Macaca Leonina Research Articles

Patterns of nesting and nest success in an evergreen forest in Southeast Asia

ABSTRACTSoutheast Asian forest birds are threatened by the highest rate of tropical deforestation globally, but conservation efforts regionally have very limited information from which to make policy and management plans. To provide baseline data on nesting and nest success for forest birds from an intact forest, we monitored 1506 nests of 54 species during 2003–2011 in a seasonally wet forest at 14°N in north-eastern Thailand. We estimated daily nest survival (DSR) for 37 species (n = 1082 nests). Early nesting species were more successful and ground-nesting birds had higher DSR (0.962) than above-ground nests (0.934). DSR for 13 focal species (n = 956 nests) varied from 0.842 to 0.975. In general, DSR was unrelated to season or nest height for focal species although one species was more successful early in their breeding season while for another, higher nests were more successful. Nest survival was low, and predation accounted for 92% of nest failures. Two nest predators, Northern Pig-tailed Macaque Macaca nemestrina and Green Cat Snake Boiga cyanea accounted for 43.7% and 21.8% of the predation events, respectively. We suggest that local conditions, even in intact forests, may produce complex dynamics for reproductive success of breeding birds, and we posit that presence of the dominant nest predators was largely responsible for patterns we observed among species, particularly the higher DSR of ground-nesting birds. Our data further support the idea that DSR is generally lower in relatively undisturbed sites in the tropics than similarly undisturbed sites in the temperate zone.

Habitat structure affects nest predation of the Scaly-crowned Babbler (Malacopteron cinereum) by macaques and snakes in a Thai-seasonal evergreen forest

Nest success of forest birds is typically low due to high rates of predation, but little is known regarding how different nest predators affect nest-site selection and nesting success, particularly in the tropics. We studied nest-site selection and nest success of the understory-nesting Scaly-crowned Babbler (Malacopteron cinereum) in a seasonal evergreen forest in northeastern Thailand during four breeding seasons. We identified nest predators using video-monitoring and examined relationships between nest site vegetation structure and nest predation by dominant predators. Based on 71 video-monitored nests, 98.5% of failures were due to predation; 59 predation events from nine predator species were documented including Northern Pig-tailed Macaque (Macaca leonina) (47.5%, n = 28), five avian predator species (32.2%, n = 19), and two snake species (18.6%, n = 11). Nest sites had significantly higher concealment and number of lianas than random sites. Higher concealment may represent selection against visually oriented predators which were responsible for approximately 80% of predation events. Vegetation parameters suggested opposing patterns for macaques versus snakes; nests surrounded by higher density of saplings and lower density of taller stems (5–10 m) were depredated by macaques, whereas snake depredated nests were associated with a lower density of saplings, a higher density of taller stems and a higher density of lianas. Nests depredated by avian predators were not associated with any measured variables. Our data suggest that different vegetation structures perhaps facilitate or impede different predators and different predators may generate conflicting selection pressures for nesting birds within a given habitat. Our data also imply that impacts on nesting success from vegetation disturbance (e.g., logging, road edges, etc.) may be difficult to predict, as these effects are likely to vary among sites and regions depending on the foraging behavior of dominant local predators.

Human Plasmodium knowlesi infections in South-East Asian countries.

Plasmodium knowlesi is now regarded as the fifth malaria parasite causing human malaria as it is widely distributed in South-East Asian countries especially east Malaysia where two Malaysian states namely Sabah and Sarawak are situated. In 2004, Polymerase Chain Reaction (PCR) was applied for diagnosing knowlesi malaria in the Kapit Division of Sarawak, Malaysia, so that human P. knowlesi infections could be detected correctly while blood film microscopy diagnosed incorrectly as Plasmodium malariae. This parasite is transmitted from simian hosts to humans via Anopheles vectors. Indonesia is the another country in South East Asia where knowlesi malaria is moderately prevalent. In the last decade, Sarawak and Sabah, the two states of east Malaysia became the target of P. knowlesi research due to prevalence of cases with occasional fatal infections. The host species of P. knowlesi are three macaque species namely Macaca fascicularis, Macaca nemestrina and Macaca leonina while the vector species are the Leucosphyrus Complex and the Dirus Complex of the Leucophyrus Group of Anopheles mosquitoes. Rapid diagnostic tests (RDT) are non-existent for knowlesi malaria although timely treatment is necessary for preventing complications, fatality and drug resistance. Development of RDT is essential in dealing with P. knowlesi infections in poor rural healthcare services. Genetic studies of the parasite on possibility of human-to-human transmission of P. knowlesi were recommended for further studies.

Nesting near road edges improves nest success and post-fledging survival of White-rumped Shamas (Copsychus malabaricus) in northeastern Thailand

ABSTRACT Road edges in the temperate zone often negatively affect reproductive success, post-fledging survival, and dispersal of forest birds through processes associated with edge habitats. This pattern is less clear in the tropics due to a lack of studies using natural nests and radio-tagged fledglings as well as an almost complete absence of information on nest and fledgling predators. We investigated the influence of road edge on nest success, post-fledging survival, and dispersal of White-rumped Shama (Copsychus malabaricus) in a dry evergreen forest in northeastern Thailand. One hundred nest boxes were placed in forest interior (≥1,000 m from edge of a 5-lane highway) and 100 near forest edge (≤200 m) to assess nesting success. We radio-tracked 50 fledglings from these boxes, 25 each for edge and interior, for 7 weeks after fledging. Nest success and post-fledging survival were 11.6% and 23.6% higher at the edge versus the interior. Predation had the strongest influence on survival, accounting for 100% of nest and 94% of fledgling mortality. Fledglings used locations with denser understory vegetation cover relative to the available habitat, probably to reduce predation risk. Green cat snake (Boiga cyanea) and northern pig-tailed macaque (Macaca leonina), which likely prefer forest interiors over edges, were the primary predators of nests and fledglings in this landscape. There were no significant differences in timing of dispersal and dispersal distance or dispersal direction in relation to proximity to edge. Our results suggest that the impacts of edge effects on the reproductive success of birds appear to be strongly dependent on the habitat preferences of locally dominant predators. Further research will be needed to identify key predators and broadly assess their foraging behaviors in individual landscapes.

Superior intestinal integrity and limited microbial translocation are associated with lower immune activation in SIVmac239-infected northern pig-tailed macaques (Macaca leonina).

Microbial translocation is a cause of systemic immune activation in HIV/SIV infection. In the present study, we found a lower CD8+ T cell activation level in Macaca leonina (northern pig-tailed macaques, NPMs) than in Macaca mulatta (Chinese rhesus macaques, ChRMs) during SIVmac239 infection. Furthermore, the levels of plasma LPS-binding protein and soluble CD14 in NPMs were lower than those in ChRMs. Compared with ChRMs, SIV-infected NPMs had lower Chiu scores, representing relatively normal intestinal mucosa. In addition, no obvious damage to the ileum or colon epithelial barrier was observed in either infected or uninfected NPMs, which differed to that found in ChRMs. Furthermore, no significant microbial translocation ( Escherichia coli) was detected in the colon or ileum of infected or uninfected NPMs, which again differed to that observed in ChRMs. In conclusion, NPMs retained superior intestinal integrity and limited microbial translocation during SIV infection, which may contribute to their lower immune activation compared with ChRMs.

Foraging strategies underlying bird egg predation by macaques: A study using artificial nests.

Bird egg predation is widespread in non-human primates. Although nest predation is often described as opportunistic, little is known about foraging strategies and nest detection in primates. Since it is the prevalent cause of nest failure in the tropics, birds select nest sites within specific microhabitats and use different nest types to increase nesting success. Identifying the nests targeted by the northern pigtailed macaques (Macaca leonina), an omnivorous cercopithecine species, and known nest predator, will shine light on nest foraging strategies in primates. The aim of this research was to reveal if nest predation is a selective or opportunistic feeding behavior. We studied, using artificial nests and camera traps, the influence of nest type (open-cup vs. cavity), microhabitat (i.e., understory density, canopy cover, canopy height, ground cover, and presence vs. absence of thorns and lianas), and nest height, on nest predation by a troop of northern pigtailed macaques in the Sakaerat Biosphere Reserve (Thailand), a degraded environment. In our study, macaque predation on artificial nests was high; out of the 200 nests that were set up, 112 were plundered by macaques. Although predation rates decreased with nest height, nest type, and microhabitat had no significant effect on predation by macaques. Nest detectability and accessibility did not affect predation rates. Macaques actively searched for nests in different microhabitats, suggesting that nest predation by this primate might be considered a selective feeding behavior in this degraded habitat. Consequently, nest predation by this primate might have important conservation implications on the population dynamics of forest-dwelling bird species. Behavior observation methods, such as instantaneous scan sampling, may underestimate nest predation by primates, a furtive and cryptic behavior.

Effects of roadside edge on nest predators and nest survival of Asian tropical forest birds

Creation of roadside forest edges can have indirect effects on forest bird communities, as edges can promote species detrimental to forest-nesting birds such as nest predators. We assessed species-specific rates of nest survival of understory birds, relative abundances of specific nest predators and predator-specific rates of nest predation relative to the distance from roadside forest edge in a dry evergreen forest in northeastern Thailand. During the breeding seasons (February–August) of 2014–2016 we searched for nests along two, 1-km transects which ran perpendicular from the edge of a five-lane highway into the forest interior. To assess nest predator species, video cameras were placed on active nests of understory birds and multiple techniques were used to assess the relative abundances of the documented nest predators. We found 306 active nests of 26 species and recorded 179 predation events from 13 species of nest predators. Distance to edge influenced the daily nest survival rates for four of seven focal bird species, with three species having higher survival rates nearer to the edge. Four of six predators had higher relative abundances in the forest interior. Rats and the Common Green Magpie (Cissa chinensis) had higher abundances nearer the edge. Snake detections were too few to assess statistically. Nest predation rates for the top three predators, Northern Pig-tailed Macaque (Macaca leonina), Green Cat Snake (Boiga cyanea) and Crested Goshawk (Accipiter trivirgratus) were significantly greater in the forest interior. The fourth-most important, Common Green Magpie, was the only predator responsible for more nest predation events closer to habitat edge compared to interior. Our study suggests that the impacts of edges on nesting success are highly dependent on the nest predator community and the species-specific responses of predators to edges.

Host Restriction Factors APOBEC3G/3F and Other Interferon-Related Gene Expressions Affect Early HIV-1 Infection in Northern Pig-Tailed Macaque (Macaca leonina).

The northern pig-tailed macaques (NPMs) lack TRIM5α, an antiviral restriction factor, and instead have TRIM5-CypA. In our previous study, we demonstrated that HIV-1NL4−3 successfully infected NPMs and formed a long-term viral reservoir in vivo. However, the HIV-1-infected NPMs showed relatively high viremia in the first 6 weeks of infection, which declined thereafter suggesting that HIV-1 NL4−3 infection in these animals was only partly permissive. To optimize HIV-1 infection in NPMs therefore, we generated HIV-1NL4−R3A and stHIV-1sv, and infected NPMs with these viruses. HIV-1NL4−R3A and stHIV-1sv can replicate persistently in NPMs during 41 weeks of acute infection stage. Compared to the HIV-1NL4−R3A, stHIV-1sv showed a notably higher level of replication, and the NPMs infected with the latter induced a more robust neutralizing antibody but a weaker cellular immune response. In addition, IFN-I signaling was significantly up-regulated with the viral replication, and was higher in the stHIV-1sv infected macaques. Consequently, the sequences of pro-viral env showed fewer G-A hyper-mutations in stHIV-1sv, suggesting that vif gene of SIV could antagonize the antiviral effects of APOBEC3 proteins in NPMs. Taken together, NPMs infected with HIV-1NL4−R3A and stHIV-1sv show distinct virological and immunological features. Furthermore, interferon-related gene expression might play a role in controlling primary HIV-1NL4−R3A and stHIV-1sv replication in NPMs. This result suggests NPM is a potential HIV/AIDS animal model.

Activation of NF-κB induced by TRIMCyp showing a discrepancy between owl monkey and northern pig-tailed macaque

TRIMCyp generated by retrotransposition of a cyclophilin A inserting into TRIM5 locus, has been identified in owl monkey and most of Old World monkeys (OWM). Owl monkey TRIMCyp (omTRIMCyp) inhibits HIV-1 infection by direct interaction with viral capsid and indirect innate immune induction, whereas most of TRIMCyps from OWM cannot inhibit HIV-1, and the impact of which on immunoregulation is largely unknown. Here we reported that omTRIMCyp induces NF-κB, AP-1 and IFN-β activation in a dose-dependent manner, while TRIMCyp from northern pig-tailed macaque (npmTRIMCyp) does not activate NF-κB and moderately enhances AP-1 and IFN-β activities. The Cyclophilin A (CypA) domain plays an important role in omTRIMCyp-mediated NF-κB activation, and RBCC domains have a synergetic effect. We further indicated the mechanism by which npmTRIMCyp unable to activate NF-κB is that npmTRIMCyp hardly phosphorylates IκBα, different from omTRIMCyp which dramatically induces IκBα phosphorylation. Ubiquitination activity of omTRIMCyp was greater than npmTRIMCyp, although both could be ubiquitylated. Given that npmTRIMCyp neither interacts with viral capsid resulting in susceptibility to HIV-1 infection, nor activates NF-κB that is indispensable to HIV-1 provirus transcription, we proposed a model that npmTRIMCyp may play an important role in HIV-1 infected northern pig-tailed macaque with latency.

Parasites may exit immunocompromised northern pig-tailed macaques (Macaca leonina) infected with SIVmac239.

Parasites can increase infection rates and pathogenicity in immunocompromised human immunodeficiency virus (HIV) patients. However, in vitro studies and epidemiological investigations also suggest that parasites might escape immunocompromised hosts during HIV infection. Due to the lack of direct evidence from animal experiments, the effects of parasitic infections on immunocompromised hosts remain unclear. Here, we detected 14 different parasites in six northern pig-tailed macaques (NPMs) before or at the 50th week of simian immunodeficiency virus (SIV) infection by ELISA. The NPMs all carried parasites before viral injection. At the 50th week after viral injection, the individuals with negative results in parasitic detection (i.e., 08247 and 08287) were characterized as the Parasites Exit (PE) group, with the other individuals (i.e., 09203, 09211, 10205, and 10225) characterized as the Parasites Remain (PR) group. Compared with the PR group, the NPMs in the PE group showed higher viral loads, lower CD4+ T cells counts, and lower CD4/CD8 rates. Additionally, the PE group had higher immune activation and immune exhaustion of both CD4+ and CD8+ T cells. Pathological observation showed greater injury to the liver, cecum, colon, spleen, and mesenteric lymph nodes in the PE group. This study showed more seriously compromised immunity in the PE group, strongly indicating that parasites might exit an immunocompromised host.

Extractive foraging of toxic caterpillars in wild northern pig-tailed macaques (Macaca leonina).

Extractive foraging in nonhuman primates may involve different levels of technical complexity in terms of the number of actions that must be performed and the manual dexterity involved. We describe the extractive foraging of caterpillars in wild northern pig-tailed macaques (Macaca leonina) at Khao Yai National Park, Thailand. The study group, observed from May to December 2016 (n=146days), comprised 60-70 habituated individuals, including 3-4 adult males, 20-23 adult females, and 36-47 immatures. Four adult males and five adult females, observed from September to November 2016 for a total of 24days, were selected for focal animal sampling. Northern pig-tailed macaques were observed eating at least two families (Erebidae and Limacodidae) and three genera (Macrobrochis sp., Phlossa sp. and Scopelodes sp.) of caterpillars. While the monkeys ate short and small caterpillars with stinging setae and non-setae caterpillars without processing, they performed extensive caterpillar-rubbing behavior on large and long caterpillars with stinging setae. Based on 61 extractive foraging bouts, we found that caterpillar rubbing was hierarchically organized into five stages and 12 elements. Five stages of behavior sequence started with picking the caterpillar up, transporting it to a substrate, rubbing it to remove stinging setae, ingesting it, and then cleaning hands and mouth. Only adult macaques were observed using a leaf to rub stinging caterpillars.

Characterization of classical major histocompatibility complex (MHC) class II genes in northern pig-tailed macaques (Macaca leonina)

The northern pig-tailed macaque (Macaca leonina) has been identified as an independent species from the pig-tailed macaque group. The species is a promising animal model for HIV/AIDS pathogenesis and vaccine studies due to susceptibility to HIV-1. However, the major histocompatibility complex (MHC) genetics in northern pig-tailed macaques remains poorly understood. We have previously studied the MHC class I genes in northern pig-tailed macaques and identified 39 novel alleles. Here, we describe the MHC class II alleles in all six classical loci (DPA, DPB, DQA, DQB, DRA, and DRB) from northern pig-tailed macaques using a sequence-based typing method for the first time. A total of 60 MHC-II alleles were identified of which 27 were shared by other macaque species. Additionally, northern pig-tailed macaques expressed a single DRA and multiple DRB genes similar to the expression in humans and other macaque species. Polymorphism and positive selection were detected, and phylogenetic analysis suggested the presence of a common ancestor in human and northern pig-tailed macaque MHC class II allelic lineages at the DQA, DQB, and DRB loci. The characterization of full-length MHC class II alleles in this study significantly improves understanding of the immunogenetics of northern pig-tailed macaques and provides the groundwork for future animal model studies.

Identification of the major histocompatibility complex class-II DM and DO alleles in a cohort of northern pig-tailed macaques (Macaca leonina).

The northern pig-tailed macaque (Macaca leonina) has been considered as an independent species from the pig-tailed macaque group. We have previously reported that this species macaque has the potential to be a useful animal model in HIV/AIDS pathogenesis and vaccine studies due to its susceptibility to HIV-1. To develop this animal into a potential HIV/AIDS model, we have studied the classical MHC genes of this animal. In this study, the non-classical MHC genes Malo-DM and Malo-DO alleles were first characterized by sequencing and cloning in 12 unrelated northern pig-tailed macaques. A total of 20 full-length sequences identified include 4 Malo-DMA, 5 Malo-DMB, 7 Malo-DOA, and 4 Malo-DOB alleles. Most of these allele sequences were shared between northern pig-tailed macaque and other macaque species in exon 2. The full-length MHC-DM and MHC-DO sequences provide more comprehensive analysis of immunogenetics of northern pig-tailed macaques and increase the value of the macaques in further biomedical studies.

HIV-1 can infect northern pig-tailed macaques (Macaca leonina) and form viral reservoirs in vivo

Viral reservoirs of HIV-1 are a major obstacle for curing AIDS. The novel animal models that can be directly infected with HIV-1 will contribute to develop effective strategies for eradicating infections. Here, we inoculated 4 northern pig-tailed macaques (NPM) with the HIV-1 strain HIV-1NL4.3 and monitored the infection for approximately 3years (150weeks). The HIV-1-infected NPMs showed transient viremia for about 10weeks after infection. However, cell-associated proviral DNA and viral RNA persisted in the peripheral blood and lymphoid organs for about 3years. Moreover, replication-competent HIV-1 could be successfully recovered from peripheral blood mononuclear cells (PBMCs) during long-term infection. The numbers of resting CD4+ T cells in HIV-1 infected NPMs harboring proviruses fell within a range of 2- to 3-log10 per million cells, and these proviruses could be reactivated both ex vivo and in vivo in response to co-stimulation with the latency-reversing agents JQ1 and prostratin. Our results suggested that NPMs can be infected with HIV-1 and a long-term viral reservoir was formed in NPMs, which might serve asa potential model for HIV-1 reservoir research.

Predict disease progression from T-cell phenotypes in northern pig-tailed macaques (Macaca leonina) during SIVmac239 infection.

Macaca leonina (northern pig-tailed macaques, NPMs) have variable disease progression during SIVmac239 infection. In the present study, we analysed, for the first time, the correlations between T-cell phenotypes and disease progression in NPMs during SIVmac239 infection. In comparison to normal progressors (NPs), slow progressors (SPs) had lower chronic T-cell activation and exhaustion levels. In addition, SPs showed higher peripheral CD4+ T-cell count and CD4:CD8 ratio, and lower plasma viral load than NPs. CD4+ T-cell count and CD4:CD8 ratio decreased more sharply in NPs than in SPs. Furthermore, T cells in NPs were more highly differentiated, at least in acute infection, than in SPs. These results indicated that T-cell phenotypes were correlated with disease progression in SIVmac239-infected NPMs and these correlations may provide valuable guidance for the improvement of therapeutic strategies tested in NPMs.

HIV-1 can infect northern pig-tailed macaques (Macaca leonina) and form viral reservoirs in vivo

HIV-1 can infect northern pig-tailed macaques (Macaca leonina) and form viral reservoirs in vivo

Hand preference during bimanual coordinated task in northern pig-tailed macaques Macaca leonina.

In humans, handedness is one defining characteristic regardless of cultures and ethnicity. Population-level right handedness is considered to be related with the evolution of left hemisphere for manual control and language. In order to further understand evolutionary origins of human cerebral lateralization and its behavioral adaptation, standardized measures on hand preference are required to make reliable comparison in nonhuman primate species. In this study, we present the first evidence on hand preference during bimanual coordinated tasks in northern pig-tailed macaques Macaca leonina. The classical TUBE task was applied to examine hand preference among nine individuals from Tianjin Zoo of China. We recorded and made analysis on both frequency and bout data on manual laterality. The results consistently show that subjects displayed strong individual hand preferences, whereas no significant group-level handedness was found. There were no sex and age significant differences on both direction and strength of hand preference. The M. leonina preferred to use the index finger to extract the baited food inside the tube. Our findings fill the knowledge gap on primate handedness, and efficiently affirm the robustness of the TUBE task as one efficient measure of hand preference in primates.

Molecular cloning and anti-HIV-1 activities of APOBEC3s from northern pig-tailed macaques (Macaca leonina).

Northern pig-tailed macaques (NPMs, Macaca leonina) are susceptible to HIV-1 infection largely due to the loss of HIV-1-restricting factor TRIM5α. However, great impediments still exist in the persistent replication of HIV-1 in vivo, suggesting some viral restriction factors are reserved in this host. The APOBEC3 proteins have demonstrated a capacity to restrict HIV-1 replication, but their inhibitory effects in NPMs remain elusive. In this study, we cloned the NPM A3A-A3H genes, and determined by BLAST searching that their coding sequences (CDSs) showed 99% identity to the corresponding counterparts from rhesus and southern pig-tailed macaques. We further analyzed the anti-HIV-1 activities of the A3A-A3H genes, and found that A3G and A3F had the greatest anti-HIV-1 activity compared with that of other members. The results of this study indicate that A3G and A3F might play critical roles in limiting HIV-1 replication in NPMs in vivo. Furthermore, this research provides valuable information for the optimization of monkey models of HIV-1 infection.

Watering holes: The use of arboreal sources of drinking water by Old World monkeys and apes

Water is one of the most important components of an animal’s diet, as it is essential for life. Primates, as do most animals, procure water directly from standing or free-flowing sources such as pools, ponds and rivers, or indirectly by the ingestion of certain plant parts. The latter is frequently described as the main source of water for predominantly arboreal species. However, in addition to these, many species are known to drink water accumulated in tree-holes. This has been commonly observed in several arboreal New World primate species, but rarely reported systematically from Old World primates. Here, we report observations of this behaviour from eight great ape and Old World monkey species, namely chimpanzee, orangutan, siamang, western hoolock gibbon, northern pig-tailed macaque, bonnet macaque, rhesus macaque and the central Himalayan langur. We hypothesise three possible reasons why these primates drink water from tree-holes: (1) coping with seasonal or habitat-specific water shortages, (2) predator/human conflict avoidance, and (3) potential medicinal benefits. We also suggest some alternative hypotheses that should be tested in future studies. This behaviour is likely to be more prevalent than currently thought, and may have significant, previously unknown, influences on primate survival and health, warranting further detailed studies.

Viral seroprevalence in northern pig-tailed macaques (Macaca leonina) derived from Ho Chi Minh City, Vietnam.

Non-human primates are natural virus reservoirs, whether wild or domestic. In this study, we determined the seroprevalence of common viruses by ELISA in a northern pig-tailed macaque (Macaca leonina) colony derived from Ho Chi Minh City, Vietnam. A total of 20 types of virus which are commonly selected as target microorganisms for specific-pathogen-free colonies, or which have zoonotic potential were included in this study. The results showed only 2 in 90 northern pig-tailed macaques were seronegative for all the detected viruses, and at least 16 out of the total 20 types of virus tested were prevalent in this colony, so these macaques were commonly infected by various viruses. These macaques should be carefully assessed for viral seroprevalence in order to prevent zoonotic diseases from being transferred to human beings.