Measuring and modelling microclimatic air temperature in a historically degraded tropical forest.

Climate change is predicted to cause widespread disruptions to global biodiversity. Most climate models are at the macroscale, operating at a ~ 1 km resolution and predicting future temperatures at 1.5-2 m above ground level, making them unable to predict microclimates at the scale that many organisms experience temperature. We studied the effects of forest structure and vertical position on microclimatic air temperature within forest canopy in a historically degraded tropical forest in Sikundur, Northern Sumatra, Indonesia. We collected temperature measurements in fifteen plots over 20 months, alongside vegetation structure data from the same fifteen 25 × 25 m plots. We also performed airborne surveys using an unmanned aerial vehicle (UAV) to record canopy structure remotely, both over the plot locations and a wider area. We hypothesised that old-growth forest structure would moderate microclimatic air temperature. Our data showed that Sikundur is a thermally dynamic environment, with simultaneously recorded temperatures at different locations within the canopy varying by up to ~ 15 °C. Our models (R2 = 0.90 to 0.95) showed that temperature differences between data loggers at different sites were largely determined by variation in recording height and the amount of solar radiation reaching the topmost part of the canopy, although strong interactions between these abiotic factors and canopy structure shaped microclimate air temperature variation. The impacts of forest degradation have smaller relative influence on models of microclimatic air temperature than abiotic factors, but the loss of canopy density increases temperature. This may render areas of degraded tropical forests unsuitable for some forest-dwelling species with the advent of future climate change.

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.

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.

Sleeping trees and sleep-related behaviours of the siamang (Symphalangus syndactylus) in a tropical lowland rainforest, Sumatra, Indonesia.

Sleeping tree selection and related behaviours of a family group and a solitary female siamang (Symphalangus syndactylus) were investigated over a 5-month period in northern Sumatra, Indonesia. We performed all day follows, sleeping tree surveys and forest plot enumerations in the field. We tested whether: (1) physical characteristics of sleeping trees and the surrounding trees, together with siamang behaviours, supported selection based on predation risk and access requirements; (2) the preferences of a solitary siamang were similar to those of a family group; and (3) sleeping site locations within home ranges were indicative of home range defence, scramble competition with other groups or other species, or food requirements. Our data showed that (1) sleeping trees were tall, emergent trees with some, albeit low, connectivity to the neighbouring canopy, and that they were surrounded by other tall trees. Siamangs showed early entry into and departure from sleeping trees, and slept at the ends of branches. These results indicate that the siamangs' choice of sleeping trees and related behaviours were strongly driven by predator avoidance. The observed regular reuse of sleeping sites, however, did not support anti-predation theory. (2) The solitary female displayed selection criteria for sleeping trees that were similar to those of the family group, but she slept more frequently in smaller trees than the latter. (3) Siamangs selected sleeping trees to avoid neighbouring groups, monopolise resources (competition), and to be near their last feeding tree. Our findings indicate selectivity in the siamangs' use of sleeping trees, with only a few trees in the study site being used for this purpose. Any reduction in the availability of such trees might make otherwise suitable habitat unsuitable for these highly arboreal small apes.

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.

Implanted Radio Telemetry in Orangutan Reintroduction and Post-release Monitoring and its Application in Other Ape Species.

Designed as a new method to facilitate the reintroduction and post-release monitoring of orangutans and other apes, implanted radio-telemetry (IRT) was developed and first deployed in 2009. Since that time, it has been necessary to collate and review information on its uptake and general efficacy to inform its ongoing development and that of other emerging tracking technologies. We present here technical specifications and the surgical procedure used to implant miniaturized radio transmitters, as well as a formal testing procedure for measuring detectable transmission distances of implanted devices. Feedback from IRT practitioners (veterinarians and field managers) was gathered through questionnaires and is also presented. To date, IRT has been used in at least 250 individual animals (mainly orangutans) from four species of ape in both Asia and Africa. Median surgical and wound healing times were 30 min and 15 days, respectively, with implants needing to be removed on at least 36 separate occasions. Confirmed failures within the first year of operation were 18.1%, while longer distances were reported from positions of higher elevation relative to the focal animal. IRT has been a transformational technology in facilitating the relocation of apes after their release, resulting in much larger amounts of post-release data collection than ever before. It is crucial however, that implant casings are strengthened to prevent the requirement for recapture and removal surgeries, especially for gradually adapting apes. As with all emerging technological solutions, IRT carries with it inherent risk, especially so due to the requirement for subcutaneous implantation. These risks must, however, be balanced with the realities of releasing an animal with no means of relocation, as has historically been, and is still, the case with orangutans and gorillas.

Morphometric, Behavioral, and Genomic Evidence for a New Orangutan Species.

Six extant species of non-human great apes are currently recognized: Sumatran and Bornean orangutans, eastern and western gorillas, and chimpanzees and bonobos [1]. However, large gaps remain in our knowledge of fine-scale variation in hominoid morphology, behavior, and genetics, and aspects of great ape taxonomy remain in flux. This is particularly true for orangutans (genus: Pongo), the only Asian great apes and phylogenetically our most distant relatives among extant hominids [1]. Designation of Bornean and Sumatran orangutans, P. pygmaeus (Linnaeus 1760) and P. abelii (Lesson 1827), as distinct species occurred in 2001 [1, 2]. Here, we show that an isolated population from Batang Toru, at the southernmost range limit of extant Sumatran orangutans south of Lake Toba, is distinct from other northern Sumatran and Bornean populations. By comparing cranio-mandibular and dental characters of an orangutan killed in a human-animal conflict to those of 33 adult male orangutans of a similar developmental stage, we found consistent differences between the Batang Toru individual and other extant Ponginae. Our analyses of 37 orangutan genomes provided a second line of evidence. Model-based approaches revealed that the deepest split in the evolutionary history of extant orangutans occurred ∼3.38 mya between the Batang Toru population and those to the north of Lake Toba, whereas both currently recognized species separated much later, about 674 kya. Our combined analyses support a new classification of orangutans into three extant species. The new species, Pongo tapanuliensis, encompasses the Batang Toru population, of which fewer than 800 individuals survive. VIDEO ABSTRACT.

Land-cover changes predict steep declines for the Sumatran orangutan (Pongo abelii).

Positive news about Sumatran orangutans is rare. The species is critically endangered because of forest loss and poaching, and therefore, determining the impact of future land-use change on this species is important. To date, the total Sumatran orangutan population has been estimated at 6600 individuals. On the basis of new transect surveys, we estimate a population of 14,613 in 2015. This higher estimate is due to three factors. First, orangutans were found at higher elevations, elevations previously considered outside of their range and, consequently, not surveyed previously. Second, orangutans were found more widely distributed in logged forests. Third, orangutans were found in areas west of the Toba Lake that were not previously surveyed. This increase in numbers is therefore due to a more wide-ranging survey effort and is not indicative of an increase in the orangutan population in Sumatra. There are evidently more Sumatran orangutans remaining in the wild than we thought, but the species remains under serious threat. Current scenarios for future forest loss predict that as many as 4500 individuals could vanish by 2030. Despite the positive finding that the population is double the size previously estimated, our results indicate that future deforestation will continue to be the cause of rapid declines in orangutan numbers. Hence, we urge that all developmental planning involving forest loss be accompanied by appropriate environmental impact assessments conforming with the current national and provincial legislations, and, through these, implement specific measures to reduce or, better, avoid negative impacts on forests where orangutans occur.

Feeding and resting postures of wild northern muriquis (Brachyteles hypoxanthus).

Increased body size in Brachyteles has been regarded as an important evolutionary adaptation that allowed a greater reliance on leaves compared to other more frugivorous Atelidae, but its association with muriqui positional behavior and substrate use is still unknown. Here, we present original data on the feeding and resting postures of the northern muriqui (Brachyteles hypoxanthus) and evaluate predictions about the relationships between body size, postural behavior, and substrate use derived from previously published data for other atelids (e.g. Alouatta, Ateles, and Lagothrix). The study was undertaken from August 2002 to July 2003 on a large group of well-habituated muriquis inhabiting the Reserva Particular do Patrimônio Natural - Felíciano Miguel Abdala in Minas Gerais, Brazil. Consistent with our predictions, we found that B. hypoxanthus was highly suspensory during postural feeding (60.9%) and commonly used tail-hind limb suspension/horizontal tripod (38.0%) or tail-forelimb/hind limb suspension (21.4%). However, although tail-suspensory postures permitted the muriquis to use the terminal canopy and small-sized substrates, these areas were also accessed via tail-assisted above-branch postural behaviors involving multiple substrates. Unexpectedly, tail-suspensory postures were found to be frequently associated with large substrates, tree trunks, and the understory. We suggest that Brachyteles' ability to access food resources from all areas of a feeding tree and from tree crowns at different canopy levels may account for their ability to efficiently exploit food resources in seasonal disturbed forest fragments of the Brazilian Atlantic Forest today.

Human Alzheimer's disease synaptic O-GlcNAc site mapping and iTRAQ expression proteomics with ion trap mass spectrometry.

Neuronal synaptic functional deficits are linked to impaired learning and memory in Alzheimer's disease (AD). We recently demonstrated that O-GlcNAc, a novel cytosolic and nuclear carbohydrate post-translational modification, is enriched at neuronal synapses and positively regulates synaptic plasticity linked to learning and memory in mice. Reduced levels of O-GlcNAc have been observed in AD, suggesting a possible link to deficits in synaptic plasticity. Using lectin enrichment and mass spectrometry, we mapped several human cortical synaptic O-GlcNAc modification sites. Overlap in patterns of O-GlcNAcation between mouse and human appears to be high, as previously mapped mouse synaptic O-GlcNAc sites in Bassoon, Piccolo, and tubulin polymerization promoting protein p25 were identified in human. Novel O-GlcNAc modification sites were identified on Mek2 and RPN13/ADRM1. Mek2 is a signaling component of the Erk 1/2 pathway involved in synaptic plasticity. RPN13 is a component of the proteasomal degradation pathway. The potential interplay of phosphorylation with mapped O-GlcNAc sites, and possible implication of those sites in synaptic plasticity in normal versus AD states is discussed. iTRAQ is a powerful differential isotopic quantitative approach in proteomics. Pulsed Q dissociation (PQD) is a recently introduced fragmentation strategy that enables detection of low mass iTRAQ reporter ions in ion trap mass spectrometry. We optimized LTQ ion trap settings for PQD-based iTRAQ quantitation and demonstrated its utility in O-GlcNAc site mapping. Using iTRAQ, abnormal synaptic expression levels of several proteins previously implicated in AD pathology were observed in addition to novel changes in synaptic specific protein expression including Synapsin II.

Apparent density of the primate calcaneo-cuboid joint and its association with locomotor mode, foot posture, and the "midtarsal break".

Primates use a range of locomotor modes during which they incorporate various foot postures. Humans are unique compared with other primates in that humans lack a mobile fore- and midfoot. Rigidity in the human foot is often attributed to increased propulsive and stability requirements during bipedalism. Conversely, fore- and midfoot mobility in nonhuman primates facilitates locomotion in arboreal settings. Here, we evaluated apparent density (AD) in the subchondral bone of human, ape, and monkey calcanei exhibiting different types of foot loading. We used computed tomography osteoabsorptiometry and maximum intensity projection (MIP) maps to visualize AD in subchondral bone at the cuboid articular surface of calcanei. MIPs represent 3D volumes (of subchondral bone) condensed into 2D images by extracting AD maxima from columns of voxels comprising the volumes. False-color maps are assigned to MIPs by binning pixels in the 2D images according to brightness values. We compared quantities and distributions of AD pixels in the highest bin to test predictions relating AD patterns to habitual locomotor modes and foot posture categories of humans and several nonhuman primates. Nonhuman primates exhibit dorsally positioned high AD concentrations, where maximum compressive loading between the calcaneus and cuboid likely occurs during "midtarsal break" of support. Humans exhibit less widespread areas of high AD, which could reflect reduced fore- and midfoot mobility. Analysis of the internal morphology of the tarsus, such as subchondral bone AD, potentially offers new insights for evaluating primate foot function during locomotion.

A nonradioactive plate-based assay for stimulators of nonspecific DNA nicking by HIV-1 integrase and other nucleases.

Retroviral integrase enzymes have a nonspecific endonuclease activity that is stimulated by certain compounds, suggesting that integrase could be manipulated to damage viral DNA. To identify integrase stimulator (IS) compounds as potential antiviral agents, we have developed a nonradioactive assay that is suitable for high-throughput screening. The assay uses a 49-mer oligonucleotide that is 5'-labeled with a fluorophore, 3'-tagged with a quencher, and designed to form a hairpin that mimics radioactive double-stranded substrates in gel-based nicking assays. Reactions in 384-well plates are analyzed on a real-time PCR machine after a single heat denaturation and subsequent cooling to a point between the melting temperatures of unnicked substrate and nicked products (no cycling is required). Under these conditions, unnicked DNA reforms the hairpin and quenches fluorescence, whereas completely nicked DNA yields a large signal. The assay was linear with time, stimulator concentration, and amount of integrase, and 20% concentrations of the solvent used for many chemical libraries did not interfere with the assay. The assay had an excellent Z' factor, and it reliably detected known IS compounds. This assay, which is adaptable to other nonspecific nucleases, will be useful for identifying additional IS compounds to develop the novel antiviral strategy of stimulating integrase to destroy retroviral DNA.

Identifying amino acid residues that contribute to the cellular-DNA binding site on retroviral integrase.

Although retroviral integrase specifically trims the ends of viral DNA and inserts these ends into any sequence in cellular DNA, little information is available to explain how integrase distinguishes between its two DNA substrates. We recently described novel integrase mutants that were improved for specific nicking of viral DNA but impaired at joining these ends into nonviral DNA. An acidic or bulky substitution at one particular residue was critical for this activity profile, and the prototypic protein--Rous sarcoma virus integrase with an S124D substitution--was defective at nonspecifically binding DNA. We have now characterized 19 (including 16 new) mutants that contain one or more aspartic acid substitutions at residues that extend over the surface of the protein and might participate with residue 124 in binding cellular DNA. In particular, every mutant with an aspartate substitution at residue 98 or 128, similar to the original S124D protein, showed improved specific nicking of viral DNA but disturbed nonspecific nicking of nonviral DNA. These data describe a probable cellular-DNA binding platform that involves at least 5 amino acids, in the following order of importance: 124>128>(98, 125)>123. These experimental data are vital for new models of integrase and will contribute to identifying targets for the next generation of integrase inhibitors.