MEDICAL-SURGICAL MANAGEMENT OF INTESTINAL INFECTION BY PROSTHENORCHIS ELEGANS IN NONHUMAN PRIMATES FROM COSTA RICA.

Parasitism is one of the most important diseases in nonhuman primates (NHP). Parasitism by Prosthenorchis elegans can be a threat to health and conservation of NHP in Costa Rica. Surgical management of intestinal acanthocephalan infection in two squirrel monkeys (Saimiri oerstedii) and one white-faced monkey (Cebus imitator) is described as an alternative to the lack of pharmacologic control options when there is a high burden of parasites present. A complete physical evaluation, including medical ultrasound techniques, allow for diagnosis of the parasite and its lesions. When animals present with a high burden of parasites, surgical management has shown to promote good health outcomes and increase the probability of survival.

Distribution of Blastocystis subtypes isolated from various animal hosts in Thailand.

Blastocystis is a parasitic protist of a variety of hosts, including humans. Mapping the distribution of Blastocystis and its genetic variants across different host species can help us understand the epidemiology of this organism and its role in health and disease. This study aimed to identify subtypes of Blastocystis detected in different animal hosts in Thailand. A total of 825 fecal samples belonging to 18 vertebrate orders, 36 families, 68 genera, and 80 species were collected. Of these, 111 specimens were Blastocystis-positive by culture. Seventy-nine samples were subjected to small subunit (SSU) ribosomal DNA amplification by PCR, and reliable subtype data were obtained for 61 specimens. At least 14 subtypes (ST), namely ST1 to ST10, ST14/ST24/ST25 complex, ST23, ST26, and ST29 were detected. In addition, Blastocystis was found in tortoises. ST1 (3.2%) and ST5 (11.5%) were found in pigs, ST2 (1.6%) and ST3 (3.2%) in non-human primates, ST4 (14.7%) in rodents and ruminants, ST6 (4.9%), ST7 (30%), ST9 (1.6%), and ST29 (1.6%) in birds, ST8 (6.6%) in Green peafowl and East Asian Porcupine, and ST10 (4.9%), ST14/ST24/ST25 (9.8%), ST23 (1.6%) and ST26 (1.6%) in ruminants. The sequence recovered from the elongated tortoises (Indotestudo elongata) (3.2%) was phylogenetically placed within the reptilian cluster of Blastocystis, for which no subtype system is available yet. Of note, we did not obtain Blastocystis sequences from any of the many canids and felids sampled in the study, and our data are in support of host specificity of Blastocystis, according to both colonization and subtype distribution.

Gastrointestinal parasites in non-human primates in zoological institutions in France.

Gastrointestinal parasites are frequently encountered in captive non-human primates and infestation may have severe consequences on the animal's health status. Most of these parasites are also transmissible to humans. Nevertheless, little is known about the prevalence and monitoring modalities of gastrointestinal parasitoses in non-human primates housed in zoological institutions and there are currently no guidelines available for their detection and identification. The objective of this study was to identify the main gastrointestinal parasites that may be observed in non-human primates in zoological institutions in France, as well as to develop a decision-making tree to ease their identification. Twenty-four zoological institutions were surveyed, most of which performed fecal examinations routinely on their non-human primates (91.7%). Most institutions used flotation enrichment protocols to detect gastrointestinal parasites (95.2%) and nematodes were the most frequently encountered parasites (73.0%). A total of 252 fecal samples corresponding to 68 different non-human primate species from these institutions were analyzed using sedimentation and flotation protocols. Protozoa (47.3%) were found to be more frequent than helminths (15.6%). Furthermore, old-world monkeys exhibited a higher parasite load (93.6%) than any other non-human primate species category. Compiled data from fecal examinations allowed the development of a decision-making tree and diagnostic atlas to facilitate parasite diagnosis in captive non-human primates.

Title: Parasites gastro-intestinaux chez les primates non-humains dans les parcs zoologiques français. Abstract: Les parasites gastro-intestinaux sont fréquemment rencontrés chez les primates non-humains en captivité et peuvent avoir des conséquences graves sur l'état de santé de l'animal. La plupart sont également transmissibles à Homme. Néanmoins, on sait peu de choses sur la prévalence et les modalités de surveillance des parasitoses gastro-intestinales chez les primates non-humains hébergés dans des institutions zoologiques et il n'existe actuellement aucune ligne directrice disponible pour leur détection et leur identification. L'objectif de cette étude était d'identifier les principaux parasites gastro-intestinaux pouvant être observés chez les primates non-humains dans les institutions zoologiques françaises, ainsi que de développer un arbre décisionnel pour faciliter leur identification. Vingt-quatre institutions zoologiques françaises ont été interrogées : la plupart (91,7 %) effectuaient des examens fécaux en routine sur leurs primates non-humains. La plupart des établissements utilisaient des protocoles d'enrichissement par flottation pour détecter les parasites gastro-intestinaux (95,2 %) et les nématodes étaient les parasites les plus fréquemment rencontrés (73,0 %). Un total de 252 échantillons fécaux correspondant à 68 espèces différentes de primates non-humains provenant de ces institutions ont été analysés à l'aide de protocoles de sédimentation et de flottation. Les protozoaires (47,3 %) étaient plus fréquents que les helminthes (15,6 %). De plus, les singes de l'ancien monde présentaient une charge parasitaire plus élevée (93,6 %) que toute autre catégorie d'espèces de primates non-humains. Les données compilées des examens fécaux ont permis le développement d'un arbre décisionnel et d'un atlas diagnostique pour faciliter le diagnostic des parasites chez les primates non-humains en captivité.

The evolution of primate malaria parasites: A study on the origin and diversification of Plasmodium in lemurs.

Among the primate malaria parasites, those found in lemurs have been neglected. Here, six Plasmodium lineages were detected in 169 lemurs. Nearly complete mitochondrial genomes (mtDNA, ≈6Kb) and apicoplast loci (≈6Kb) were obtained from these parasites and other Haemosporida species. Plasmodium spp. in lemurs are a diverse clade that shares a common ancestor with other primate parasites from continental Africa. Time-trees for the mtDNA were estimated under different scenarios, and the origin of the lemur clade coincides with the proposed time of their host species' most recent common ancestor (Lemuridae-Indriidae). A time tree with fewer taxa was estimated with mtDNA + Apicoplast loci. Those time estimates overlapped but were younger and had narrower credibility intervals than those from mtDNA alone. Importantly, the mtDNA + Apicoplast estimates that the clade including the most lethal malaria parasite in humans, Plasmodium falciparum, may have originated with Homininae (African apes). Finally, the phylogenetic congruence of the lemurs and their parasites was explored. A statistically significant scenario identified four cospeciation, two duplications, four transfer (host-switches), and zero loss events. Thus, the parasite species sampled in lemurs seem to be radiating with their hosts.

The Movement of Pathogen Carrying Flies at the Human-Wildlife Interface.

Flies form high-density associations with human settlements and groups of nonhuman primates and are implicated in transmitting pathogens. We investigate the movement of nonhuman primate-associated flies across landscapes surrounding Kibale National Park, Uganda, using a mark-recapture experiment. Flies were marked in nine nonhuman primate groups at the forest edge ([Formula: see text] = 929 flies per group), and we then attempted to recapture them in more anthropized areas (50 m, 200 m and 500 m from where marked; 2-21 days after marking). Flies marked in nonhuman primate groups were recaptured in human areas (19/28,615 recaptured). Metabarcoding of the flies in nonhuman primate groups revealed the DNA of multiple eukaryotic primate parasites. Taken together, these results demonstrate the potential of flies to serve as vectors between nonhuman primates, livestock and humans at this biodiverse interface.

Predictions of primate-parasite coextinction.

Future biodiversity loss threatens the integrity of complex ecological associations, including among hosts and parasites. Almost half of primate species are threatened with extinction, and the loss of threatened hosts could negatively impact parasite associations and ecosystem functions. If endangered hosts are highly connected in host-parasite networks, then future host extinctions will also drive parasite extinctions, destabilizing ecological networks. If threatened hosts are not highly connected, however, then network structure should not be greatly affected by the loss of threatened hosts. Networks with high connectance, modularity, nestedness and robustness are more resilient to perturbations such as the loss of interactions than sparse, nonmodular and non-nested networks. We analysed the interaction network involving 213 primates and 763 parasites and removed threatened primates (114 species) to simulate the effects of extinction. Our analyses revealed that connections to 23% of primate parasites (176 species) may be lost if threatened primates go extinct. In addition, measures of network structure were affected, but in varying ways because threatened hosts have fewer parasite interactions than non-threatened hosts. These results reveal that host extinctions will perturb the host-parasite network and potentially lead to secondary extinctions of parasites. The ecological consequences of these extinctions remain unclear. This article is part of the theme issue 'Infectious disease macroecology: parasite diversity and dynamics across the globe'.

Soil-transmitted helminth infections in free-ranging non-human primates from Cameroon and Gabon.

BACKGROUND: Zoonotic diseases are a serious threat to both public health and animal conservation. Most non-human primates (NHP) are facing the threat of forest loss and fragmentation and are increasingly living in closer spatial proximity to humans. Humans are infected with soil-transmitted helminths (STH) at a high prevalence, and bidirectional infection with NHP has been observed. The aim of this study was to determine the prevalence, genetic diversity, distribution and presence of co-infections of STH in free-ranging gorillas, chimpanzees and other NHP species, and to determine the potential role of these NHP as reservoir hosts contributing to the environmental sustenance of zoonotic nematode infections in forested areas of Cameroon and Gabon. METHODS: A total of 315 faecal samples from six species of NHPs were analysed. We performed PCR amplification, sequencing and maximum likelihood analysis of DNA fragments of the internal transcribed spacer 2 (ITS2) nuclear ribosomal DNA to detect the presence and determine the genetic diversity of Oesophagostomum spp., Necator spp. and Trichuris spp., and of targeted DNA fragments of the internal transcribed spacer 1 (ITS1) to detect the presence of Ascaris spp. RESULTS: Necator spp. infections were most common in gorillas (35 of 65 individuals), but also present in chimpanzees (100 of 222 individuals) and in one of four samples from greater spot-nosed monkeys. These clustered with previously described type II and III Necator spp. Gorillas were also the most infected NHP with Oesophagostomum (51/65 individuals), followed by chimpanzees (157/222 individuals), mandrills (8/12 samples) and mangabeys (7/12 samples), with O. stephanostomum being the most prevalent species. Oesophagostomum bifurcum was detected in chimpanzees and a red-capped mangabey, and a non-classified Oesophagostomum species was detected in a mandrill and a red-capped mangabey. In addition, Ternidens deminutus was detected in samples from one chimpanzee and three greater spot-nosed monkeys. A significant relative overabundance of co-infections with Necator and Oesophagostomum was observed in chimpanzees and gorillas. Trichuris sp. was detected at low prevalence in a gorilla, a chimpanzee and a greater spot-nosed monkey. No Ascaris was observed in any of the samples analysed. CONCLUSIONS: Our results on STH prevalence and genetic diversity in NHP from Cameroon and Gabon corroborate those obtained from other wild NHP populations in other African countries. Future research should focus on better identifying, at a molecular level, the species of Necator and Oesophagostomum infecting NHP and determining how human populations may be affected by increased proximity resulting from encroachment into sylvatic STH reservoir habitats.

Echinococcus multilocularis genetic diversity in Swiss domestic pigs assessed by EmsB microsatellite analyzes.

Assessing the genetic diversity of the parasite Echinococcus multilocularis provides key information about the temporal and spatial strain flow in a given area. Previous studies indicated that a historical endemic area conventionally presents a relatively high genetic diversity, whereas peripheral or newly endemic areas exhibit a more restricted variability of the parasite. The Swiss plateau region is part of the European historically endemic area, and the genetic diversity has already been investigated by assessing either human metacestode isolates or adult worms from foxes. To date, there have been no studies covering the whole geographical area affected by the parasite. The aim of the present study was to make use of the domestic pig to investigate the genetic diversity of E. multilocularis in relation to spatial distribution. A total of 55 E. multilocularis-induced hepatic lesions from slaughtered pigs from Switzerland were studied using EmsB microsatellite analyzes, and findings were compared to already published data (originating from human, primate, foxes, and rodent samples). A total of 12 EmsB profiles were described among the domestic pigs, some of them presenting a clear spatial organization in the Swiss plateau, with three of the main profiles geographically separated. One of the 12 EmsB profiles has been newly identified for Switzerland in this study, while the other 11 profiles had been previously described in other Swiss E. multilocularis isolates from other hosts. Overall, a total of 18 EmsB profiles have so far been described within the Swiss endemic area. Six profiles appeared only among human, primate, rodent, and fox samples. Based on a richness and diversity accumulation analysis, the sampling efficiency for the whole studied area has now been improved considerably by compilation of 178 E. multilocularis specimens obtained from four different intermediate and one definitive host species in Switzerland.

Current status of Blastocystis sp. in animals from Southeast Asia: a review.

Blastocystis is the most frequently observed eukaryotic gastrointestinal symbiont in humans and animals. Its low host specificity and zoonotic potential suggest that animals might serve as possible reservoirs for transmission. The prevalence and subtype distributions of Blastocystis sp. in animal populations in Southeast Asia, a hotspot for zoonotic diseases, are reviewed. Recommendations for future research aimed at understanding the zoonotic role of Blastocystis are also included. Seven countries have, so far, reported Blastocystis infection in various animals, such as livestock, poultry, companion animals, and non-human primates. Pigs were the most studied animals, and there were records of 100% prevalence in pigs, cattle, and ostriches. Using polymerase chain reaction (PCR)-based approaches, twelve Blastocystis sp. subtypes (STs), namely ST1, ST2, ST3, ST4, ST5, ST6, ST7, ST8, ST9, ST10, ST12, and ST14 have been recognised infecting animals of Southeast Asia. ST1 and ST5 were the most frequently identified, and Malaysia observed the most diverse distribution of subtypes. Further investigations on Blastocystis sp. in various animal hosts, using adequate sample sizes and uniform detection methods, are essential for a better understanding of the distribution of this organism. Detailed genome studies, especially on STs shared by humans and animals, are also recommended.

Prevalência e distribuição espacial da ocorrência de helmintos em primatas não humanos de vida livre no estado do Rio de Janeiro, Brasil / [Prevalence and spatial distribution of the occurrence of helminths in free-living nonhuman primates in the State of Rio de Janeiro, Brazil]

Seiscentos primatas neotropicais foram submetidos a exames post mortem para avaliação da prevalência parasitária de helmintos gastrointestinais. Foram examinados 556 calitriquídeos (Callithrix spp.), 23 bugios (Alouatta guariba), 19 macacos-pregos (Sapajus nigritus), um mico-leão-dourado (Leontopithecus rosalia) e um mico-leão-da-cara-dourada (Leontopithecus chrysomelas). Do total de 600 animais, foram encontrados espécimes parasitos pertencentes aos filos Acanthocephala, Nemathelmintes e Platyhelminthes (classes Trematoda e Cestoda) em 110 primatas. A prevalência de primatas positivos para, pelo menos, uma espécie de helminto foi de 18,3% (110/600), sendo destes 83,6% (92/110) calitriquídeos, 8,2% (9/110) bugios, 6,4% (7/110) macacos-pregos, 0,9% (1/110) mico-leão-dourado e 0,9% (1/110) mico-leão-da-cara dourada. Em 80,4% (74/92) dos calitriquídeos foram encontrados nematoides Primasubulura sp. e em 1,1% (1/92) nematoides Trypanoxyuris callithrix, em 26,1% (24/92) acantocéfalos (Pachysentis sp.) e em 5,4% (5/92) digenéticos (Platynosomum sp.); em 77,8% (7/9) dos bugios foram encontrados nematoides (Trypanoxyuris minutus), em 11,1% (1/9) acantocéfalos (Pachysentis sp.) e em 11,1% (1/9) cestoides (Bertiella sp.); em 14,3% (1/7) dos macacos-pregos foram encontrados nematoides (Physaloptera sp.), em 28,6% (2/7) acantocéfalos (Prostenorchis sp.) e em 14,3% (1/7) digenéticos (Platynosomum sp.) e no mico-leão-da-cara-dourada foram encontrados acantocéfalos (Prostenorchis sp.). Foi realizado o georreferenciamento dos pontos de encontro dos cadáveres para pontuar a distribuição dos helmintos por região.(AU)

Six hundred neotropical primates underwent postmortem examinations to evaluate the parasitic prevalence of gastrointestinal helminths. Fifty-five callitrichids tamarins (Callithrix spp.), 23 howlers (Alouatta guariba), 19 nail monkeys (Sapajus nigritus), a golden lion tamarin (Leontopithecus rosalia) and a golden-faced lion tamarin (Leontopithecus chrysomelas) were examined. Parasitic specimens belonging to phylums Acantocephala, Nemathelmintes and Platyhelmintes (Trematoda and Cestoda Classes) were found. The prevalence of primates positive for at least one species of helminth was 18.3% (110/600), of which 83.6% (92/110) callitrichids, 8.2% (9/110) howler monkeys, 6.4% (7/110) capuchin monkeys, 0.9% (1/110) golden lion tamarin and 0.9% (1/110) golden faced lion tamarin. In 80.4% (74/92) of callitrichids nematodes (Primasubulura sp.) were found, and in 1.1% (1/92) nematodes (Trypanoxyuris callithricis), in 26.1% (24/92) acanthocephalus (Pachysentis sp.) and 5.4% (5/92) digenetics (Platynosomum sp.); in 77.8% (7/9) of howler monkeys presented nematodes (Trypanoxyuris minutus), 11.1% (1/9) acanthocephalus (Pachysentis sp.) and 11.1% (1/9) cestoids (Bertiella sp.); in 14.3% (1/7) of capuchin monkeys presented nematodes (Physaloptera sp.), 28.6% (2/7) acanthocephalus (Prostenorchis sp.) and 14.3% (1/7) digenetics (Platynosomum sp.) and in the golden-faced lion tamarin acanthocephalus (Prostenorchis sp.) were found. Georreferencing of the meeting points of the cadavers was performed in order to punctuate the distribution of helminths by region.(AU)

Prevalence and subtype diversity of Blastocystis in human and nonhuman primates in North China.

Blastocystis is of public health concern due to its global distribution in diverse animals including humans. Here, fecal specimens sampled from human and nonhuman primates were examined for Blastocystis by PCR and sequence analysis of the small subunit ribosomal RNA gene. Among age cohorts, the parasite was positive only for three of 126 (2.4%) adults admitted to a hospital in Harbin, Heilongjiang province, with a less common human subtype (ST), ST5, determined. Blastocystis was identified in 7.0% of nonhuman primates (NHPs), giving an infection rate of 6.8% (4/59) to zoo NHPs in Harbin and 7.1% (9/126) to lab NHPs in Beijing. No significant prevalence differences by macaque species, age, gender, and sample source were observed. Among the subtypes found in NHPs, seven belonged to ST1, three to ST2, one to ST3, and the remaining two to mixed ST1/ST3 and ST2/ST3. Although the data here showed no direct evidence linking human infections to Blastocystis of NHP origin, individuals might acquire colonization of ST5 from livestock sources judged by occurrence of this subtype also in cattle in Harbin and pigs and sheep in unspecified cities of Heilongjiang as noted in previous reports. In addition, given the nonrigid (but sometimes, perhaps cryptic) host specificity of ST1, ST2, and ST3 and their dominant role in human affections globally as discussed in a previous NHP report by Alfellani et al. (Parasitology 140:966-971, 2013a), precautions should be taken to minimize the possible transmission of those subtypes from NHPs to humans in North China.

Detection of DNA of filariae closely related to Mansonella perstans in faecal samples from wild non-human primates from Cameroon and Gabon.

BACKGROUND: The Onchocercidae is a family of filarial nematodes with several species of medical or veterinary importance. Microfilariae are found in the blood and/or the dermis and are usually diagnosed in humans by microscopy examination of a blood sample or skin biopsy. The main objectives of this study were to evaluate whether filariae DNA can be detected in faecal samples of wild non-human primates (NHPs), whether the detected parasites were closely related to those infecting humans and whether filarial DNA detection in faeces is associated with co-infections with nematodes (Oesophagostumum sp. and Necator sp.) known to cause blood loss while feeding on the host intestinal mucosa. METHODS: A total of 315 faecal samples from 6 species of NHPs from Cameroon and Gabon were analysed. PCRs targeted DNA fragments of cox1 and 12S rDNA genes, to detect the presence of filariae, and the internal transcribed spacer 2 (ITS2), to detect the presence of Oesophagostomum sp. and Necator sp. infections. RESULTS: Among the 315 samples analysed, 121 produced sequences with > 90% homology with Onchocercidae reference sequences. However, 63% of the 12S rDNA and 78% of the cox1 gene sequences were exploitable for phylogenetic analyses and the amplification of the 12S rDNA gene showed less discriminating power than the amplification of the cox1 fragment. Phylogenetic analyses showed that the cox1 sequences obtained from five chimpanzee DNA faecal samples from Gabon and two from Cameroon cluster together with Mansonella perstans with high bootstrap support. Most of the remaining sequences clustered together within the genus Mansonella, but the species could not be resolved. Among the NHP species investigated, a significant association between filarial DNA detection and Oesophagostomum sp. and Necator sp. infection was observed only in gorillas. CONCLUSIONS: To our knowledge, this is the first study reporting DNA from Mansonella spp. in faecal samples. Our results raise questions about the diversity and abundance of these parasites in wildlife, their role as sylvatic reservoirs and their potential for zoonotic transmission. Future studies should focus on detecting variants circulating in both human and NHPs, and improve the molecular information to resolve or support taxonomy classification based on morphological descriptions.

Machine learning-based analyses support the existence of species complexes for Strongyloides fuelleborni and Strongyloides stercoralis.

Human strongyloidiasis is a serious disease mostly attributable to Strongyloides stercoralis and to a lesser extent Strongyloides fuelleborni, a parasite mainly of non-human primates. The role of animals as reservoirs of human-infecting Strongyloides is ill-defined, and whether dogs are a source of human infection is debated. Published multi-locus sequence typing (MLST) studies attempt to elucidate relationships between Strongyloides genotypes, hosts, and distributions, but typically examine relatively few worms, making it difficult to identify population-level trends. Combining MLST data from multiple studies is often impractical because they examine different combinations of loci, eliminating phylogeny as a means of examining these data collectively unless hundreds of specimens are excluded. A recently-described machine learning approach that facilitates clustering of MLST data may offer a solution, even for datasets that include specimens sequenced at different combinations of loci. By clustering various MLST datasets as one using this procedure, we sought to uncover associations among genotype, geography, and hosts that remained elusive when examining datasets individually. Multiple datasets comprising hundreds of S. stercoralis and S. fuelleborni individuals were combined and clustered. Our results suggest that the commonly proposed 'two lineage' population structure of S. stercoralis (where lineage A infects humans and dogs, lineage B only dogs) is an over-simplification. Instead, S. stercoralis seemingly represents a species complex, including two distinct populations over-represented in dogs, and other populations vastly more common in humans. A distinction between African and Asian S. fuelleborni is also supported here, emphasizing the need for further resolving these taxonomic relationships through modern investigations.

Gastrointestinal Parasites in Captive Animals at the Rio de Janeiro Zoo.

BACKGROUND: Gastrointestinal parasites may determine diarrhea, dysentery or even death in captive mammals. These animals tend to be more susceptible to parasitic infections due to confinement and stress. Purpose To increase the information about these etiological agents in captive animals in Brazil, the gastrointestinal parasites of the captive mammals of the Rio de Janeiro Zoo were investigated. METHODS: From 2016 to 2018, 180 fecal samples were collected from animals housed in the Rio de Janeiro Zoo: 63 from animals of the order Primates, 26 of Carnivora, 78 of Artiodactyla, 9 of Perissodactyla and 4 of the order Rheiformes. The feces were processed by direct examination and by the techniques of Faust et al., Sheather, Ritchie, Lutz, and smears were stained with safranin. Immunoenzymatic assays were also performed to investigate antigens of Giardia duodenalis, Cryptosporidium spp., Entamoeba histolytica/Entamoeba dispar. RESULTS: Parasite positivity was identified in 68.3% of the fecal samples, with a parasite positivity rate of 68.2% among primates, 65.3% among carnivores, 69.2% among artiodactyls, 33.3% among perissodactyls, and 100% among rheiformes. The most frequently detected parasite was Entamoeba histolytica/E. dispar antigens, which showed a statistically significant positivity rate (33.3%; p = 0.000), particularly in the feces of carnivores (30.7%) and artiodactyls (53.8%). A statistically significant positivity rate of Balantioides coli (11.1%; p = 0.001) was also detected in feces from nonhuman primates, tapirs, collared peccaries and rheas. The positivity of Cryptosporidium sp. antigens in feces of the orders Carnivora, Artiodactyla and Primates was also statistically significant (7.2%, p = 0.010). Oocysts compatible with Cryptosporidium spp. were detected in 6.3% from primates. The helminths most frequently detected were thin-shelled eggs of nematodes (17.7%, p = 0.000), nematode larvae (15.5%, p = 0.000) and Trichuris trichiura eggs (6.1%, p = 0.018). CONCLUSION: The positivity rate for gastrointestinal parasites demonstrates the need for a sanitation management program to be implemented in the zoo, including routine diagnostic parasitology tests followed by specific treatment for each parasitosis.

Metabarcoding of eukaryotic parasite communities describes diverse parasite assemblages spanning the primate phylogeny.

Despite their ubiquity, in most cases little is known about the impact of eukaryotic parasites on their mammalian hosts. Comparative approaches provide a powerful method to investigate the impact of parasites on host ecology and evolution, though two issues are critical for such efforts: controlling for variation in methods of identifying parasites and incorporating heterogeneity in sampling effort across host species. To address these issues, there is a need for standardized methods to catalogue eukaryotic parasite diversity across broad phylogenetic host ranges. We demonstrate the feasibility of a metabarcoding approach for describing parasite communities by analysing faecal samples from 11 nonhuman primate species representing divergent lineages of the primate phylogeny and the full range of sampling effort (i.e. from no parasites reported in the literature to the best-studied primates). We detected a number of parasite families and regardless of prior sampling effort, metabarcoding of only ten faecal samples identified parasite families previously undescribed in each host (x̅ = 8.5 new families per species). We found more overlap between parasite families detected with metabarcoding and published literature when more research effort-measured as the number of publications-had been conducted on the host species' parasites. More closely related primates and those from the same continent had more similar parasite communities, highlighting the biological relevance of sampling even a small number of hosts. Collectively, results demonstrate that metabarcoding methods are sensitive and powerful enough to standardize studies of eukaryotic parasite communities across host species, providing essential new tools for macroecological studies of parasitism.

Biodiversity of protists and nematodes in the wild nonhuman primate gut.

Documenting the natural diversity of eukaryotic organisms in the nonhuman primate (NHP) gut is important for understanding the evolution of the mammalian gut microbiome, its role in digestion, health and disease, and the consequences of anthropogenic change on primate biology and conservation. Despite the ecological significance of gut-associated eukaryotes, little is known about the factors that influence their assembly and diversity in mammals. In this study, we used an 18S rRNA gene fragment metabarcoding approach to assess the eukaryotic assemblage of 62 individuals representing 16 NHP species. We find that cercopithecoids, and especially the cercopithecines, have substantially higher alpha diversity than other NHP groups. Gut-associated protists and nematodes are widespread among NHPs, consistent with their ancient association with NHP hosts. However, we do not find a consistent signal of phylosymbiosis or host-species specificity. Rather, gut eukaryotes are only weakly structured by primate phylogeny with minimal signal from diet, in contrast to previous reports of NHP gut bacteria. The results of this study indicate that gut-associated eukaryotes offer different information than gut-associated bacteria and add to our understanding of the structure of the gut microbiome.

Shoo fly don't bother me: Flies track social primates and carry viable anthrax.

Flies-a small name for an enormous taxonomic group of over 110,000 described species that have unique ecological roles. Nonbiting flies ingest organic material in faecal matter or carrion, which is rich in microbes and nutrients that benefit both adults and their offspring (maggots). These are often referred to as "filth flies" because they are often pests in human settlements and responsible for the spread of enteric pathogens. Filth flies associate with human populations; however, whether this association is simply due to the presence of organic waste produced, or if flies move with social groups remains unknown. In this issue of Molecular Ecology, Gogarten et al. (2019) use a unique combination of field methods and molecular tools to show that filth flies (predominantly Muscidae [house flies] and Calliphoridae [blow flies]) associate and move with social nonhuman primate (NHP) groups (mangabeys and chimpanzees) for up to 12 days and over 1 km. Filth flies captured near these groups were found to have pathogen DNA on them from the causative agents of sylvatic anthrax and yaws. Furthermore, the authors were able to show that the anthrax bacteria on the flies was viable. Previous research emphasized sylvatic anthrax as a major conservation threat to wildlife at this field site (Hoffmann et al., 2017), highlighting the significance of filth flies as potential vectors of anthrax. The authors present a suite of methods and approaches that utilize flies to better understand rainforest biodiversity, pathogen transmission potential, and filth fly-host associations. This work represents new directions and opportunities to integrate entomology into field research and exploit the natural history of flies to understand the pathogen landscape and address outstanding questions in ecology and evolution.

The changing ecology of primate parasites: Insights from wild-captive comparisons.

Host movements, including migrations or range expansions, are known to influence parasite communities. Transitions to captivity-a rarely studied yet widespread human-driven host movement-can also change parasite communities, in some cases leading to pathogen spillover among wildlife species, or between wildlife and human hosts. We compared parasite species richness between wild and captive populations of 22 primate species, including macro- (helminths and arthropods) and micro-parasites (viruses, protozoa, bacteria, and fungi). We predicted that captive primates would have only a subset of their native parasite community, and would possess fewer parasites with complex life cycles requiring intermediate hosts or vectors. We further predicted that captive primates would have parasites transmitted by close contact and environmentally-including those shared with humans and other animals, such as commensals and pests. We found that the composition of primate parasite communities shifted in captive populations, especially because of turnover (parasites detected in captivity but not reported in the wild), but with some evidence of nestedness (holdovers from the wild). Because of the high degree of turnover, we found no significant difference in overall parasite richness between captive and wild primates. Vector-borne parasites were less likely to be found in captivity, whereas parasites transmitted through either close or non-close contact, including through fecal-oral transmission, were more likely to be newly detected in captivity. These findings identify parasites that require monitoring in captivity and raise concerns about the introduction of novel parasites to potentially susceptible wildlife populations during reintroduction programs.

SEROLOGICAL DIAGNOSIS OF BAYLISASCARIS PROCYONIS IN PRIMATES USING A HUMAN ELISA TEST.

The usefulness of a human enzyme-linked immunosorbent assay (ELISA) for serological diagnosis of Baylisascaris procyonis larva migrans was assessed in nonhuman primates (NHP). The test was originally developed as an assay performed on human samples at Purdue University. Six participating zoos submitted 258 NHP serum samples, spanning these major phylogenetic groups: 1) great apes (n = 84), 2) lesser apes (n = 17), 3) Old World monkeys (n = 84), 4) New World monkeys (n = 20), and 5) prosimians (n = 53). Sera were tested in duplicate using a microtiter-well ELISA with B. procyonis larval excretory-secretory proteins as antigen, and serum from an experimentally infected baboon (Papio anubis) served as positive control. The ELISA clearly identified seropositive animals in all zoos. With putative cutoffs of optical density (OD) measured at 405 nm (OD405) of <0.150 = negative, 0.150-0.250 = indeterminate, and >0.250 = positive, 149 of 258 (57.8%) were clearly negative (mean OD 0.046), and 78 of 258 (30.2%) were clearly positive (mean OD 0.657, range 0.253-1.773), the rest being indeterminate. Of these, 15 were high positive with OD 1.095-1.773 (mean 1.314). Positive animals were seen from all zoos; 76 (97.4%) were great apes, lesser apes, or Old World monkeys. The four highest ODs were in a siamang (Symphalangus syndactylus), lion-tailed macaque (Macaca silenus), Sumatran orangutan (Pongo abelii), and western lowland gorilla (Gorilla gorilla gorilla), all from different zoos. Prosimians had a mean OD of 0.039 and New World monkeys 0.021, indicating that human reagents either did not work for these groups or few infected animals were represented. These results indicate that the human ELISA for B. procyonis works well for at least higher phylogeny NHP and that serologic evidence of infection is surprisingly common, correlating with what is known for exposure to this parasite in zoos.

Serological survey of Toxoplasma gondii in captive nonhuman primates in zoos in Spain.

Toxoplasma gondii is a widely distributed zoonotic protozoan parasite, which can affect most warm-blooded species. Some species of non-human primates (NHPs) are highly susceptible to T. gondii infection. The aim of the study was to determine the seroprevalence and risk factors associated with T. gondii infection in NHPs housed in zoos in Spain. Sera from 189 NHPs belonging to 33 species were collected in eight zoos. Additionally, 10 of the 189 animals were longitudinally sampled. Anti-T. gondii antibodies were detected in 48 NHPs (25.4%; confidence interval of 95% (CI95%): 19.2-31.6) using a modified agglutination test (MAT; cut-off = 25). Seropositive animals had titers of 25 (6.3%), 50 (8.3%), 100 (8.3%) and ≥500 (68.8%). Seropositivity was detected in 15 of the 33 species (45.5%). Of the 10 NHPs sampled more than once, two animals (one Barbary macaque [Macaca sylvanus] and one common chimpanzee [Pan toglodytes]) seroconverted along the study period, while one seropositive chimpanzee increased antibody titers over time. The Hominidae family (OR = 5.9; CI95%: 2.7-12.8) and sex (females) (OR = 2.1; CI95%: 1.1-4.1) were risk factors potentially associated with seropositivity to T. gondii. Our results evince a widespread circulation of T. gondii in NHPs in zoos in Spain, which may be of conservation concern. Control measures should be implemented to minimize the risk of exposure of these species to T. gondii.