Displaying publications 1 - 20 of 55 in total

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  1. 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.
  2. 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.
  3. 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. Nájera F, Hearn AJ, Ross J, Ramírez Saldivar DA, Evans MN, Guerrero-Sánchez S, et al.
    J Vet Med Sci, 2017 Nov 17;79(11):1892-1898.
    PMID: 28904261 DOI: 10.1292/jvms.17-0259
    There is currently no available information regarding the veterinary management of Sunda clouded leopards (Neofelis diardi), either in captivity or in the wild. In this study, 12 Sunda clouded leopards were anesthetized between January 2008 and February 2014 for medical exams, and/or GPS-collaring. Seven wild-caught individuals were kept in captivity and 5 free-ranging animals were captured by cage traps. Two anesthesia combinations were used: medetomidine-ketamine (M-K) or tiletamine-zolazepam (T-Z). Atipamezole (0.2 mg/kg im) was used as an antagonist for medetomidine. Medetomidine (range: 0.039-0.054 mg/kg) and ketamine (range: 3-4.39 mg/kg) were administered during 5 immobilizations, resulting in median induction times of 7 min. After a median anesthesia time of 56 min, atipamezole was injected, observing effects of antagonism at a median time of 12 min. T-Z (range: 6.8-10.8 mg/kg) was administered on 7 occasions. Median induction times observed with this combination were shorter than with M-K (4 min vs 7 min; P=0.04), and anesthesia and recovery times were significantly longer (244 and 35 min vs 56 and 16 min, respectively; P=0.02). Lower heart rates were measured in the M-K group, while lower rectal temperatures were found in the T-Z group. Both combinations resulted in safe and reliable immobilizations, although given the favorable anesthesia and recovery times of M-K, we recommend this approach over T-Z for the veterinary handling of Sunda clouded leopards.
  5. 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.
  6. Ancrenaz M, Sollmann R, Meijaard E, Hearn AJ, Ross J, Samejima H, et al.
    Sci Rep, 2014;4:4024.
    PMID: 24526001 DOI: 10.1038/srep04024
    The orangutan is the world's largest arboreal mammal, and images of the red ape moving through the tropical forest canopy symbolise its typical arboreal behaviour. Records of terrestrial behaviour are scarce and often associated with habitat disturbance. We conducted a large-scale species-level analysis of ground-based camera-trapping data to evaluate the extent to which Bornean orangutans Pongo pygmaeus come down from the trees to travel terrestrially, and whether they are indeed forced to the ground primarily by anthropogenic forest disturbances. Although the degree of forest disturbance and canopy gap size influenced terrestriality, orangutans were recorded on the ground as frequently in heavily degraded habitats as in primary forests. Furthermore, all age-sex classes were recorded on the ground (flanged males more often). This suggests that terrestrial locomotion is part of the Bornean orangutan's natural behavioural repertoire to a much greater extent than previously thought, and is only modified by habitat disturbance. The capacity of orangutans to come down from the trees may increase their ability to cope with at least smaller-scale forest fragmentation, and to cross moderately open spaces in mosaic landscapes, although the extent of this versatility remains to be investigated.
  7. Santika T, Ancrenaz M, Wilson KA, Spehar S, Abram N, Banes GL, et al.
    Sci Rep, 2017 07 07;7(1):4839.
    PMID: 28687788 DOI: 10.1038/s41598-017-04435-9
    For many threatened species the rate and drivers of population decline are difficult to assess accurately: species' surveys are typically restricted to small geographic areas, are conducted over short time periods, and employ a wide range of survey protocols. We addressed methodological challenges for assessing change in the abundance of an endangered species. We applied novel methods for integrating field and interview survey data for the critically endangered Bornean orangutan (Pongo pygmaeus), allowing a deeper understanding of the species' persistence through time. Our analysis revealed that Bornean orangutan populations have declined at a rate of 25% over the last 10 years. Survival rates of the species are lowest in areas with intermediate rainfall, where complex interrelations between soil fertility, agricultural productivity, and human settlement patterns influence persistence. These areas also have highest threats from human-wildlife conflict. Survival rates are further positively associated with forest extent, but are lower in areas where surrounding forest has been recently converted to industrial agriculture. Our study highlights the urgency of determining specific management interventions needed in different locations to counter the trend of decline and its associated drivers.
  8. 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.
  9. Koda H, Murai T, Tuuga A, Goossens B, Nathan SKSS, Stark DJ, et al.
    Sci Adv, 2018 02;4(2):eaaq0250.
    PMID: 29507881 DOI: 10.1126/sciadv.aaq0250
    Male proboscis monkeys have uniquely enlarged noses that are prominent adornments, which may have evolved through their sexually competitive harem group social system. Nevertheless, the ecological roles of the signals encoded by enlarged noses remain unclear. We found significant correlations among nose, body, and testis sizes and a clear link between nose size and number of harem females. Therefore, there is evidence supporting both male-male competition and female choice as causal factors in the evolution of enlarged male noses. We also observed that nasal enlargement systematically modifies the resonance properties of male vocalizations, which probably encode male quality. Our results indicate that the audiovisual contributions of enlarged male noses serve as advertisements to females in their mate selection. This is the first primate research to evaluate the evolutionary processes involved in linking morphology, acoustics, and socioecology with unique masculine characteristics.
  10. 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
  11. Meijaard E, Erman A, Ancrenaz M, Goossens B
    Science, 2024 Jan 19;383(6680):267.
    PMID: 38236988 DOI: 10.1126/science.adn3857
  12. 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 
  13. 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.
  14. Abram NK, MacMillan DC, Xofis P, Ancrenaz M, Tzanopoulos J, Ong R, et al.
    PLoS One, 2016;11(6):e0156481.
    PMID: 27276218 DOI: 10.1371/journal.pone.0156481
    Reducing Emissions from Deforestation and forest Degradation (REDD+) aims to avoid forest conversion to alternative land-uses through financial incentives. Oil-palm has high opportunity costs, which according to current literature questions the financial competitiveness of REDD+ in tropical lowlands. To understand this more, we undertook regional fine-scale and coarse-scale analyses (through carbon mapping and economic modelling) to assess the financial viability of REDD+ in safeguarding unprotected forest (30,173 ha) in the Lower Kinabatangan floodplain in Malaysian Borneo. Results estimate 4.7 million metric tons of carbon (MgC) in unprotected forest, with 64% allocated for oil-palm cultivations. Through fine-scale mapping and carbon accounting, we demonstrated that REDD+ can outcompete oil-palm in regions with low suitability, with low carbon prices and low carbon stock. In areas with medium oil-palm suitability, REDD+ could outcompete oil palm in areas with: very high carbon and lower carbon price; medium carbon price and average carbon stock; or, low carbon stock and high carbon price. Areas with high oil palm suitability, REDD+ could only outcompete with higher carbon price and higher carbon stock. In the coarse-scale model, oil-palm outcompeted REDD+ in all cases. For the fine-scale models at the landscape level, low carbon offset prices (US $3 MgCO2e) would enable REDD+ to outcompete oil-palm in 55% of the unprotected forests requiring US $27 million to secure these areas for 25 years. Higher carbon offset price (US $30 MgCO2e) would increase the competitiveness of REDD+ within the landscape but would still only capture between 69%-74% of the unprotected forest, requiring US $380-416 million in carbon financing. REDD+ has been identified as a strategy to mitigate climate change by many countries (including Malaysia). Although REDD+ in certain scenarios cannot outcompete oil palm, this research contributes to the global REDD+ debate by: highlighting REDD+ competitiveness in tropical floodplain landscapes; and, providing a robust approach for identifying and targeting limited REDD+ funds.
  15. Abram NK, Xofis P, Tzanopoulos J, MacMillan DC, Ancrenaz M, Chung R, et al.
    PLoS One, 2014;9(6):e95388.
    PMID: 24887555 DOI: 10.1371/journal.pone.0095388
    Lowland tropical forests are increasingly threatened with conversion to oil palm as global demand and high profit drives crop expansion throughout the world's tropical regions. Yet, landscapes are not homogeneous and regional constraints dictate land suitability for this crop. We conducted a regional study to investigate spatial and economic components of forest conversion to oil palm within a tropical floodplain in the Lower Kinabatangan, Sabah, Malaysian Borneo. The Kinabatangan ecosystem harbours significant biodiversity with globally threatened species but has suffered forest loss and fragmentation. We mapped the oil palm and forested landscapes (using object-based-image analysis, classification and regression tree analysis and on-screen digitising of high-resolution imagery) and undertook economic modelling. Within the study region (520,269 ha), 250,617 ha is cultivated with oil palm with 77% having high Net-Present-Value (NPV) estimates ($413/ha-yr-$637/ha-yr); but 20.5% is under-producing. In fact 6.3% (15,810 ha) of oil palm is commercially redundant (with negative NPV of $-299/ha-yr-$-65/ha-yr) due to palm mortality from flood inundation. These areas would have been important riparian or flooded forest types. Moreover, 30,173 ha of unprotected forest remain and despite its value for connectivity and biodiversity 64% is allocated for future oil palm. However, we estimate that at minimum 54% of these forests are unsuitable for this crop due to inundation events. If conversion to oil palm occurs, we predict a further 16,207 ha will become commercially redundant. This means that over 32,000 ha of forest within the floodplain would have been converted for little or no financial gain yet with significant cost to the ecosystem. Our findings have globally relevant implications for similar floodplain landscapes undergoing forest transformation to agriculture such as oil palm. Understanding landscape level constraints to this crop, and transferring these into policy and practice, may provide conservation and economic opportunities within these seemingly high opportunity cost landscapes.
  16. Estes JG, Othman N, Ismail S, Ancrenaz M, Goossens B, Ambu LN, et al.
    PLoS One, 2012;7(10):e44601.
    PMID: 23071499 DOI: 10.1371/journal.pone.0044601
    The approximately 300 (298, 95% CI: 152-581) elephants in the Lower Kinabatangan Managed Elephant Range in Sabah, Malaysian Borneo are a priority sub-population for Borneo's total elephant population (2,040, 95% CI: 1,184-3,652). Habitat loss and human-elephant conflict are recognized as the major threats to Bornean elephant survival. In the Kinabatangan region, human settlements and agricultural development for oil palm drive an intense fragmentation process. Electric fences guard against elephant crop raiding but also remove access to suitable habitat patches. We conducted expert opinion-based least-cost analyses, to model the quantity and configuration of available suitable elephant habitat in the Lower Kinabatangan, and called this the Elephant Habitat Linkage. At 184 km(2), our estimate of available habitat is 54% smaller than the estimate used in the State's Elephant Action Plan for the Lower Kinabatangan Managed Elephant Range (400 km(2)). During high flood levels, available habitat is reduced to only 61 km(2). As a consequence, short-term elephant densities are likely to surge during floods to 4.83 km(-2) (95% CI: 2.46-9.41), among the highest estimated for forest-dwelling elephants in Asia or Africa. During severe floods, the configuration of remaining elephant habitat and the surge in elephant density may put two villages at elevated risk of human-elephant conflict. Lower Kinabatangan elephants are vulnerable to the natural disturbance regime of the river due to their limited dispersal options. Twenty bottlenecks less than one km wide throughout the Elephant Habitat Linkage, have the potential to further reduce access to suitable habitat. Rebuilding landscape connectivity to isolated habitat patches and to the North Kinabatangan Managed Elephant Range (less than 35 km inland) are conservation priorities that would increase the quantity of available habitat, and may work as a mechanism to allow population release, lower elephant density, reduce human-elephant conflict, and enable genetic mixing.
  17. Gregory SD, Brook BW, Goossens B, Ancrenaz M, Alfred R, Ambu LN, et al.
    PLoS One, 2012;7(9):e43846.
    PMID: 22970145 DOI: 10.1371/journal.pone.0043846
    Southeast Asian deforestation rates are among the world's highest and threaten to drive many forest-dependent species to extinction. Climate change is expected to interact with deforestation to amplify this risk. Here we examine whether regional incentives for sustainable forest management will be effective in improving threatened mammal conservation, in isolation and when combined with global climate change mitigation.
  18. Alfred R, Ahmad AH, Payne J, Williams C, Ambu LN, How PM, et al.
    PLoS One, 2012;7(2):e31400.
    PMID: 22347469 DOI: 10.1371/journal.pone.0031400
    Home range is defined as the extent and location of the area covered annually by a wild animal in its natural habitat. Studies of African and Indian elephants in landscapes of largely open habitats have indicated that the sizes of the home range are determined not only by the food supplies and seasonal changes, but also by numerous other factors including availability of water sources, habitat loss and the existence of man-made barriers. The home range size for the Bornean elephant had never been investigated before.
  19. 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.
  20. Klaus A, Strube C, Röper KM, Radespiel U, Schaarschmidt F, Nathan S, et al.
    PLoS One, 2018;13(4):e0195584.
    PMID: 29630671 DOI: 10.1371/journal.pone.0195584
    Understanding determinants shaping infection risk of endangered wildlife is a major topic in conservation medicine. The proboscis monkey, Nasalis larvatus, an endemic primate flagship species for conservation in Borneo, is endangered through habitat loss, but can still be found in riparian lowland and mangrove forests, and in some protected areas. To assess socioecological and anthropogenic influence on intestinal helminth infections in N. larvatus, 724 fecal samples of harem and bachelor groups, varying in size and the number of juveniles, were collected between June and October 2012 from two study sites in Malaysian Borneo: 634 samples were obtained from groups inhabiting the Lower Kinabatangan Wildlife Sanctuary (LKWS), 90 samples were collected from groups of the Labuk Bay Proboscis Monkey Sanctuary (LBPMS), where monkeys are fed on stationary feeding platforms. Parasite risk was quantified by intestinal helminth prevalence, host parasite species richness (PSR), and eggs per gram feces (epg). Generalized linear mixed effect models were applied to explore whether study site, group type, group size, the number of juveniles per group, and sampling month predict parasite risk. At the LBPMS, prevalence and epg of Trichuris spp., strongylids, and Strongyloides spp. but not Ascaris spp., as well as host PSR were significantly elevated. Only for Strongyloides spp., prevalence showed significant changes between months; at both sites, the beginning rainy season with increased precipitation was linked to higher prevalence, suggesting the external life cycle of Strongyloides spp. to benefit from humidity. Higher prevalence, epgs, and PSR within the LBPMS suggest that anthropogenic factors shape host infection risk more than socioecological factors, most likely via higher re-infection rates and chronic stress. Noninvasive measurement of fecal parasite stages is an important tool for assessing transmission dynamics and infection risks for endangered tropical wildlife. Findings will contribute to healthcare management in nature and in anthropogenically managed environments.
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