Changing parasite landscapes in captive primates: methodological advances and findings from the Wrocław Zoo.

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 captivityand raise concerns about the introduction of novel parasites to potentially susceptible wildlife populations during reintroduction programs.

Non-human primates (NHPs) living in captive conditions are susceptible to intestinal parasites that can contribute to mortality and morbidity, and cause zoonotic infections. Thus, parasite surveys on NHP populations under human care are relevant as part of the evaluation of NHPs welfare and in the zoonotic disease risk assessment, as well as in the exploration of parasite transmission pathways, according to the One-Health concept. This study aimed to identify intestinal parasites infecting NHPs living in two wildlife recovery centers and in a zoological garden, in Italy. Ninety-three fecal samples from Macaca tonkeana, Macaca fascicularis, Sapajus apella, Chlorocebus aethiops, Macaca fuscata, Macaca sylvanus, and Cebus capucinus were collected at Piano dell'Abatino Park (Lazio), and fecal smears and flotation were performed in order to identify parasites according to morphological keys. Additionally, one carcass of M. fuscata from the Bioparco Zoological Garden of Rome (Lazio) and one of M. fascicularis from the Center for the Recovery of Exotic and Maremma Wild Animals (Tuscany) were necropsied and intestinal adult nematodes were collected and characterized at morphological and molecular level, using the mitochondrial cox1 and rrnL markers. Protozoans (Entamoeba coli, Iodamoeba bütschlii, Dientamoeba fragilis-like, Giardia sp.), chromists (Balantidium/Buxtonella sp.) and nematodes (Capillaria sp., Trichuris sp., strongyliform larvae and Oesophagostomum sp.) were found through fecal smears and flotation. The collected adult nematodes from dead NHPs were morphologically identified as whipworms (genus Trichuris). Phylogenetic analyses grouped Trichuris specimens into the Trichuris trichiura complex of species, with specimens from M. fuscata clustering into a host-specific branch, and whipworms from M. fascicularis clustering within a clade formed by Trichuris infecting several primate species, including humans. The results here collected revealed the presence of potentially zoonotic parasites circulating in captive primates in Italy, providing useful information for the formulation of management and care plans for captive NHPs, and for the elaboration of safety measures for visitors and animal keepers.

A study on the gastrointestinal parasites among free-living and captive primates at the Afi Mountain, Primate Conservation Area in Calabar, Nigeria was undertaken for the first time to ascertain their zoonotic implications. Faecal samples were subjected to direct smear, floatation, quantitative estimation of helminth eggs (epg) and oocysts (opg), larval isolation and identification by modified Baerman's technique and oocyst sporulation for specie identification. Out of the 108 primates examined, 75(69.44%) were found to be shedding the ova and oocysts of several gastrointestinal parasites of which, the mona monkeys (Cercopethicus mona) 16(80%) followed by the white collared mangabey (Cercocebus torquatus) 7 (77.78) had the highest (p < 0.05) prevalence of infection. Meanwhile, the chimpanzees (Pan troglodytes) had the highest ova or oocyst counts and variety of gastrointestinal parasites such as Ascaris lumbricoides, Trichuris trichiura, Balantidium coli, Enterobius vermicularis, Entamoeba histolytica, Strongyloides stercoralis, Blastocystis hominis, Hymenolepis nana, Schistosoma mansoni, Ancylostosoma duodenale and Cryptosporidium species. Similarly, the drill (Mandrillus leucophaeus), Sclater's white-nosed monkey (Cercopethicus erythrotis sclateri), white-collared mangabey (Cercocebus torquatus) and others, had Ascaris lumbricoides or Ancylostoma duodenale. All captive primates were more infected than those under free-roam. The young (< 12 months) and females had higher infection rates (p < 0.05) than their counterparts. In conclusion, the primates harboured several parasites of zoonotic importance.

Captive primates are susceptible to gastrointestinal (GIT) parasitic infections, which are often zoonotic and can contribute to morbidity and mortality. Fecal samples were examined by the means of direct smear, fecal flotation, fecal sedimentation, and fecal cultures. Of 26.51% (317/1196) of the captive primates were diagnosed gastrointestinal parasitic infections. Trichuris spp. were the most predominant in the primates, while Entamoeba spp. were the most prevalent in Old World monkeys (P < 0.05). These preliminary data will improve the management of captive primates and the safety of animal keepers and visitors.

Simple SummaryLittle information is currently available on the epidemiology of parasitic and commensal protist species in captive non-human primates (NHP) and their zoonotic potential. This study investigates the occurrence, molecular diversity, and potential transmission dynamics of parasitic and commensal protist species in a zoological garden in southern Spain. The prevalence and genotypes of the main enteric protist species were investigated in faecal samples from NHP, zookeepers and free-living rats by molecular (PCR and sequencing) methods. A high prevalence of the diarrhoea-causing protists Giardia duodenalis and Blastocystis sp. (but not Cryptosporidium spp.) was observed in captive NHP at the Córdoba Zoo Conservation Centre. NHP can harbour zoonotic genotypes of G. duodenalis, Blastocystis sp., and Enterocytozoon bieneusi. Indeed, strong evidence of the occurrence of Blastocystis zoonotic transmission between NHP and their handlers was provided, despite the use of personal protective equipment and the implementation of strict health and safety protocols. Free-living sympatric rats are infected by host-specific species/genotypes of the investigated protists and seem to play a limited role as source of infections to NHP or humans in this setting. The extent of these findings should be confirmed in similar epidemiological surveys targeting other captive NHP populations.Little information is currently available on the epidemiology of parasitic and commensal protist species in captive non-human primates (NHP) and their zoonotic potential. This study investigates the occurrence, molecular diversity, and potential transmission dynamics of parasitic and commensal protist species in a zoological garden in southern Spain. The prevalence and genotypes of the main enteric protist species were investigated in faecal samples from NHP (n = 51), zookeepers (n = 19) and free-living rats (n = 64) by molecular (PCR and sequencing) methods between 2018 and 2019. The presence of Leishmania spp. was also investigated in tissues from sympatric rats using PCR. Blastocystis sp. (45.1%), Entamoeba dispar (27.5%), Giardia duodenalis (21.6%), Balantioides coli (3.9%), and Enterocytozoon bieneusi (2.0%) (but not Troglodytella spp.) were detected in NHP. Giardia duodenalis (10.5%) and Blastocystis sp. (10.5%) were identified in zookeepers, while Cryptosporidium spp. (45.3%), G. duodenalis (14.1%), and Blastocystis sp. (6.25%) (but not Leishmania spp.) were detected in rats. Blastocystis ST1, ST3, and ST8 and G. duodenalis sub-assemblage AII were identified in NHP, and Blastocystis ST1 in zookeepers. Giardia duodenalis isolates failed to be genotyped in human samples. In rats, four Cryptosporidium (C. muris, C. ratti, and rat genotypes IV and V), one G. duodenalis (assemblage G), and three Blastocystis (ST4) genetic variants were detected. Our results indicate high exposure of NHP to zoonotic protist species. Zoonotic transmission of Blastocysts ST1 was highly suspected between captive NHP and zookeepers.

A study to determine the prevalence and morphotype diversity of soil-transmitted helminths in captive non-human primates (NHPs) in northern Nigeria was conducted. Simple flotation and sedimentation methods were used to examine fecal samples. A Morphometric analysis was done on Trichuris spp. eggs to determine the diversity of whipworm circulating in NHPs in the study area. High prevalence (60%) of infection was recorded in captive NHPs; Patas Monkey (n=17), Tantalus Monkey (n=9), Mona Monkey (n=7), Vervet Monkey (n=2), Mangabey Monkey (n=1), Baboon (n=14), and Chimpanzee (n=8) from parks and zoological gardens located in four Nigerian states (Borno, Gombe, Kano, and Plateau) and the Federal Capital Territory (FCT), Abuja. Captive NHPs examined were infected with helminths either as single, double or triple infections. Four zoonotic soil transmitted helminth (STH) genera, Trichuris, Strongyloides, Ancylostoma, and Enterobius were detected in the examined animals. Eggs of Trichuris spp. were the most prevalent with four morphotypes suggesting several morphotypes of whipworm were circulating among the NHPs in this region. Further studies are required to elucidate the epidemiologic and public health implications of these findings.

Parasitic diseases often represent a major concern in zoo animals for the high environmental contamination due to the maintenance of animals in confined areas. In wild conditions, animals have some natural resistance against parasitic diseases and there is a state of equilibrium between the parasite and the host and it seldom led to harmful infection unless stressed. The aim of the research work is on the conditional state of primates in selected zoological garden primates in selected Zoological Gardens in Nigeria. Survey method was adapted for this research 87 questionnaires was distributed among staff taking care of the zoological gardens. The findings of this work shows, that captive primates are housed according to their species. From the responses, the nutritional status of the captive primates is moderate, based on their physical appearance, and shows 34 respondents, representing (39.1%) Agreed, 29 respondents, representing (33.3%) strongly agreed that the captive primates are constantly dewormed against parasitic infections, while 20 respondents, representing (4.6%) strongly disagreed. On the accountability of the funds, 36 respondents, representing (41.4%) Agreed, 18 respondents, representing (20.7%) strongly agreed, while 24 respondents, which represents (27.6%) disagreed and 9 representing (10.3%) strongly disagreed based on the data, there is adequate accountability of the funds allocated to zoos.

Species introductions often coincide with loss of genetic diversity and natural enemies. Anthropogenic translocation of the North-American pumpkinseed Lepomis gibbosus (L., 1758) (Centrarchidae) and its further spread have resulted in recent species establishment in most European countries. This study determines genetic differentiation of non-native European pumpkinseed populations and identifies how their genetic structure relates to the distribution and abundance of parasite species. Microsatellite analysis indicated presence of three genetic lineages, which were well supported by discriminant analysis based on parasite abundance data. The first lineage clustered pumpkinseed populations from northern and southern France and showed high allelic richness, heterozygosity and parasite richness. The second included populations along the “Southern invasion corridor” connecting the rivers Rhine, Main and Danube. The fish exhibited low to high genetic and parasite diversity and generally high parasite abundance. The third lineage clustered populations with low genetic and parasite diversity, located in Portuguese reservoirs and water bodies along the upper Elbe. Parasite species richness was significantly associated with host microsatellite heterozygosity and allelic richness, a trend partially affected by richness of North-American parasites. Furthermore, our results indicate that parasite community composition may serve as a useful biological tool to discriminate non-native fish populations and their inter-relationships.

Presence and genetic diversity of enteric protists in captive and semi-captive non-human primates in côte d'Ivoire, Sierra Leone, and Peru.

Currently, there is limited available information on the epidemiology of parasitic infections in captive non-human primates (NHPs) and their zoonotic potential. However, numerous cases of helminth infections in NHPs have been documented in several zoos around the world, with one of the most prevalent being those of the genus Trichuris. The main objective of this study is to investigate the occurrence of infection by Trichuris spp. in primates from zoological gardens in Spain and to ascertain, at the species level, the specific Trichuris species harbored by these hosts by using mitochondrial and ribosomal markers. A total of 315 stools collected from NPHs (n = 47) in the 13 zoological gardens analyzed yielded a prevalence rate of 19.05%. Nevertheless, not all the zoos exhibited parasitic infections; this was observed in only 53.85% of the zoos. Moreover, 15 host groups of 12 different species were found to be infected by Trichuris species, among which the identified species included Trichuris trichiura, Trichuris colobae, and Trichuris sp. Our findings suggest a substantial exposure of primates to zoonotic Trichuris species, suggesting that NHPs could potentially act as reservoirs capable of transmitting this parasite to humans. Hence, it is crucial to implement additional control and prevention measures and explore ways to eradicate parasitic infections in these areas. Further examination is warranted to minimize the risk of spreading drug-resistant parasite strains.

The diversity of fish parasites reflects the diversity of parasites in the water source, providing insights into the effects of pathogens and essential information about parasite-host relationships. Parasitic infections are valuable indicators of the aquatic ecosystem, influenced by various factors. This study aimed to investigate the prevalence and seasonality of parasite species and pathogenic bacteria in Siamese fighting fish (Betta splendens) over 12 months, involving sixty ornamental Siamese fighting fish collected from commercial sources and 81 wild Siamese fighting fish from different natural habitats. Parasite prevalence in ornamental Siamese fighting fish (25.00%) was lower than in the wild (34.57%). The protozoa parasite Trichodina was found in both Siamese fighting fish, with the highest prevalence recorded for Trichodina sp. in wild Siamese fighting fish. The winter season exhibited the highest parasitic prevalence, with a tremendous diversity of parasites found at each location, followed by the rainy and summer seasons. This study also reported the first finding of Henneguya sp. infection in Siamese fighting fish and on the body surface. The prevalence and seasonality of parasite genera were significant in the wild compared to ornamental Siamese fighting fish. Bacterial isolation was performed on internal organs, and isolates were identified using PCR techniques. Aeromonas veronii and Mycobacterium marinum were detected in ornamental Siamese fighting fish, while A. veronii was found in wild Siamese fighting fish. These findings indicate that infections in Siamese fighting fish display seasonal variation and are impacted by their ecology. This information is fundamental for managing the biodiversity of parasites in fish and preventing parasite infections in aquaculture.

To identify demographic, behavioural and environmental determinants of intestinal parasitic infection, evaluate the impact of a variety of dry sanitation systems on intestinal parasitic infection, and evaluate the safety of using stored biosolids in agriculture in order to guide future sanitation interventions in rural areas of El Salvador. Interviews were conducted with 109 households in eight communities where double-vaulted and solar urine-diverting desiccating latrines, pit latrines or no latrines were used. Faecal samples from 499 individuals were tested for enteric helminths and protozoa. Users of solar desiccating latrines had the lowest prevalence of enteric parasite infection. Double-vault, urine-diverting desiccating latrines effectively reduced the transmission of some pathogens, but may not achieve the conditions sufficient for the complete destruction of the more environmentally persistent pathogens, Ascaris lumbricoides and Trichuris trichiura. Contact with inadequately treated latrine biosolids was associated with an increased risk of Ascaris infection. Solar latrines were associated with the overall lowest prevalence of enteric parasitic infections. Members of households where latrine biosolids were used in agriculture had a higher prevalence of infection than those where biosolids were buried. We therefore recommend the promotion of solar latrines in rural areas of El Salvador over other dry sanitation systems, and recommend that stored biosolids not be used in agriculture.

Gastrointestinal protozoa in non-human primates of four zoological gardens in Belgium

Primates are known to harbour different gastrointestinal parasite species that affect their survival and reproductive activity. Entamoeba histolytica infects humans predominantly as well as non-human (NH) primates causing amoebiasis. Amoebic dysentery is common amongst non-human primates in captive sites. The purpose of the study was to evaluate the risk factors associated with the prevalence of amoebic dysentery in captive NH primates of the Mefou Primate Sanctuary (MPS) in Cameroon. The faecal samples of 277 NH primates were analysed by qualitative (direct smear and evergreen kit sedimentation technique) coprology from January to July 2019. Factors such as habitat type, keeper’s age and level of education were assessed to evaluate their effect on the prevalence of amoebic dysentery. The prevalence of Entamoeba histolytica was 46.2% (P=0,079 and χ2=18.13). E histolytica was the most predominant parasite species detected and it was present in all instances of mixed parasite infections. Amongst the NH primates positive for E. histolytica, 28 suffered from amoebic dysentery giving a prevalence of 21.9% and one of the infected primates (Cercopithecus pogonias) actually died from amoebic dysentery. The prevalence of mixed infections was significantly lower amongst NH primates living in outdoor enclosures compared to those living in other habitat types (P=0.015, χ2=10.46). The rate of re-infection was significantly higher amongst NH primates under the care of keepers with the lowest (primary school) level of education (P=0.001, χ2=13.09) on one hand and of older keepers (≥50s) (P = 0.008, χ2=13.708) on the other hand. This study shows that amoebic dysentery is a cause for a major concern in the MPS. The housing conditions of the NH primates at the sanctuary, the keeper’s age and level of education were important factors that influenced the prevalence of amoebic dysentery. Adequate measures should be put in place to address the situation.

Helminth and protozoan gastrointestinal tract parasites in captive and wild-trapped African non-human primates