Anatomopathological lesions of infection caused by Platynosomum illiciens (Braun, 1901) in Neotropical primates kept in captivity

This study described the hepatobiliary anatomopathological lesions associated with trematode Platynosomum illiciens parasitism in Neotropical primates kept in captivity. In the evaluated organs, we observed portal fibrosis, biliary epithelial hyperplasia, and inflammatory reaction with a predominance of lymphocytes and plasmocytes, and in some cases infiltration of eosinophils and neutrophils.     

A multiyear survey of helminths from wild saddleback (Leontocebus weddelli) and emperor (Saguinus imperator) tamarins

The establishment of baseline data on parasites from wild primates is essential to understand how changes in habitat or climatic disturbances will impact parasite–host relationships. In nature, multiparasitic infections of primates usually fluctuate temporally and seasonally, implying that the acquisition of reliable data must occur over time. Individual parasite infection data from two wild populations of New World primates, the saddleback (Leontocebus weddelli) and emperor (Saguinus imperator) tamarin, were collected over 3 years to establish baseline levels of helminth prevalence and parasite species richness (PSR). Secondarily, we explored variation in parasite prevalence across age and sex classes, test nonrandom associations of parasite co‐occurrence, and assess the relationship between group size and PSR. From 288 fecal samples across 105 individuals (71 saddleback and 34 emperor tamarins), 10 parasite taxa were identified by light microscopy following centrifugation and ethyl‐acetate sedimentation. Of these taxa, none were host‐specific, Dicrocoeliidae and Cestoda prevalences differed between host species, Prosthenorchis and Strongylida were the most prevalent. Host age was positively associated with Prosthenorchis ova and filariform larva, but negatively with cestode and the Rhabditoidea ova. We detected no differences between expected and observed levels of co‐infection, nor between group size and parasite species richness over 30 group‐years. Logistic models of individual infection status did not identify a sex bias; however, age and species predicted the presence of four and three parasite taxa, respectively, with saddleback tamarins exhibiting higher PSR. Now that we have reliable baseline data for future monitoring of these populations, next steps involve the molecular characterization of these parasites, and exploration of linkages with health parameters.     

Molecular characterization of nodule worm in a community of Bornean primates

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.     

Epizootic fatal amebiasis in an outdoor group of Old World monkeys

Background Entamoeba (E.) histolytica is an obligate parasite of humans and non‐human primates. Methods This report describes the pathomorphological, immunohistological, and microbiological findings of fatal E. histolytica infection in two mantled guerezas (Colobus guereza) and one Hanuman langur (Semnopithecus entellus) from an epizootic outbreak of amebiasis in an open‐range recreation park. Results Pathomorphological examination revealed multifocal necrotizing and granulomatous hepatitis with intralesional protozoan trophozoites in all three cases. In addition, necrotizing and ulcerative gastritis was detected in both mantled guerezas. Furthermore, oligofocal acute pulmonary embolization was detected in one of these cases. No extra‐hepatic lesions were observed in the Hanuman langur. Immunohistological examination confirmed the etiologic diagnosis of E. histolytica‐induced lesions. Conclusions Although E. histolytica is a rarely diagnosed pathogen in Western European countries, veterinarians and animal keepers involved in handling and care taking of non‐human primates should be aware of the potential threat caused by this zoonotic parasite.     

First Characterization in China of Encephalitozoon cuniculi in the Blue Fox (Alopex lagopus)

Encephalitozoon cuniculi is a microsporidian parasite that infects a wide range of vertebrates, including primates. It has recently emerged as an opportunistic parasite of patients infected with the human immunodeficiency virus. The blue fox (Alopex lagopus; also known as the arctic fox) is one of the most susceptible species for encephalitozoonosis. Here, we report an outbreak of encephalitozoonosis at a fox farm in China. The isolated parasites displayed the typical morphology of E. cuniculi as assessed by Masson's trichrome staining. Analysis of the internal transcribed spacer sequence indicated that the isolated parasite is a genotype III strain of E. cuniculi. Furthermore, phylogenetic analysis of the PTP1 gene verifies classification of this new strain (termed LN‐1) with other genotype III E. cuniculi strains, though the PTP3 and SWP1 sequences diverge from the reference strain. This is the first report of encephalitozoonosis in farmed blue foxes in China.     

Parasites of Wild Howlers (Alouatta spp.)

A literature review of howler parasites provides the basis for an overview of the ecological significance of parasite surveys in primates. Within this framework, we have added insights into the interactions between primate hosts and their parasites from a long-term study in Costa Rica. We collected fecal samples from mantled howlers (Alouatta palliata) over a 9-year period (1986–1994 inclusive) and analyzed them for parasite eggs, larvae, cysts, and oocysts. We found many misperceptions inherent in the typical methodology of primate parasite surveys and in the reporting of the findings. Our work in Costa Rica suggests that a snapshot effect occurs with most surveys. A static view does not reflect the dynamic and changing ecological interaction between host and parasite. We describe some problems with parasite data analyses that emphasize the need for long-term longitudinal surveys in wild primate groups.     

Dicrocoeliidae (Trematoda: Digenea) of Australian mammals with description of Dicrocoelium antechini n. sp., Athesmioides aiolos n. g., n. sp. and Platynosomum burrman n. sp.

Dicrocoelium antechini n. sp. is described from the bile ducts of Antechinus swainsonii and A. stuartii (Marsupialia: Dasyuridae) from New South Wales. The species differs from all others in the genus in that the caecal bifurcation is well posterior to the ventral sucker and testes. Athesmioides aiolos n. g., n. sp. is described from Rattus fuscipes and R. lutreolus from New South Wales and from R. norvegicus, R. lutreolus and Pseudomys higginsi from Tasmania (all Rodentia: Muridae). The genus Athesmioides is characterised by the presence of unilateral vitelline follicles and an undivided caecum. Platynosomum burrman n. sp. is described from Isoodon macrourus (Marsupialia: Peramelidae) from the Northern Territory. It differs from other species in a combination of characters regarding the shape of the forebody, the arrangement of the gonads, the disposition of the uterus and the size of the eggs. The taxonomic status of Platynosomum australiense (Sandars, 1958), Brachylecithum insulare Angel & Pearson, 1977 and Brachylecithum hydromyos Angel & Pearson, 1977 are summarised. Records are presented of undescribed dicrocoeliids from the marsupials Petaurus breviceps, Planigale maculata and Dasyurus hallucatus and the murids Rattus fuscipes and Melomys sp.     

Gastrointestinal Parasites of Indigenous and Introduced Primate Species of Rubondo Island National Park,Tanzania

Translocation programs releasing animals into the wild need to assess the potential risks associated with the exchange of parasites and other pathogens between native and translocated species. We assessed the composition of the parasite communities in sympatric native and introduced primates. Over a 3-yr period we monitored the gastrointestinal parasites of 3 primate species living in the isolated ecosystem of Rubondo Island National Park, Tanzania: translocated chimpanzees (Pan troglodytes) and guerezas (Colobus guereza) and the indigenous vervets (Chlorocebus aethiops pygerythrus). We detected Troglodytella abrassarti and Enterobius cf. anthropopitheci only in chimpanzees and Chilomastix mesnili in chimpanzees and guerezas. In vervets, we recorded Anatrichosoma sp. and Subulura sp., previously reported in Rubondo chimpanzees. We found Blastocystis sp., Giardia sp., Iodamoeba buetschlii, Entamoeba coli, Entamoeba spp., Trichuris sp., Strongyloides spp., spirurids (cf. Protospirura muricola), and undetermined strongylids in all 3 primate species. Considering the absence of Protospirura muricola in other wild populations of chimpanzees and guerezas, it has probably been acquired from the native vervets, as have Anatrichosoma sp. and Subulura sp. Lower parasite load in Rubondo chimpanzees, in comparison with wild populations at other study sites of this species, might be due to their stay in captivity in Europe before being released on the island. Despite a lack of any apparent health problems from infections in introduced Rubondo primates, parasite monitoring during reintroduction/introduction projects is necessary to decrease potential risks resulting from the exchange of parasites between translocated and native species.     

Intestinal parasites of sympatric Pan troglodytes and Papio Spp. at two sites: Gombe (Tanzania) and Mt. Assirik (Senegal)

Experimental and clinical parasitology need natural baselines or “controls”. We present normative data intestinal parasite loads in two genera of African primates. Wild Pan troglodytes and Papio spp. were studied at two sites: Gombe in Tanzania (P. anubis) and Mt. Assirik in Senegal (P. papio). Presence or absence of parasites, especially nematodes, was recorded from fecal specimens. Gombe's primates were more often infected than were Mt. Assirik's. At Gombe, but not at Mt. Assirik, chimpanzees seemed to have a higher incidence of infection than baboons. Comparison of three baboon troops yielded apparent differences in prevalence of infection. No differences in infection were found between the wet and dry seasons in Mt. Assirik's chimpanzees.     

Genetic diversity of primate strongylid nematodes: Do sympatric nonhuman primates and humans share their strongylid worms?

The close phylogenetic relationship between humans and nonhuman primates (NHPs) can result in a high potential for pathogen exchange. In recent decades, NHP and human interactions have become more frequent due to increasing habitat encroachment and ecotourism. Strongylid communities, which include members of several genera, are typically found in NHPs. Using optimized high‐throughput sequencing for strain‐level identification of primate strongylids, we studied the structure of strongylid communities in NHPs and humans co‐habiting a tropical forest ecosystem in the Central African Republic. General taxonomic assignment of 85 ITS‐2 haplotypes indicated that the studied primates harbour at least nine genera of strongylid nematodes, with Oesophagostomum and Necator being the most prevalent. We detected both host‐specific and shared strongylid haplotypes. Skin‐penetrating Necator gorillaehaplotypes were shared between humans and gorillas but Necator americanus were much more restricted to humans. Strongylid communities of local hunter‐gatherers employed as trackers were more similar to those of gorillas compared to their relatives, who spent more time in villages. This was due to lower abundance of human‐origin N. americanus in both gorillas and trackers. Habituated gorillas or those under habituation did not show larger overlap of strongylids with humans compared to unhabituated. We concluded that the occurrence of the human‐specific strongylids in gorillas does not increase with direct contact between gorillas and humans due to the habituation. Overall, our results indicate that the degree of habitat sharing between hosts, together with mode of parasite transmission, are important factors for parasite spillover among primates.     

Effects of Ecology on the Gastrointestinal Parasites of Alouatta pigra

We examined the effects of demographic and ecological variables on the prevalence of intestinal parasites in free-ranging black howlers, Alouatta pigra, from Belize and Mexico. We collected 253 fecal samples from 50 individually identified monkeys during 2003. We processed all samples via standard centrifugation concentration techniques with sugar and zinc sulfate as flotation media. We used antigen capture enzyme-linked immunosorbent assays to detect protozoa. We analyzed data for each season separately. The most important factor in predicting whether an Alouatta pigra would be infected with a parasite was its membership in a particular social troop. It was not possible to isolate the effects of human presence, forest fragmentation, primate density, and the absence of Ateles geoffroyi on the prevalence of parasites in Alouatta pigra because the factors covaried. We detected few species of gastrointestinal parasites, possibly due to Alouatta pigra’s arboreal and herbivorous lifestyle and small geographic range. The prevalence of each parasite had a different pattern, with Controrchis sp. (presumed to be C. biliophilus), a fluke, tending to be more prevalent in Alouatta pigra that inhabited disturbed habitats, and Trypanoxyuris minutus, a pinworm, tending to be more prevalent in primates from undisturbed habitats. Giardia sp. tended to be more prevalent in primates at high densities. These results indicated that it is important to examine each parasite’s infection pattern separately to obtain a more accurate representation of the dynamics among the host, parasites, and ecology.     

Plasmodium vivax under the microscope: the Aotus model

The Aotus model for vivax malaria is extremely useful both as a source of living parasites in non-endemic areas, and as a model for vaccine and drug development research. Several species of New World primates can be infected with numerous different strains of Plasmodium vivax. This article reviews some aspects of the Aotus model, discusses the frequently observed hematological changes that can confound interpretation of hemogram data during the course of vivax infection, and provides a partial atlas of parasite forms and Aotus nancymai blood cells.     

<Emphasis Type="Italic">Strongyloides stercoralis</Emphasis> infection in a Finnish kennel

Background  

Intestinal threadworm Strongyloides stercoralis is a parasite of dog, cat and primates that occurs worldwide being most prevalent in tropical and subtropical countries. The adult parasitic worm is about 2 mm long and slender. It possesses both parasitic and free-living lifecycles. The parasitic worms are females. Strongyloides stercoralis infects the host via percutaneous, peroral or transmammary transmission in addition to autoinfection. Clinical disease varies from inapparent to severe enteritis and pneumonia. The diagnosis is based on demonstration of larvae in fresh faeces, which is best made by Baermann technique.     

Enzootic simian piroplasm (Entopolypoides macaci ) in wild-caught Kenyan non-human primates

Background Three species of non‐human primates comprising African green monkeys (AGMs), (Cercopithecus aethiops, n = 89), Syke’s monkeys (Cercopithecus mitis, n = 60) and olive baboons (Papio cynocephalus anubis, n = 30), were screened for Entopolypoides macaci. Methods Observation of blood smears prepared from these animals revealed E. macaci infection rate of 42.7% in AGMs, 35% in Syke’s monkeys and 33.3% in baboons. Results Gender infection rate was 38.2% in females and 29% in males. Statistically, there was no significant difference in infection rates between the monkey species and sexes (P > 0.05). Subsequent indirect immuno fluorescent antibody test supported the morphological appearance of E. macaci observed by microscopy. Sera from infected animals reacted positively (1:625) with E. macaci antigen, but not to Babesia bigemina or B. bovis antigen at 1:125 titer. Conclusion This study has revealed high prevalence of E. macaci infection in all three widely distributed Kenyan non‐human primates. With the continued use of these animals as models for human parasitic diseases, the presence of this highly enzootic parasite should be noted.     

Trypanosoma cruzi in non-human primates with a history of stillbirths: a retrospective study (Papio hamadryas spp.) and case report (Macaca fascicularis)

Background Congenital transmission of Trypanosoma cruzi has been described in humans and experimental work has been conducted with mice, but not with non‐human primates (NHPs). Methods We conducted a retrospective study of female baboons (Papio hamadryas spp.) naturally seropositive or seronegative for T. cruzi with history of fetal loss, and we report a stillbirth in a cynomolgus macaque (Macaca fascicularis) with placental T. cruzi amastigotes. Results There were no differences in menstrual cycle parameters and the number of fetal losses between seropositive and seronegative baboons with history of fetal loss. The amount of parasite DNA detected using quantitative polymerase chain reaction (Q‐PCR) in M. fascicularis placenta was within the range detected in infected baboon tissues. Conclusions There is no evidence that chronic maternal T. cruzi infection causes fetal loss in baboons. Q‐PCR is a useful diagnostic tool to study archived NHP placentas.     

Links between habitat degradation,and social group size,ranging, fecundity,and parasite prevalence in the Tana River mangabey (Cercocebus galeritus)

We investigated the effects of anthropogenic habitat degradation on group size, ranging, fecundity, and parasite dynamics in four groups of the Tana River mangabey (Cercocebus galeritus). Two groups occupied a forest disturbed by human activities, while the other two occupied a forest with no human disturbance. We predicted that the groups in the disturbed forest would be smaller, travel longer distances daily, and have larger home ranges due to low food tree abundance. Consequently, these groups would have lower fecundity and higher parasite prevalence and richness (number of parasite species). We measured the abundance of food trees and anthropogenic activity in the forests, the groups' daily travel distances and home range sizes, and censused social groups over 12 months. We also analyzed fecal samples for gastrointestinal parasites from three of the groups. The disturbed forest had a lower abundance of food trees, and groups in this forest traveled longer distances, had larger home range sizes, were smaller, and had lower fecundity. The groups in the disturbed forest had higher, although not statistically significant, parasite prevalence and richness. This study contributes to a better understanding of how anthropogenic habitat change influences fecundity and parasite infections in primates. Our results also emphasize the strong influence of habitat quality in determining daily travel distance and home range size in primates. Am J Phys Anthropol, 2009. © 2009 Wiley‐Liss, Inc.     

A taxonomic study of Strongyloides Grassi, 1879 (Nematoda) with special reference to Strongyloides fuelleborni von linstow, 1905 in man in Papua New Guinea and the description of a new subspecies

The taxonomic position of a Strongyloides species parasitic in man in Papua New Guinea (PNG) that apparently resembled S. fuelleborni (a parasite of man and other primates in tropical Africa) has not been resolved since its discovery in 1973. The results of a morphological (by scanning electron microscopy) and morphometric study were considered together with the results of a separate isoenzyme electrophoretic study of the same material. The nature of the peri-vulval cuticle of the parasitic female and the position of the phasmidial pore of the free-living male were found to be of particular use in addressing this taxonomic problem. We concluded that the Strongyloides in Africa and PNG are subspecies of S. fuelleborni. We propose the name S. fuelleborni kellyi n. subsp. for the Strongyloides found in man in PNG.     

Evolution of the primate cytochrome c oxidase subunit II gene

We examined the nucleotide and amino acid sequence variation of the cytochrome c oxidase subunit II (COII) gene from 25 primates (4 hominoids, 8 Old World monkeys, 2 New World monkeys, 2 tarsiers, 7 lemuriforms, 2 lorisiforms). Marginal support was found for three phylogenetic conclusions: (1) sister-group relationship between tarsiers and a monkey/ape clade, (2) placement of the aye-aye (Daubentonia) sister to all other strepsirhine primates, and (3) rejection of a sister-group relationship of dwarf lemurs (i.e., Cheirogaleus) with lorisiform primates. Stronger support was found for a sister-group relationship between the ring-tail lemur (Lemur catta) and the gentle lemurs (Hapalemur). In congruence with previous studies on COII, we found that the monkeys and apes have undergone a nearly two-fold increase in the rate of amino acid replacement relative to other primates. Although functionally important amino acids are generally conserved among all primates, the acceleration in amino acid replacements in higher primates is associated with increased variation in the amino terminal end of the protein. Additionally, the replacement of two carboxyl-bearing residues (glutamate and aspartate) at positions 114 and 115 may provide a partial explanation for the poor enzyme kinetics in cross-reactions between the cytochromes c and cytochrome c oxidases of higher primates and other mammals. Correspondence to: R.L. Honeycutt     

Positive selection underlies the species‐specific binding of Plasmodium falciparum RH5 to human basigin

Plasmodium falciparum, the causative agent of the deadliest form of malaria, is a member of the Laverania subgenus, which includes ape‐infecting parasites. P. falciparum is thought to have originated in gorillas, although infection is now restricted to humans. Laverania parasites display remarkable host‐specificity, which is partially mediated by the interaction between parasite ligands and host receptors. We analyse the evolution of BSG (basigin) and GYPA (glycophorin A) in primates/hominins, as well as of their Plasmodium‐encoded ligands, PfRH5 and PfEBA175. We show that, in primates, positive selection targeted two sites in BSG (F27 and H102), both involved in PfRH5 binding. A population genetics–phylogenetics approach detected the strongest selection for the gorilla lineage: one of the positively selected sites (K191) is a major determinant of PfRH5 binding affinity. Analysis of RH5 genes indicated episodic selection on the P. falciparum branch; the positively selected W447 site is known to stabilize the interaction with human basigin. Conversely, we detect no selection in the receptor‐binding region of EBA175 in the P. falciparum lineage. Its host receptor, GYPA, shows evidence of positive selection in all hominid lineages; selected codons include glycosylation sites that modulate PfEBA175 binding affinity. Data herein provide an evolutionary explanation for species‐specific binding of the PfRH5‐BSG ligand–receptor pair and support the hypothesis that positive selection at these genes drove the host shift leading to the emergence of P. falciparum as a human pathogen.