonstrates how advances in sequencing technologies, combined with the development of landscape genetics approaches, can resolve ambiguities in the genetic history of critical populations and better inform conservation efforts of endangered species.

Understanding External Influences on Target Detection and Classification Using Camera Trap Images and Machine Learning.

Using machine learning (ML) to automate camera trap (CT) image processing is advantageous for time-sensitive applications. However, little is currently known about the factors influencing such processing. Here, we evaluate the influence of occlusion, distance, vegetation type, size class, height, subject orientation towards the CT, species, time-of-day, colour, and analyst performance on wildlife/human detection and classification in CT images from western Tanzania. Additionally, we compared the detection and classification performance of analyst and ML approaches. We obtained wildlife data through pre-existing CT images and human data using voluntary participants for CT experiments. We evaluated the analyst and ML approaches at the detection and classification level. Factors such as distance and occlusion, coupled with increased vegetation density, present the most significant effect on DP and CC. Overall, the results indicate a significantly higher detection probability (DP), 81.1%, and correct classification (CC) of 76.6% for the analyst approach when compared to ML which detected 41.1% and classified 47.5% of wildlife within CT images. However, both methods presented similar probabilities for daylight CT images, 69.4% (ML) and 71.8% (analysts), and dusk CT images, 17.6% (ML) and 16.2% (analysts), when detecting humans. Given that users carefully follow provided recommendations, we expect DP and CC to increase. In turn, the ML approach to CT image processing would be an excellent provision to support time-sensitive threat monitoring for biodiversity conservation.

Orangutan information broadcast via consonant-like and vowel-like calls breaches mathematical models of linguistic evolution.

The origin of language is one of the most significant evolutionary milestones of life on Earth, but one of the most persevering scientific unknowns. Two decades ago, game theorists and mathematicians predicted that the first words and grammar emerged as a response to transmission errors and information loss in language's precursor system, however, empirical proof is lacking. Here, we assessed information loss in proto-consonants and proto-vowels in human pre-linguistic ancestors as proxied by orangutan consonant-like and vowel-like calls that compose syllable-like combinations. We played back and re-recorded calls at increasing distances across a structurally complex habitat (i.e. adverse to sound transmission). Consonant-like and vowel-like calls degraded acoustically over distance, but no information loss was detected regarding three distinct classes of information (viz. individual ID, context and population ID). Our results refute prevailing mathematical predictions and herald a turning point in language evolution theory and heuristics. Namely, explaining how the vocal-verbal continuum was crossed in the hominid family will benefit from future mathematical and computational models that, in order to enjoy empirical validity and superior explanatory power, will be informed by great ape behaviour and repertoire.

Fermented food consumption in wild nonhuman primates and its ecological drivers.

OBJECTIVES: Although fermented food use is ubiquitous in humans, the ecological and evolutionary factors contributing to its emergence are unclear. Here we investigated the ecological contexts surrounding the consumption of fruits in the late stages of fermentation by wild primates to provide insight into its adaptive function. We hypothesized that climate, socioecological traits, and habitat patch size would influence the occurrence of this behavior due to effects on the environmental prevalence of late-stage fermented foods, the ability of primates to detect them, and potential nutritional benefits. MATERIALS AND METHODS: We compiled data from field studies lasting at least 9 months to describe the contexts in which primates were observed consuming fruits in the late stages of fermentation. Using generalized linear mixed-effects models, we assessed the effects of 18 predictor variables on the occurrence of fermented food use in primates. RESULTS: Late-stage fermented foods were consumed by a wide taxonomic breadth of primates. However, they generally made up 0.01%-3% of the annual diet and were limited to a subset of fruit species, many of which are reported to have mechanical and chemical defenses against herbivores when not fermented. Additionally, late-stage fermented food consumption was best predicted by climate and habitat patch size. It was more likely to occur in larger habitat patches with lower annual mean rainfall and higher annual mean maximum temperatures. DISCUSSION: We posit that primates capitalize on the natural fermentation of some fruits as part of a nutritional strategy to maximize periods of fruit exploitation and/or access a wider range of plant species. We speculate that these factors contributed to the evolutionary emergence of the human propensity for fermented foods.

Small room for compromise between oil palm cultivation and primate conservation in Africa.

Despite growing awareness about its detrimental effects on tropical biodiversity, land conversion to oil palm continues to increase rapidly as a consequence of global demand, profitability, and the income opportunity it offers to producing countries. Although most industrial oil palm plantations are located in Southeast Asia, it is argued that much of their future expansion will occur in Africa. We assessed how this could affect the continent's primates by combining information on oil palm suitability and current land use with primate distribution, diversity, and vulnerability. We also quantified the potential impact of large-scale oil palm cultivation on primates in terms of range loss under different expansion scenarios taking into account future demand, oil palm suitability, human accessibility, carbon stock, and primate vulnerability. We found a high overlap between areas of high oil palm suitability and areas of high conservation priority for primates. Overall, we found only a few small areas where oil palm could be cultivated in Africa with a low impact on primates (3.3 Mha, including all areas suitable for oil palm). These results warn that, consistent with the dramatic effects of palm oil cultivation on biodiversity in Southeast Asia, reconciling a large-scale development of oil palm in Africa with primate conservation will be a great challenge.

An Evaluation of the Factors Affecting 'Poacher' Detection with Drones and the Efficacy of Machine-Learning for Detection.

Drones are being increasingly used in conservation to tackle the illegal poaching of animals. An important aspect of using drones for this purpose is establishing the technological and the environmental factors that increase the chances of success when detecting poachers. Recent studies focused on investigating these factors, and this research builds upon this as well as exploring the efficacy of machine-learning for automated detection. In an experimental setting with voluntary test subjects, various factors were tested for their effect on detection probability: camera type (visible spectrum, RGB, and thermal infrared, TIR), time of day, camera angle, canopy density, and walking/stationary test subjects. The drone footage was analysed both manually by volunteers and through automated detection software. A generalised linear model with a logit link function was used to statistically analyse the data for both types of analysis. The findings concluded that using a TIR camera improved detection probability, particularly at dawn and with a 90° camera angle. An oblique angle was more effective during RGB flights, and walking/stationary test subjects did not influence detection with both cameras. Probability of detection decreased with increasing vegetation cover. Machine-learning software had a successful detection probability of 0.558, however, it produced nearly five times more false positives than manual analysis. Manual analysis, however, produced 2.5 times more false negatives than automated detection. Despite manual analysis producing more true positive detections than automated detection in this study, the automated software gives promising, successful results, and the advantages of automated methods over manual analysis make it a promising tool with the potential to be successfully incorporated into anti-poaching strategies.

Palm fruit colours are linked to the broad-scale distribution and diversification of primate colour vision systems.

A long-standing hypothesis in ecology and evolution is that trichromatic colour vision (the ability to distinguish red from green) in frugivorous primates has evolved as an adaptation to detect conspicuous (reddish) fruits. This could provide a competitive advantage over dichromatic frugivores which cannot distinguish reddish colours from a background of green foliage. Here, we test whether the origin, distribution and diversity of trichromatic primates is positively associated with the availability of conspicuous palm fruits, i.e. keystone fruit resources for tropical frugivores. We combine global data of colour vision, distribution and phylogenetic data for more than 400 primate species with fruit colour data for more than 1700 palm species, and reveal that species richness of trichromatic primates increases with the proportion of palm species that have conspicuous fruits, especially in subtropical African forests. By contrast, species richness of trichromats in Asia and the Americas is not positively associated with conspicuous palm fruit colours. Macroevolutionary analyses further indicate rapid and synchronous radiations of trichromats and conspicuous palms on the African mainland starting 10 Ma. These results suggest that the distribution and diversification of African trichromatic primates is strongly linked to the relative availability of conspicuous (versus non-conspicuous) palm fruits, and that interactions between primates and palms are related to the coevolutionary dynamics of primate colour vision systems and palm fruit colours.

Grouping behavior of Sumatran orangutans (Pongo abelii) and Tapanuli orangutans (Pongo tapanuliensis) living in forest with low fruit abundance.

In contrast to the African great apes, orangutans (Pongo spp.) are semisolitary: Individuals are often on their own, but form aggregations more often than expected by chance. These temporary aggregations provide social benefits such as mating opportunities. When fruit availability is high, costs of aggregating should be lower, because competition is less pronounced. Therefore, average party size is expected to be higher when fruit availability is high. This hypothesis would also explain why orangutans in highly fruit-productive habitats on Sumatra are more gregarious than in the usually less productive habitats of Borneo. Here, we describe the aggregation behavior of orangutans in less productive Sumatran habitats (Sikundur and Batang Toru), and compare results with those of previously surveyed field sites. Orangutans in Sikundur were more likely to form parties when fruit availability was higher, but the size of daily parties was not significantly affected by fruit availability. With regard to between-site comparisons, average party sizes of females and alone time of parous females in Sikundur and Batang Toru were substantially lower than those for two previously surveyed Sumatran sites, and both fall in the range of values for Bornean sites. Our results indicate that the assessment of orangutans on Sumatra as being more social than those on Borneo needs revision. Instead, between-site differences in sociality seem to reflect differences in average fruit availability.

A global risk assessment of primates under climate and land use/cover scenarios.

Primates are facing an impending extinction crisis, driven by extensive habitat loss, land use change and hunting. Climate change is an additional threat, which alone or in combination with other drivers, may severely impact those taxa unable to track suitable environmental conditions. Here, we investigate the extent of climate and land use/cover (LUC) change-related risks for primates. We employed an analytical approach to objectively select a subset of climate scenarios, for which we then calculated changes in climatic and LUC conditions for 2050 across primate ranges (N = 426 species) under a best-case scenario and a worst-case scenario. Generalized linear models were used to examine whether these changes varied according to region, conservation status, range extent and dominant habitat. Finally, we reclassified primate ranges based on different magnitudes of maximum temperature change, and quantified the proportion of ranges overall and of primate hotspots in particular that are likely to be exposed to extreme temperature increases. We found that, under the worst-case scenario, 74% of Neotropical forest-dwelling primates are likely to be exposed to maximum temperature increases up to 7°C. In contrast, 38% of Malagasy savanna primates will experience less pronounced warming of up to 3.5°C. About one quarter of Asian and African primates will face up to 50% crop expansion within their range. Primary land (undisturbed habitat) is expected to disappear across species' ranges, whereas secondary land (disturbed habitat) will increase by up to 98%. With 86% of primate ranges likely to be exposed to maximum temperature increases >3°C, primate hotspots in the Neotropics are expected to be particularly vulnerable. Our study highlights the fundamental exposure risk of a large percentage of primate ranges to predicted climate and LUC changes. Importantly, our findings underscore the urgency with which climate change mitigation measures need to be implemented to avert primate extinctions on an unprecedented scale.

Community motivations to engage in conservation behavior to conserve the Sumatran orangutan.

Community-based conservation programs in developing countries are often based on the assumption that heteronomous motivation (e.g., extrinsic incentives such as economic rewards and pressure or coercion to act) will incite local communities to adopt conservation behaviors. However, this may not be as effective or sustainable as autonomous motivations (e.g., an intrinsic desire to act due to inherent enjoyment or self-identification with a behavior and through freedom of choice). We analyzed the comparative effectiveness of heteronomous versus autonomous approaches to community-based conservation programs through a case study of Sumatran orangutan (Pongo abelii) conservation in 3 villages in Indonesia. Each village had a different conservation program design. We surveyed people (n = 240) to determine their motivations for and behavior changes relative to orangutan and orangutan habitat (forest) protection. Heteronomous motivations (e.g., income from tourism) led to greater self-reporting of behavior change toward orangutan protection. However, they did not change self-reported behavior toward forest (i.e., orangutan habitat) protection. The most effective approach to creating self-reported behavior change throughout the community was a combination of autonomous and heteronomous motivations. Individuals who were heteronomously motivated to protect the orangutan were more likely to have changed attitudes than to have changed their self-reported behavior. These findings demonstrate that the current paradigm of motivating communities in developing countries to adopt conservation behaviors primarily through monetary incentives and rewards should consider integrating autonomous motivational techniques that promote the intrinsic values of conservation. Such a combination has a greater potential to achieve sustainable and cost-effective conservation outcomes. Our results highlight the importance of using in-depth sociopsychological analyses to inform the design and implementation of community-based conservation programs.

Anticipated climate and land-cover changes reveal refuge areas for Borneo's orang-utans.

Habitat loss and climate change pose a double jeopardy for many threatened taxa, making the identification of optimal habitat for the future a conservation priority. Using a case study of the endangered Bornean orang-utan, we identify environmental refuges by integrating bioclimatic models with projected deforestation and oil-palm agriculture suitability from the 1950s to 2080s. We coupled a maximum entropy algorithm with information on habitat needs to predict suitable habitat for the present day and 1950s. We then projected to the 2020s, 2050s and 2080s in models incorporating only land-cover change, climate change or both processes combined. For future climate, we incorporated projections from four model and emission scenario combinations. For future land cover, we developed spatial deforestation predictions from 10 years of satellite data. Refuges were delineated as suitable forested habitats identified by all models that were also unsuitable for oil palm - a major threat to tropical biodiversity. Our analyses indicate that in 2010 up to 260,000 km(2) of Borneo was suitable habitat within the core orang-utan range; an 18-24% reduction since the 1950s. Land-cover models predicted further decline of 15-30% by the 2080s. Although habitat extent under future climate conditions varied among projections, there was majority consensus, particularly in north-eastern and western regions. Across projections habitat loss due to climate change alone averaged 63% by 2080, but 74% when also considering land-cover change. Refuge areas amounted to 2000-42,000 km(2) depending on thresholds used, with 900-17,000 km(2) outside the current species range. We demonstrate that efforts to halt deforestation could mediate some orang-utan habitat loss, but further decline of the most suitable areas is to be expected given projected changes to climate. Protected refuge areas could therefore become increasingly important for ongoing translocation efforts. We present an approach to help identify such areas for highly threatened species given environmental changes expected this century.

Acoustic models of orangutan hand-assisted alarm calls.

Orangutans produce alarm calls called kiss-squeaks, which they sometimes modify by putting a hand in front of their mouth. Through theoretical models and observational evidence, we show that using the hand when making a kiss-squeak alters the acoustics of the production in such a way that more formants per kilohertz are produced. Our theoretical models suggest that cylindrical wave propagation is created with the use of the hand and face as they act as a cylindrical extension of the lips. The use of cylindrical wave propagation in animal calls appears to be extremely rare, but is an effective way to lengthen the acoustic system; it causes the number of resonances per kilohertz to increase. This increase is associated with larger animals, and thus using the hand in kiss-squeak production may be effective in exaggerating the size of the producer. Using the hand appears to be a culturally learned behavior, and therefore orangutans may be able to associate the acoustic effect of using the hand with potentially more effective deterrence of predators.

Locating chimpanzee nests and identifying fruiting trees with an unmanned aerial vehicle.

Monitoring of animal populations is essential for conservation management. Various techniques are available to assess spatiotemporal patterns of species distribution and abundance. Nest surveys are often used for monitoring great apes. Quickly developing technologies, including unmanned aerial vehicles (UAVs) can be used to complement these ground-based surveys, especially for covering large areas rapidly. Aerial surveys have been used successfully to detect the nests of orang-utans. It is unknown if such an approach is practical for African apes, which usually build their nests at lower heights, where they might be obscured by forest canopy. In this 2-month study, UAV-derived aerial imagery was used for two distinct purposes: testing the detectability of chimpanzee nests and identifying fruiting trees used by chimpanzees in Loango National Park (Gabon). Chimpanzee nest data were collected through two approaches: we located nests on the ground and then tried to detect them in UAV photos and vice versa. Ground surveys were conducted using line transects, reconnaissance trails, and opportunistic sampling during which we detected 116 individual nests in 28 nest groups. In complementary UAV images we detected 48% of the individual nests (68% of nest groups) in open coastal forests and 8% of individual nests (33% of nest groups) in closed canopy inland forests. The key factor for nest detectability in UAV imagery was canopy openness. Data on fruiting trees were collected from five line transects. In 122 UAV images 14 species of trees (N = 433) were identified, alongside 37 tree species (N = 205) in complementary ground surveys. Relative abundance of common tree species correlated between ground and UAV surveys. We conclude that UAVs have great potential as a rapid assessment tool for detecting chimpanzee presence in forest with open canopy and assessing fruit tree availability. UAVs may have limited applicability for nest detection in closed canopy forest.

Food mechanical properties, feeding ecology, and the mandibular morphology of wild orangutans.

Bornean orangutan mandibular morphology has been functionally linked to the exploitation of hard and tough foods, based on evidence that Pongo pygmaeus wurmbii spends a greater percentage of time feeding on bark, seeds and vegetation compared with Pongo abelii (Sumatran orangutans) and the assumption that these tissues are more challenging to process than fruit pulp. We measured and compared toughness (R) and Young's modulus (E) of ripe and unripe foods exploited by P. abelii and P. p. wurmbii. Additionally, we recorded and compared the percentage of time these orangutans fed on plants/plant parts of varying degrees of R and E. Compared with P. abelii, P. p. wurmbii consumed significantly tougher and more displacement limited (R/E)(0.5) fruit parts, leaves and inner bark, and spent a significantly greater percentage of time feeding on immature leaves, unripe fruit and other vegetation. Modulus did not vary as expected between species, likely because we failed to capture the high-end range of modulus values for tissues consumed by P. p. wurmbii. Notably, P. p. wurmbii spent ∼40% of its feeding time on the toughest foods consumed (between 1000 and 4000 J m(-2)). Thus, the hypothesis that mandibular robusticity in P. p. wurmbii is functionally linked to feeding on tough foods is supported and is likely related to countering relatively larger external forces and/or repetitive loads required to process the toughest tissues. The importance of elastic modulus on morphological divergence awaits future studies capturing the full range of this material property for P. p. wurmbii. Finally, phenophase and fruit availability influence orangutan species differences in food material properties and percentage of time spent feeding on various foods, emphasizing the importance of incorporating these variables in future studies of feeding ecology and craniodental morphology in extant taxa.

Soils on exposed Sunda shelf shaped biogeographic patterns in the equatorial forests of Southeast Asia.

The marked biogeographic difference between western (Malay Peninsula and Sumatra) and eastern (Borneo) Sundaland is surprising given the long time that these areas have formed a single landmass. A dispersal barrier in the form of a dry savanna corridor during glacial maxima has been proposed to explain this disparity. However, the short duration of these dry savanna conditions make it an unlikely sole cause for the biogeographic pattern. An additional explanation might be related to the coarse sandy soils of central Sundaland. To test these two nonexclusive hypotheses, we performed a floristic cluster analysis based on 111 tree inventories from Peninsular Malaysia, Sumatra, and Borneo. We then identified the indicator genera for clusters that crossed the central Sundaland biogeographic boundary and those that did not cross and tested whether drought and coarse-soil tolerance of the indicator genera differed between them. We found 11 terminal floristic clusters, 10 occurring in Borneo, 5 in Sumatra, and 3 in Peninsular Malaysia. Indicator taxa of clusters that occurred across Sundaland had significantly higher coarse-soil tolerance than did those from clusters that occurred east or west of central Sundaland. For drought tolerance, no such pattern was detected. These results strongly suggest that exposed sandy sea-bed soils acted as a dispersal barrier in central Sundaland. However, we could not confirm the presence of a savanna corridor. This finding makes it clear that proposed biogeographic explanations for plant and animal distributions within Sundaland, including possible migration routes for early humans, need to be reevaluated.

Marked population structure and recent migration in the critically endangered Sumatran orangutan (Pongo abelii).

A multitude of factors influence how natural populations are genetically structured, including dispersal barriers, inhomogeneous habitats, and social organization. Such population subdivision is of special concern in endangered species, as it may lead to reduced adaptive potential and inbreeding in local subpopulations, thus increasing the risk of future extinctions. With only 6600 animals left in the wild, Sumatran orangutans (Pongo abelii) are among the most endangered, but also most enigmatic, great ape species. In order to infer the fine-scale population structure and connectivity of Sumatran orangutans, we analyzed the most comprehensive set of samples to date, including mitochondrial hyper-variable region I haplotypes for 123 individuals and genotypes of 27 autosomal microsatellite markers for 109 individuals. For both mitochondrial and autosomal markers, we found a pronounced population structure, caused by major rivers, mountain ridges, and the Toba caldera. We found that genetic diversity and corresponding long-term effective population size estimates vary strongly among sampling regions for mitochondrial DNA, but show remarkable similarity for autosomal markers, hinting at male-driven long-distance gene flow. In support of this, we identified several individuals that were most likely sired by males originating from other genetic clusters. Our results highlight the effect of natural barriers in shaping the genetic structure of great ape populations, but also point toward important dispersal corridors on northern Sumatra that allow for genetic exchange.

Metabolic adaptation for low energy throughput in orangutans.

Energy is the fundamental currency of life--needed for growth, repair, and reproduction--but little is known about the metabolic physiology and evolved energy use strategies of the great apes, our closest evolutionary relatives. Here we report daily energy use in free-living orangutans (Pongo spp.) and test whether observed differences in energy expenditure among orangutans, humans, and other mammals reflect known differences in life history. Using the doubly labeled water method, we measured daily energy expenditure (kCal/d) in orangutans living in a large indoor/outdoor habitat at the Great Ape Trust. Despite activity levels similar to orangutans in the wild, Great Ape Trust orangutans used less energy, relative to body mass, than nearly any eutherian mammal ever measured, including sedentary humans. Such an extremely low rate of energy use has not been observed previously in primates, but is consistent with the slow growth and low rate of reproduction in orangutans, and may be an evolutionary response to severe food shortages in their native Southeast Asian rainforests. These results hold important implications for the management of orangutan populations in captivity and in the wild, and underscore the flexibility and interdependence of physiological, behavioral, and life history strategies in the evolution of apes and humans.

Orangutan (Pongo spp.) whistling and implications for the emergence of an open-ended call repertoire: a replication and extension.

One of the most apparent discontinuities between non-human primate (primate) call communication and human speech concerns repertoire size. The former is essentially fixed to a limited number of innate calls, while the latter essentially consists of numerous learned components. Consequently, primates are thought to lack laryngeal control required to produce learned voiced calls. However, whether they may produce learned voiceless calls awaits investigation. Here, a case of voiceless call learning in primates is investigated--orangutan (Pongo spp.) whistling. In this study, all known whistling orangutans are inventoried, whistling-matching tests (previously conducted with one individual) are replicated with another individual using original test paradigms, and articulatory and acoustic whistle characteristics are compared between three orangutans. Results show that whistling has been reported for ten captive orangutans. The test orangutan correctly matched human whistles with significantly high levels of performance. Whistle variation between individuals indicated voluntary control over the upper lip, lower lip, and respiratory musculature, allowing individuals to produce learned voiceless calls. Results are consistent with inter- and intra-specific social transmission in whistling orangutans. Voiceless call learning in orangutans implies that some important components of human speech learning and control were in place before the homininae-ponginae evolutionary split.