Skip to main content Accessibility help

Extensive diversity of intestinal trichomonads of non-human primates



Despite the fact that the non-human primates are our closest relatives and represent a species-rich mammalian group, little is known about their intestinal protistan parasites/commensals. Particularly, the intestinal trichomonads represent a neglected part of the fauna of the primate digestive system. We have established 30 trichomonad strains isolated from feces of 11 primate species kept in 3 Czech zoos and performed an analysis of their SSU rDNA and ITS1-5·8S rDNA-ITS2. Our results showed that intestinal trichomonads are rather common among non-human primates. Molecular phylogenetic analysis showed that the strains are unexpectedly diversified, belonging to 8 or 9 distinct species. Interestingly, the vast majority of the strains from non-human primates belonged to the genus Tetratrichomonas while no member of this genus has been found in the human intestine so far. In addition, hominoid and non-hominoid primates differed in their intestinal trichomonads. Our results suggest that captive primates possibly may be infected by intestinal trichomonads of other vertebrates such as pigs, cattle, birds, tortoises and lizards.


Corresponding author

*Corresponding author: Department of Zoology, Faculty of Science, Charles University in Prague, Viničná 7, 128 44, Prague, Czech Republic. Tel: +420 221951842. Fax: +420 221951841. E-mail:


Hide All
Abraham, R. (1961). The morphology of Monocercomonas lori n. sp., from the Indian slender loris. Archiv für Protistenkunde 105, 445449.
Abraham, R. (1962). A new species of Trichomonas (Protozoa: Mastigophora) parasitic in slender loris. Zeitschrift für Parasitenkunde 21, 202206.
Adl, S. M., Leander, B. S., Simpson, A. G. B., Archibald, J. M., Anderson, O. R., Bass, D., Bowser, S. S., Brugerolle, G., Farmer, M. A., Karpov, S., Kolisko, M., Lane, C. E., Lodge, D. J., Mann, D. G., Meisterfeld, R., Mendoza, L., Moestrup, Ø., Mozley-Standridge, S. E., Smirnov, A. V. and Spiegel, F. (2007). Diversity, nomenclature, and taxonomy of protists. Systematic Biology 56, 684689. doi: 10.1080/10635150701494127.
Carmody, R. N. and Wrangham, R. W. (2009). The energetic significance of cooking. Journal of Human Evolution 57, 379391. doi: 10.1016/j.jhevol.2009.02.011.
Carmona, M. C., Bermudez, O. G., Gutierrez-Espeleta, G. A., Porras, R. S. and Ortiz, B. R. (2005). Intestinal parasites in howler monkeys Alouatta palliata (Primates: Cebidae) of Costa Rica. Revista de Biologia Tropical 53, 437445.
Cavalier-Smith, T. (2002). The phagotrophic origin of eukaryotes and phylogenetic classification of Protozoa. International Journal of Systematic and Evolutionary Microbiology 52, 297354. doi: 10.1099/ijs.0.02058-0.
Cepicka, I., Hampl, V. and Kulda, J. (2010). Critical taxonomic revision of parabasalids with description of one new genus and three new species. Protist 161, 400433. doi: 10.1016/j.protis.2009.11.005.
Cepicka, I., Hampl, V., Kulda, J. and Flegr, J. (2006). New evolutionary lineages, unexpected diversity, and host specificity in the parabasalid genus Tetratrichomonas. Molecular Phylogenetics and Evolution 39, 542551. doi:10.1016/j.ympev.2006.01.005.
Cepicka, I., Kutišová, K., Tachezy, J., Kulda, J. and Flegr, J. (2005). Cryptic species within the Tetratrichomonas gallinarum species complex revealed by molecular polymorphism. Veterinary Parasitology 128, 1121. doi:10.1016/j.vetpar.2004.11.003.
Cleveland, L. R. (1928). Tritrichomonas fecalis nov. sp. of man; its ability to grow and multiply indefinitely in faeces with tap water and in frogs and tadpoles. American Journal of Hygiene 8, 232255.
Culbertson, D. E., Pindak, F. F., Gardner, W. A. and Honigberg, B. M. (1986). Tritrichomonas mobilensis n. sp. (Zoomastigophorea: Trichomonadida) from the Bolivian squirrel monkey Saimiri boliviensis boliviensis. Journal of Protozoology 33, 301304.
Cutillas, C., Callejon, R., de Rojas, M., Tewes, B., Ubeda, J. M., Ariza, C. and Guevara, D. C. (2009). Trichuris suis and Trichuris trichiura are different nematode species. Acta Tropica 111, 299307. doi:10.1016/j.actatropica.2009.05.011.
Deschiens, R. (1927). Sur les protozoaires intestinaux des singes. Bulletin of the Exotic Pathology Society 20, 1923.
Dobell, C. and Leidlaw, P. P. (1926). On the cultivation of Entamoeba histolytica and some other entozoic amoebae. Parasitology 18, 283318.
Duboucher, C., Caby, S., Dufernez, F., Chabé, M., Gantois, N., Delgado-Viscogliosi, P., Billy, C., Barré, E., Torabi, E., Capron, M., Pierce, R. J., Dei-Cas, E. and Viscolgiosi, E. (2006). Molecular identification of Tritrichomonas foetus-like organisms as coinfecting agents of human Pneumocystis pneumonia. Journal of Clinical Microbiology 44, 11651168. doi:10.1128/JCM.44.3.1165-1168.2006.
Dufernez, F., Walker, R. L., Noël, C., Caby, S., Mantini, C., Delgado-Viscogliosi, P., Ohkuma, M., Kudo, T., Capron, M., Pierce, R. J., Villanueva, M. R. and Viscogliosi, E. (2007). Morphological and molecular identification of non-Tritrichomonas foetus trichomonad protozoa from the bovine preputial cavity. Journal of Eukaryotic Microbiology 54, 161168. doi: 10.1111/j.1550-7408.2007.00247.x.
Flick, E. W. (1954). Experimental analysis of some factors influencing variation in the flagellar number of Trichomonas hominis from man and other primates and their relationship to nomenclature. Experimental Parasitology 3, 105121.
Greiner, E. C. and McIntosh, A. (2009). Collection methods and diagnostic procedures for primate parasitology. In Primate Parasite Ecology (ed. Huffman, M. A. and Chapman, C.), pp. 327. Cambridge University Press, Cambridge, UK.
Guindon, S. and Gascuel, O. (2003). A simple, fast, and accurate algorithm to estimate large phylogenies by maximum likelihood. Systematic Biology 52, 696704. doi: 10.1080/10635150390235520.
Hall, T. A. (1999). BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucleic Acids Symposium Series 41, 9598.
Hampl, V., Cepicka, I., Flegr, J., Tachezy, J. and Kulda, J. (2007). Morphological diversity of the monocercomonadid genera Monocercomonas, Hexamastix, and Honigbergiella gen. nov. Protist 158, 365383. doi: 10.1016/j.protis.2007.02.003.
Hasegawa, H., Sato, H., Fujita, S., Nguema, P. P. M., Nobusue, K., Miyagi, K., Kooriyama, T., Takenoshita, Y., Noda, S., Sato, A, Morimoto, A., Ikeda, Y. and Nishida, T. (2010). Molecular identification of the causative agent of human strongyloidiasis acquired in Tanzania: Dispersal and diversity of Strongyloides spp. and their hosts. Parasitology International 59, 407413. doi: 10.1016/j.parint.2010.05.007.
Hegner, R. and Ratcliffe, H. (1927). Trichomonads from the vagina of the monkey, from the mouth of the cat and man, and from the intestine of the monkey, opossum and prairie-dog. Journal of Parasitology 14, 2735.
Honigberg, B. M. (1978 a). Trichomonads of veterinary importance. In Parasitic Protozoa II (ed. Kreier, J. P.), pp. 163273. Academic Press, New York, USA.
Honigberg, B. M. (1978 b). Trichomonads of importance in human medicine. In Parasitic Protozoa II (ed. Kreier, J. P.), pp. 275454. Academic Press, New York, USA.
Huelsenbeck, J. P. and Ronquist, F. (2001). MRBAYES: Bayesian inference of phylogenetic trees. Bioinformatics 17, 754755. doi: 10.1093/bioinformatics/17.8.754.
Johnston, A. R., Gillespie, T. R., Rwego, I. B., McLachlan, T. L. T., Kent, A. D. and Goldberg, T. L. (2010). Molecular epidemiology of cross-Species Giardia duodenalis transmission in Western Uganda. PLOS Neglected Tropical Diseases 4: e683. doi: 10.1371/journal.pntd.0000683.
Katoh, K., Misawa, K., Kuma, K. and Miyata, T. (2002). MAFFT: a novel method for rapid multiple sequence alignment based on fast Fourier transform. Nucleic Acids Research 30, 30593066. doi: 10.1093/nar/gkf436.
Krief, S., Vermeulen, B., Lafosse, S., Kasenene, J. M., Nieguitsila, A., Berthelemy, M., L'Hostis, M., Bain, O. and Guillot, J. (2010). Nodular worm infection in wild chimpanzees in Western Uganda: A risk for human health? PLOS Neglected Tropical Diseases 4, e630. doi: 10.1371/journal.pntd.0000630.
Kutisova, K., Kulda, J., Cepicka, I., Flegr, J., Koudela, B., Teras, J. and Tachezy, J. (2005). Tetratrichomonads from the oral cavity and respiratory tract of humans. Parasitology 131, 309319. doi: 10.1017/S0031182005008000.
Lankester, F., Kiyang, J. A., Bailey, W., Unwin, S. (2010). Dientamoeba fragilis: initial evidence of pathogenicity in the western lowland gorilla (Gorilla gorilla gorilla). Journal of Zoo and Wildlife Medicine 41, 350352. doi: 10.1638/2009-0190.1.
Levecke, B., Geldhof, P., Claerebout, E., Dorny, P., Vercammen, F., Cacciò, S. M., Vercuysse, J. and Geurden, T. (2009). Molecular characterisation of Giardia duodenalis in captive non-human primates reveals mixed assemblage A and B infections and novel polymorphisms. International Journal for Parasitology 39, 15951601. doi: 10.1016/j.ijpara.2009.05.013
Levy, M. G., Gookin, J. L., Poore, M., Birkenheuer, A. J., Dykstra, M. J. and Litaker, R. W. (2003). Tritrichomonas foetus and not Pentatrichomonas hominis is the etiological agent of the feline trichomonal diarrhea. Journal of Parasitology 89, 99104.
Lilly, A. A., Mehlman, P. T. and Doran, D. (2002). Intestinal parasites in gorillas, chimpanzees, and human at Mondika research site, Dzanga-Ndoki national park, Central African Republic. International Journal of Primatology 23, 555573.
Mantini, C., Souppart, L., Noël, C., Duong, T. H., Mornet, M., Carroger, G., Dupont, P., Masseret, E., Goustille, J., Capron, M., Duboucher, C., Dei-Cas, E. and Viscogliosi, E. (2009). Molecular characterization of a new Tetratrichomonas species in a patient with empyema. Journal of Clinical Microbiology 47, 22362339. doi: 10.1128/JCM.00353-09.
McDougald, L. R. and Reid, W. M. (1978). Histomonas meleagridis and relatives. In Parasitic Protozoa II (ed. Kreier, J. P.), pp. 139161. Academic Press, New York, USA.
Myers, B. J. and Kuntz, R. E. (1972). A checklist of parasites and commensals reported for the chimpanzee (Pan). Primates 13, 433471.
Parkar, U., Traub, R. J., Vitali, S., Vitali, S., Elliot, A., Levecke, B., Robertson, I., Geurden, T., Steele, J., Drake, B. and Thompson, R. C. A. (2010). Molecular characterization of Blastocystis isolates from zoo animals and their animal-keepers. Veterinary Parasitology 169, 817. doi: 10.1016/j.vetpar.2009.12.032.
Pindak, F. F. and de Pindak, M. M. (1998). Diagnostic characteristics of owl monkey (Aotus trivirgatus) intestinal trichomonads. Acta Protozoologica 37, 159172.
Pomajbíková, K., Petrželková, K. J., Profousová, I., Petrašová, J., Kišidayová, S., Varadyová, Z. and Modrý, D. (2010). A survey of entodiniomorphid ciliates in chimpanzees and bonobos. American Journal of Physical Anthropology 42, 4248. DOI: 10.1002/ajpa.21191.
Posada, D. and Crandall, K. A. (1998). Modeltest: testing the model of DNA substitution. Bioinformatics 14, 817818.
Prugnolle, F., Duran, P., Neel, C., Ollomo, B., Ayala, F. J., Arnathau, C., Etienne, L., Mpondi-Ngole, E., Nkoghe, D., Leroy, E., Delaporte, E., Peeters, M. and Renaud, F. (2009). African great apes are natural hosts of multiple related malaria species, including Plasmodium falciparum. Proceedings of the National Academy of Sciences, USA 107, 14581463. doi: 10.1073/pnas.0914440107.
Ratcliffe, H. L. (1928). The numbers of trichomonads in rats on diets of different protein content in relation to the pH and bacteria in the cecum. Americal Journal of Epidemiology 8, 910934.
Reardon, L. V. and Rininger, B. F. (1968). A survey of parasites in laboratory primates. Laboratory Animal Care 18, 577580.
Stahl, A. B, Dunbar, R. I. M., Homewood, K., Ikawa-Smith, F., Kortlandt, A., McGrew, W. C., Milton, K., Paterson, D. J., Poirier, F. E., Sugardjito, J., Tanner, N. M. and Wrangham, R. W. (1984). Hominid dietary selection before fire [and Comments and Reply]. Current Anthropology 25, 151168.
Stark, D., Phillips, O., Peckett, D., Munro, U., Marriott, D., Harkness, J. and Ellis, J. (2008). Gorillas are a host for Dientamoeba fragilis: an update on the life cycle and host distribution. Veterinary Parasitology 151, 2126. doi: 10.1016/j.vetpar.2007.10.002.
Stensvold, C. R., Alfellani, M. A., Nørskov-Lauritsen, S., Prip, K., Victory, E. L., Maddox, C., Nielsen, H. V. and Clark, C. G. (2009). Subtype distribution of Blastocystis isolates from synanthropic and zoo animals and identification of a new subtype. International Journal for Parasitology 39, 473479. doi: 10.1016/j.ijpara.2008.07.006.
Suzuki, J., Kobayashi, S., Murata, R., Tajima, H., Hashizaki, F., Yanagawa, Y. and Takeuchi, T. (2008). A survey of amoebic infections and differentiation of an Entamoeba histolytica-like variant (JSK2004) in nonhuman primates by a multiplex polymerase chain reaction. Journal of Zoo and Wildlife Medicine 39, 370379. doi: 10.1638/2007-0171.1.
Swofford, D. L. (2002). PAUP*. Phylogenetic Analysis Using Parsimony (* and Other Methods). Version 4.0b10. Sinauer Associates, Sunderland, MA, USA.
Tachezy, J., Tachezy, R., Hampl, V., Šedinová, M., Vaňáčová, Š., Vrlík, M., Van Ranst, M., Flegr, J. and Kulda, J. (2002). Cattle pathogen Tritrichomonas foetus (Riedmüller, 1928) and pig commensal Tritrichomonas suis (Gruby & Delafond, 1843) belong to the same species. Journal of Eukaryotic Microbiology 49, 154163. doi: 10.1111/j.1550-7408.2002.tb00360.x.
Tachibana, H., Yanagi, T., Akatsuka, A., Kobayash, S., Kanbara, H. and Tsutsumi, V. (2009). Isolation and characterization of a potentially virulent species Entamoeba nuttalli from captive Japanese macaques. Parasitology 136, 11691177. doi: 10.1017/S0031182009990576.
Tokiwa, T., Modrý, D., Ito, A., Pomajbíková, K., Petrželková, K. J. and Imai, S. (2010). A new entodiniomorphid ciliate, Troglocorys cava n. g., n. sp., from the wild Eastern chimpanzee. Journal of Eukaryotic Microbiology 57, 115120. DOI: 10.1111/j.1550-7408.2009.00456.x.
Wenrich, D. H. (1944 a). Morphology of the intestinal trichomonad flagellates in man and of similar forms in monkeys, cats, dogs and rats. Journal of Morphology 74, 189211.
Wenrich, D. H. (1944 b). Comparative morphology of the trichomonad flagellates of man. American Journal of Tropical Medicine and Hygiene 24, 3951.
Wenrich, D. H. and Nie, D. (1949). The morphology of Trichomonas wenyoni (Protozoa, Mastigophora). Journal of Morphology 85, 519531.
Wrangham, R. and Conklin-Brittain, N. L. (2003). ‘Cooking as a biological trait.’. Comparative Biochemistry and Physiology Part A 136, 3546. doi: 10.1016/S1095-6433(03)00020-5.
Yubuki., N., Céza, V., Cepicka, I., Yabuki, A., Inagaki, Y., Nakayama, T., Ionuye, I. and leander, B. S. (2010). Cryptic diversity of free-living parabasalids, Pseudotrichomonas keilini and Lacusteria cypriaca n. gen., n. sp., as inferred from small subunit rDNA sequences. Journal of Eukaryotic Microbiology 57, 554561. doi: 10.1111/j.1550-7408.2010.00509.x.


Extensive diversity of intestinal trichomonads of non-human primates



Full text views

Total number of HTML views: 0
Total number of PDF views: 0 *
Loading metrics...

Abstract views

Total abstract views: 0 *
Loading metrics...

* Views captured on Cambridge Core between <date>. This data will be updated every 24 hours.

Usage data cannot currently be displayed