Displaying publications 41 - 57 of 57 in total

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  1. 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.

  2. 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.
  3. 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.
  4. 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.
  5. Fulltext Genetic analyses favour an ancient and natural origin of elephants on Borneo
    Sharma R, Goossens B, Heller R, Rasteiro R, Othman N, Bruford MW, et al.
    Sci Rep, 2018 01 17;8(1):880.
    PMID: 29343863 DOI: 10.1038/s41598-017-17042-5
    The origin of the elephant on the island of Borneo remains elusive. Research has suggested two alternative hypotheses: the Bornean elephant stems either from a recent introduction in the 17th century or from an ancient colonization several hundreds of thousands years ago. Lack of elephant fossils has been interpreted as evidence for a very recent introduction, whereas mtDNA divergence from other Asian elephants has been argued to favor an ancient colonization. We investigated the demographic history of Bornean elephants using full-likelihood and approximate Bayesian computation analyses. Our results are at odds with both the recent and ancient colonization hypotheses, and favour a third intermediate scenario. We find that genetic data favour a scenario in which Bornean elephants experienced a bottleneck during the last glacial period, possibly as a consequence of the colonization of Borneo, and from which it has slowly recovered since. Altogether the data support a natural colonization of Bornean elephants at a time when large terrestrial mammals could colonise from the Sunda shelf when sea levels were much lower. Our results are important not only in understanding the unique history of the colonization of Borneo by elephants, but also for their long-term conservation.
  6. Fulltext Evaluating methods for estimating home ranges using GPS collars: A comparison using proboscis monkeys (Nasalis larvatus)
    Stark DJ, Vaughan IP, Ramirez Saldivar DA, Nathan SK, Goossens B
    PLoS One, 2017;12(3):e0174891.
    PMID: 28362872 DOI: 10.1371/journal.pone.0174891
    The development of GPS tags for tracking wildlife has revolutionised the study of home ranges, habitat use and behaviour. Concomitantly, there have been rapid developments in methods for estimating habitat use from GPS data. In combination, these changes can cause challenges in choosing the best methods for estimating home ranges. In primatology, this issue has received little attention, as there have been few GPS collar-based studies to date. However, as advancing technology is making collaring studies more feasible, there is a need for the analysis to advance alongside the technology. Here, using a high quality GPS collaring data set from 10 proboscis monkeys (Nasalis larvatus), we aimed to: 1) compare home range estimates from the most commonly used method in primatology, the grid-cell method, with three recent methods designed for large and/or temporally correlated GPS data sets; 2) evaluate how well these methods identify known physical barriers (e.g. rivers); and 3) test the robustness of the different methods to data containing either less frequent or random losses of GPS fixes. Biased random bridges had the best overall performance, combining a high level of agreement between the raw data and estimated utilisation distribution with a relatively low sensitivity to reduced fixed frequency or loss of data. It estimated the home range of proboscis monkeys to be 24-165 ha (mean 80.89 ha). The grid-cell method and approaches based on local convex hulls had some advantages including simplicity and excellent barrier identification, respectively, but lower overall performance. With the most suitable model, or combination of models, it is possible to understand more fully the patterns, causes, and potential consequences that disturbances could have on an animal, and accordingly be used to assist in the management and restoration of degraded landscapes.
  7. Fulltext Co-infection patterns of intestinal parasites in arboreal primates (proboscis monkeys, Nasalis larvatus) in Borneo
    Klaus A, Zimmermann E, Röper KM, Radespiel U, Nathan S, Goossens B, et al.
    Int J Parasitol Parasites Wildl, 2017 Dec;6(3):320-329.
    PMID: 29988805 DOI: 10.1016/j.ijppaw.2017.09.005
    Non-human primates of South-East Asia remain under-studied concerning parasite epidemiology and co-infection patterns. Simultaneously, efforts in conservation demand knowledge of parasite abundance and biodiversity in threatened species. The Endangered proboscis monkey, Nasalis larvatus, a primate flagship species for conservation in Borneo, was investigated in the present study. Habitat loss and fragmentation are among the greatest threats to bachelor and harem groups of this folivorous colobine. Designed as a follow-up study, prevalence and co-infection status of intestinal parasites from N. larvatus in a protected area in Malaysian Borneo were analyzed from fecal samples using a flotation method. For the first time, the intestinal parasite co-infection patterns were examined using quantitative analyses. Overall, 92.3% of fecal samples (N = 652) were positive for helminth eggs. Five helminth groups were detected: (1) trichurids (82.7% prevalence) including Trichuris spp. (82.1%) and Anatrichosoma spp. (1.4%), (2) strongyles (58.9%) including Trichostrongylus spp. (48.5%) and Oesophagostomum/Ternidens spp. (22.8%), (3) Strongyloides fuelleborni (32.7%), (4) Ascaris lumbricoides (8.6%), and (5) Enterobius spp. (5.5%). On average, an individual was co-infected with two different groups. Significant positive associations were found for co-infections of trichurids with strongyles and S. fuelleborni as well as S. fuelleborni with A. lumbricoides and strongyles. This study shows a high prevalence of various gastrointestinal helminths with potential transmission pathways primarily related to soil and with zoonotic relevance in wild proboscis monkeys in their remaining natural habitats. Observed positive associations of trichurids with strongyles and Strongyloides spp. may result from the high prevalence of trichurids. Similarly, positive associations between Strongyloides and Ascaris were found, both of which typically occur predominantly in juvenile hosts. These findings should be considered when proposing conservation actions in altered habitats nearby human settlements and when managing captive populations.
  8. Riverine effects on mitochondrial structure of Bornean orangutans (Pongo pygmaeus) at two spatial scales
    Jalil MF, Cable J, Sinyor J, Lackman-Ancrenaz I, Ancrenaz M, Bruford MW, et al.
    Mol Ecol, 2008 Jun;17(12):2898-909.
    PMID: 18494768 DOI: 10.1111/j.1365-294X.2008.03793.x
    We examined mitochondrial DNA control region sequences of 73 Kinabatangan orangutans to test the hypothesis that the phylogeographical structure of the Bornean orangutan is influenced by riverine barriers. The Lower Kinabatangan Wildlife Sanctuary contains one of the most northern populations of orangutans (Pongo pygmaeus) on Borneo and is bisected by the Kinabatangan River, the longest river in Sabah. Orang-utan samples on either side of the river were strongly differentiated with a high Phi(ST) value of 0.404 (P < 0.001). Results also suggest an east-west gradient of genetic diversity and evidence for population expansion along the river, possibly reflecting a postglacial colonization of the Kinabatangan floodplain. We compared our data with previously published sequences of Bornean orangutans in the context of river catchment structure on the island and evaluated the general relevance of rivers as barriers to gene flow in this long-lived, solitary arboreal ape.
  9. 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
  10. Spatial Ecology of Estuarine Crocodile (Crocodylus porosus) Nesting in a Fragmented Landscape
    Evans LJ, Jones TH, Pang K, Saimin S, Goossens B
    Sensors (Basel), 2016 Sep 19;16(9).
    PMID: 27657065
    The role that oil palm plays in the Lower Kinabatangan region of Eastern Sabah is of considerable scientific and conservation interest, providing a model habitat for many tropical regions as they become increasingly fragmented. Crocodilians, as apex predators, widely distributed throughout the tropics, are ideal indicator species for ecosystem health. Drones (or unmanned aerial vehicles (UAVs)) were used to identify crocodile nests in a fragmented landscape. Flights were targeted through the use of fuzzy overlay models and nests located primarily in areas indicated as suitable habitat. Nests displayed a number of similarities in terms of habitat characteristics allowing for refined modelling of survey locations. As well as being more cost-effective compared to traditional methods of nesting survey, the use of drones also enabled a larger survey area to be completed albeit with a limited number of flights. The study provides a methodology for targeted nest surveying, as well as a low-cost repeatable flight methodology. This approach has potential for widespread applicability across a range of species and for a variety of study designs.
  11. 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.
  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 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.
  14. Fulltext Riparian vegetation structure and the hunting behavior of adult estuarine crocodiles
    Evans LJ, Davies AB, Goossens B, Asner GP
    PLoS One, 2017;12(10):e0184804.
    PMID: 29020111 DOI: 10.1371/journal.pone.0184804
    Riparian ecosystems are amongst the most biodiverse tropical habitats. They are important, and essential, ecological corridors, linking remnant forest fragments. In this study, we hypothesised that crocodile's actively select nocturnal resting locations based on increased macaque predation potential. We examined the importance of riparian vegetation structure in the maintenance of crocodile hunting behaviours. Using airborne Light Detection and Ranging (LiDAR) and GPS telemetry on animal movement, we identified the repeated use of nocturnal resting sites by adult estuarine crocodiles (Crocodylus porosus) throughout the fragmented Lower Kinabatangan Wildlife Sanctuary in Sabah, Malaysia. Crocodile resting locations were found to resemble, in terms of habitat characteristics, the sleeping sites of long-tailed macaque; positioned in an attempt to avoid predation by terrestrial predators. We found individual crocodiles were actively selecting overhanging vegetation and that the protrusion of trees from the tree line was key to site selection by crocodiles, as well as influencing both the presence and group size of sleeping macaques. Although these findings are correlational, they have broad management implications, with the suggestion that riparian corridor maintenance and quality can have implications beyond that of terrestrial fauna. We further place our findings in the context of the wider ecosystem and the maintenance of trophic interactions, and discuss how future habitat management has the potential to mitigate human-wildlife conflict.
  15. 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.
  16. 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
  17. 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.
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