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Hematological and blood chemistry values in captive Japanese macaques (Macaca fuscata fuscata)

Miyabe-Nishiwaki T, MacIntosh AJJ, Kaneko A, Morimoto M, Suzuki J, Akari H, et al.

J Med Primatol, 2019 Dec;48(6):338-350.
PMID: 31418873 DOI: 10.1111/jmp.12434

BACKGROUND: Biological information about captive Japanese macaques, including hematology and blood chemistry, is still lacking despite the fact that ethological and ecological data have accumulated during decades of field research.
METHODS: Hematological (511 examinations of 280 Japanese macaques) and blood chemistry data (between 33 and 284 examinations from between 29 and 257 individual macaques) in clinically healthy, simian retrovirus-free Japanese macaques tested between 2009 and 2013 were reviewed.
RESULTS AND CONCLUSIONS: Specific hematological and blood chemistry data for Japanese macaques without clinical signs of disease were provided in this study. Averages presented can be used as hematological parameters for Japanese macaques. Some differences between Japanese macaques and other closely related macaque species were found. Some parameters varied according to macaque age and sex, as well as regional origin. The data in this study will provide useful clinical indices for Japanese macaques in captive and similar conditions.
Evaluation of anaesthetic and cardiorespiratory effects after intramuscular administration of alfaxalone alone, alfaxalone-ketamine and alfaxalone-butorphanol-medetomidine in common marmosets (Callithrix jacchus)

Miyabe-Nishiwaki T, Miwa M, Konoike N, Kaneko A, Ishigami A, Natsume T, et al.

J Med Primatol, 2020 12;49(6):291-299.
PMID: 32654222 DOI: 10.1111/jmp.12482

BACKGROUND: Anaesthesia is often required in common marmosets undergoing various procedures. The aim of this study was to evaluate anaesthetic and cardiopulmonary effects of alfaxalone, alfaxalone-ketamine and alfaxalone-butorphanol-medetomidine in common marmosets.
METHODS: The following treatments were repeatedly administered to seven female common marmosets: Treatment A, alfaxalone (12 mg kg-1 ) alone; treatment AK, alfaxalone (1 mg animal-1 ) plus ketamine (2.5 mg animal-1 ); treatment AMB, alfaxalone (4 mg kg-1 ), medetomidine (50 µg kg-1 ) plus butorphanol (0.3 mg kg-1 ); and treatment AMB-Ati, AMB with atipamezole at 45 minutes.
RESULTS AND CONCLUSIONS: Marmosets became laterally recumbent and unresponsive for approximately 30 minutes in A and AK and for approximately 60 minutes in AMB. The animals showed rapid recovery following atipamezole injection in AMB-Ati. The decrease in heart rate and SpO2 was significantly greater in AMB compared to A and AK. Oxygen supplementation, anaesthetic monitors and atipamezole should be available especially when AMB is administered.
Fulltext Lurking in the dark: Cryptic Strongyloides in a Bornean slow loris

Frias L, Stark DJ, Lynn MS, Nathan SK, Goossens B, Okamoto M, et al.

Int J Parasitol Parasites Wildl, 2018 Aug;7(2):141-146.
PMID: 29988792 DOI: 10.1016/j.ijppaw.2018.03.003

Within host communities, related species are more likely to share common parasitic agents, and as a result, morphological similarities have led researchers to conclude that parasites infecting closely related hosts within a community represent a single species. However, genetic diversity within parasite genera and host range remain poorly investigated in most systems. Strongyloides is a genus of soil-transmitted nematode that has been reported from several primate species in Africa and Asia, and has been estimated to infect hundreds of millions of people worldwide, although no precise estimates are available. Here we describe a case of infection with a cryptic species of Strongyloides in a Bornean (Philippine) slow loris (Nycticebus menagensis) living within a diverse community of several primate species in the Lower Kinabatangan Wildlife Sanctuary, Malaysian Borneo. Fresh fecal samples were collected from five primate species and nematode larvae cultured from these samples were selected for phylogenetic analyses. Sequences obtained for most larvae were identified as S. fuelleborni, grouping into three different clusters and showing no aggregation within specific hosts or geographic location. In contrast, a set of parasite sequences obtained from a slow loris clustered closely with S. stercoralis into a different group, being genetically distinct to sequences reported from other primate hosts, humans included. Our results suggest that although S. fuelleborni infects all haplorrhines sampled in this primate community, a different species might be infecting the slow loris, the only strepsirrhine in Borneo and one of the least studied primates in the region. Although more data are needed to support this conclusion, we propose that Strongyloides species in primates might be more diverse than previously thought, with potential implications for ecological and evolutionary host-parasite associations, as well as epidemiological dynamics.
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.
Fulltext A pinworm's tale: The evolutionary history of Lemuricola (Protenterobius) nycticebi

Frias L, Hasegawa H, Stark DJ, Lynn MS, Nathan SK, Chua TH, et al.

Int J Parasitol Parasites Wildl, 2019 Apr;8:25-32.
PMID: 30619706 DOI: 10.1016/j.ijppaw.2018.11.009

Lemuricola (Protenterobius) nycticebi is the only pinworm species known to infect strepsirrhine primates outside Africa, and the only pinworm species yet described in slow lorises. Here, we provided a detailed morphological comparison of female and male worms, and a first description of fourth-stage larvae collected from free-living slow lorises (Nycticebus menagensis) in Sabah, Malaysian Borneo. Using mitochondrial and nuclear markers, we also reconstructed the species' phylogenetic relationship with other pinworms infecting primates. Both morphological and molecular results indicated a distinct association between L. (P.) nycticebi and its host. However, while taxonomy identified this species as a member of the Lemuricola clade and grouped pinworms infecting lemurs and slow lorises together, phylogenetic reconstruction split them, placing L. (P.) nycticebi within the Enterobius clade. Our results suggest that L. (P.) nycticebi may represent a different taxon altogether, and that it is more closely related to pinworm species infecting Old World primates outside Madagascar. Pongobius pongoi (Foitová et al., 2008) n. comb. is also proposed.
Fulltext Parasite community structure in sympatric Bornean primates

Frias L, Hasegawa H, Chua TH, Sipangkui S, Stark DJ, Salgado-Lynn M, et al.

Int J Parasitol, 2021 10;51(11):925-933.
PMID: 33862059 DOI: 10.1016/j.ijpara.2021.03.003

Parasites are important components of ecosystems, influencing trophic networks, competitive interactions and biodiversity patterns. Nonetheless, we are not nearly close to disentangling their complex roles in natural systems. Southeast Asia falls within global areas targeted as most likely to source parasites with zoonotic potential, where high rates of land conversion and fragmentation have altered the circulation of wildlife species and their parasites, potentially resulting in altered host-parasite systems. Although the overall biodiversity in the region predicts equally high, or even higher, parasite diversity, we know surprisingly little about wild primate parasites, even though this constitutes the first step towards a more comprehensive understanding of parasite transmission processes. Here, we characterise the gastrointestinal helminth parasite assemblages of a community of Bornean primates living along the Kinabatangan floodplain in Sabah (Malaysian Borneo), including two species endemic to the island. Through parasitological analyses, and by using several measures of parasite infection as proxies for parasite diversity and distribution, we show that (i) most parasite taxonomic groups are not limited to a single host, suggesting a greater flexibility for habitat disturbance, (ii) parasite infracommunities of nocturnal primates differ from their diurnal counterparts, reflecting both phylogenetic and ecological constraints, and (iii) soil-transmitted helminths such as whipworm, threadworm and nodule worm are widespread across the primate community. This study also provides new parasite records for southern pig-tailed macaques (Macaca nemestrina), silvered langurs (Trachypithecus cristatus) and Western tarsiers (Cephalopachus bancanus) in the wild, while adding to the limited records for the other primate species in the community. Given the information gap regarding primate-parasite associations in the region, the information presented here should prove relevant for future studies of parasite biodiversity and infectious disease ecology in Asia and elsewhere.
First description of male worms of Enterobius (Colobenterobius) serratus (Nematoda: Oxyuridae), the pinworm parasite of proboscis monkeys

Hasegawa H, Frias L, Peter S, Hasan NH, Stark DJ, Lynn MS, et al.

Zootaxa, 2020 Jan 14;4722(3):zootaxa.4722.3.6.
PMID: 32230627 DOI: 10.11646/zootaxa.4722.3.6

Males of Enterobius (Colobenterobius) serratus Hasegawa et al., 2003 (Nematoda: Oxyuridae) are described for the first time based on six individuals collected from the feces of proboscis monkeys, Nasalis larvatus, in the Lower Kinabatangan Wildlife Sanctuary, Sabah, Malaysian Borneo. The males show identical cephalic morphology to females, being readily distinguishable from their congeners by the serrated inner margins of the lips. The bicolored esophageal corpus, long thin spicule and developed spicular pouch with paired muscular bands are also remarkable characteristics, presumably shared by other Asian members of the subgenus.
Fulltext Dominance style only partially predicts differences in neophobia and social tolerance over food in four macaque species

Amici F, Widdig A, MacIntosh AJJ, Francés VB, Castellano-Navarro A, Caicoya AL, et al.

Sci Rep, 2020 Dec 16;10(1):22069.
PMID: 33328593 DOI: 10.1038/s41598-020-79246-6

Primates live in complex social systems with social structures ranging from more to less despotic. In less despotic species, dominance might impose fewer constraints on social choices, tolerance is greater than in despotic species and subordinates may have little need to include novel food items in the diet (i.e. neophilia), as contest food competition is lower and resources more equally distributed across group members. Here, we used macaques as a model to assess whether different dominance styles predict differences in neophilia and social tolerance over food. We provided familiar and novel food to 4 groups of wild macaques (N = 131) with different dominance styles (Macaca fuscata, M. fascicularis, M. sylvanus, M. maura). Our study revealed inter- and intra-specific differences in individuals' access to food, which only partially reflected the dominance styles of the study subjects. Contrary to our prediction, social tolerance over food was higher in more despotic species than in less despotic species. Individuals with a higher dominance rank and being better socially integrated (i.e. higher Eigenvector centrality) were more likely to retrieve food in all species, regardless of their dominance style. Partially in line with our predictions, less integrated individuals more likely overcame neophobia (as compared to more integrated ones), but only in species with more tolerance over food. Our study suggests that individual characteristics (e.g. social integration or personality) other than dominance rank may have a stronger effect on an individual's access to resources.
Fulltext Novel insight into the genetic diversity of strongylid nematodes infecting South-East and East Asian primates

Mason B, Cervena B, Frias L, Goossens B, Hasegawa H, Keuk K, et al.

Parasitology, 2024 Apr;151(5):514-522.
PMID: 38629119 DOI: 10.1017/S0031182024000386

With many non-human primates (NHPs) showing continued population decline, there is an ongoing need to better understand their ecology and conservation threats. One such threat is the risk of disease, with various bacterial, viral and parasitic infections previously reported to have damaging consequences for NHP hosts. Strongylid nematodes are one of the most commonly reported parasitic infections in NHPs. Current knowledge of NHP strongylid infections is restricted by their typical occurrence as mixed infections of multiple genera, which are indistinguishable through traditional microscopic approaches. Here, modern metagenomics approaches were applied for insight into the genetic diversity of strongylid infections in South-East and East Asian NHPs. We hypothesized that strongylid nematodes occur in mixed communities of multiple taxa, dominated by Oesophagostomum, matching previous findings using single-specimen genetics. Utilizing the Illumina MiSeq platform, ITS-2 strongylid metabarcoding was applied to 90 samples from various wild NHPs occurring in Malaysian Borneo and Japan. A clear dominance of Oesophagostomum aculeatum was found, with almost all sequences assigned to this species. This study suggests that strongylid communities of Asian NHPs may be less species-rich than those in African NHPs, where multi-genera communities are reported. Such knowledge contributes baseline data, assisting with ongoing monitoring of health threats to NHPs.