{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,3,31]],"date-time":"2026-03-31T01:40:08Z","timestamp":1774921208959,"version":"3.50.1"},"reference-count":101,"publisher":"MDPI AG","issue":"11","license":[{"start":{"date-parts":[[2021,11,17]],"date-time":"2021-11-17T00:00:00Z","timestamp":1637107200000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":["Animals"],"abstract":"<jats:p>Wild chimpanzee populations in West Africa (Pan troglodytes verus) have dramatically decreased as a direct consequence of anthropogenic activities and infectious diseases. Little information is currently available on the epidemiology, pathogenic significance, and zoonotic potential of protist species in wild chimpanzees. This study investigates the occurrence and genetic diversity of intestinal and blood protists as well as filariae in faecal samples (n = 234) from wild chimpanzees in the Dindefelo Community Nature Reserve, Senegal. PCR-based results revealed the presence of intestinal potential pathogens (Sarcocystis spp.: 11.5%; Giardia duodenalis: 2.1%; Cryptosporidium hominis: 0.9%), protist of uncertain pathogenicity (Blastocystis sp.: 5.6%), and commensal species (Entamoeba dispar: 18.4%; Troglodytella abrassarti: 5.6%). Entamoeba histolytica, Enterocytozoon bieneusi, and Balantioides coli were undetected. Blood protists including Plasmodium malariae (0.4%), Trypanosoma brucei (1.3%), and Mansonella perstans (9.8%) were also identified. Sanger sequencing analyses revealed host-adapted genetic variants within Blastocystis, but other parasitic pathogens (C. hominis, P. malariae, T. brucei, M. perstans) have zoonotic potential, suggesting that cross-species transmission between wild chimpanzees and humans is possible in areas where both species overlap. Additionally, we explored potential interactions between intestinal\/blood protist species and seasonality and climate variables. Chimpanzees seem to play a more complex role on the epidemiology of pathogenic and commensal protist and nematode species than initially anticipated.<\/jats:p>","DOI":"10.3390\/ani11113291","type":"journal-article","created":{"date-parts":[[2021,11,17]],"date-time":"2021-11-17T21:32:07Z","timestamp":1637184727000},"page":"3291","update-policy":"https:\/\/doi.org\/10.3390\/mdpi_crossmark_policy","source":"Crossref","is-referenced-by-count":11,"title":["Molecular Detection and Characterization of Intestinal and Blood Parasites in Wild Chimpanzees (Pan troglodytes verus) in Senegal"],"prefix":"10.3390","volume":"11","author":[{"given":"Pamela C.","family":"K\u00f6ster","sequence":"first","affiliation":[{"name":"Parasitology Reference and Research Laboratory, Spanish National Centre for Microbiology, 28220 Majadahonda, Spain"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Justinn","family":"Renelies-Hamilton","sequence":"additional","affiliation":[{"name":"Section for Ecology and Evolution, Department of Biology, University of Copenhagen, DK-1165 Copenhagen, Denmark"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Laia","family":"Dotras","sequence":"additional","affiliation":[{"name":"Jane Goodall Institute Spain and Senegal, Dindefelo Biological Station, Dindefelo, Kedougou, Senegal"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Manuel","family":"Llana","sequence":"additional","affiliation":[{"name":"Jane Goodall Institute Spain and Senegal, Dindefelo Biological Station, Dindefelo, Kedougou, Senegal"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Celia","family":"Vinagre-Izquierdo","sequence":"additional","affiliation":[{"name":"Evolutionary Ecology, Biology Department, Lund University, 223 62 Lund, Sweden"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Petras","family":"Prakas","sequence":"additional","affiliation":[{"name":"Nature Research Centre, LT-08412 Vilnius, Lithuania"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-7559-9316","authenticated-orcid":false,"given":"Donatas","family":"Sneideris","sequence":"additional","affiliation":[{"name":"Nature Research Centre, LT-08412 Vilnius, Lithuania"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"ORCID":"https:\/\/orcid.org\/0000-0001-8707-5731","authenticated-orcid":false,"given":"Alejandro","family":"Dashti","sequence":"additional","affiliation":[{"name":"Parasitology Reference and Research Laboratory, Spanish National Centre for Microbiology, 28220 Majadahonda, Spain"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Bego\u00f1a","family":"Bailo","sequence":"additional","affiliation":[{"name":"Parasitology Reference and Research Laboratory, Spanish National Centre for Microbiology, 28220 Majadahonda, Spain"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Marta","family":"Lanza","sequence":"additional","affiliation":[{"name":"Parasitology Reference and Research Laboratory, Spanish National Centre for Microbiology, 28220 Majadahonda, Spain"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Alejandra","family":"Jim\u00e9nez-Mej\u00edas","sequence":"additional","affiliation":[{"name":"Parasitology Reference and Research Laboratory, Spanish National Centre for Microbiology, 28220 Majadahonda, Spain"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Carlota","family":"Mu\u00f1oz-Garc\u00eda","sequence":"additional","affiliation":[{"name":"Parasitology Reference and Research Laboratory, Spanish National Centre for Microbiology, 28220 Majadahonda, Spain"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-4167-0129","authenticated-orcid":false,"given":"Aly S.","family":"Muadica","sequence":"additional","affiliation":[{"name":"Parasitology Reference and Research Laboratory, Spanish National Centre for Microbiology, 28220 Majadahonda, Spain"},{"name":"Departamento de Ci\u00eancias e Tecnologia, Universidade Licungo, Quelimane 106, Mozambique"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"ORCID":"https:\/\/orcid.org\/0000-0001-5083-8854","authenticated-orcid":false,"given":"David","family":"Gonz\u00e1lez-Barrio","sequence":"additional","affiliation":[{"name":"Parasitology Reference and Research Laboratory, Spanish National Centre for Microbiology, 28220 Majadahonda, Spain"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-1903-6711","authenticated-orcid":false,"given":"Jos\u00e9 M.","family":"Rubio","sequence":"additional","affiliation":[{"name":"Parasitology Reference and Research Laboratory, Spanish National Centre for Microbiology, 28220 Majadahonda, Spain"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Isabel","family":"Fuentes","sequence":"additional","affiliation":[{"name":"Parasitology Reference and Research Laboratory, Spanish National Centre for Microbiology, 28220 Majadahonda, Spain"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"ORCID":"https:\/\/orcid.org\/0000-0001-9034-8606","authenticated-orcid":false,"given":"Francisco","family":"Ponce-Gordo","sequence":"additional","affiliation":[{"name":"Department of Microbiology and Parasitology, Faculty of Pharmacy, Complutense University of Madrid, 28040 Madrid, Spain"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"ORCID":"https:\/\/orcid.org\/0000-0003-2323-0135","authenticated-orcid":false,"given":"Rafael","family":"Calero-Bernal","sequence":"additional","affiliation":[{"name":"Salud Veterinaria y Zoonosis (SALUVET), Department of Animal Health, Faculty of Veterinary, Complutense University of Madrid, 28040 Madrid, Spain"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-4015-8553","authenticated-orcid":false,"given":"David","family":"Carmena","sequence":"additional","affiliation":[{"name":"Parasitology Reference and Research Laboratory, Spanish National Centre for Microbiology, 28220 Majadahonda, Spain"}],"role":[{"role":"author","vocabulary":"crossref"}]}],"member":"1968","published-online":{"date-parts":[[2021,11,17]]},"reference":[{"key":"ref_1","doi-asserted-by":"crossref","first-page":"e22681","DOI":"10.1002\/ajp.22681","article-title":"The Critically Endangered western chimpanzee declines by 80%","volume":"79","author":"Sop","year":"2017","journal-title":"Am. J. Primatol."},{"key":"ref_2","unstructured":"IUCN SSC Primate Specialist Group (2020). Regional Action Plan for the Conservation of Western Chimpanzees (Pan troglodytes verus) 2020\u20132030, IUCN."},{"key":"ref_3","doi-asserted-by":"crossref","first-page":"148","DOI":"10.1007\/s10393-017-1306-1","article-title":"Pathogen transmission from humans to great apes is a growing threat to primate conservation","volume":"15","author":"Dunay","year":"2018","journal-title":"Ecohealth"},{"key":"ref_4","doi-asserted-by":"crossref","first-page":"1667","DOI":"10.1017\/S0031182014001085","article-title":"Cryptosporidium species in humans and animals: Current understanding and research needs","volume":"141","author":"Ryan","year":"2014","journal-title":"Parasitology"},{"key":"ref_5","doi-asserted-by":"crossref","first-page":"283","DOI":"10.1016\/j.rvsc.2020.09.034","article-title":"Giardia duodenalis in humans and animals\u2014Transmission and disease","volume":"135","author":"Dixon","year":"2021","journal-title":"Res. Vet. Sci."},{"key":"ref_6","doi-asserted-by":"crossref","first-page":"e23124","DOI":"10.1002\/ajp.23124","article-title":"Entamoeba histolytica infections in wild and semi-wild orangutans in Sumatra and Kalimantan","volume":"82","author":"Stuart","year":"2020","journal-title":"Am. J. Primatol."},{"key":"ref_7","doi-asserted-by":"crossref","first-page":"51","DOI":"10.1016\/j.rvsc.2021.02.008","article-title":"Zoonotic Sarcocystis","volume":"136","author":"Rosenthal","year":"2021","journal-title":"Res. Vet. Sci."},{"key":"ref_8","doi-asserted-by":"crossref","first-page":"436","DOI":"10.1016\/j.pt.2019.04.004","article-title":"Host specificity of Enterocytozoon bieneusi and public health implications","volume":"35","author":"Li","year":"2019","journal-title":"Trends Parasitol."},{"key":"ref_9","doi-asserted-by":"crossref","first-page":"260","DOI":"10.1016\/j.rvsc.2020.09.031","article-title":"Blastocystis in domesticated and wild mammals and birds","volume":"135","author":"Hublin","year":"2021","journal-title":"Res. Vet. Sci."},{"key":"ref_10","doi-asserted-by":"crossref","first-page":"424","DOI":"10.1016\/j.rvsc.2020.10.028","article-title":"Balantioides coli\u00a0","volume":"135","year":"2021","journal-title":"Res. Vet. Sci."},{"key":"ref_11","doi-asserted-by":"crossref","first-page":"83","DOI":"10.1111\/j.1550-7408.2008.00369.x","article-title":"The occurrence and ape-to-ape transmission of the entodiniomorphid ciliate Troglodytella abrassarti in captive gorillas","volume":"56","author":"Tokiwa","year":"2009","journal-title":"J. Eukaryot. Microbiol."},{"key":"ref_12","doi-asserted-by":"crossref","first-page":"111","DOI":"10.1186\/s12936-015-0622-6","article-title":"Diversity of malaria parasites in great apes in Gabon","volume":"14","author":"Boundenga","year":"2015","journal-title":"Malar. J."},{"key":"ref_13","doi-asserted-by":"crossref","first-page":"737","DOI":"10.1016\/j.ijpara.2016.06.004","article-title":"The host specificity of ape malaria parasites can be broken in confined environments","volume":"46","author":"Ngoubangoye","year":"2016","journal-title":"Int. J. Parasitol."},{"key":"ref_14","doi-asserted-by":"crossref","first-page":"277","DOI":"10.1016\/j.ijppaw.2015.05.001","article-title":"Wild chimpanzees are infected by Trypanosoma brucei","volume":"4","author":"Lankester","year":"2015","journal-title":"Int. J. Parasitol. Parasites Wildl."},{"key":"ref_15","doi-asserted-by":"crossref","first-page":"313","DOI":"10.1186\/s13071-020-04184-1","article-title":"Detection of DNA of filariae closely related to Mansonella perstans in faecal samples from wild non-human primates from Cameroon and Gabon","volume":"13","author":"Gaillard","year":"2020","journal-title":"Parasites Vectors"},{"key":"ref_16","doi-asserted-by":"crossref","unstructured":"Zahedi, A., Bolland, S.J., Oskam, C.L., and Ryan, U. (2021). Cryptosporidium abrahamseni n. sp. (Apicomplexa: Cryptosporidiiae) from red-eye tetra (Moenkhausia sanctaefilomenae). Exp. Parasitol., in press.","DOI":"10.1016\/j.exppara.2021.108089"},{"key":"ref_17","doi-asserted-by":"crossref","first-page":"943","DOI":"10.1016\/j.ijpara.2013.06.001","article-title":"Zoonotic potential of Giardia","volume":"43","author":"Ryan","year":"2013","journal-title":"Int. J. Parasitol."},{"key":"ref_18","doi-asserted-by":"crossref","unstructured":"Maloney, J.G., and Santin, M. (2021). Mind the gap: New full-length sequences of Blastocystis subtypes generated via Oxford Nanopore Minion sequencing allow for comparisons between full-length and partial sequences of the small subunit of the ribosomal RNA Gene. Microorganisms, 9.","DOI":"10.3390\/microorganisms9050997"},{"key":"ref_19","doi-asserted-by":"crossref","first-page":"3158","DOI":"10.3390\/su4113158","article-title":"Perspectives on sustainable resource conservation in community nature reserves: A case study from Senegal","volume":"4","author":"Pacheco","year":"2012","journal-title":"Sustainability"},{"key":"ref_20","first-page":"114","article-title":"Nesting patterns of chimpanzees (Pan troglodytes verus) in a savannah habitat, Dindefelo, Senegal","volume":"88","author":"Enthoven","year":"2017","journal-title":"Folia Primatol."},{"key":"ref_21","unstructured":"JGIS, and APES Wiki Team (2021, September 11). Dindefelo. Available online: https:\/\/apeswiki.eva.mpg.de\/index.php\/Dindefelo."},{"key":"ref_22","first-page":"167","article-title":"The fruit of discord? Saba senegalensis use by chimpanzees (Pan troglodytes verus) and local people in the Dindefelo Community Nature Reserve (RNCD), Southeastern Senegal","volume":"88","author":"Ramon","year":"2017","journal-title":"Folia Primatol."},{"key":"ref_23","doi-asserted-by":"crossref","first-page":"439","DOI":"10.1136\/bmj.300.6722.439","article-title":"Detection of pseudodiarrhoea by simple clinical assessment of intestinal transit rate","volume":"300","author":"Virjee","year":"1990","journal-title":"BMJ"},{"key":"ref_24","unstructured":"Savtchenko, A. (2019). GPM IMERG Final Precipitation L3 1 Day 0.1 Degree \u00d7 0.1 Degree V06, Goddard Earth Sciences Data and Information Services Center (GES DISC)."},{"key":"ref_25","unstructured":"AIRS Science Team\/Joao Teixeira (2013). AIRS\/Aqua L3 Daily Standard Physical Retrieval (AIRS-only) 1 Degree \u00d7 1 Degree V006, Goddard Earth Sciences Data and Information Services Center (GES DISC)."},{"key":"ref_26","doi-asserted-by":"crossref","first-page":"357","DOI":"10.1046\/j.1365-3156.2002.00855.x","article-title":"Molecular analysis of Cryptosporidium species isolated from HIV-infected patients in Thailand","volume":"7","author":"Tiangtip","year":"2002","journal-title":"Trop. Med. Int. Health"},{"key":"ref_27","doi-asserted-by":"crossref","first-page":"4303","DOI":"10.1128\/JCM.01067-06","article-title":"Evidence supporting zoonotic transmission of Cryptosporidium spp. in Wisconsin","volume":"44","author":"Feltus","year":"2006","journal-title":"J. Clin. Microbiol."},{"key":"ref_28","doi-asserted-by":"crossref","first-page":"145","DOI":"10.1179\/136485910X12607012373759","article-title":"Application of real-time PCR for the differentiation of Entamoeba histolytica and E. dispar in cyst-positive faecal samples from 130 immigrants living in Spain","volume":"104","author":"Cogollos","year":"2010","journal-title":"Ann. Trop. Med. Parasitol."},{"key":"ref_29","doi-asserted-by":"crossref","first-page":"1153","DOI":"10.1046\/j.1360-2276.2003.01145.x","article-title":"Prevalence of Entamoeba histolytica and Entamoeba dispar in northern Ghana","volume":"8","author":"Verweij","year":"2003","journal-title":"Trop. Med. Int. Health"},{"key":"ref_30","doi-asserted-by":"crossref","first-page":"223","DOI":"10.1016\/S0890-8508(03)00057-4","article-title":"Real-time PCR for the detection of Giardia lamblia","volume":"17","author":"Verweij","year":"2003","journal-title":"Mol. Cell. Probes"},{"key":"ref_31","doi-asserted-by":"crossref","first-page":"125","DOI":"10.1016\/j.meegid.2004.02.001","article-title":"Discrimination of all genotypes of Giardia duodenalis at the glutamate dehydrogenase locus using PCR-RFLP","volume":"4","author":"Read","year":"2004","journal-title":"Infect. Genet. Evol."},{"key":"ref_32","doi-asserted-by":"crossref","first-page":"207","DOI":"10.1016\/j.ijpara.2004.10.022","article-title":"Genetic heterogeneity at the beta-giardin locus among human and animal isolates of Giardia duodenalis and identification of potentially zoonotic subgenotypes","volume":"35","author":"Lalle","year":"2005","journal-title":"Int. J. Parasitol."},{"key":"ref_33","doi-asserted-by":"crossref","first-page":"1444","DOI":"10.3201\/eid0911.030084","article-title":"Triosephosphate isomerase gene characterization and potential zoonotic transmission of Giardia duodenalis","volume":"9","author":"Sulaiman","year":"2003","journal-title":"Emerg. Infect. Dis."},{"key":"ref_34","doi-asserted-by":"crossref","first-page":"77","DOI":"10.1016\/j.protis.2005.12.001","article-title":"DNA barcoding of Blastocystis","volume":"157","author":"Scicluna","year":"2006","journal-title":"Protist"},{"key":"ref_35","doi-asserted-by":"crossref","first-page":"2595","DOI":"10.1128\/AEM.68.5.2595-2599.2002","article-title":"Prevalence of Enterocytozoon bieneusi in swine: An 18-month survey at a slaughterhouse in Massachusetts","volume":"68","author":"Buckholt","year":"2002","journal-title":"Appl. Environ. Microbiol."},{"key":"ref_36","doi-asserted-by":"crossref","first-page":"774","DOI":"10.1016\/j.protis.2011.06.008","article-title":"Genetic heterogeneity in internal transcribed spacer genes of Balantidium coli (Litostomatea, Ciliophora)","volume":"162","year":"2011","journal-title":"Protist"},{"key":"ref_37","doi-asserted-by":"crossref","first-page":"525","DOI":"10.1002\/ajpa.22067","article-title":"Molecular diversity of entodiniomorphid ciliate Troglodytella abrassarti and its coevolution with chimpanzees","volume":"148","author":"Vallo","year":"2012","journal-title":"Am. J. Phys. Anthropol."},{"key":"ref_38","doi-asserted-by":"crossref","first-page":"12","DOI":"10.1016\/j.actatropica.2017.12.030","article-title":"Geographical distribution and species identification of human filariasis and onchocerciasis in Bioko Island, Equatorial Guinea","volume":"180","author":"Ta","year":"2018","journal-title":"Acta Trop."},{"key":"ref_39","first-page":"406","article-title":"The neighbor-joining method: A new method for reconstructing phylogenetic trees","volume":"4","author":"Saitou","year":"1987","journal-title":"Mol. Biol. Evol."},{"key":"ref_40","unstructured":"R Core Team (2019). R: A Language and Environment for Statistical Computing, R Foundation for Statistical Computing. Available online: https:\/\/www.R-project.org\/."},{"key":"ref_41","doi-asserted-by":"crossref","first-page":"377","DOI":"10.2307\/2347111","article-title":"Algorithm AS 89: The upper tail probabilities of Spearman\u2019s rho","volume":"24","author":"Best","year":"1975","journal-title":"Appl. Stat."},{"key":"ref_42","first-page":"427","article-title":"A network algorithm for performing Fisher\u2019s exact test in r \u00d7 c contingency tables","volume":"78","author":"Mehta","year":"1983","journal-title":"J. Am. Stat. Assoc."},{"key":"ref_43","doi-asserted-by":"crossref","first-page":"289","DOI":"10.1111\/j.2517-6161.1995.tb02031.x","article-title":"Controlling the false discovery rate: A practical and powerful approach to multiple testing","volume":"57","author":"Benjamini","year":"1995","journal-title":"J. R. Stat. Soc. Ser. B"},{"key":"ref_44","doi-asserted-by":"crossref","first-page":"316","DOI":"10.1016\/j.pt.2005.05.010","article-title":"Trypanosoma equiperdum: Master of disguise or historical mistake?","volume":"21","author":"Claes","year":"2005","journal-title":"Trends Parasitol."},{"key":"ref_45","doi-asserted-by":"crossref","first-page":"423","DOI":"10.1186\/s12936-016-1476-2","article-title":"A comparative molecular survey of malaria prevalence among Eastern chimpanzee populations in Issa Valley (Tanzania) and Kalinzu (Uganda)","volume":"15","author":"Mapua","year":"2016","journal-title":"Malar. J."},{"key":"ref_46","doi-asserted-by":"crossref","first-page":"38","DOI":"10.1186\/s12936-018-2187-7","article-title":"Seasonal and inter-annual variation of malaria parasite detection in wild chimpanzees","volume":"17","author":"Wu","year":"2018","journal-title":"Malar. J."},{"key":"ref_47","doi-asserted-by":"crossref","first-page":"557","DOI":"10.1007\/s10393-010-0283-4","article-title":"A legacy of low-impact logging does not elevate prevalence of potentially pathogenic protozoa in free-ranging gorillas and chimpanzees in the Republic of Congo: Logging and parasitism in African apes","volume":"6","author":"Gillespie","year":"2009","journal-title":"Ecohealth"},{"key":"ref_48","doi-asserted-by":"crossref","first-page":"393","DOI":"10.1007\/s00436-012-3147-8","article-title":"Prevalence and climatic associated factors of Cryptosporidium sp. infections in savanna chimpanzees from Ugalla, Western Tanzania","volume":"112","author":"Piel","year":"2013","journal-title":"Parasitol. Res."},{"key":"ref_49","doi-asserted-by":"crossref","first-page":"104010","DOI":"10.1016\/j.meegid.2019.104010","article-title":"Exploring interactions between Blastocystis sp., Strongyloides spp. and the gut microbiomes of wild chimpanzees in Senegal","volume":"74","author":"Parera","year":"2019","journal-title":"Infect. Genet. Evol."},{"key":"ref_50","doi-asserted-by":"crossref","unstructured":"Parsons, M.B., Travis, D., Lonsdorf, E.V., Lipende, I., Roellig, D.M., Collins, A., Kamenya, S., Zhang, H., Xiao, L., and Gillespie, T.R. (2015). Epidemiology and molecular characterization of Cryptosporidium spp. in humans, wild primates, and domesticated animals in the Greater Gombe Ecosystem, Tanzania. PLoS Negl. Trop. Dis., 9.","DOI":"10.1371\/journal.pntd.0003529"},{"key":"ref_51","doi-asserted-by":"crossref","first-page":"195","DOI":"10.1186\/s13071-017-2111-y","article-title":"Cryptosporidium and Giardia in Africa: Current and future challenges","volume":"10","author":"Squire","year":"2017","journal-title":"Parasites Vectors"},{"key":"ref_52","doi-asserted-by":"crossref","first-page":"253","DOI":"10.1016\/j.ijpara.2020.01.005","article-title":"Cryptosporidium hominis infections in non-human animal species: Revisiting the concept of host specificity","volume":"50","author":"Widmer","year":"2020","journal-title":"Int. J. Parasitol."},{"key":"ref_53","doi-asserted-by":"crossref","first-page":"98","DOI":"10.1016\/j.vetpar.2017.12.002","article-title":"Entamoeba histolytica infection in wild lemurs associated with proximity to humans","volume":"249","author":"Ragazzo","year":"2018","journal-title":"Vet. Parasitol."},{"key":"ref_54","first-page":"723","article-title":"Natural infection of baboons by Entamoeba histolytica elicits anti-gal-lectin heavy subunit IgA and IgG antibodies with shared epitope specificity to that of humans","volume":"43","author":"Abdallah","year":"2013","journal-title":"J. Egypt Soc. Parasitol."},{"key":"ref_55","doi-asserted-by":"crossref","first-page":"173","DOI":"10.1002\/ajp.20884","article-title":"Patterns of gastro-intestinal parasites and commensals as an index of population and ecosystem health: The case of sympatric western chimpanzees (Pan troglodytes verus) and guinea baboons (Papio hamadryas papio) at Fongoli, Senegal","volume":"73","author":"Howells","year":"2011","journal-title":"Am. J. Primatol."},{"key":"ref_56","doi-asserted-by":"crossref","first-page":"741","DOI":"10.1017\/S0031182016000263","article-title":"Molecular identification of Entamoeba species in savanna woodland chimpanzees (Pan troglodytes schweinfurthii)","volume":"143","author":"Stewart","year":"2016","journal-title":"Parasitology"},{"key":"ref_57","unstructured":"Deere, J.R., Parsons, M.B., Lonsdorf, E.V., Lipende, I., Kamenya, S., Collins, D.A., Travis, D.A., and Gillespie, T.R. (2018). Entamoeba Histolytica\u20131122, Cambridge University Press."},{"key":"ref_58","doi-asserted-by":"crossref","first-page":"519","DOI":"10.1016\/j.ijpara.2017.11.008","article-title":"Diversity of Entamoeba spp. in African great apes and humans: An insight from Illumina MiSeq high-throughput sequencing","volume":"48","author":"Kreisinger","year":"2018","journal-title":"Int. J. Parasitol."},{"key":"ref_59","doi-asserted-by":"crossref","first-page":"1032","DOI":"10.1002\/ajp.22170","article-title":"Gastrointestinal symbionts of chimpanzees in Cantanhez National Park, Guinea-Bissau with respect to habitat fragmentation","volume":"75","author":"Sousa","year":"2013","journal-title":"Am. J. Primatol."},{"key":"ref_60","doi-asserted-by":"crossref","unstructured":"Sak, B., Petrzelkova, K.J., Kvetonova, D., Mynarova, A., Shutt, K.A., Pomajbikova, K., Kalousova, B., Modry, D., Benavides, J., and Todd, A. (2013). Long-term monitoring of microsporidia, Cryptosporidium and Giardia infections in western Lowland Gorillas (Gorilla gorilla gorilla) at different stages of habituation in Dzanga Sangha Protected Areas, Central African Republic. PLoS ONE, 8.","DOI":"10.1371\/journal.pone.0071840"},{"key":"ref_61","doi-asserted-by":"crossref","first-page":"21","DOI":"10.7589\/2012-09-229","article-title":"Giardia in mountain gorillas (Gorilla beringei beringei), forest buffalo (Syncerus caffer), and domestic cattle in Volcanoes National Park, Rwanda","volume":"50","author":"Hogan","year":"2014","journal-title":"J. Wildl. Dis."},{"key":"ref_62","doi-asserted-by":"crossref","first-page":"905","DOI":"10.1645\/0022-3395(2002)088[0905:AGDGAA]2.0.CO;2","article-title":"Anthropozoonotic Giardia duodenalis genotype (assemblage) a infections in habitats of free-ranging human-habituated gorillas, Uganda","volume":"88","author":"Graczyk","year":"2002","journal-title":"J. Parasitol."},{"key":"ref_63","doi-asserted-by":"crossref","first-page":"498","DOI":"10.1002\/ajpa.21098","article-title":"Ecology of the gastrointestinal parasites of Colobus vellerosus at Boabeng-Fiema, Ghana: Possible anthropozoonotic transmission","volume":"140","author":"Teichroeb","year":"2009","journal-title":"Am. J. Phys. Anthropol."},{"key":"ref_64","doi-asserted-by":"crossref","unstructured":"Johnston, A.R., Gillespie, T.R., Rwego, I.B., McLachlan, T.L., Kent, A.D., and Goldberg, T.L. (2010). Molecular epidemiology of cross-species Giardia duodenalis transmission in western Uganda. PLoS Negl. Trop. Dis., 4.","DOI":"10.1371\/journal.pntd.0000683"},{"key":"ref_65","first-page":"116","article-title":"Beitr\u00e4ge zum lebenszyklus der Sarkosporidien. VIII. Sporozysten von Sarcocystis bovihominis in den f\u00e4zes von rhesusaffen (Macaca rhesus) und pavianen (Papio cynocephalus)","volume":"89","author":"Heydorn","year":"1976","journal-title":"Berl. Munch. Tierarztl. Wochenschr."},{"key":"ref_66","doi-asserted-by":"crossref","first-page":"15","DOI":"10.1007\/BF00927841","article-title":"Transmission of Sarcocystis suihominis from humans to swine to nonhuman primates (Pan troglodytes, Macaca mulatta, Macaca irus)","volume":"59","author":"Fayer","year":"1979","journal-title":"Z. Parasitenkd."},{"key":"ref_67","doi-asserted-by":"crossref","unstructured":"Dubey, J.P., Calero-Bernal, R., Rosenthal, B.M., Speer, C.A., and Fayer, R. (2016). Sarcocystosis of Animals and Humans, CRC Press. [2nd ed.].","DOI":"10.1201\/b19184"},{"key":"ref_68","doi-asserted-by":"crossref","first-page":"1473","DOI":"10.1007\/s00436-015-4881-5","article-title":"Molecular characterisation of Sarcocystis bovifelis, Sarcocystis bovini n. sp., Sarcocystis hirsuta and Sarcocystis cruzi from Cattle (Bos taurus) and Sarcocystis sinensis from Water Buffaloes (Bubalus bubalis)","volume":"115","author":"Gjerde","year":"2016","journal-title":"Parasitol. Res."},{"key":"ref_69","doi-asserted-by":"crossref","first-page":"252","DOI":"10.1016\/j.ijppaw.2019.10.002","article-title":"Morphological and molecular characteristics of seven Sarcocystis species from sika deer (Cervus nippon centralis) in Japan, including three new species","volume":"10","author":"Abe","year":"2019","journal-title":"Int. J. Parasitol. Parasites Wildl."},{"key":"ref_70","doi-asserted-by":"crossref","first-page":"2541","DOI":"10.1007\/s00436-014-3904-y","article-title":"Assessment of gastrointestinal parasites in wild chimpanzees (Pan troglodytes troglodytes) in southeast Cameroon","volume":"113","author":"Drakulovski","year":"2014","journal-title":"Parasitol. Res."},{"key":"ref_71","doi-asserted-by":"crossref","first-page":"1113","DOI":"10.1016\/j.ijpara.2011.06.010","article-title":"Diversity and host specificity of Blastocystis in syntopic primates on Rubondo Island, Tanzania","volume":"41","author":"Kostka","year":"2011","journal-title":"Int. J. Parasitol."},{"key":"ref_72","doi-asserted-by":"crossref","unstructured":"Muadica, A.S., K\u00f6ster, P.C., Dashti, A., Bailo, B., Hern\u00e1ndez-de-Mingo, M., Reh, L., Balasegaram, S., Verlander, N.Q., Ruiz Ch\u00e9rcoles, E., and Carmena, D. (2020). Molecular diversity of Giardia duodenalis, Cryptosporidium spp. and Blastocystis sp. in asymptomatic school children in Legan\u00e9s, Madrid (Spain). Microorganisms, 8.","DOI":"10.3390\/microorganisms8040466"},{"key":"ref_73","doi-asserted-by":"crossref","unstructured":"Muadica, A.S., K\u00f6ster, P.C., Dashti, A., Bailo, B., Hern\u00e1ndez-de-Mingo, M., Balasegaram, S., and Carmena, D. (2021). Molecular diversity of Giardia duodenalis, Cryptosporidium spp., and Blastocystis sp. in symptomatic and asymptomatic schoolchildren in Zamb\u00e9zia Province (Mozambique). Pathogens, 10.","DOI":"10.3390\/pathogens10030255"},{"key":"ref_74","doi-asserted-by":"crossref","first-page":"81","DOI":"10.14411\/fp.2011.008","article-title":"Diversity of microsporidia (Fungi: Microsporidia) among captive great apes in European zoos and African sanctuaries: Evidence for zoonotic transmission?","volume":"58","author":"Sak","year":"2011","journal-title":"Folia Parasitol."},{"key":"ref_75","doi-asserted-by":"crossref","first-page":"104807","DOI":"10.1016\/j.meegid.2021.104807","article-title":"Diversity of parasites in two captive chimpanzee populations in souther Gabon","volume":"91","author":"Boudenga","year":"2021","journal-title":"Infect. Genet. Evol."},{"key":"ref_76","doi-asserted-by":"crossref","first-page":"43","DOI":"10.1007\/s10764-008-9329-7","article-title":"Variation over time in parasite prevalence among free-ranging chimpanzees at Gombe National Park, Tanzania","volume":"30","author":"Bakuza","year":"2009","journal-title":"Int. J. Primatol."},{"key":"ref_77","doi-asserted-by":"crossref","first-page":"1139","DOI":"10.1645\/GE-2433.1","article-title":"Discrepancies in the occurrence of Balantidium coli between wild and captive African great apes","volume":"96","year":"2010","journal-title":"J. Parasitol."},{"key":"ref_78","doi-asserted-by":"crossref","first-page":"42","DOI":"10.1002\/ajpa.21191","article-title":"A survey of entodiniomorphid ciliates in chimpanzees and bonobos","volume":"142","year":"2010","journal-title":"Am. J. Phys. Anthropol."},{"key":"ref_79","doi-asserted-by":"crossref","first-page":"555","DOI":"10.1023\/A:1014969617036","article-title":"Intestinal parasites in gorillas, chimpanzees, and humans at Mondika Research Site, Dzanga-Ndoki National Park, Central African Republic","volume":"23","author":"Lilly","year":"2002","journal-title":"Int. J. Primatol."},{"key":"ref_80","doi-asserted-by":"crossref","first-page":"264","DOI":"10.1111\/j.1755-263X.2012.00288.x","article-title":"Impact of human activities on chimpanzee ground use and parasitism (Pan troglodytes)","volume":"6","author":"Zommers","year":"2013","journal-title":"Conserv. Lett."},{"key":"ref_81","doi-asserted-by":"crossref","first-page":"69","DOI":"10.1638\/2010-0100.1","article-title":"Survival and morphological changes of entodiniomorphid ciliate Troglodytella abrassarti in chimpanzee feces","volume":"42","year":"2011","journal-title":"Zoo Wild Med."},{"key":"ref_82","first-page":"634","article-title":"Detection of Plasmodium spp. in human feces","volume":"18","year":"2012","journal-title":"Emerg. Infect. Dis."},{"key":"ref_83","doi-asserted-by":"crossref","first-page":"570","DOI":"10.1590\/0074-02760160222","article-title":"Detection of Plasmodium in faeces of the New World primate Alouatta clamitans","volume":"111","author":"Assis","year":"2016","journal-title":"Mem. Inst. Oswaldo Cruz"},{"key":"ref_84","doi-asserted-by":"crossref","first-page":"109","DOI":"10.1186\/s12936-019-2748-4","article-title":"Non-invasive surveillance of Plasmodium infection by real-time PCR analysis of ethanol preserved faeces from Ugandan school children with intestinal schistosomiasis","volume":"18","author":"Power","year":"2019","journal-title":"Malar. J."},{"key":"ref_85","doi-asserted-by":"crossref","first-page":"68","DOI":"10.1186\/1475-2875-13-68","article-title":"First case of a naturally acquired human infection with Plasmodium cynomolgi","volume":"13","author":"Ta","year":"2014","journal-title":"Malar. J."},{"key":"ref_86","first-page":"219","article-title":"First case of detection of Plasmodium knowlesi in Spain by Real Time PCR in a traveller from Southeast Asia","volume":"27","author":"Ta","year":"2010","journal-title":"Malar. J."},{"key":"ref_87","unstructured":"Coatney, G.R., Collins, W.E., Warren, M., and Contacos, P.G. (2003). CD-ROM. The Primate Malarias, CDC. Original Book Published, 1971; Division of Parasitic Disease, Producers; Version 1.0."},{"key":"ref_88","doi-asserted-by":"crossref","unstructured":"Hayakawa, T., Arisue, N., Udono, T., Hirai, H., Sattabongkot, J., Toyama, T., Tsuboi, T., Horii, T., and Tanabe, K. (2009). Identification of Plasmodium malariae, a human malaria parasite, in imported chimpanzees. PLoS ONE, 4.","DOI":"10.1371\/journal.pone.0007412"},{"key":"ref_89","doi-asserted-by":"crossref","first-page":"5329","DOI":"10.1073\/pnas.1603008113","article-title":"Ape malaria transmission and potential for ape-to-human transfers in Africa","volume":"113","author":"Makanga","year":"2016","journal-title":"Proc. Natl. Acad. Sci. USA"},{"key":"ref_90","doi-asserted-by":"crossref","unstructured":"Simarro, P.P., Diarra, A., Postigo, J.A.R., Franco, J.R., and Jannin, J.G. (2011). The human African trypanosomiasis control and surveillance programme of the World Health Organization 2000\u20132009: The way forward. PLoS Negl. Trop. Dis., 5.","DOI":"10.1371\/journal.pntd.0001007"},{"key":"ref_91","doi-asserted-by":"crossref","first-page":"535","DOI":"10.1111\/j.1365-3156.2009.02271.x","article-title":"Trypanosoma brucei gambiense in domestic livestock of Kogo and Mbini foci (Equatorial Guinea)","volume":"14","author":"Berzosa","year":"2009","journal-title":"Trop. Med. Int. Health"},{"key":"ref_92","doi-asserted-by":"crossref","first-page":"781","DOI":"10.1016\/0035-9203(67)90035-1","article-title":"Cyclically transmitted infections of Trypanosoma brucei, T. rhodesiense and T. gambiense in chimpanzees","volume":"61","author":"Godfrey","year":"1967","journal-title":"Trans. R. Soc. Trop. Med. Hyg."},{"key":"ref_93","doi-asserted-by":"crossref","first-page":"322","DOI":"10.1016\/j.ijppaw.2018.09.003","article-title":"An unexpected diversity of trypanosomatids in fecal samples of great apes","volume":"7","author":"Mbohli","year":"2018","journal-title":"Int. J. Parasitol. Parasites Wildl."},{"key":"ref_94","first-page":"93","article-title":"An overview of the management of Mansonellosis","volume":"12","author":"Luz","year":"2021","journal-title":"Res. Rep. Trop. Med."},{"key":"ref_95","doi-asserted-by":"crossref","unstructured":"McLennan, M.R., Hasegawa, H., Bardi, M., and Huffman, M.A. (2017). Gastrointestinal parasite infections and self-medication in wild chimpanzees surviving in degraded forest fragments within an agricultural landscape mosaic in Uganda. PLoS ONE, 12.","DOI":"10.1371\/journal.pone.0180431"},{"key":"ref_96","doi-asserted-by":"crossref","first-page":"920","DOI":"10.1007\/s10764-010-9439-x","article-title":"Gastrointestinal parasites of indigenous and introduced primate species of Rubondo Island National Park, Tanzania","volume":"31","author":"Huffman","year":"2010","journal-title":"Int. J. Primatol."},{"key":"ref_97","doi-asserted-by":"crossref","first-page":"463","DOI":"10.1007\/s10764-014-9753-9","article-title":"Gastrointestinal parasites of savanna chimpanzees (Pan troglodytes schweinfurthii) in Ugalla, Tanzania","volume":"35","author":"Piel","year":"2014","journal-title":"Int. J. Primatol."},{"key":"ref_98","doi-asserted-by":"crossref","first-page":"173","DOI":"10.1080\/00034983.2000.11813526","article-title":"Intestinal parasites of the chimpanzee Pan troglodytes in Kibale Forest, Uganda","volume":"94","author":"Ashford","year":"2000","journal-title":"Ann. Trop. Med. Parasitol."},{"key":"ref_99","doi-asserted-by":"crossref","unstructured":"Masi, S., Chauffour, S., Bain, O., Todd, A., Guillot, J., and Krief, S. (2012). Seasonal effects on great ape health: A case study of wild chimpanzees and Western gorillas. PLoS ONE, 7.","DOI":"10.1371\/journal.pone.0049805"},{"key":"ref_100","first-page":"569","article-title":"TREECON for Windows: A software package for the construction and drawing of evolutionary trees for the Microsoft Windows environment","volume":"10","year":"1994","journal-title":"Comput. Appl. BioSci."},{"key":"ref_101","doi-asserted-by":"crossref","first-page":"4673","DOI":"10.1093\/nar\/22.22.4673","article-title":"CLUSTAL W: Improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice","volume":"22","author":"Thompson","year":"1994","journal-title":"Nucleic Acids Res."}],"container-title":["Animals"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/www.mdpi.com\/2076-2615\/11\/11\/3291\/pdf","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2025,10,11]],"date-time":"2025-10-11T07:31:48Z","timestamp":1760167908000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.mdpi.com\/2076-2615\/11\/11\/3291"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2021,11,17]]},"references-count":101,"journal-issue":{"issue":"11","published-online":{"date-parts":[[2021,11]]}},"alternative-id":["ani11113291"],"URL":"https:\/\/doi.org\/10.3390\/ani11113291","relation":{},"ISSN":["2076-2615"],"issn-type":[{"value":"2076-2615","type":"electronic"}],"subject":[],"published":{"date-parts":[[2021,11,17]]}}}