Captive Non-human Primates Research Articles

Gastrointestinal parasites of captive and free range non-human primates in savanna zone of Nigeria

Primates being reservoirs of parasites that cause major problems to humans, livestock and under stressful conditions to themselves is a major concern to wildlife conservation, our study compared the gastrointestinal parasites of some Non-human Primates at University of Ilorin Zoological Garden (Unilorin Zoo) and Kainji Lake National Park (KLNP), Nigeria in order to determine the level of their prevalence and possibility of infection on tourists visiting the sites. Species sampled were restricted to those common to both sites; Papio anubis, Erythrocebus patas and Chlorocebus aethiops tantalus. A total of 128 faecal samples were screened from apparent healthy individuals. Samples were processed using sedimentation, sugar floatation technique, Stoll's dilution technique, cultured and infective larvae were recovered using Baermann technique.110 (85.7%) samples were positive for infestation of at least one eggs. Among the positive samples were three species of nematodes; Strongyloides spp., Ascaris spp., Ancyclostoma spp. Primates on free-range had higher prevalence of infection. However, under both conditions, there is no significant difference in the prevalence and intensity of parasites harboured over seasonst (4) = 1.968, p =0.120).

Gastrointestinal Helminths of Captive Non-human Primates in Cameroon

Gastrointestinal Helminths of Captive Non-human Primates in Cameroon

The effect of captivity on the primate gut microbiome varies with host dietary niche.

Despite careful attention to animal nutrition and wellbeing, gastrointestinal distress remains relatively common in captive non-human primates (NHPs), particularly dietary specialists such as folivores. These patterns may be a result of marked dietary differences between captive and wild settings and associated impacts on the gut microbiome. However, given that most existing studies target NHP dietary specialists, it is unclear if captive environments have distinct impacts on the gut microbiome of NHPs with different dietary niches. To begin to examine this question, we used 16S ribosomal RNA gene amplicon sequences to compare the gut microbiomes of five NHP genera categorized either as folivores (Alouatta, Colobus) or non-folivores (Cercopithecus, Gorilla, Pan) sampled both in captivity and in the wild. Though captivity affected the gut microbiomes of all NHPs in this study, the effects were largest in folivorous NHPs. Shifts in gut microbial diversity and in the relative abundances of fiber-degrading microbial taxa suggest that these findings are driven by marked dietary shifts for folivorous NHPs in captive settings. We propose that zoos and other captive care institutions consider including more natural browse in folivorous NHP diets and regularly bank fecal samples to further explore the relationship between NHP diet, the gut microbiome, and health outcomes.

Short communication: Important role of Non Tuberculous Mycobacteria in Non-Human primate TB testing in Ethiopia

Tuberculosis is an important disease in captive non-human primates (NHP) but remains challenging to diagnose accurately. The tuberculin skin test (TST) remains the standard test used worldwide, whereby the single intradermal tuberculin test (SIDT) in the eye-lid is the most frequently used method to diagnose TB in NHP. In this study, 9 NHP (5 baboon spp.) and 4 geladas (T. gelada) were tested for TB using the Primagam (whole blood immunoassay) in order to assess the feasibility of relocation into the wild. Although the results showed that all species reacted to non-tuberculous mycobacteria (NTM), the geladas showed a consistent distinct reaction pattern with very high reactivity to NTM. The results suggest that using the SIDT in Ethiopian primates, particularly the endemic geladas, would lead to a high number of false positive animals, highlighting the current challenge to accurately diagnose NHP for TB, which could help in the conservation efforts in the country.Key words: Ethiopia; TB; Non-human primate; Gelada; non-tuberculous mycobacteria

Natural infection of captive cynomolgus monkeys (Macaca fascicularis) with hepatitis E virus genotype 4

Data on natural HEV infection of infection in monkeys are limited. We report a case of hepatitis E virus genotype 4 infection in captive non-human primates (cynomolgus monkeys) imported from Vietnam. Phylogenetic analysis demonstrated that HEV infection was not the result of spillover from single source of infection, but rather the persistent circulation of HEV-4 among cynomolgus monkeys or multiple infections by related strains from a human or swine reservoir.

Epilepsy in nonhuman primates.

Nonhuman primates (NHPs) are model organisms for understanding the pathophysiology and treatment of epilepsy in humans, while data from human patients informs the diagnosis and treatment of NHP with seizures and epilepsy. We reviewed the literature and surveyed veterinarians at zoos and NHP research centers to (a) better define the range of seizures and epilepsy in NHP, (b) understand how NHPs can inform our knowledge of the pathophysiology and treatment of epilepsy in humans, and (c) identify gaps of knowledge and develop more effective guidelines to treat seizures and epilepsy in NHP. We searched PrimateLit, PubMed, and Google Scholar for studies on experimental models of epilepsy in NHPs and on naturally occurring seizures and epilepsy in NHPs in captivity. In addition, we created a survey to assess methods to diagnose and treat epilepsy in NHPs. This survey was sent to 41 veterinarians at major international zoos and research facilities with NHP populations to study seizure phenomenology, diagnostic criteria for seizures and epilepsy, etiology, and antiseizure therapies in NHPs. We summarize the data from experimental and natural models of epilepsy in NHPs and case reports of epilepsy of unknown origin in captive primates. In addition, we present survey data collected from veterinarians at eight zoos and one research facility. Experimental data from NHP epilepsy models is abundant, whereas data from primates who develop epilepsy in the wild or in zoos is very limited, constraining our ability to advance evidence-based medicine. Characterization of seizure or epilepsy models in NHPs will provide insights into mechanisms and new therapies that cannot be addressed by other animal models. NHP research will better inform species-specific diagnoses and outcomes.

Alopecia in rhesus macaques (Macaca mulatta): Association with pregnancy and chronic stress.

Alopecia in captive non-human primates is often presented as a welfare issue. However, it is a complex condition with a number of possible causes. The purpose of this study was to assess the impact of pregnancy and hair cortisol concentrations on alopecia in rhesus macaques. Subjects were 113 socially housed adult female rhesus macaques (27 pregnant, 35 nursing infants, 51 controls). During routine physicals, photographs were taken for alopecia assessment and hair samples were collected for cortisol assay. Alopecia was more prevalent in pregnant than in control females, but there was no association between alopecia and hair cortisol. However, there was a significant effect of pregnancy on hair cortisol. Nursing females had higher hair cortisol levels than pregnant females, which had higher levels than control females. Although alopecia does not appear to be associated with hair cortisol, both alopecia and hair cortisol were associated with pregnancy.

Competence of non-human primates to transmit Leishmania infantum to the invertebrate vector Lutzomyia longipalpis.

Leishmaniasis is a zoonotic disease of worldwide relevance. Visceral leishmaniasis is endemic in Brazil, where it is caused by Leishmania infantum with Lutzomyia longipalpis being the most important invertebrate vector. Non-human primates are susceptible to L. infantum infection. However, little is known about the role of these species as reservoirs. The aim of this study was to evaluate the transmissibility potential of visceral leishmaniasis by non-human primates through xenodiagnosis using the phlebotomine Lu. longipalpis as well as to identify phlebotomine species prevalent in the area where the primates were kept in captivity, and assess infection by Leishmania in captured phlebotomine specimens. Fifty two non-human primates kept in captivity in an endemic area for leishmaniasis were subjected to xenodiagnosis. All primates were serologically tested for detection of anti-Leishmania antibodies. Additionally, an anti-Lu. longipalpis saliva ELISA was performed. Sand flies fed on all animals were tested by qPCR to identify and quantify L. infantum promastigotes. Eight of the 52 non-human primates were positive by xenodiagnosis, including three Pan troglodytes, three Leontopithecus rosalia, one Sapajus apella, and one Miopithecus talapoin, with estimated numbers of promastigotes ranging from 5.67 to 1,181.93 per μg of DNA. Positive animals had higher levels of IgG anti-Lu. longipalpis saliva when compared to negative animals, prior to xenodiagnosis. Captive non-human primates are capable of infecting Lu. longipalpis with L. infantum. Our findings also demonstrate the relevance of non-human primates as sentinels to zoonotic diseases. Several phlebotomine species, including Lu. longipalpis, have been identified in the area where the primates were maintained, but only one pool of Lutzomyia lenti was infected with L. infantum. This study has implications for public health strategies and conservation medicine.

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.

Gastrointestinal Amebiasis Due to Entamoeba Histolytica in a Captive Male Zebra (Equus quagga)

A 16 year-old captive male zebra (Equus quagga) at Bannerghatta Biological Park, died after seven days of initial symptoms. Symptoms included complete anorexia, severe watery diarrhoea, dehydration and colic. Faecal sample examination by direct smear method revealed the presence of Entamoeba oocysts. On post-mortem examination, petechial haemorrhages were found on serosa along with streaks and diffused haemorrhages in the mucosa of intestine, cecum and colon. The characteristic sub-mucosal haemorrhages in the glandular portion of the stomach resembling button-shaped ulcers were found embedded deep into the mucosa and no lesions in the fibrous part of the stomach. Impression smears from the glandular stomach mucosa revealed numerous trophozoites of Entamoeba histolytica.E. histolytica most commonly causes necrotising and ulcerative colitis in humans and captive non-human primates. Rare cases of gastric amebiasis also have been reported in captive horses. To the best of our knowledge, this appears to be the first report confirming E. histolytica as the cause of gastrointestinal amebiasis in a captive male zebra.

Cestode infections in non-human primates suggest the existence of zoonotic cycles in the area surrounding the Strasbourg primatology center.

Background: Several cases of infections due to Echinococcus multilocularis, Taenia martis and Taenia crassiceps were recently described in various species of captive non-human primates (NHPs) harbored in the Strasbourg Primate Center (SPC). Furthermore, one of the first cases of human cysticercosis due to T. martis was described in the Strasbourg region. These data suggest the existence of zoonotic cycles of tapeworm infections in the direct environment of the SPC. The aim of our study was to assess the prevalence of larval cestode infections among intermediate and definitive hosts in the close neighborhood of the center. We analyzed carnivore mammal fecal samples as well as rodent carcasses, collected inside or near the SPC, using PCR. Furthermore, we performed serology for Echinococcus spp. and Taenia spp. on NHP sera. Results: We found that 14.5% (95% CI [8.6; 20.4]) of 138 carnivore feces were positive for E. multilocularis-DNA, as well as 25% (95% CI [5.5; 57.2]) of 12 rodent carcasses, and 5.1% (95% CI [1.4; 8.7]) for T. martis or T. crassiceps. Of all NHPs tested, 10.1% (95% CI [3.8; 16.4]) were seropositive for Echinococcus spp. and 8.2% (95% CI [1.3; 15.1]) for Taenia spp. Conclusions: Our data support the existence of zoonotic cycles of larval cestode infections in the direct environment of the primatology center affecting NHPs harbored in the SPC, potentially threatening the human population living in this area. Since this zoonotic risk is borne by local wildlife, and given the severity of these infections, it seems necessary to put in place measures to protect captive NHPs, and further studies to better assess the risk to human populations.

Prevalence of gastrointestinal parasites in captive non-human primates of zoological gardens in North-Eastern region of India

ABSTRACT The increasing emergence of wildlife diseases with the possibility of ecological threats as well as domestic animals and human health has prompted the importance of understanding disease dynamics and associated risks in biological conservation. The present study was undertaken from the North Eastern part of India from July 2017 to June 2018 to identify different gastrointestinal parasites based on faecal sample examination in various captive non-human primates (NHPs). Fresh stool sample (10–15 g) was collected and examined by both sedimentation and floatation techniques to identify parasitic ova and cysts. Out of 145 NHPs examined, 32 (22.06%) were found positive for any of the gastrointestinal (GIT) parasites based on morphological characteristics of either ova or cyst. It can be inferred from the study that captive NHPs are much more susceptible to GI parasite infection. Proper management is necessary to maintain this part of the ecosystem.

Refinements to captive chimpanzee (Pan troglodytes) care: a self-medication Paradigm.

In an effort to enhance welfare, behavioural management continually refines methods of non-human primate (NHP) care. Chimpanzees (Pan troglodytes) are one of the most cognitively complex captive NHPs and they have been observed to self-medicate in the wild. The population of captive chimpanzees in the US is aged (due to a breeding moratorium instituted in 1998) and will progressively require more medical care as they get older. To functionally simulate natural self-medication behaviour, provide chimpanzees with the opportunity to voluntarily participate in their own healthcare, and open new avenues of communication between caregivers and chimpanzees, we used a medication choice paradigm that allowed chimpanzees to choose their daily arthritis medication. We provided four arthritic, mobility-impaired chimpanzees with meloxicam or ibuprofen in blue or green Gatorade® to establish associations between the coloured drinks and the effects of the medications. We subsequently gave each chimpanzee a choice between the two medications. Behaviour was recorded using 15-min focal animal observations. Mobility was assessed using interactive mobility tests and a caregiver-rating system. One chimpanzee showed a medication preference (ibuprofen over meloxicam). The chimpanzees exhibited no significant behavioural or mobility differences over time, suggesting that ibuprofen and meloxicam may not differ significantly in their ability to alleviate arthritic symptoms. Whether or not the chimpanzees show a medication preference, the opportunity to make meaningful choices and the functional simulation of a complex behaviour, self-medication, is present when using this medication choice technique. Furthermore, the paradigm itself could have potential applications for additional medication options and treatment regimens.

Gastrointestinal parasites of zoonotic importance observed in the wild, urban, and captive populations of non-human primates in Malaysia.

A study was undertaken to determine gastrointestinal (GI) parasites commonly found in Malaysia's non-human primates (NHP) living in three different types of populations (wild, urban, and captive) and the basis of major GI parasites of zoonotic importance. A total of 308 samples was collected and microscopically screened from the NHP in the wild (n=163), urban (n=76), and captive (n=69) populations. The samples were taken from 12 species of local NHPs. At least, 44 species of GI parasites comprising of protozoans (seven species), nematodes (26 species), cestodes (five species), trematodes (five species), and pentastomida (one species) were detected. There were no significant differences for the overall prevalence and no great differences in GI parasite species among the wild, urban, and captive NHP populations. The most common GI parasite was Ascaris spp. (49.7%), followed by Oesophagostomum spp. (26.9%), and 31 species discovered in this study are of known public health importance.

PARV4 found in wild chimpanzee faeces: an alternate route of transmission?

Human parvovirus 4 (PARV4, family Parvoviridae, genus Tetraparvovirus) displays puzzling features, such as uncertain clinical importance/significance, unclear routes of transmission, and discontinuous geographical distribution. The origin, or the general reservoir, of human PARV4 infection is unknown. We aimed to detect and characterize PARV4 virus in faecal samples collected from two wild chimpanzee populations and 19 species of captive non-human primates. We aimed to investigate these species as a potential reservoir and alternate route of transmission on the African continent. From almost 500 samples screened, a single wild Pan troglodytes schweinfurthii sample tested positive. Full genome analysis, as well as single ORF phylogenies, confirmed species-specific PARV4 infection.

Genetic characterisation and phylogenetic status of whipworms (Trichuris spp.) from captive non-human primates in China, determined by nuclear and mitochondrial sequencing

BackgroundWhipworms (Nematoda: Trichuridae), among the most common soil-transmitted helminths (STHs), can cause the socioeconomically important disease trichuriasis in various mammalian hosts including humans and non-human primates. For many years, Trichuris from non-human primates has been assigned to the same species as the one infecting humans Trichuris trichiura. More recently, several molecular reports challenged this assumption following recognition of a Trichuris species complex observed in humans and non-human primates. A refined concept for species limits within Trichuris contributes to an understanding of diversity and the potential (zoonotic) transmission among humans and non-human primates. In this study, we expanded previous investigations by exploring the diversity of Trichuris among eight primates including three Asian autochthonous species (i.e. Rhinopithecus roxellana, Rhinopithecus bieti and Nomascus leucogenys). Species-level identification, whether novel or assignable to known lineages of Trichuris, was based on analyses of nuclear internal transcribed spacers (ITS) and mitochondrial cytochrome c oxidase subunit 1 (cox1) genes.ResultsIn total, seven genetically distinct subgroups of whipworms were determined to be present among the primates sampled. Most Trichuris lineages, including Subgroups 1, 1’, 3, 5 and 6, showed a broad host range and were not restricted to particular primate species; in addition to T. trichiura, a complex of Trichuris species was shown infecting primates. Furthermore, it was assumed that Trichuris spp. from either N. leucogenys and P. hamadryas or R. roxellana and R. bieti, respectively, were conspecific. Each pair was indicated to be a discrete lineage of Trichuris, designated, respectively, as Subgroups 1 or 1’ and 2, based on integrated genetic and phylogenetic evidence.ConclusionThese results emphasise that the taxonomy and genetic variations of Trichuris are more complicated than previously acknowledged. These cumulative molecular and phylogenetic data provide a better understanding of the taxonomy, genetics and evolutionary biology of the whipworms.

Serological and molecular investigation for hepatitis E virus (HEV) in captive non-human primates, Italy

Hepatitis E virus (HEV) is the leading cause of human enterically-transmitted viral hepatitis occurring around the world both as outbreaks and as sporadic cases. Non-human primates (NHPs) have been experimentally infected with HEV, but few studies have been reported about natural infection in wild-living and zoo monkeys. In order to provide a more complete picture on the epidemiology of HEV in NHPs living in controlled environment, we investigated the presence of HEV by screening serologically and molecularly a historical collection of 86 sera from seven different species of primates housed at the Zoological Garden (Bioparco) of Rome, Italy. By using an enzyme-linked immunosorbent assay based on the recombinant capsid protein of a Gt3 HEV strain, IgG antibodies were detected in three macaques (4.8%; 3/62) and in a white-crowned mangabey (16.6%; 1/6), with an overall prevalence of 4.6% (4/86). This positivity was confirmed when assessed the sera by western blotting. Rescreening the sera for IgM and viral RNA, all the samples resulted negative. Also, HEV RNA was not found when 17 stool samples were analyzed by RT-PCR. Although these results suggest that none of the monkeys housed at the Bioparco of Rome in the 17-year time frame spanning 2001 to 2017 developed acute or at least sub-acute HEV disease, the detection of IgG antibodies demonstrated that animals living in this setting were exposed to HEV or to antigenically related viruses.

Enterovirus-A76 of South-East Asian Ancestry in a Captive Chimpanzee (Pan troglodytes) in Jos, Nigeria

We recently detected EV-A119 and EV-B111 (previously shown to co-circulate between nonhuman primates (NHPs) and humans) in Nigerian children diagnosed with acute flaccid paralysis (AFP). This study was designed to investigate and catalogue EVs present in captive NHPs in Nigeria. Twenty-seven fecal samples collected from captive NHPs in a Wild Life Park and Zoological garden at Jos, Nigeria in April 2016 were analyzed in this study. Samples were resuspended in a phosphate buffered saline (PBS)/chloroform mixture, and the clarified supernatant was subjected to RNA extraction, cDNA synthesis, a Panenterovirus 5I-UTR assay, and three different enterovirus VP1 snPCR assays. All amplicons from the snPCR assays were sequenced, and enteroviruses identified using the enterovirus genotyping tool and phylogenetic analysis. Eight (29.63%) (two each from Chimpanzees, Patas Monkey, Mona Monkey and Baboon) of the 27 samples were positive for the 5I-UTR assay. One (3.70%) of the 27 samples was positive for the enterovirus VP1 snPCR assays in addition to its positivity by 5I-UTR assay. The same sample happens to be one of the two samples from Chimpanzees that tested positive for the 5I-UTR assay, and it was subsequently identified as EV-A76 of South-East Asia ancestry. This study documents the first recorded attempt to detect and identify enteroviruses in NHPs in Nigeria. It also reports the first detection and identification of EV-A76 in Nigeria and particularly in a NHP. It is of utmost importance that the enterovirus VP1 assays be improved to enable detection of EVs that have been detected in NHPs but yet to be described in humans.

Correction: Multilocus genotyping of Giardia duodenalis in captive non-human primates in Sichuan and Guizhou provinces, Southwestern China.

[This corrects the article DOI: 10.1371/journal.pone.0184913.].

Trypanosoma cruzi Transmission Among Captive Nonhuman Primates, Wildlife, and Vectors

Natural infection of captive nonhuman primates (NHPs) with Trypanosoma cruzi (agent of Chagas disease) is an increasingly recognized problem in facilities across the southern USA, with negative consequences for NHP health and biomedical research. We explored a central Texas NHP facility as a nidus of transmission by characterizing parasite discrete typing units (DTU) in seropositive rhesus macaques (Macaca mulatta), identifying the wildlife reservoirs, and characterizing vector infection. In seropositive NHPs, we documented low and intermittent concentrations of circulating T. cruzi DNA, with two DTUs in equal proportions, TcI and TcIV. In contrast, consistently high concentrations of T. cruzi DNA were found in wild mesomammals at the facility, yet rodents were PCR-negative. Strong wildlife host associations were found in which raccoons (Procyon lotor) harbored TcIV and opossums (Didelphis virginiana) harbored TcI, while skunks (Mephitis mephitis) were infected with both DTUs. Active and passive vector surveillance yielded three species of triatomines from the facility and in proximity to the NHP enclosures, with 17% T. cruzi infection prevalence. Interventions to protect NHP and human health must focus on interrupting spillover from the robust sylvatic transmission in the surrounding environment.