Population status of proboscis monkeys in Balikpapan Bay and their potential survival challenges in Nusantara, the proposed new capital city of Indonesia.

Populations of rare and endangered species are nowadays in peril due to large-scale habitat conversion, and even sizeable and stable populations are confronted with unexpected challenges. We conducted a full census of a proboscis monkey (Nasalis larvatus) population in Balikpapan Bay and located 292 one-male-multifemale units and 67 all-male units in 2022. Using data on average group size, subsampled from Balikpapan Bay, we estimated a total population size of 3907 individuals. The rate of proboscis monkey habitat loss in Balikpapan Bay has been slowing down to the current 0.69% per year. It is predicted that habitat recovery may exceed habitat loss after 13 years. The Indonesian capital city relocation was announced in 2019 with spatial plans designed to cover a total land area of 2,560 km2 across various habitats until 2045. A total number of 1449 individuals (37.08% of the population) were found on 80.55 km2 (41.29%) of habitat that overlapped with current spatial plans of Nusantara Capital city. The construction work just started; before that, the government had already claimed it would be a "smart, green, beautiful, and sustainable city". We, therefore, include our recommendations to mitigate the impact of the construction and to pursue the goal to construct the most sustainable capital city, concerning local biodiversity and thus become a pioneer in a new direction of proboscis monkey conservation.

Age, but not hand preference, is related to personality traits in common marmosets (Callithrix jacchus).

The proximate mechanisms underlying animal personalities, i.e. consistent inter-individual differences in behaviour, are a matter of discussion. Brain lateralization, expressed as the preferred use of the contralateral limb, has been suggested as one of these mechanisms. In this study, we measured a proxy of brain lateralization in captive common marmosets (N = 28) by testing hand preference in a simple food-reaching task and evaluated personality by coding a wide range of behaviours observed in daily situations. We explored the links between personality and both direction and strength of hand preference, as well as age and sex, using linear models. Principal component analysis revealed that the stable behavioural variables were organized in three personality dimensions: Agreeableness, Extraversion and Neuroticism. Regarding hand preference, 14 individuals were left-handed, seven were right-handed and seven were ambilateral. Contrary to our predictions, we did not find any relationship between personality scores and hand preference or sex. Instead, age was a significant predictor of personality scores, with older individuals being more agreeable and less extraverted. The link between brain lateralization and personality seems to be equivocal and dependent on personality and brain lateralization assessment methods. Further examinations of other proximate mechanisms, such as physiology or (epi)genetics, may elucidate what drives personality variation in common marmosets.

Is Malaysia's "mystery monkey" a hybrid between Nasalis larvatus and Trachypithecus cristatus? An assessment of photographs.

Interspecific hybridization in primates is common but hybridization between distantly related sympatric primate species is rarely observed in the wild. We present evidence for a possible hybridization event between Nasalis larvatus and Trachypithecus cristatus in the Lower Kinabatangan Wildlife Sanctuary, Sabah, through assessment of photographs. We used a set of categorical characters and metric measurements to compare the putative hybrid with the likely parent species. Nonmetric comparison showed that this "mystery monkey" is intermediate in several characters. Measurements of limb proportions on photographs showed that the brachial, humerofemoral, and intermembral indexes are above 100 for N. larvatus and below 100 for T. cristatus on all photographs, whereas the crural index is higher than 100 in both species and the distributions of this index in the two species overlap. Brachial and intermembral indices of the putative hybrid were similar to those of N. larvatus. Crural and humerofemoral indices were closer to the values for T. cristatus than those of N. larvatus. Multiple observers confirmed the occurrence of mixed-species groups in the area, and interspecific mating has been photographed. The putative hybrid is now an adult female and was last photographed in September 2020 with an infant and swollen breast, suggesting lactation. We propose further noninvasive fecal sampling for genetic analyses to confirm the origins of this "mystery monkey." This case of hybridization may be related to anthropogenic changes to the landscape, whereby expansion of oil palm plantations confines N. larvatus and T. obscurus to narrow riverine forest patches along the Kinabatangan. This observation therefore also may have conservation implications, indicating limited mate access and dispersal opportunities for these threatened primates. Supplementary Information: The online version contains supplementary material available at 10.1007/s10764-022-00293-z.

A decade of proboscis monkey (Nasalis larvatus) population monitoring in Balikpapan Bay: Confronting predictions with empirical data.

Systematic and well-structured monitoring is essential for taxa with high extinction risk such as primates. Endangered proboscis monkeys Nasalis larvatus are endemic to Borneo, where they are found scattered across lowland habitats of the island, which are under strong anthropogenic pressure. A large population of proboscis monkeys in Balikpapan Bay, Indonesian Borneo, was predicted to decline due to the ongoing habitat loss and degradation, notably because of forest fires. We examined changes in the number and composition of groups of a part of this population from 2007 to 2017, which included a period of forest fires linked to the El Niño-Southern Oscillation events. We conducted a census from a boat; attempting to locate all proboscis monkey groups within the Balikpapan City administrative area in 2007, 2012, and 2017. During the most recent census, we observed a total number of 60 proboscis monkey groups in two subpopulations. The population density was 1.14 group per km2 of suitable habitat. Contrary to previously published predictions, we did not find evidence of a population decline. Contrary to predictions, the 2015 El Niño induced fires impacted mainly forests on ridges and slopes, thus affecting only a small part of the proboscis monkey habitat located close to rivers and mangrove swamps. However, the increasing population density of monkeys, coupled with ongoing habitat degradation and habitat loss in one of the subpopulations, suggests that proboscis monkey population in Balikpapan Bay may be approaching a limit of resilience to habitat changes. In case it proves infeasible to census all individuals in the whole population, we recommend using a group-level census, connected with systematic group counts to obtain a reasonably precise proboscis monkey population size estimate.

Northern lesser galagos (Galago senegalensis) increase the production of loud calls before and at dawn.

Functional explanations for loud calling in nocturnal primates include territorial or sexual advertisement, maintenance of cohesiveness, and group coordination. It is generally accepted that loud calls of lesser galagos (genus Galago) are used for territorial advertisement and long-distance spacing. Field studies suggest that they are uttered at dusk and dawn, when the animals leave and reunite at their sleeping sites. However, empirical validation of these inferences is lacking. We conducted 16-night-long acoustic monitoring of a northern lesser galago (G. senegalensis) population in Senegal and quantified the occurrence of loud calls throughout the night. We hypothesized that significantly more of these calls would be emitted at dusk and dawn if they were used for territorial advertisement and long-distance spacing. This hypothesis was only partially supported, as we found an asymmetrical distribution of loud calls, which significantly increased only before and at dawn. The finding that the relatively early increase in vocal activity was not directly related to approaching and entering sleeping sites suggests that the northern lesser galagos' loud calls differ in function from reassembly calls described for other species of nocturnal primates. Furthermore, the early onset cannot be explained by changes in the intensity of sunlight, moonlight or starlight, which suggests that a different stimulus, most likely internal, elicits early-morning calling behavior in northern lesser galagos.

Complex patterns of grooming and sexual activity in Barbary macaques (Macaca sylvanus).

Grooming in primates is often considered a "currency" that can be exchanged for other "services" or "commodities" such as reciprocal grooming, coalitionary support, infant handling, tolerance around food sources, active food sharing, or mating opportunities. Previous studies on primate grooming-for-sex exchange viewed the males as the demanding class, with the females as suppliers of mating opportunities. In this study, we examine the broader context of grooming-for-mating exchange in Barbary macaques in Gibraltar. Our data show that Barbary macaque males groom females with whom they are mating more frequently and for longer periods than other females, and the relationship between grooming and mating remains significant in both sexual and nonsexual contexts. In addition, females groomed males with whom they were mating more frequently and for longer periods than other males. In both sexes, grooming was observed to be far more frequent and to occur for longer durations in sexual compared to nonsexual contexts. We did not find any difference in grooming behavior between presexual and postsexual contexts. Our data suggest that there is no simple model to describe Barbary macaque grooming patterns in sexual contexts. Although our results are partly consistent with male use of grooming as payment for mating, broadly assessed grooming-mating patterns cannot be solely explained by a male-driven grooming-for-mating exchange.

Author Correction: Long-term carbon sink in Borneo's forests halted by drought and vulnerable to edges.

The original version of this Article contained an error in the third sentence of the abstract and incorrectly read "Here, using long-term plot monitoring records of up to half a century, we find that intact forests in Borneo gained 0.43 Mg C ha-1 year-1 (95% CI 0.14-0.72, mean period 1988-2010) above-ground live biomass", rather than the correct "Here, using long-term plot monitoring records of up to half a century, we find that intact forests in Borneo gained 0.43 Mg C ha-1 year-1 (95% CI 0.14-0.72, mean period 1988-2010) in above-ground live biomass carbon". This has now been corrected in both the PDF and HTML versions of the Article.

Long-term carbon sink in Borneo's forests halted by drought and vulnerable to edge effects.

Less than half of anthropogenic carbon dioxide emissions remain in the atmosphere. While carbon balance models imply large carbon uptake in tropical forests, direct on-the-ground observations are still lacking in Southeast Asia. Here, using long-term plot monitoring records of up to half a century, we find that intact forests in Borneo gained 0.43 Mg C ha-1 per year (95% CI 0.14-0.72, mean period 1988-2010) above-ground live biomass. These results closely match those from African and Amazonian plot networks, suggesting that the world's remaining intact tropical forests are now en masse out-of-equilibrium. Although both pan-tropical and long-term, the sink in remaining intact forests appears vulnerable to climate and land use changes. Across Borneo the 1997-1998 El Niño drought temporarily halted the carbon sink by increasing tree mortality, while fragmentation persistently offset the sink and turned many edge-affected forests into a carbon source to the atmosphere.

Vocal activity of lesser galagos (Galago spp.) at zoos.

Almost nothing is known about the natural vocal behavior of lesser galagos living in zoos. This is perhaps because they are usually kept in nocturnal exhibits separated from the visitors by a transparent and acoustically insulating glass barrier. The aim of the present study was therefore to fill this gap in knowledge of the vocal behavior of lesser galagos from zoos. This knowledge might be beneficial because the vocalizations of these small primates can be used for species determination. We performed a 10-day-long acoustic monitoring of vocal activity in each of seven various groups of Galago senegalensis and G. moholi living at four zoos. We quantitatively evaluated the occurrence of four loud vocalization types present in both species, including the most species-specific advertisement call. We found that qualitative as well as quantitative differences exist in the vocal behavior of the studied groups. We confirmed that the observed vocalization types can be collected from lesser galagos living at zoos, and the success can be increased by selecting larger and more diverse groups. We found two distinct patterns of diel vocal activity in the most vocally active groups. G. senegalensis groups were most vocally active at the beginning and at the end of their activity period, whereas one G. moholi group showed an opposite pattern. The latter is surprising, as it is generally accepted that lesser galagos emit advertisement calls especially at dawn and dusk, i.e., at the beginning and at the end of their diel activity.

Where and how are roads endangering mammals in Southeast Asia's forests?

Habitat destruction and overhunting are two major drivers of mammal population declines and extinctions in tropical forests. The construction of roads can be a catalyst for these two threats. In Southeast Asia, the impacts of roads on mammals have not been well-documented at a regional scale. Before evidence-based conservation strategies can be developed to minimize the threat of roads to endangered mammals within this region, we first need to locate where and how roads are contributing to the conversion of their habitats and illegal hunting in each country. We interviewed 36 experts involved in mammal research from seven Southeast Asian countries to identify roads that are contributing the most, in their opinion, to habitat conversion and illegal hunting. Our experts highlighted 16 existing and eight planned roads - these potentially threaten 21% of the 117 endangered terrestrial mammals in those countries. Apart from gathering qualitative evidence from the literature to assess their claims, we demonstrate how species-distribution models, satellite imagery and animal-sign surveys can be used to provide quantitative evidence of roads causing impacts by (1) cutting through habitats where endangered mammals are likely to occur, (2) intensifying forest conversion, and (3) contributing to illegal hunting and wildlife trade. To our knowledge, ours is the first study to identify specific roads threatening endangered mammals in Southeast Asia. Further through highlighting the impacts of roads, we propose 10 measures to limit road impacts in the region.

Discovery of Miller's Grizzled Langur (Presbytis hosei canicrus) in Wehea Forest confirms the continued existence and extends known geographical range of an endangered primate.

Miller's Grizzled Langur (Presbytis hosei canicrus) is one of the least known and rarest primates in Borneo. With a limited geographic range along the central coast of East Kalimantan and the highly degraded Kutai National Park, its former stronghold, this subspecies is now extremely rare and has been listed as one of the world's 25 most endangered primates. From June 6 to August 2, 2011, we carried out both direct observation and camera trap surveys at two mineral springs (sepans) in the Wehea Forest, East Kutai district, East Kalimantan. Presbytis hosei canicrus was observed at the large sepan on 3 of 6 observation days and at the small sepan on 2 of 3 observation days with up to 11 individuals observed in a single day at a single site. Camera traps recorded a per day capture rate of 0.72 at the small sepan and 0.25 at the large sepan and a per photo capture rate of 0.50 and 0.005, respectively. These data suggest relatively frequent occurrence of P. h. canicrus at the sepans, but the langurs are rarely encountered elsewhere in the Wehea Forest. The discovery of P. h. canicrus in the Wehea Forest confirms the continued existence of this endangered primate and is the first solid evidence demonstrating that its geographic range extends further inland than previously thought. It is not known whether the population of P. h. canicrus within Wehea Forest is large and stable enough to be considered viable, but it is likely part of a larger population that may possibly occur across surrounding protected forests and logging concessions. Surveying this potentially large population, and securing its protection, should be a priority measure for ensuring the continued existence of P. h. canicrus.

Revisiting play elements and self-handicapping in play: a comparative ethogram of five Old World monkey species.

Play behavior has been viewed as a mixture of elements drawn from "serious" behavior, interspersed by ritualized play signals. Two other types of play behaviors have been overlooked: patterns that are dissimilar from any serious behavior and patterns with self-handicapping character, that is, those that put the animal into unnecessary disadvantageous positions or situations. Here the authors show that these 2 types of patterns can constitute a major part of play repertoire. From our own videorecordings and observations, we constructed play ethograms of 5 monkey species (Semnopithecus entellus, Erythrocebus patas, Chlorocebus pygerythrus, Cercopithecus neglectus, and Cercopithecus diana). The authors evaluated the self-handicapping character of each pattern and in Hanuman langurs also the (dis)similarity to serious behavior. Of the 74 patterns in the 5 species, 33 (45%) were judged to have a self-handicapping character. Of 48 patterns observed in langurs, 16 (33%) were totally dissimilar to any serious langur behavior known to us. The authors discuss the possibility that the different types of play elements may have different functions in play.

Personality in free-ranging Hanuman langur (Semnopithecus entellus) males: subjective ratings and recorded behavior.

The authors obtained behavioral observations and personality ratings for 27 free-ranging Hanuman langur males. Subjects were rated using a questionnaire based on the human Five-Factor Model (FFM). Behavioral observations were taken over 5 months using an ethogram that included 50 behaviors. Principal Component Analysis (PCA) of ratings revealed Agreeableness_(R), Confidence_(R), and Extraversion_(R) components. Each personality dimension was associated with a unique set of observed behaviors. PCA of 36 behavioral indices revealed Dominance_(B), Involvement_(B), and Activity_(B) components. Bivariate correlations showed that Agreeableness_(R) was negatively correlated with Dominance_(B); Confidence_(R) was positively correlated with Dominance_(B) and Involvement_(B) but negatively correlated with Activity_(B); and Extraversion_(R) was positively correlated with Activity_(B). Dominance rank was positively correlated with Confidence_(R) and Dominance_(B) but negatively correlated with Agreeableness_(R) and Activity_(B). These results highlight the comparability of behavioral coding and personality ratings and suggest that some aspects of personality structure were present in the common ancestor of Old World monkeys.

Specialized use of two fingers in free-ranging aye-ayes (Daubentonia madagascariensis).

The aye-aye (Daubentonia madagascariensis) possesses a highly specialized hand with two fingers, the third and the fourth, being used in a way unparalleled by any other primate. We observed the use of the third and the fourth fingers in various activities in four free-ranging aye-ayes. We found that the thin third finger was used exclusively or preferably for tapping, inserting into the mouth (probably for cleaning the teeth) and probing for nectar, kernels and insects in bamboo, twigs and live wood. In contrast, the robust fourth finger was used preferably when eating jackfruit (Artocarpus heterophyllus). When probing for invertebrates in soft plant tissues and in dead wood, both fingers were used in high proportions. To extract the contents from coconuts, the two fingers were apparently used for different tasks. From this small (686 observations), but unique, study of free-ranging aye-ayes, we conclude that the third finger appears to be specialized for use in tasks requiring high mobility, sensitivity and precision, whereas the fourth finger appears to be specialized for tasks requiring strength, scooping action and deep access.

Head rotations in the play of Hanuman langurs (Semnopithecus entellus): description and analysis of function.

Although head rotations are frequent patterns in play behavior in many mammalian species and differ from head movements used in other contexts, they have not been quantitatively described and their function remains unclear. The head rotations occurring in the play behavior of free-ranging Hanuman langurs (Semnopithecus entellus) were described from videotaped sequences. The authors tested 2 possible hypotheses about their function. Either the head rotations serve to create unexpected situations and should therefore occur in both solitary and social play and also be very variable, or they serve as play signals and should therefore occur only in social play and be ritualized. If head rotations have both functions, they should be less variable in social play. The data revealed that head rotations were very variable and were present both in solitary and social play. Furthermore, there was no difference in the variability between the head rotations present in the 2 types of play. The results do not support the function of head rotations as play signals but, rather, suggest that head rotations may serve to create unexpected situations in play.