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.

A practical approach with drones, smartphones, and tracking tags for potential real-time animal tracking.

Drones are increasingly used for fauna monitoring and wildlife tracking; however, their application for wildlife tracking is restricted by developing such systems. Here we explore the potential of drones for wildlife tracking using an off-the-shelf system that is easy to use by non-specialists consisting of a multirotor drone, smartphones, and commercial tracking devices via Bluetooth and Ultra-Wide Band (UWB). We present the system configuration, explore the operational parameters that can affect detection capabilities, and test the effectiveness of the system for locating targets by simulating target animals in savanna and forest environments. The self-contained tracking system was built without hardware or software customization. In 40 tracking flights carried out in the Brazilian Cerrado, we obtained a detection rate of 90% in savanna and 40% in forest areas. Tests for targets in movement (N = 20), the detection rates were 90% in the savanna and 30% in the forest areas. The spatial accuracy obtained by the system was 14.61 m, being significantly more accurate in savanna ( x ¯ = 10.53) than in forest areas ( x ¯ = 13.06). This approach to wildlife tracking facilitates the use of drones by non-specialists at an affordable cost for conservation projects with limited resources. The reduced size of the tags, the long battery life, and the lower cost compared to GPS-tags open up a range of opportunities for animal tracking.

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.

Effectiveness of 20 years of conservation investments in protecting orangutans.

Conservation strategies are rarely systematically evaluated, which reduces transparency, hinders the cost-effective deployment of resources, and hides what works best in different contexts. Using data on the iconic and critically endangered orangutan (Pongo spp.), we developed a novel spatiotemporal framework for evaluating conservation investments. We show that around USD 1 billion was invested between 2000 and 2019 into orangutan conservation by governments, nongovernmental organizations, companies, and communities. Broken down by allocation to different conservation strategies, we find that habitat protection, patrolling, and public outreach had the greatest return on investment for maintaining orangutan populations. Given the variability in threats, land-use opportunity costs, and baseline remunerations in different regions, there were differential benefits per dollar invested across conservation activities and regions. We show that although challenging from a data and analysis perspective, it is possible to fully understand the relationships between conservation investments and outcomes and the external factors that influence these outcomes. Such analyses can provide improved guidance toward a more effective biodiversity conservation. Insights into the spatiotemporal interplays between the costs and benefits driving effectiveness can inform decisions about the most suitable orangutan conservation strategies for halting population declines. Although our study focuses on the three extant orangutan species of Sumatra and Borneo, our findings have broad application for evidence-based conservation science and practice worldwide.

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.

Disease Risk and Conservation Implications of Orangutan Translocations.

Critically Endangered orangutans are translocated in several situations: reintroduced into historic range where no wild populations exist, released to reinforce existing wild populations, and wild-to-wild translocated to remove individuals from potentially risky situations. Translocated orangutans exposed to human diseases, including Coronavirus Disease 2019 (COVID-19), pose risks to wild and previously released conspecifics. Wildlife disease risk experts recommended halting great ape translocations during the COVID-19 pandemic to minimize risk of disease transmission to wild populations. We collected data on orangutan releases and associated disease risk management in Indonesia during the COVID-19 pandemic, and developed a problem description for orangutan disease and conservation risks. We identified that at least 15 rehabilitated ex-captive and 27 wild captured orangutans were released during the study period. Identified disease risks included several wild-to-wild translocated orangutans in direct contact or proximity to humans without protective equipment, and formerly captive rehabilitated orangutans that have had long periods of contact and potential exposure to human diseases. While translocation practitioners typically employ mitigation measures to decrease disease transmission likelihood, these measures cannot eliminate all risk, and are not consistently applied. COVID-19 and other diseases of human origin can be transmitted to orangutans, which could have catastrophic impacts on wild orangutans, other susceptible fauna, and humans should disease transmission occur. We recommend stakeholders conduct a Disease Risk Analysis for orangutan translocation, and improve pathogen surveillance and mitigation measures to decrease the likelihood of potential outbreaks. We also suggest refocusing conservation efforts on alternatives to wild-to-wild translocation including mitigating human-orangutan interactions, enforcing laws and protecting orangutan habitats to conserve orangutans in situ.

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.

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.

Correction: Ecological correlates of chimpanzee (Pan troglodytes schweinfurthii) density in Mahale Mountains National Park, Tanzania.

[This corrects the article DOI: 10.1371/journal.pone.0246628.].

Measuring disturbance at swift breeding colonies due to the visual aspects of a drone: a quasi-experiment study.

There is a growing body of research indicating that drones can disturb animals. However, it is usually unclear whether the disturbance is due to visual or auditory cues. Here, we examined the effect of drone flights on the behavior of great dusky swifts Cypseloides senex and white-collared swifts Streptoprocne zonaris in 2 breeding sites where drone noise was obscured by environmental noise from waterfalls and any disturbance must be largely visual. We performed 12 experimental flights with a multirotor drone at different vertical, horizontal, and diagonal distances from the colonies. From all flights, 17% caused <1% of birds to temporarily abandon the breeding site, 50% caused half to abandon, and 33% caused more than half to abandon. We found that the diagonal distance explained 98.9% of the variability of the disturbance percentage and while at distances >50 m the disturbance percentage does not exceed 20%, at <40 m the disturbance percentage increase to > 60%. We recommend that flights with a multirotor drone during the breeding period should be conducted at a distance of >50 m and that recreational flights should be discouraged or conducted at larger distances (e.g. 100 m) in nesting birds areas such as waterfalls, canyons, and caves.

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.

Ecological correlates of chimpanzee (Pan troglodytes schweinfurthii) density in Mahale Mountains National Park, Tanzania.

Understanding the ecological factors that drive animal density patterns in time and space is key to devising effective conservation strategies. In Tanzania, most chimpanzees (~75%) live outside national parks where human activities threaten their habitat's integrity and connectivity. Mahale Mountains National Park (MMNP), therefore, is a critical area for chimpanzees (Pan troglodytes schweinfurthii) in the region due to its location and protective status. Yet, despite its importance and long history of chimpanzee research (>50 years), a park-wide census of the species has never been conducted. The park is categorized as a savanna-woodland mosaic, interspersed with riparian forest, wooded grassland, and bamboo thicket. This heterogeneous landscape offers an excellent opportunity to assess the ecological characteristics associated with chimpanzee density, a topic still disputed, which could improve conservation plans that protect crucial chimpanzee habitat outside the park. We examined the influence of fine-scale vegetative characteristics and topographical features on chimpanzee nest density, modeling nest counts using hierarchical distance sampling. We counted 335 nests in forest and woodland habitats across 102 transects in 13 survey sites. Nests were disproportionately found more in or near evergreen forests, on steep slopes, and in feeding tree species. We calculated chimpanzee density in MMNP to be 0.23 ind/km2, although density varied substantially among sites (0.09-3.43 ind/km2). Density was associated with factors related to the availability of food and nesting trees, with topographic heterogeneity and the total basal area of feeding tree species identified as significant positive predictors. Species-rich habitats and floristic diversity likely play a principal role in shaping chimpanzee density within a predominately open landscape with low food abundance. Our results provide valuable baseline data for future monitoring efforts in MMNP and enhance our understanding of this endangered species' density and distribution across Tanzania.

The historical range and drivers of decline of the Tapanuli orangutan.

The Tapanuli Orangutan (Pongo tapanuliensis) is the most threatened great ape species in the world. It is restricted to an area of about 1,000 km2 of upland forest where fewer than 800 animals survive in three declining subpopulations. Through a historical ecology approach involving analysis of newspaper, journals, books and museum records from the early 1800s to 2009, we demonstrate that historically Pongo tapanuliensis inhabited a much larger area, and occurred across a much wider range of habitat types and at lower elevations than now. Its current Extent of Occurrence is 2.5% and 5.0% of the historical range in the 1890s and 1940s respectively. A combination of historical fragmentation of forest habitats, mostly for small-scale agriculture, and unsustainable hunting likely drove various populations to the south, east and west of the current population to extinction. This happened prior to the industrial-scale forest conversion that started in the 1970s. Our findings indicate how sensitive P. tapanuliensis is to the combined effects of habitat fragmentation and unsustainable take-off rates. Saving this species will require prevention of any further fragmentation and killings or other removal of animals from the remaining population. Without concerted action to achieve this, the remaining populations of P. tapanuliensis are doomed to become extinct within several orangutan generations.

The environmental impacts of palm oil in context.

Delivering the Sustainable Development Goals (SDGs) requires balancing demands on land between agriculture (SDG 2) and biodiversity (SDG 15). The production of vegetable oils and, in particular, palm oil, illustrates these competing demands and trade-offs. Palm oil accounts for ~40% of the current global annual demand for vegetable oil as food, animal feed and fuel (210 Mt), but planted oil palm covers less than 5-5.5% of the total global oil crop area (approximately 425 Mha) due to oil palm's relatively high yields. Recent oil palm expansion in forested regions of Borneo, Sumatra and the Malay Peninsula, where >90% of global palm oil is produced, has led to substantial concern around oil palm's role in deforestation. Oil palm expansion's direct contribution to regional tropical deforestation varies widely, ranging from an estimated 3% in West Africa to 50% in Malaysian Borneo. Oil palm is also implicated in peatland draining and burning in Southeast Asia. Documented negative environmental impacts from such expansion include biodiversity declines, greenhouse gas emissions and air pollution. However, oil palm generally produces more oil per area than other oil crops, is often economically viable in sites unsuitable for most other crops and generates considerable wealth for at least some actors. Global demand for vegetable oils is projected to increase by 46% by 2050. Meeting this demand through additional expansion of oil palm versus other vegetable oil crops will lead to substantial differential effects on biodiversity, food security, climate change, land degradation and livelihoods. Our Review highlights that although substantial gaps remain in our understanding of the relationship between the environmental, socio-cultural and economic impacts of oil palm, and the scope, stringency and effectiveness of initiatives to address these, there has been little research into the impacts and trade-offs of other vegetable oil crops. Greater research attention needs to be given to investigating the impacts of palm oil production compared to alternatives for the trade-offs to be assessed at a global scale.

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.

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.

Tourist photographs as a scalable framework for wildlife monitoring in protected areas.

Protected areas are critical to conservation efforts in the face of rapid biodiversity declines [1]. Yet the resources for conservation are often limited and shared amongst many competing priorities [2]. As a consequence, even basic monitoring surveys are absent within most protected areas [3]. Although a range of wildlife monitoring methods exist, considerable focused survey effort is often required to yield accurate and precise estimates [4]. This makes monitoring difficult to sustain or replicate, limiting access to the data required for evidence-based conservation decisions. Citizen-scientists have been proposed as an important complement to the finite resources available for basic monitoring within protected areas [5]; however, the full potential of this approach has yet to be realised. Wildlife tourists and guides are especially focussed on encountering and photographing fauna and flora, yet the data collected in these efforts is rarely harnessed for conservation monitoring within protected areas. A detailed understanding of photographic tourism's potential role in wildlife monitoring has been lacking, but is essential for the development of new tools to harness the data being collected through tourism. Here, we demonstrate that tourist-contributed data can aid wildlife monitoring in protected areas by providing population estimates of large carnivores comparable to those from traditional survey methods. Our approach could capitalize upon the immense number of wildlife photographs being taken daily as part of the global > 30-billion USD, wildlife-based tourism industry.

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.