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Functional uniqueness of a small carnivore as seed dispersal agents: a case study of the common palm civets in the Tabin Wildlife Reserve, Sabah, Malaysia

Nakashima Y, Inoue E, Inoue-Murayama M, Abd Sukor JR

Oecologia, 2010 Nov;164(3):721-30.
PMID: 20602116 DOI: 10.1007/s00442-010-1714-1

Many carnivorous mammals consume fruits and disperse the intact seeds to specific sites. Few studies have attempted to quantify this seed dispersal or evaluate its effectiveness, despite its potential importance and functional uniqueness. In the study reported here, we found that a frugivorous carnivore, the common palm civet (Paradoxurus hermaphroditus), generated seed shadows that are distinct from those of the sympatric frugivore, the pig-tailed macaque (Macaca nemestrina), and played a unique and important role in the regeneration of Leea aculeata (Leeaceae). We found that macaques dispersed the seeds randomly, while civets dispersed them non-randomly to sites such as the banks of small rivers, rain-flow paths, abandoned trails, and treefall gaps, which are characterized by low stem density and canopy cover. Seeds of L. aculeata that were dispersed by civets to the banks of rivers and gaps had significantly higher survival and growth rates than those dispersed to rain-flow paths or abandoned trails. Seeds dispersed by macaques or to random locations also had low survival. Although the effects of the civets on seed fate were not straightforward, compared with macaques and random dispersal, civets significantly enhanced the survival and growth of L. aculeata seeds after 1 year. These results indicate that non-random dispersal by civets is important for the persistence of L. aculeata. Civets may disperse other plant species and thus could have profound effects on forest dynamics.

Matched MeSH terms: Macaca nemestrina/physiology*
Phylogeographic analysis of pigtail macaque populations (Macaca nemestrina) inferred from mitochondrial DNA

Rosenblum LL, Supriatna J, Melnick DJ

Am. J. Phys. Anthropol., 1997 Sep;104(1):35-45.
PMID: 9331452

Mitochondrial DNA variation was surveyed in nine populations of the pigtail macaque (Macaca nemestrina), covering all three recognized subspecies in Southeast Asia. To do this, a 2,300 base pair fragment spanning the mitochondrial NAD 3 and NAD 4 genes and flanking tRNA subunits leucine and glycine was targeted for amplification and digested with a battery of 16 restriction endonucleases. Out of a total of 107 individuals, 32 unique haplotypes could be distinguished. Parsimony and neighbor-joining analyses grouped the haplotypes into five strongly supported assemblages representing China/Thailand, Malaysia, Sumatra, Borneo, and Siberut. These results indicate that the mainland and island mtDNA haplotypes are strictly and uniquely limited to the geographic ranges of the recognized morphological subspecies. Cladistic and neighbor-joining analyses indicate that inferred phylogenies of mtDNA haplotypes are congruent with subspecies designations. Furthermore, in support of morphological studies, results indicate that the Mentawai macaque is most likely not a distinct species but a subspecies of M. nemestrina.

Matched MeSH terms: Macaca nemestrina/genetics*
[Observation of a photosensitive syndrome in Macaca nemestrina (author's transl)]

Balzamo E

Rev Electroencephalogr Neurophysiol Clin, 1981 Nov;11(2):289-93.
PMID: 7323374

Out of a group of 12 M. nemestrina (originating from Malaysia), 9 adults had shown clinical signs induced by ILS at 25 c/sec. Six of them (3 males, 3 females) were very photosensitive; however, only 2 presented eyelid and/or head jerks after the end of ILS (level 4), but never a generalized seizure. Tactile periorbital stimuli favoured myoclonus. In all but the two of level 4, the intensity of clinical signs varied from one day to the next. In all implanted adult macaques, spontaneous paroxysmal EEG activities were seen during slow sleep in mostly anterior areas, but also during waking and REM sleep in some of them; however, their occurrence depended upon the individual and were not in all cases related to their level of photosensitivity. During ILS, paroxysmal discharges (spikes and waves and/or polyspikes and waves), isolated or in bursts at 3-4/sec were bilateral and symmetrical. They started in fronto-rolandic regions, then became generalized. This observation constitutes a new fact since the discovery, in 1966, of the photomyoclonic syndrome of Papio papio, Macaca nemestrina being another species of subhuman primates with a marked predisposition to photosensitive epilepsy.

Matched MeSH terms: Macaca nemestrina/physiology*
Macaques can contribute to greener practices in oil palm plantations when used as biological pest control

Holzner A, Ruppert N, Swat F, Schmidt M, Weiß BM, Villa G, et al.

Curr Biol, 2019 10 21;29(20):R1066-R1067.
PMID: 31639346 DOI: 10.1016/j.cub.2019.09.011

Conversion of tropical forests into oil palm plantations reduces the habitats of many species, including primates, and frequently leads to human-wildlife conflicts. Contrary to the widespread belief that macaques foraging in the forest-oil palm matrix are detrimental crop pests, we show that the impact of macaques on oil palm yield is minor. More importantly, our data suggest that wild macaques have the potential to act as biological pest control by feeding on plantation rats, the major pest for oil palm crops, with each macaque group estimated to reduce rat populations by about 3,000 individuals per year (mitigating annual losses of 112 USD per hectare). If used for rodent control in place of the conventional method of poison, macaques could provide an important ecosystem service and enhance palm oil sustainability.

Matched MeSH terms: Macaca nemestrina*
Melioidotic osteomyelitis in an imported primate

Britt JO, Howard EB, Kean CJ, Jones J

J Am Vet Med Assoc, 1981 Dec 1;179(11):1303-5.
PMID: 7328029
Matched MeSH terms: Macaca nemestrina*
Fulltext Analysis of nuclear and organellar genomes of Plasmodium knowlesi in humans reveals ancient population structure and recent recombination among host-specific subpopulations

Diez Benavente E, Florez de Sessions P, Moon RW, Holder AA, Blackman MJ, Roper C, et al.

PLoS Genet, 2017 Sep;13(9):e1007008.
PMID: 28922357 DOI: 10.1371/journal.pgen.1007008

The macaque parasite Plasmodium knowlesi is a significant concern in Malaysia where cases of human infection are increasing. Parasites infecting humans originate from genetically distinct subpopulations associated with the long-tailed (Macaca fascicularis (Mf)) or pig-tailed macaques (Macaca nemestrina (Mn)). We used a new high-quality reference genome to re-evaluate previously described subpopulations among human and macaque isolates from Malaysian-Borneo and Peninsular-Malaysia. Nuclear genomes were dimorphic, as expected, but new evidence of chromosomal-segment exchanges between subpopulations was found. A large segment on chromosome 8 originating from the Mn subpopulation and containing genes encoding proteins expressed in mosquito-borne parasite stages, was found in Mf genotypes. By contrast, non-recombining organelle genomes partitioned into 3 deeply branched lineages, unlinked with nuclear genomic dimorphism. Subpopulations which diverged in isolation have re-connected, possibly due to deforestation and disruption of wild macaque habitats. The resulting genomic mosaics reveal traits selected by host-vector-parasite interactions in a setting of ecological transition.

Matched MeSH terms: Macaca nemestrina/genetics; Macaca nemestrina/parasitology
Fulltext Oil palm cultivation critically affects sociality in a threatened Malaysian primate

Holzner A, Balasubramaniam KN, Weiß BM, Ruppert N, Widdig A

Sci Rep, 2021 May 14;11(1):10353.
PMID: 33990658 DOI: 10.1038/s41598-021-89783-3

Human-induced habitat alterations globally threaten animal populations, often evoking complex behavioural responses in wildlife. This may be particularly dramatic when negatively affecting social behaviour, which fundamentally determines individual fitness and offspring survival in group-living animals. Here, we provide first evidence for significant behavioural modifications in sociality of southern pig-tailed macaques visiting Malaysian oil palm plantations in search of food despite elevated predation risk. Specifically, we found critical reductions of key positive social interactions but higher rates of aggression in the plantation interior compared to the plantation edge (i.e. plantation areas bordering the forest) and the forest. At the plantation edge, affiliation even increased compared to the forest, while central positions in the macaques' social network structure shifted from high-ranking adult females and immatures to low-ranking individuals. Further, plantations also affected mother-infant relationships, with macaque mothers being more protective in the open plantation environment. We suggest that although primates can temporarily persist in human-altered habitats, their ability to permanently adapt requires the presence of close-by forest and comes with a trade-off in sociality, potentially hampering individual fitness and infant survival. Studies like ours remain critical for understanding species' adaptability to anthropogenic landscapes, which may ultimately contribute to facilitating their coexistence with humans and preserving biodiversity.

Matched MeSH terms: Macaca nemestrina/psychology*
Fulltext Human infections with Plasmodium knowlesi--zoonotic malaria

Millar SB, Cox-Singh J

Clin Microbiol Infect, 2015 Jul;21(7):640-8.
PMID: 25843504 DOI: 10.1016/j.cmi.2015.03.017

In 2004 a large focus of Plasmodium knowlesi malaria was reported in the human population in Sarawak, Malaysian Borneo. Plasmodium knowlesi, a parasite of the South-East Asian macaques (Macaca fascicularis and Macaca nemestrina), had entered the human population. Plasmodium knowlesi is transmitted by the leucosphyrus group of Anopheline mosquitoes and transmission is largely zoonotic and restricted to the jungle setting. Humans entering jungle transmission sites are at risk. Since 2004, human cases of P. knowlesi have been continuously reported in local communities and in travellers returning from South East Asia. Plasmodium knowlesi is the most common type of indigenous malaria reported in Malaysia. Infections are most often uncomplicated but at least 10% of patients report with severe malaria and 1-2% of cases have a fatal outcome. Parasitaemia is positively associated with the clinical and laboratory markers of severe malaria. The current literature on P. knowlesi, including epidemiology, natural hosts and vectors, pathogenesis, clinical descriptions, treatment and diagnosis, is reviewed. There are many gaps in our understanding of this disease that are highlighted here with suggestions for further research to inform pre-emptive control measures that would be required to prevent a full emergence of this parasite into the human population.

Matched MeSH terms: Macaca nemestrina
Fulltext Agricultural habitat use affects infant survivorship in an endangered macaque species

Holzner A, Mohd Rameli NIA, Ruppert N, Widdig A

Curr Biol, 2024 Jan 22;34(2):410-416.e4.
PMID: 38194972 DOI: 10.1016/j.cub.2023.12.002

Infant survival is a major determinant of individual fitness and constitutes a crucial factor in shaping species' ability to maintain viable populations in changing environments.1 Early adverse conditions, such as maternal loss, social isolation, and ecological hazards, have been associated with reduced rates of infant survivorship in wild primates.2,3,4 Agricultural landscapes increasingly replacing natural forest habitats may additionally threaten the survival of infants through exposure to novel predators,5 human-wildlife conflicts,6,7 or the use of harmful chemicals.8,9 Here, we investigated potential links between agricultural habitat use and high infant mortality in wild southern pig-tailed macaques (Macaca nemestrina) inhabiting a mosaic landscape of rainforest and oil palm plantation in Peninsular Malaysia. Longitudinal data revealed that 57% of all infants born during the study period (2014-2023) died before the age of 1 year, far exceeding mortality rates reported for other wild primates.10,11,12,13,14 Importantly, prolonged time spent in the plantation during infancy decreased the likelihood of infant survival by 3-fold, likely caused by increased exposure to the threats inherent to this environment. Further, mortality risk was elevated for infants born to primiparous mothers and predicted by prolonged maternal interbirth intervals, suggesting potential long-term effects attributed to the uptake and/or accumulation of pesticides in mothers' bodies.15,16,17 Indeed, existing literature reports that pesticides may cross the placental barrier, thus impacting fetal development during pregnancy.18,19,20 Our findings emphasize the importance of minimizing anthropogenic threats to wildlife in agricultural landscapes by establishing environmentally friendly cultivation practices that can sustain wildlife populations in the long term.

Matched MeSH terms: Macaca nemestrina
Prevalence of parasites in working pig-tailed Macaques (Macaca nemestrina) in Kelantan, Malaysia

Choong SS, Mimi Armiladiana M, Ruhil HH, Peng TL

J Med Primatol, 2019 08;48(4):207-210.
PMID: 31025372 DOI: 10.1111/jmp.12416

BACKGROUND: Coconut is an important commodity in Kelantan, and pig-tailed macaques (Macaca nemestrina) have been traditionally used for coconut-plucking for over a century. Most of these animals were sourced from the wild population, and the parasitic status of these macaques is unknown, plus the impacts caused by these parasites are usually underestimated by the owners.
METHODS: A total of 30 macaques were sampled for blood, faeces and hair plucks to detect parasite.
RESULTS: Out of 21 faecal samples examined, 11 (52%) were determined positive for one or more gastrointestinal parasites, namely Trichostrongylus spp., Strongyloides spp., Anatrichosoma spp., Capillaria spp., Trichuris spp. and Paramphisotomum spp. Filaria was detected in one (3%) of the blood samples. For ectoparasites, only lice, Pedicinus sp., were found in 9 (30%) macaques.
CONCLUSIONS: It is imperative that the parasitic status of these animals be determined so that necessary actions and preventive measures can be implemented to prevent zoonotic transmissions.

Matched MeSH terms: Macaca nemestrina*
Reversible anesthesia of Southeast Asian primates with medetomidine, zolazepam, and tiletamine

Fahlman A, Bosi EJ, Nyman G

J. Zoo Wildl. Med., 2006 Dec;37(4):558-61.
PMID: 17315446

Medetomidine (0.02-0.06 mg/kg) in combination with zolazepam-tiletamine (0.8-2.3 mg/kg) were evaluated for reversible anesthesia in four species of Southeast Asian primates: Bornean orangutan (Pongo pygmaeus pygmaeus), Bornean gibbon (Hylobates muelleri), long-tailed macaque (Macaca fascicularis), and pig-tailed macaque (Macaca nemestrina). Twenty-three anesthetic procedures of captive-held and free-ranging primates were studied in Sabah, Malaysia. The induction was smooth and rapid. Respiratory and heart rates were stable throughout anesthesia, whereas body temperature and systolic arterial blood pressure decreased significantly. Atipamezole at five times the medetomidine dose effectively reversed anesthesia, with first signs of recovery within 3-27 min.

Matched MeSH terms: Macaca nemestrina/physiology*
Fulltext Admixture in Humans of Two Divergent Plasmodium knowlesi Populations Associated with Different Macaque Host Species

Divis PC, Singh B, Anderios F, Hisam S, Matusop A, Kocken CH, et al.

PLoS Pathog, 2015 May;11(5):e1004888.
PMID: 26020959 DOI: 10.1371/journal.ppat.1004888

Human malaria parasite species were originally acquired from other primate hosts and subsequently became endemic, then spread throughout large parts of the world. A major zoonosis is now occurring with Plasmodium knowlesi from macaques in Southeast Asia, with a recent acceleration in numbers of reported cases particularly in Malaysia. To investigate the parasite population genetics, we developed sensitive and species-specific microsatellite genotyping protocols and applied these to analysis of samples from 10 sites covering a range of >1,600 km within which most cases have occurred. Genotypic analyses of 599 P. knowlesi infections (552 in humans and 47 in wild macaques) at 10 highly polymorphic loci provide radical new insights on the emergence. Parasites from sympatric long-tailed macaques (Macaca fascicularis) and pig-tailed macaques (M. nemestrina) were very highly differentiated (FST = 0.22, and K-means clustering confirmed two host-associated subpopulations). Approximately two thirds of human P. knowlesi infections were of the long-tailed macaque type (Cluster 1), and one third were of the pig-tailed-macaque type (Cluster 2), with relative proportions varying across the different sites. Among the samples from humans, there was significant indication of genetic isolation by geographical distance overall and within Cluster 1 alone. Across the different sites, the level of multi-locus linkage disequilibrium correlated with the degree of local admixture of the two different clusters. The widespread occurrence of both types of P. knowlesi in humans enhances the potential for parasite adaptation in this zoonotic system.

Matched MeSH terms: Macaca nemestrina/parasitology*
Fulltext Defining the ecological and evolutionary drivers of Plasmodium knowlesi transmission within a multi-scale framework

Davidson G, Chua TH, Cook A, Speldewinde P, Weinstein P

Malar J, 2019 Mar 08;18(1):66.
PMID: 30849978 DOI: 10.1186/s12936-019-2693-2

Plasmodium knowlesi is a zoonotic malaria parasite normally residing in long-tailed and pig-tailed macaques (Macaca fascicularis and Macaca nemestrina, respectively) found throughout Southeast Asia. Recently, knowlesi malaria has become the predominant malaria affecting humans in Malaysian Borneo, being responsible for approximately 70% of reported cases. Largely as a result of anthropogenic land use changes in Borneo, vectors which transmit the parasite, along with macaque hosts, are both now frequently found in disturbed forest habitats, or at the forest fringes, thus having more frequent contact with humans. Having access to human hosts provides the parasite with the opportunity to further its adaption to the human immune system. The ecological drivers of the transmission and spread of P. knowlesi are operating over many different spatial (and, therefore, temporal) scales, from the molecular to the continental. Strategies to prevent and manage zoonoses, such as P. knowlesi malaria require interdisciplinary research exploring the impact of land use change and biodiversity loss on the evolving relationship between parasite, reservoir hosts, vectors, and humans over multiple spatial scales.

Matched MeSH terms: Macaca nemestrina

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