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Intraspecific variation of Taenia taeniaeformis as determined by various criteria

Azuma H, Okamoto M, Oku Y, Kamiya M

Parasitol Res, 1995;81(2):103-8.
PMID: 7731915

The intraspecific variation of four laboratory-reared isolates of Taenia taeniaformis the SRN and KRN isolates from Norway rats, Rattus norvegicus, captured in Japan and Malaysia, respectively; the BMM isolated from a house mouse, Mus musculus, captured in Belgium; and the ACR isolate from a gray red-backed vole, Clethrionomys rufocanus bedfordiae, captured in Japan was examined by various criteria. Eggs of each of the four isolates were orally inoculated into several species of intermediate host. They were most infective to the rodent species from which the original metacestode of each isolate had been isolated in the field, and only the ACR isolate was infective to the gray red-backed vole. Although little difference was found between the SRN, KRN, and BMM isolates by the other criteria, including the morphology of rostellar hooks, the protein composition of the metacestode, and restriction endonuclease analysis of DNA, the ACR isolate was clearly different from the others. It was considered that the ACR isolate was independent as a strain distinct from the other three isolates.
Geographical genetic structure within the human lung fluke, Paragonimus westermani, detected from DNA sequences

Blair D, Agatsuma T, Watanobe T, Okamoto M, Ito A

Parasitology, 1997 Oct;115 ( Pt 4):411-7.
PMID: 9364568

Nucleotide sequences were obtained for the second internal transcribed spacer of the ribosomal gene repeat and for part of the mitochondrial-cytochrome c oxidase subunit I gene from geographical isolates of Paragonimus westermani from Japan, China, Korea, Taiwan, the Philippines, peninsular Malaysia and Thailand. Sequences were obtained from several other species of Paragonimus for comparative purposes. Two groups were recognized within P. westermani: an NE group (China, Japan, Korea, Taiwan) which was relatively uniform and included both diploid and triploid forms, and a southern group (Malaysia, Thailand, Philippines), members of which were genetically distant from one another. According to both ITS2 and COI data, genetic distances among P. westermani isolates equalled or exceeded those between some distinct species of Paragonimus. The ITS2 sequences were conserved relative to COI sequences. Substitutions among the latter may be approaching saturation within the genus Paragonimus.
Developmental and morphological characteristics of Taenia taeniaeformis (Batsch, 1786) in Clethrionomys rufocanus bedfordiae and Rattus norvegicus from different geographical locations

Iwaki T, Nonaka N, Okamoto M, Oku Y, Kamiya M

J Parasitol, 1994 Jun;80(3):461-7.
PMID: 8195949

Developmental and morphological characteristics of 3 isolates of Taenia taeniaeformis isolated from Clethrionomys rufocanus bedfordiae in Abuta (70 km southwest of Sapporo), Japan (isolate ACR), and from Rattus norvegicus in Sapporo, Japan (isolate SRN) and Kuala Lumpur, Malaysia (isolate KRN) were compared. Eggs of 3 isolates were administered to several species of rodents. Isolate ACR infected C. rufocanus bedfordiae, Apodemus speciosus, and Apodemus argenteus, but not rats or mice, whereas isolate SRN and isolate KRN were infective to rats, mice, A. speciosus, and A. argenteus, but not to C. rufocanus bedfordiae. The increase in cyst size of isolate ACR continued during the experimental period, whereas that of the other 2 isolates had ceased growing after 30 days postinfection. However, significant differences were observed in the length of the small rostellar hooks, number and distribution of testes, and the length of the cirrus sac between isolate ACR and the other 2 isolates. Thus it is suggested that isolate ACR is a distinct strain or even a new species.
Intraspecific variation of isoenzymes in Taenia taeniaeformis

Okamoto M, Ito A, Kurosawa T, Oku Y, Kamiya M, Agatsuma T

Int J Parasitol, 1995 Feb;25(2):221-8.
PMID: 7622329

The technique of isoenzyme electrophoresis was applied to Japanese wild populations of Taenia taeniaeformis (isolated from Norway rats) and three laboratory reared isolates (KRN isolated from a Malaysian Norway rat, BMM from a Belgian house mouse and ACR from a Japanese gray red-backed vole). The average heterozygosities of Japanese wild populations were fairly small and total genetic variability was 0.0499. The genetic make-up of T. taeniaeformis in Norway rats was rather uniform in the whole of Japan. In KRN isolate, each of all 10 loci examined possessed the allele which was predominant in Japanese wild populations. Similarly, each of 9 loci in BMM isolate possessed the same alleles, but one of 2 alleles at HK locus was different from that in the others. T. taeniaeformis parasitizing house mice and rats were considered to be genetically closely related to each other. In ACR isolate, 7 out of 10 loci possessed different alleles from those in the other populations. It was considered that ACR isolate was genetically distant and its phylogenetic origin in Japan should be different from worms parasitizing Norway rats.
Infectivities of four isolates of Taenia taeniaeformis to various rodents

Nonaka N, Iwaki T, Okamoto M, Ooi HK, Oku Y, Ohbayashi M, et al.

J Vet Med Sci, 1994 Jun;56(3):565-7.
PMID: 7948394

Taenia taeniaeformis were isolated from Norway rats captured at Sapporo (SRN isolate) and Kuala Lumpur, Malaysia (KRN) and from Bedford's gray red-backed voles at Toubetsu (TCR) and Abuta (ACR). SRN, KRN and TCR isolates showed similar degree of infectivity to various rodents in which cysticerci with hooks were obtained in laboratory rats, white tuberous lesions in mice and no cysts or lesions in Mongolian gerbils and voles. Contrary to this, inoculation with ACR isolate eggs resulted in strobilocerci formation in the liver of voles, but no cysts were observed in rats, mice or gerbils. This host specificity of ACR isolate to voles suggests that it might be a new species of Taenia.
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.
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 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.

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