Displaying publications 1 - 20 of 56 in total

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  1. Novel insight into the genetic diversity of strongylid nematodes infecting South-East and East Asian primates
    Mason B, Cervena B, Frias L, Goossens B, Hasegawa H, Keuk K, et al.
    Parasitology, 2024 Apr 17.
    PMID: 38629119 DOI: 10.1017/S0031182024000386
    With many non-human primates (NHPs) showing continued population decline, there is an ongoing need to better understand their ecology and conservation threats. One such threat is the risk of disease, with various bacterial, viral and parasitic infections previously reported to have damaging consequences for NHP hosts. Strongylid nematodes are one of the most commonly reported parasitic infections in NHPs. Current knowledge of NHP strongylid infections is restricted by their typical occurrence as mixed infections of multiple genera, which are indistinguishable through traditional microscopic approaches. Here, modern metagenomics approaches were applied for insight into the genetic diversity of strongylid infections in South-East and East Asian NHPs. We hypothesized that strongylid nematodes occur in mixed communities of multiple taxa, dominated by Oesophagostomum, matching previous findings using single-specimen genetics. Utilizing the Illumina MiSeq platform, ITS-2 strongylid metabarcoding was applied to 90 samples from various wild NHPs occurring in Malaysian Borneo and Japan. A clear dominance of Oesophagostomum aculeatum was found, with almost all sequences assigned to this species. This study suggests that strongylid communities of Asian NHPs may be less species-rich than those in African NHPs, where multi-genera communities are reported. Such knowledge contributes baseline data, assisting with ongoing monitoring of health threats to NHPs.
  2. Pig virus imperils food security in Borneo
    Meijaard E, Erman A, Ancrenaz M, Goossens B
    Science, 2024 Jan 19;383(6680):267.
    PMID: 38236988 DOI: 10.1126/science.adn3857
  3. Connect elephant habitats in Asia
    Davidar P, Sharma R, de Silva S, Campos-Arceiz A, Goossens B, Puyravaud JP, et al.
    Science, 2023 Feb 24;379(6634):765.
    PMID: 36821683 DOI: 10.1126/science.adg7470
  4. Modifying the diets of captive proboscis monkeys in a temperate zoo to reduce weight loss and renal disease
    Hoshino S, Seino S, Azumano A, Tuuga A, Nathan SKSS, Ramirez Saldivar DA, et al.
    Primates, 2023 Jan;64(1):123-141.
    PMID: 36357633 DOI: 10.1007/s10329-022-01031-y
    In animal husbandry, diets should help in maintaining a healthy body condition, support reproduction, and promote species-specific longevity. It is recommended to feed folivorous primates kept in zoos a high-fiber diet, i.e., leaves, although satisfying such a requirement is challenging in temperate regions because it is difficult to obtain fresh leaves, especially in autumn and winter. As equally important for their appropriate treatment, it is valuable to provide details of clinical reports of medical problems and pathological findings, although such clinical reports are rather limited. Therefore, in foregut-fermenting proboscis monkeys (Nasalis larvatus), we (1) described the individual clinical reports of renal disease and weight loss at the Yokohama Zoological Gardens in Japan, (2) determined the nutritional profile of the diets supplied to these animals because other potential triggers for their renal disease and weight loss could be excluded, (3) modified the diet regimen to minimize weight loss and the development of hypercalcemia and hypophosphatemia, and (4) assessed the effects of such dietary modification by comparing the body weight and the Ca and P concentrations and the Ca/P ratios in the blood before and after diet modification with a comparison of these measurements between zoo and free-ranging individuals. Based on the nutritional profile of the diets, we concluded that the reported cases of renal failure might be caused by consumption of leaves with a Ca/P ratio far above the appropriate level in autumn and winter. Additionally, the dietary modification of minerals and metabolizable energy achieved certain beneficial effects on zoo-kept proboscis monkeys.
  5. 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.
  6. Fulltext Whole genome analysis of clouded leopard species reveals an ancient divergence and distinct demographic histories
    Bursell MG, Dikow RB, Figueiró HV, Dudchenko O, Flanagan JP, Aiden EL, et al.
    iScience, 2022 Dec 22;25(12):105647.
    PMID: 36590460 DOI: 10.1016/j.isci.2022.105647
    Similar to other apex predator species, populations of mainland (Neofelis nebulosa) and Sunda (Neofelis diardi) clouded leopards are declining. Understanding their patterns of genetic variation can provide critical insights on past genetic erosion and a baseline for understanding their long-term conservation needs. As a step toward this goal, we present draft genome assemblies for the two clouded leopard species to quantify their phylogenetic divergence, genome-wide diversity, and historical population trends. We estimate that the two species diverged 5.1 Mya, much earlier than previous estimates of 1.41 Mya and 2.86 Mya, suggesting they separated when Sundaland was becoming increasingly isolated from mainland Southeast Asia. The Sunda clouded leopard displays a distinct and reduced effective population size trajectory, consistent with a lower genome-wide heterozygosity and SNP density, relative to the mainland clouded leopard. Our results provide new insights into the evolutionary history and genetic health of this unique lineage of felids.
  7. Fulltext Serological evidence of exposure of Bornean wild carnivores to feline-related viruses at the domestic animal-wildlife interface
    Guerrero-Sánchez S, Wilson A, González-Abarzúa M, Kunde M, Goossens B, Sipangkui R, et al.
    Transbound Emerg Dis, 2022 Sep;69(5):e3250-e3254.
    PMID: 35373926 DOI: 10.1111/tbed.14549
    We conducted an exploratory serological survey to evaluate the exposure of Bornean wild carnivores to several viruses common to domestic felids, at interface areas between protected forest and industrial agriculture in the Kinabatangan floodplain (Sabah, Malaysia). Blood samples, collected from wild carnivores (n = 21) and domestic cats (n = 27), were tested for antibodies against feline coronavirus (FCoV), feline panleukopenia virus (FPLV), feline herpesvirus (FHV) and feline calicivirus (FCV), using commercial enzyme-linked immunosorbent assay (ELISA) test kits. Anti-FCoV antibodies were detected in most species, including one flat-headed cat (Prionailurus planiceps, [1/2]), leopard cats (Prionailurus bengalensis, [2/5]), Malay civets (Viverra tangalunga, [2/11]) and domestic cats (Felis catus, [2/27]). Anti-FCV antibodies were present in all domestic cats and one flat-headed cat, while anti-FPLV antibodies were identified in Sunda clouded leopards (Neofelis diardi, [2/2]), domestic cats [12/27] and Malay civets [2/11]. Anti-FHV antibodies were only detected in domestic cats [2/27]. Our findings indicate pathogen transmission risk between domestic and wild carnivore populations at the domestic animal-wildlife interface, emphasizing the concern for wildlife conservation for several endangered wild carnivores living in the area. Special consideration should be given to species that benefit from their association with humans and have the potential to carry pathogens between forest and plantations (e.g., Malay civets and leopard cats). Risk reduction strategies should be incorporated and supported as part of conservation actions in human-dominated landscapes.
  8. 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.
  9. 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.
  10. Fulltext Parasite community structure in sympatric Bornean primates
    Frias L, Hasegawa H, Chua TH, Sipangkui S, Stark DJ, Salgado-Lynn M, et al.
    Int J Parasitol, 2021 10;51(11):925-933.
    PMID: 33862059 DOI: 10.1016/j.ijpara.2021.03.003
    Parasites are important components of ecosystems, influencing trophic networks, competitive interactions and biodiversity patterns. Nonetheless, we are not nearly close to disentangling their complex roles in natural systems. Southeast Asia falls within global areas targeted as most likely to source parasites with zoonotic potential, where high rates of land conversion and fragmentation have altered the circulation of wildlife species and their parasites, potentially resulting in altered host-parasite systems. Although the overall biodiversity in the region predicts equally high, or even higher, parasite diversity, we know surprisingly little about wild primate parasites, even though this constitutes the first step towards a more comprehensive understanding of parasite transmission processes. Here, we characterise the gastrointestinal helminth parasite assemblages of a community of Bornean primates living along the Kinabatangan floodplain in Sabah (Malaysian Borneo), including two species endemic to the island. Through parasitological analyses, and by using several measures of parasite infection as proxies for parasite diversity and distribution, we show that (i) most parasite taxonomic groups are not limited to a single host, suggesting a greater flexibility for habitat disturbance, (ii) parasite infracommunities of nocturnal primates differ from their diurnal counterparts, reflecting both phylogenetic and ecological constraints, and (iii) soil-transmitted helminths such as whipworm, threadworm and nodule worm are widespread across the primate community. This study also provides new parasite records for southern pig-tailed macaques (Macaca nemestrina), silvered langurs (Trachypithecus cristatus) and Western tarsiers (Cephalopachus bancanus) in the wild, while adding to the limited records for the other primate species in the community. Given the information gap regarding primate-parasite associations in the region, the information presented here should prove relevant for future studies of parasite biodiversity and infectious disease ecology in Asia and elsewhere.
  11. Fulltext Genomic insights into the conservation status of the world's last remaining Sumatran rhinoceros populations
    von Seth J, Dussex N, Díez-Del-Molino D, van der Valk T, Kutschera VE, Kierczak M, et al.
    Nat Commun, 2021 Apr 26;12(1):2393.
    PMID: 33896938 DOI: 10.1038/s41467-021-22386-8
    Small populations are often exposed to high inbreeding and mutational load that can increase the risk of extinction. The Sumatran rhinoceros was widespread in Southeast Asia, but is now restricted to small and isolated populations on Sumatra and Borneo, and most likely extinct on the Malay Peninsula. Here, we analyse 5 historical and 16 modern genomes from these populations to investigate the genomic consequences of the recent decline, such as increased inbreeding and mutational load. We find that the Malay Peninsula population experienced increased inbreeding shortly before extirpation, which possibly was accompanied by purging. The populations on Sumatra and Borneo instead show low inbreeding, but high mutational load. The currently small population sizes may thus in the near future lead to inbreeding depression. Moreover, we find little evidence for differences in local adaptation among populations, suggesting that future inbreeding depression could potentially be mitigated by assisted gene flow among populations.
  12. Fulltext The critical role of natural forest as refugium for generalist species in oil palm-dominated landscapes
    Guerrero-Sanchez S, Goossens B, Saimin S, Orozco-terWengel P
    PLoS One, 2021;16(10):e0257814.
    PMID: 34614000 DOI: 10.1371/journal.pone.0257814
    In Borneo, oil palm plantations have replaced much of natural resources, where generalist species tend to be the principal beneficiaries, due to the abundant food provided by oil palm plantations. Here, we analyse the distribution of the Asian water monitor lizard (Varanus salvator) population within an oil palm-dominated landscape in the Kinabatangan floodplain, Malaysian Borneo. By using mark-recapture methods we estimated its population size, survival, and growth in forest and plantation habitats. We compared body measurements (i.e. body weight and body length) of individuals living in forest and oil palm habitats as proxy for the population's health status, and used general least squares estimation models to evaluate its response to highly fragmented landscapes in the absence of intensive hunting pressures. Contrary to previous studies, the abundance of lizards was higher in the forest than in oil palm plantations. Recruitment rates were also higher in the forest, suggesting that these areas may function as a source of new individuals into the landscape. While there were no morphometric differences among plantation sites, we found significant differences among forested areas, where larger lizards were found inhabiting forest adjacent to oil palm plantations. Although abundant in food resources, the limited availability of refugia in oil palm plantations may intensify intra-specific encounters and competition, altering the body size distribution in plantation populations, contrary to what happens in the forest. We conclude that large patches of forest, around and within oil palm plantations, are essential for the dynamics of the monitor lizard population in the Kinabatangan floodplain, as well as a potential source of individuals to the landscape. We recommend assessing this effect in other generalist species, as well as the impact on the prey communities, especially to reinforce the establishment of buffer zones and corridors as a conservation strategy within plantations.
  13. 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.
  14. 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.
  15. 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.

  16. First description of male worms of Enterobius (Colobenterobius) serratus (Nematoda: Oxyuridae), the pinworm parasite of proboscis monkeys
    Hasegawa H, Frias L, Peter S, Hasan NH, Stark DJ, Lynn MS, et al.
    Zootaxa, 2020 Jan 14;4722(3):zootaxa.4722.3.6.
    PMID: 32230627 DOI: 10.11646/zootaxa.4722.3.6
    Males of Enterobius (Colobenterobius) serratus Hasegawa et al., 2003 (Nematoda: Oxyuridae) are described for the first time based on six individuals collected from the feces of proboscis monkeys, Nasalis larvatus, in the Lower Kinabatangan Wildlife Sanctuary, Sabah, Malaysian Borneo. The males show identical cephalic morphology to females, being readily distinguishable from their congeners by the serrated inner margins of the lips. The bicolored esophageal corpus, long thin spicule and developed spicular pouch with paired muscular bands are also remarkable characteristics, presumably shared by other Asian members of the subgenus.
  17. 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.
  18. 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.
  19. Seed dispersal by proboscis monkeys: the case of Nauclea spp
    Thiry V, Bhasin O, Stark DJ, Beudels-Jamar RC, Vercauteren Drubbel R, Nathan SKSS, et al.
    Primates, 2019 Sep;60(5):449-457.
    PMID: 31342225 DOI: 10.1007/s10329-019-00736-x
    Frugivorous vertebrates such as primates are important dispersal agents in tropical forests, although the role of folivorous colobines is generally not considered. However, recent studies reported seed dispersal by endo- and epizoochory in colobine primates, including the proboscis monkey (Nasalis larvatus), suggesting that the role colobines play in seed dispersal might have been underestimated. In the Lower Kinabatangan Floodplain in Sabah, Malaysian Borneo, we investigated whether seeds were still able to germinate after being ingested by proboscis monkeys. Faecal samples (n = 201) from proboscis monkeys were collected between 2015 and 2017. Intact seeds belonging to eight plant species were found in 77% of the faecal samples. Nauclea spp. were the most abundant plant species, accounting for 98% of all intact seeds. This study is the first to conduct germination trials on seeds defecated by proboscis monkeys. Higher germination success was recorded in ingested Nauclea spp. seeds than in control seeds, from both ripe and unripe Nauclea orientalis fruits (P 
  20. Fulltext A pinworm's tale: The evolutionary history of Lemuricola (Protenterobius) nycticebi
    Frias L, Hasegawa H, Stark DJ, Lynn MS, Nathan SK, Chua TH, et al.
    Int J Parasitol Parasites Wildl, 2019 Apr;8:25-32.
    PMID: 30619706 DOI: 10.1016/j.ijppaw.2018.11.009
    Lemuricola (Protenterobius) nycticebi is the only pinworm species known to infect strepsirrhine primates outside Africa, and the only pinworm species yet described in slow lorises. Here, we provided a detailed morphological comparison of female and male worms, and a first description of fourth-stage larvae collected from free-living slow lorises (Nycticebus menagensis) in Sabah, Malaysian Borneo. Using mitochondrial and nuclear markers, we also reconstructed the species' phylogenetic relationship with other pinworms infecting primates. Both morphological and molecular results indicated a distinct association between L. (P.) nycticebi and its host. However, while taxonomy identified this species as a member of the Lemuricola clade and grouped pinworms infecting lemurs and slow lorises together, phylogenetic reconstruction split them, placing L. (P.) nycticebi within the Enterobius clade. Our results suggest that L. (P.) nycticebi may represent a different taxon altogether, and that it is more closely related to pinworm species infecting Old World primates outside Madagascar. Pongobius pongoi (Foitová et al., 2008) n. comb. is also proposed.
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