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Vocal acoustics in the endangered proboscis monkey (Nasalis larvatus)

Röper KM, Scheumann M, Wiechert AB, Nathan S, Goossens B, Owren MJ, et al.

Am J Primatol, 2014 Feb;76(2):192-201.
PMID: 24123122 DOI: 10.1002/ajp.22221

The endangered proboscis monkey (Nasalis larvatus) is a sexually highly dimorphic Old World primate endemic to the island of Borneo. Previous studies focused mainly on its ecology and behavior, but knowledge of its vocalizations is limited. The present study provides quantified information on vocal rate and on the vocal acoustics of the prominent calls of this species. We audio-recorded vocal behavior of 10 groups over two 4-month periods at the Lower Kinabatangan Wildlife Sanctuary in Sabah, Borneo. We observed monkeys and recorded calls in evening and morning sessions at sleeping trees along riverbanks. We found no differences in the vocal rate between evening and morning observation sessions. Based on multiparametric analysis, we identified acoustic features of the four common call-types "shrieks," "honks," "roars," and "brays." "Chorus" events were also noted in which multiple callers produced a mix of vocalizations. The four call-types were distinguishable based on a combination of fundamental frequency variation, call duration, and degree of voicing. Three of the call-types can be considered as "loud calls" and are therefore deemed promising candidates for non-invasive, vocalization-based monitoring of proboscis monkeys for conservation purposes.
Fulltext A Longitudinal Study on Feeding Behaviour and Activity Patterns of Released Chimpanzees in Conkouati-Douli National Park, Republic of Congo

Renaud A, Jamart A, Goossens B, Ross C

Animals (Basel), 2013 Jun 07;3(2):532-50.
PMID: 26487416 DOI: 10.3390/ani3020532

Wild chimpanzee populations are still declining due to logging, disease transmission and hunting. The bushmeat trade frequently leads to an increase in the number of orphaned primates. HELP Congo was the first project to successfully release wild-born orphan chimpanzees into an existing chimpanzee habitat. A collection of post monitoring data over 16 years now offers the unique opportunity to investigate possible behavioural adaptations in these chimpanzees. We investigated the feeding and activity patterns in eight individuals via focal observation techniques from 1997-1999 and 2001-2005. Our results revealed a decline in the number of fruit and insect species in the diet of released chimpanzees over the years, whereas within the same period of time, the number of consumed seed species increased. Furthermore, we found a decline in time spent travelling, but an increase in time spent on social activities, such as grooming, as individuals matured. In conclusion, the observed changes in feeding and activity patterns seem to reflect important long-term behavioural and ecological adaptations in wild-born orphan released chimpanzees, demonstrating that the release of chimpanzees can be successful, even if it takes time for full adaptation.
Fulltext Dispersal and genetic structure in a tropical small mammal, the Bornean tree shrew (Tupaia longipes), in a fragmented landscape along the Kinabatangan River, Sabah, Malaysia

Brunke J, Russo IM, Orozco-terWengel P, Zimmermann E, Bruford MW, Goossens B, et al.

BMC Genet, 2020 04 17;21(1):43.
PMID: 32303177 DOI: 10.1186/s12863-020-00849-z

BACKGROUND: Constraints in migratory capabilities, such as the disruption of gene flow and genetic connectivity caused by habitat fragmentation, are known to affect genetic diversity and the long-term persistence of populations. Although negative population trends due to ongoing forest loss are widespread, the consequence of habitat fragmentation on genetic diversity, gene flow and genetic structure has rarely been investigated in Bornean small mammals. To fill this gap in knowledge, we used nuclear and mitochondrial DNA markers to assess genetic diversity, gene flow and the genetic structure in the Bornean tree shrew, Tupaia longipes, that inhabits forest fragments of the Lower Kinabatangan Wildlife Sanctuary, Sabah. Furthermore, we used these markers to assess dispersal regimes in male and female T. longipes.
RESULTS: In addition to the Kinabatangan River, a known barrier for dispersal in tree shrews, the heterogeneous landscape along the riverbanks affected the genetic structure in this species. Specifically, while in larger connected forest fragments along the northern riverbank genetic connectivity was relatively undisturbed, patterns of genetic differentiation and the distribution of mitochondrial haplotypes in a local scale indicated reduced migration on the strongly fragmented southern riverside. Especially, oil palm plantations seem to negatively affect dispersal in T. longipes. Clear sex-biased dispersal was not detected based on relatedness, assignment tests, and haplotype diversity.
CONCLUSION: This study revealed the importance of landscape connectivity to maintain migration and gene flow between fragmented populations, and to ensure the long-term persistence of species in anthropogenically disturbed landscapes.
Fulltext Dispatch from the field: ecology of ground-web-building spiders with description of a new species (Araneae, Symphytognathidae)

Miller JA, Schilthuizen M, Burmester JL, van der Graaf L, Merckx V, Jocqué M, et al.

Biodivers Data J, 2014.
PMID: 24891829 DOI: 10.3897/BDJ.2.e1076

Crassignathadanaugirangensis sp. n. (Araneae: Symphytognathidae) was discovered during a tropical ecology field course held at the Danau Girang Field Centre in Sabah, Malaysia. A taxonomic description and accompanying ecological study were completed as course activities. To assess the ecology of this species, which belongs to the ground-web-building spider community, three habitat types were surveyed: riparian forest, recently inundated riverine forest, and oil palm plantation. Crassignathadanaugirangensis sp. n. is the most abundant ground-web-building spider species in riparian forest; it is rare or absent from the recently inundated forest and was not found in a nearby oil palm plantation. The availability of this taxonomic description may help facilitate the accumulation of data about this species and the role of inundated riverine forest in shaping invertebrate communities.
Dispatch from the field II: the mystery of the red and blue Opadometa male (Araneae, Tetragnathidae, Opadometa sarawakensis)

Miller JA, Freund C, Rambonnet L, Koets L, Barth N, van der Linden C, et al.

Biodivers Data J, 2018.
PMID: 29674940 DOI: 10.3897/BDJ.6.e24777

Background: Males of Opadometa are difficult to associate with conspecific females, and sex-matching errors may persist in the taxonomic literature. Recommended best practices for definitive sex matching in this genus suggest finding a male in the web of a female, or better yet, mating pairs.
New information: A male Opadometa was observed hanging on a frame line of the web of a female Opadometa sarawakensis, a species for which the male was previously undescribed. This occurred during a tropical ecology field course held at the Danau Girang Field Centre in Sabah, Malaysia. A taxonomic description was completed as a course activity.
Fulltext Large male proboscis monkeys have larger noses but smaller canines

Matsuda I, Stark DJ, Saldivar DAR, Tuuga A, Nathan SKSS, Goossens B, et al.

Commun Biol, 2020 09 21;3(1):522.
PMID: 32958853 DOI: 10.1038/s42003-020-01245-0

The uniquely enlarged noses of male proboscis monkeys are prominent adornments, and a sexually selected male trait. A recent study showed significant correlations among nose, body, and testis sizes and clear associations between nose size and the number of females in a male's harem. However, to date, the analyses of other common male traits, i.e., canines, are lacking. Whereas male nose size had a positive correlation with body size, we unexpectedly found a negative correlation between body and canine sizes. We explain this by an interaction between sexual and natural selection. Larger noses in males may interfere with the use of canines, thereby reducing their effectiveness as weapons. Additionally, longer canines are opposed by natural selection because the larger gape it imposes upon its bearer reduces foraging efficiency, particularly in folivores. This unique case of decoupling of body and canine size reveals that large canines carry an ecological cost.
Fulltext Physiological implications of life at the forest interface of oil palm agriculture: blood profiles of wild Malay civets (Viverra tangalunga)

Evans MN, Guerrero-Sanchez S, Kille P, Müller CT, Bakar MSA, Goossens B

Conserv Physiol, 2020;8(1):coaa127.
PMID: 33408869 DOI: 10.1093/conphys/coaa127

Agricultural development is a major threat to global biodiversity, and effective conservation actions are crucial. Physiological repercussions of life alongside human-modified landscapes can undermine adaptable species' health and population viability; however, baseline data are lacking for many wildlife species. We assessed the physiological status of a generalist carnivore, the Malay civet (Viverra tangalunga), persisting within an extensively human-modified system in Sabah, Malaysian Borneo. We characterized hematology and serum biochemistry panels from civets sampled across a mosaic landscape comprising tropical forest fragments and oil palm plantations. Intra-population variation in certain blood parameters were explained by expected biological drivers such as sex, age category and sampling season. Furthermore, we determined several erythrocyte measures, immune cell counts and dietary biochemistry markers significantly varied with proximity to oil palm plantation boundaries. These findings were supported by a case study, whereby blood profiles of GPS collared male civets were contrasted based on their exclusive use of forests or use of oil palm plantations. These data provide robust and valuable first insights into this species' physiological status and suggest agricultural landscapes are impacting the persisting population.
Fulltext The fast-food effect: costs of being a generalist in a human-dominated landscape

Guerrero-Sanchez S, Frias L, Saimin S, Orozco-terWengel P, Goossens B

Conserv Physiol, 2023;11(1):coad055.
PMID: 37588622 DOI: 10.1093/conphys/coad055

Agricultural expansion in Southeast Asia has converted most natural landscapes into mosaics of forest interspersed with plantations, dominated by the presence of generalist species that benefit from resource predictability. Dietary shifts, however, can result in metabolic alterations and the exposure of new parasites that can impact animal fitness and population survival. Our study focuses on the Asian water monitor lizard (Varanus salvator), one of the largest predators in the Asian wetlands, as a model species to understand the health consequences of living in a human-dominated landscape in Sabah, Malaysian Borneo. We evaluated the effects of dietary diversity on the metabolism of monitor lizards and the impact on the composition of their parasite communities in an oil palm-dominated landscape. Our results showed that (1) rodent-dominated diets were associated with high levels of lipids, proteins and electrolytes, akin to a fast-food-based diet of little representativeness of the full nutritional requirements, but highly available, and (2) lizards feeding on diverse diets hosted more diverse parasite communities, however, at overall lower parasite prevalence. Furthermore, we observed that the effect of diet on lipid concentration differed depending on the size of individual home ranges, suggesting that sedentarism plays an important role in the accumulation of cholesterol and triglycerides. Parasite communities were also affected by a homogeneous dietary behaviour, as well as by habitat type. Dietary diversity had a negative effect on both parasite richness and prevalence in plantations, but not in forested areas. Our study indicates that human-dominated landscapes can pose a negative effect on generalist species and hints to the unforeseen health consequences for more vulnerable taxa using the same landscapes. Thus, it highlights the potential role of such a widely distributed generalist as model species to monitor physiological effects in the ecosystem in an oil palm-dominated landscape.
Fulltext Pre-extinction Demographic Stability and Genomic Signatures of Adaptation in the Woolly Rhinoceros

Lord E, Dussex N, Kierczak M, Díez-Del-Molino D, Ryder OA, Stanton DWG, et al.

Curr Biol, 2020 10 05;30(19):3871-3879.e7.
PMID: 32795436 DOI: 10.1016/j.cub.2020.07.046

Ancient DNA has significantly improved our understanding of the evolution and population history of extinct megafauna. However, few studies have used complete ancient genomes to examine species responses to climate change prior to extinction. The woolly rhinoceros (Coelodonta antiquitatis) was a cold-adapted megaherbivore widely distributed across northern Eurasia during the Late Pleistocene and became extinct approximately 14 thousand years before present (ka BP). While humans and climate change have been proposed as potential causes of extinction [1-3], knowledge is limited on how the woolly rhinoceros was impacted by human arrival and climatic fluctuations [2]. Here, we use one complete nuclear genome and 14 mitogenomes to investigate the demographic history of woolly rhinoceros leading up to its extinction. Unlike other northern megafauna, the effective population size of woolly rhinoceros likely increased at 29.7 ka BP and subsequently remained stable until close to the species' extinction. Analysis of the nuclear genome from a ∼18.5-ka-old specimen did not indicate any increased inbreeding or reduced genetic diversity, suggesting that the population size remained steady for more than 13 ka following the arrival of humans [4]. The population contraction leading to extinction of the woolly rhinoceros may have thus been sudden and mostly driven by rapid warming in the Bølling-Allerød interstadial. Furthermore, we identify woolly rhinoceros-specific adaptations to arctic climate, similar to those of the woolly mammoth. This study highlights how species respond differently to climatic fluctuations and further illustrates the potential of palaeogenomics to study the evolutionary history of extinct species.
Morphometric, Behavioral, and Genomic Evidence for a New Orangutan Species

Nater A, Mattle-Greminger MP, Nurcahyo A, Nowak MG, de Manuel M, Desai T, et al.

Curr Biol, 2017 Nov 20;27(22):3487-3498.e10.
PMID: 29103940 DOI: 10.1016/j.cub.2017.09.047

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.
Fulltext Global Demand for Natural Resources Eliminated More Than 100,000 Bornean Orangutans

Voigt M, Wich SA, Ancrenaz M, Meijaard E, Abram N, Banes GL, et al.

Curr Biol, 2018 03 05;28(5):761-769.e5.
PMID: 29456144 DOI: 10.1016/j.cub.2018.01.053

Unsustainable exploitation of natural resources is increasingly affecting the highly biodiverse tropics [1, 2]. Although rapid developments in remote sensing technology have permitted more precise estimates of land-cover change over large spatial scales [3-5], our knowledge about the effects of these changes on wildlife is much more sparse [6, 7]. Here we use field survey data, predictive density distribution modeling, and remote sensing to investigate the impact of resource use and land-use changes on the density distribution of Bornean orangutans (Pongo pygmaeus). Our models indicate that between 1999 and 2015, half of the orangutan population was affected by logging, deforestation, or industrialized plantations. Although land clearance caused the most dramatic rates of decline, it accounted for only a small proportion of the total loss. A much larger number of orangutans were lost in selectively logged and primary forests, where rates of decline were less precipitous, but where far more orangutans are found. This suggests that further drivers, independent of land-use change, contribute to orangutan loss. This finding is consistent with studies reporting hunting as a major cause in orangutan decline [8-10]. Our predictions of orangutan abundance loss across Borneo suggest that the population decreased by more than 100,000 individuals, corroborating recent estimates of decline [11]. Practical solutions to prevent future orangutan decline can only be realized by addressing its complex causes in a holistic manner across political and societal sectors, such as in land-use planning, resource exploitation, infrastructure development, and education, and by increasing long-term sustainability [12]. VIDEO ABSTRACT.
Fulltext Long-Tailed Macaque Response to Deforestation in a Plasmodium knowlesi-Endemic Area

Stark DJ, Fornace KM, Brock PM, Abidin TR, Gilhooly L, Jalius C, et al.

Ecohealth, 2019 12;16(4):638-646.
PMID: 30927165 DOI: 10.1007/s10393-019-01403-9

Land-use changes can impact infectious disease transmission by increasing spatial overlap between people and wildlife disease reservoirs. In Malaysian Borneo, increases in human infections by the zoonotic malaria Plasmodium knowlesi are hypothesised to be due to increasing contact between people and macaques due to deforestation. To explore how macaque responses to environmental change impact disease risks, we analysed movement of a GPS-collared long-tailed macaque in a knowlesi-endemic area in Sabah, Malaysia, during a deforestation event. Land-cover maps were derived from satellite-based and aerial remote sensing data and models of macaque occurrence were developed to evaluate how macaque habitat use was influenced by land-use change. During deforestation, changes were observed in macaque troop home range size, movement speeds and use of different habitat types. Results of models were consistent with the hypothesis that macaque ranging behaviour is disturbed by deforestation events but begins to equilibrate after seeking and occupying a new habitat, potentially impacting human disease risks. Further research is required to explore how these changes in macaque movement affect knowlesi epidemiology on a wider spatial scale.
CamTrapAsia: A dataset of tropical forest vertebrate communities from 239 camera trapping studies

Mendes CP, Albert WR, Amir Z, Ancrenaz M, Ash E, Azhar B, et al.

Ecology, 2024 Apr 22.
PMID: 38650359 DOI: 10.1002/ecy.4299

Information on tropical Asian vertebrates has traditionally been sparse, particularly when it comes to cryptic species inhabiting the dense forests of the region. Vertebrate populations are declining globally due to land-use change and hunting, the latter frequently referred as "defaunation." This is especially true in tropical Asia where there is extensive land-use change and high human densities. Robust monitoring requires that large volumes of vertebrate population data be made available for use by the scientific and applied communities. Camera traps have emerged as an effective, non-invasive, widespread, and common approach to surveying vertebrates in their natural habitats. However, camera-derived datasets remain scattered across a wide array of sources, including published scientific literature, gray literature, and unpublished works, making it challenging for researchers to harness the full potential of cameras for ecology, conservation, and management. In response, we collated and standardized observations from 239 camera trap studies conducted in tropical Asia. There were 278,260 independent records of 371 distinct species, comprising 232 mammals, 132 birds, and seven reptiles. The total trapping effort accumulated in this data paper consisted of 876,606 trap nights, distributed among Indonesia, Singapore, Malaysia, Bhutan, Thailand, Myanmar, Cambodia, Laos, Vietnam, Nepal, and far eastern India. The relatively standardized deployment methods in the region provide a consistent, reliable, and rich count data set relative to other large-scale pressence-only data sets, such as the Global Biodiversity Information Facility (GBIF) or citizen science repositories (e.g., iNaturalist), and is thus most similar to eBird. To facilitate the use of these data, we also provide mammalian species trait information and 13 environmental covariates calculated at three spatial scales around the camera survey centroids (within 10-, 20-, and 30-km buffers). We will update the dataset to include broader coverage of temperate Asia and add newer surveys and covariates as they become available. This dataset unlocks immense opportunities for single-species ecological or conservation studies as well as applied ecology, community ecology, and macroecology investigations. The data are fully available to the public for utilization and research. Please cite this data paper when utilizing the data.
Fulltext Molecular characterization of nodule worm in a community of Bornean primates

Frias L, Stark DJ, Salgado Lynn M, Nathan S, Goossens B, Okamoto M, et al.

Ecol Evol, 2019 Apr;9(7):3937-3945.
PMID: 31015978 DOI: 10.1002/ece3.5022

Strongyles are commonly reported parasites in studies of primate parasite biodiversity. Among them, nodule worm species are often overlooked as a serious concern despite having been observed to cause serious disease in nonhuman primates and humans. In this study, we investigated whether strongyles found in Bornean primates are the nodule worm Oesophagostomum spp., and to what extent these parasites are shared among members of the community. To test this, we propose two hypotheses that use the parasite genetic structure to infer transmission processes within the community. In the first scenario, the absence of parasite genetic substructuring would reflect high levels of parasite transmission among primate hosts, as primates' home ranges overlap in the study area. In the second scenario, the presence of parasite substructuring would suggest cryptic diversity within the parasite genus and the existence of phylogenetic barriers to cross-species transmission. By using molecular markers, we identify strongyles infecting this primate community as O. aculeatum, the only species of nodule worm currently known to infect Asian nonhuman primates. Furthermore, the little to no genetic substructuring supports a scenario with no phylogenetic barriers to transmission and where host movements across the landscape would enable gene flow between host populations. This work shows that the parasite's high adaptability could act as a buffer against local parasite extinctions. Surveys targeting human populations living in close proximity to nonhuman primates could help clarify whether this species of nodule worm presents the zoonotic potential found in the other two species infecting African nonhuman primates.
Fulltext The effect of oil palm-dominated landscapes on the home range and distribution of a generalist species, the Asian water monitor

Guerrero-Sanchez S, Majewski K, Orozco-terWengel P, Saimin S, Goossens B

Ecol Evol, 2022 Jan;12(1):e8531.
PMID: 35127037 DOI: 10.1002/ece3.8531

The Asian water monitor lizard, Varanus salvator, is one of the largest predators in Southeast Asia which persists in human-dominated landscapes and, as such, is a suitable model to understand the behavioral plasticity of generalists in anthropogenic landscapes. We used Local Convex Hull with adaptive algorithm to estimate the home range size of 14 GPS-tagged individuals, followed by a MAXENT approach and community prey composition to understand the habitat preferences within the landscape. We estimated larger home ranges in forest than in oil palm plantations, as well as a larger diversity and abundance of mammals. Core home ranges were always linked to water bodies. However, the use of underproductive oil palm, freshwater swamp forest, and degraded forest by monitor lizards were higher than other kind of vegetation. This suitable habitat is proportionally larger in forest (73.7%) than in oil palm plantations (39.6%). Generalized estimation equation models showed that, while full home range size was negatively associated with the abundance of mammals, core areas depicted a positive association with mammal abundance, as well as with the proportion of suitable habitat within the home range. Besides having smaller home ranges in oil palm plantations, our findings suggest that limited suitable habitat availability forces the Asian water monitor lizard's population to establish only one or very few core areas. Contrastingly, under the protection of forest, they have more core areas, widely dispersed within larger home ranges. We conclude that regardless the plasticity of the species, human-dominated landscapes are altering natural patterns of home range establishment in the monitor lizard's population, creating a potential ecological trap where conditions may not remain favorable for them in the long run. A deeper understanding of the ecological implications on the species and the prey community is advisable.
First report of foregut microbial community in proboscis monkeys: are diverse forests a reservoir for diverse microbiomes?

Hayakawa T, Nathan SKSS, Stark DJ, Saldivar DAR, Sipangkui R, Goossens B, et al.

Environ Microbiol Rep, 2018 12;10(6):655-662.
PMID: 29992728 DOI: 10.1111/1758-2229.12677

Foregut fermentation is well known to occur in a wide range of mammalian species and in a single bird species. Yet, the foregut microbial community of free-ranging, foregut-fermenting monkeys, that is, colobines, has not been investigated so far. We analysed the foregut microbiomes in four free-ranging proboscis monkeys (Nasalis larvatus) from two different tropical habitats with varying plant diversity (mangrove and riverine forests), in an individual from a semi-free-ranging setting with supplemental feeding, and in an individual from captivity, using high-throughput sequencing based on 16S ribosomal RNA genes. We found a decrease in foregut microbial diversity from a diverse natural habitat (riverine forest) to a low diverse natural habitat (mangrove forest), to human-related environments. Of a total of 2700 bacterial operational taxonomic units (OTUs) detected in all environments, only 153 OTUs were shared across all individuals, suggesting that they were not influenced by diet or habitat. These OTUs were dominated by Firmicutes and Proteobacteria. The relative abundance of the habitat-specific microbial communities showed a wide range of differences among living environments, although such bacterial communities appeared to be dominated by Firmicutes and Bacteroidetes, suggesting that those phyla are key to understanding the adaptive strategy in proboscis monkeys living in different habitats.
The price of persistence: Assessing the drivers and health implications of metal levels in indicator carnivores inhabiting an agriculturally fragmented landscape

Evans MN, Waller S, Müller CT, Goossens B, Smith JA, Bakar MSA, et al.

Environ Res, 2022 May 01;207:112216.
PMID: 34656630 DOI: 10.1016/j.envres.2021.112216

Patterns and practices of agricultural expansion threaten the persistence of global biodiversity. Wildlife species surviving large-scale land use changes can be exposed to a suite of contaminants that may deleteriously impact their health. There is a paucity of data concerning the ecotoxicological impacts associated with the global palm oil (Elaeis guineensis) industry. We sampled wild Malay civets (Viverra tangalunga) across a patchwork landscape degraded by oil palm agriculture in Sabah, Malaysian Borneo. Using a non-lethal methodology, we quantified the levels of 13 essential and non-essential metals within the hair of this adaptable small carnivore. We robustly assessed the biological and environmental drivers of intrapopulation variation in measured levels. Metal concentrations were associated with civet age, weight, proximity to a tributary, and access to oxbow lakes. In a targeted case study, the hair metal profiles of 16 GPS-collared male civets with differing space use patterns were contrasted. Civets that entered oil palm plantations expressed elevated aluminium, cadmium, and lead, and lower mercury hair concentrations compared to civets that remained exclusively within the forest. Finally, we paired hair metal concentrations with 34 blood-based health markers to evaluate the possible sub-lethal physiological effects associated with varied hair metal levels. Our multi-facetted approach establishes these adaptable carnivores as indicator species within an extensively altered ecosystem, and provides critical and timely evidence for future studies.
Which nests to choose: collecting shed hairs from wild orang-utans

Goossens B, Abdullah ZB, Sinyor JB, Ancrenaz M

Folia Primatol., 2004 Jan-Feb;75(1):23-6.
PMID: 14716150
Jumping in the Night: An Investigation of the Leaping Activity of the Western Tarsier (Cephalopachus bancanus borneanus) Using Accelerometers

Costantini D, Sebastiano M, Goossens B, Stark DJ

Folia Primatol., 2017;88(1):46-56.
PMID: 28662508 DOI: 10.1159/000477540

Accelerometers enable scientists to quantify the activity of free-living animals whose direct observation is difficult or demanding due to their elusive nature or nocturnal habits. However, the deployment of accelerometers on small-bodied animals and, in particular, on primates has been little explored. Here we show the first application of accelerometers on the western tarsier (Cephalopachus bancanus borneanus), a nocturnal, small-bodied primate endemic to the forests of Borneo. The fieldwork was carried out in the Lower Kinabatangan Wildlife Sanctuary, Sabah, Malaysian Borneo. We provide guidelines for the deployment of accelerometers on tarsiers that might also be applied to other primate species. Our collected data on 2 females show levels of leaping activity comparable to those previously described using direct observation of wild or captive individuals. The 2 females showed different patterns of leaping activity, which calls for work to explore individual differences further. Our work demonstrates that accelerometers can be deployed on small primates to acquire body motion data that would otherwise be demanding to collect using classic field observations. Future work will be focused on using accelerometer data to discriminate in more detail the different behaviours tarsiers can display and to address the causes and consequences of individual variations in activity.
Use and Selection of Sleeping Sites by Proboscis Monkeys, Nasalislarvatus, along the Kinabatangan River, Sabah, Malaysia

Thiry V, Stark DJ, Goossens B, Slachmuylder JL, Vercauteren Drubbel R, Vercauteren M

Folia Primatol., 2016;87(3):180-196.
PMID: 27728905

The choice of a sleeping site is crucial for primates and may influence their survival. In this study, we investigated several tree characteristics influencing the sleeping site selection by proboscis monkeys (Nasalis larvatus) along Kinabatangan River, in Sabah, Malaysia. We identified 81 sleeping trees used by one-male and all-male social groups from November 2011 to January 2012. We recorded 15 variables for each tree. Within sleeping sites, sleeping trees were taller, had a larger trunk, with larger and higher first branches than surrounding trees. The crown contained more mature leaves, ripe and unripe fruits but had vines less often than surrounding trees. In addition, in this study, we also focused on a larger scale, considering sleeping and non-sleeping sites. Multivariate analyses highlighted a combination of 6 variables that revealed the significance of sleeping trees as well as surrounding trees in the selection process. During our boat surveys, we observed that adult females and young individuals stayed higher in the canopy than adult males. This pattern may be driven by their increased vulnerability to predation. Finally, we suggest that the selection of particular sleeping tree features (i.e. tall, high first branch) by proboscis monkeys is mostly influenced by antipredation strategies.

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