Skip to main content

Host specificity and basic ecology of Mammomonogamus (Nematoda, Syngamidae) from lowland gorillas and forest elephants in Central African Republic


Syngamid strongylids of the genus Mammomonogamus undoubtedly belong among the least known nematodes with apparent zoonotic potential and the real diversity of the genus remains hard to evaluate without extensive molecular data. Eggs of Mammomonogamus sp. are frequently found in feces of African forest elephants (Loxodonta cyclotis) and western lowland gorillas (Gorilla gorilla gorilla) in Dzanga-Sangha Protected Areas. Using sedimentation-based coproscopic techniques, we found the eggs of Mammomonogamus in 19·7% elephant and 54·1% gorilla fecal samples with 8–55 and 1–24 eggs per gram of fecal sediment for elephants and gorillas, respectively. We used a combination of light microscopy, scanning electron microscopy and analysis of cytochrome c oxidase subunit I (cox1) and a partial sequence of 18S rDNA isolated from single eggs to test the hypothesis of possible Mammomonogamus conspecificity in gorillas and elephants. Whereas 18S rDNA sequences were identical in both gorillas and elephants, we distinguished seven different haplotypes within the cox1. Two haplotypes were found in both gorillas and elephants suggesting sharing of Mammomonogamus. Assignment of the parasite to M. loxodontis is proposed. Provided sequences represent the first genomic data on Mammomonogamus spp.

Corresponding author
*Corresponding author: Department of Pathology and Parasitology, University of Veterinary and Pharmaceutical Sciences Brno, Palackého tř. 1946/1, 612 42 Brno, Czech Republic. E-mail:
Hide All
Baruš, V. (1966). The longevity of the parasitic stages and the dynamics of eggs production of the nematode Syngamus trachea (Montagu, 1811) in chicken and turkeys. Folia Parasitologica 13, 274277.
Baruš, V., Tenora, F. and Wiger, R. (1979). Scanning electron microscopy of eggs of European species of the genus Syphacia Seurat, 1916 (Nematoda). Folia Parasitologica 26, 2126.
Blom, A., Almaši, A., Heitkönig, I. M. A., Kpanou, J.-B. and Prins, H. H. T. (2001). A survey of the apes in the Dzanga-Ndoki National Park, Central African Republic: a comparison between the census and survey methods of estimating the gorilla (Gorilla gorilla gorilla) and chimpanzee (Pan troglodytes) nest group density. African Journal of Ecology 39, 98105.
Blom, A., Cipolletta, C., Brunsting, A. M. H. and Prins, H. H. T. (2004). Behavioral responses of gorillas to habituation in the Dzanga-Ndoki National Park, Central African Republic. International Journal of Primatology 25, 179196.
Buckley, J. J. C. (1934). On Syngamus ierei sp. nov. from domestic cats, with some observations on its life-cycle. Journal of Helminthology 9, 8998.
Bush, A. O., Lafferty, K. D., Lotz, J. M. and Shostak, A. W. (1997). Parasitology meets ecology on its own terms: Margolis et al. revisited. Journal of Parasitology 83, 575583.
Cameron, W. M. (1931). On some lungworms of the Malay tiger. Journal of Helminthology 9, 147152.
Castaño, J. C., Núñez, F. Á., González, M. M., Téllez, G. and Giraldo, M. I. (2006). Reporte del primer caso humano de infección parasitaria por Mammomonogamus laryngeus en Colombia. Biomédica 26, 337341.
Chilton, N. B., Huby-Chilton, F., Gasser, R. B. and Beveridge, I. (2006). The evolutionary origins of nematodes within the order Strongylida are related to predilection sites within hosts. Molecular Phylogenetics and Evolution 40, 118128.
Combes, C. (1991). Evolution of parasite life cycles. In Parasite–host Associations: Coexistence or Conflict? (ed. Toft, C. A., Aeschlimann, A. and Bolis, L.), pp. 6282. Oxford University Press, Oxford, UK.
Condy, J. B. (1974). Observations on internal parasites in Rhodesian elephant, Loxodonta africana . Proceedings and Transactions of the Rhodesian Scientific Association 55, 6799.
da Costa, J. C., Delgado, M. L., Vieira, P., Afonso, A., Conde, B. and Cross, J. H. (2005). Syngamoniasis in tourist. Emerging Infectious Diseases 11, 19761977.
Diesing, C. M. (1857). Sechzehn Arten von Nematoideen (Mit IV Tafeln). Bande der Denkschriften der mathematisch-naturwissenschaftlichen Classe der Kaiserlichen Akademie der Wissenschaften 13, 626.
Faust, E. C. and Tang, C.-C. (1934). A new species of Syngamus (S. auris) from the middle ear of the cat in Foochow, China. Parasitology 26, 455459.
Foitová, I., Koubková, B., Baruš, V. and Nurcahyo, W. (2008). Presence and species identification of the gapeworm Mammomonogamus laryngeus (Railliet, 1899) (Syngamidae: Nematoda) in a semi-wild population of Sumatran orangutan (Pongo abelii) in Indonesia. Research in Veterinary Science 84, 232236.
Folmer, O., Black, M., Hoeh, W., Lutz, R. and Vrijenhoek, R. (1994). DNA primers for amplification of mitochondrial cytochrome c oxidase subunit I from diverse metazoan invertebrates. Molecular Marine Biology and Biotechnology 3, 294299.
Freeman, A. S., Kinsella, J. M., Cipoletta, C., Deem, S. L. and Karesh, W. B. (2004). Endoparasites of western lowland gorillas (Gorilla gorilla gorilla) at Bai Hokou, Central African Republic. Journal of Wildlife Diseases 40, 775781.
Gedoelst, L. (1924). Un syngame parasite de l'hippopotame. Annales de Parasitologie 2, 307311.
Ghai, R. R., Fugère, V., Chapman, C. A., Goldberg, T. L. and Davies, T. J. (2015). Sickness behaviour associated with non-lethal infections in wild primates. Proceedings of the Royal Society of London B: Biological Sciences 282, 20151436.
Goldsmith, M. (1996). Ecological influences on the ranging and grouping behavior of western lowland gorillas at Bai Hokou, Central African Republic. Ph.D. thesis. State University of New York, Stony Brook, New York.
Graber, M., Euzeby, J., Gevrey, J., Troncy, P. M. and Thal, J. (1971). La mammomonogamose des ruminants domestiques et sauvages. Revue d’Élevage et de Médecine Vétérinaire des Pays Tropicaux 24, 525541.
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.
Hasegawa, H., Modrý, D., Kitagawa, M., Shutt, K. A., Todd, A., Kalousová, B., Profousová, I. and Petrželková, K. J. (2014). Humans and great apes cohabiting the forest ecosystem in Central African Republic harbour the same hookworms. PLoS Neglected Tropical Diseases 8, e2715.
Hastings, W. K. (1970). Monte Carlo sampling methods using Markov chanis and their applications. Biometrika 57, 97109.
Huffman, M. A., Gotoh, S., Turner, L. A., Hamai, M. and Yoshida, K. (1997). Seasonal trends in intestinal nematode infection and medicinal plant use among chimpanzees in the Mahale Mountains, Tanzania. Primates 38, 111125.
Jirků, M., Jirků, M., Oborník, M., Lukeš, J. and Modrý, D. (2009). Goussia Labbé, 1896 (Apicomplexa, Eimeriorina) in Amphibia: diversity, biology, molecular phylogeny and comments on the status of the genus. Protist 160, 123136.
Jirků-Pomajbíková, K. and Hůzová, Z. (2015). Coproscopic techniques. In Parasites of African Great Apes Atlas of Coproscopic Diagnostics (ed. Modrý, D., Petrželková, K. J., Kalousová, B. and Hasegawa, H.), pp. 1424. HPI-lab, Department of Pathology and Parasitology, University of Veterinary and Pharmaceutical Sciences Brno, Brno, Czech Republic.
Kalousová, B. (2013). Gastrointestinal parasites of wild western lowland gorillas (Gorilla gorilla gorilla) in Dzanga Sector of Dzanga-Ndoki National Park, Central African Republic. Master thesis. Masaryk University, Brno, Czech Republic, 109 pp.
Kalousová, B., Hasegawa, H., Petrželková, K. J., Sakamaki, T., Kooriyma, T. and Modrý, D. (2016). Adult hookworms (Necator spp.) collected from researchers working with wild western lowland gorillas. Parasites & Vectors 9, 75.
Kinsella, J. M., Deem, S. L., Blake, S. and Freeman, A. S. (2004). Endoparasites of African forest elephant (Loxodonta africana cyclotis) from the Republic of Congo and Central African Republic. Comparative Parasitology 71, 104110.
Larkin, M. A., Blackshields, G., Brown, N. P., Chenna, R., McGettigan, P. A., McWilliam, H., Valentin, F., Wallace, I. M., Wilm, A., Lopez, R., Thompson, J. D., Gibson, T. J. and Higgins, D. G. (2007). Clustal W and ClustalX version 2.0. Bioinformatics (Oxford, England) 23, 29472948.
Lehnhardt, J. (2006). Husbandry. In Biology, medicine and surgery of elephants (ed. Fowler, M. E. and Mikota, S. K.), pp. 4556. Blackwell Publishing, Ames, Iowa, USA.
Lilly, A. A., Mehlman, P. T. and Doran, D. (2002). Intestinal parasites in gorillas, chimpanzees and humans at Mondika Research Site, Dzanga-Ndoki National Park, Central African Republic. International Journal of Primatology 23, 555573.
Limawongpranee, S., Samanthai, S. and Yoolek, A. (2004). Human Mammomonogamus laryngeus infection (Syngamosis): the second case report in Thailand. Siriraj Hospital Gazette 56, 8286.
Magdeleine, J., Magnaval, J.-F., Brossard, B., Michel, M. and Turiaf, J. (1974). La syngamose humaine à la Martinique. Médecine d'Afrique Noire 21, 651655.
Magi, M., Guardone, L., Prati, M. C., Torracca, B. and Macchioni, F. (2012). First report of Eucoleus boehmi (syn. Capillaria boehmi) in dogs in north-western Italy, with scanning electron microscopy of the eggs. Parasite 19, 433435.
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, e49805.
Miranda, R. R., Tennessen, J. A., Blouin, M. S. and Rabelo, É. M. (2008). Mitochondrial DNA variation of the dog hookworm Ancylostoma caninum in Brazilian populations. Veterinary Parasitology 151, 6167.
Mönnig, H. O. (1932). Syngamus indicus. 18th Report of Director of Veterinary Services and Animal Industry, PLACE, Union of South Africa, p. 173.
Muehlenbein, M. P. (2005). Parasitological analyses of the male chimpanzees (Pan troglodytes schweinfurthii) at Ngogo, Kibale National Park, Uganda. American Journal of Primatology 65, 167179.
Ngui, R., Mahdy, M. A. K., Chua, K. H., Traub, R. and Lim, Y. A. L. (2013). Genetic characterization of the partial mitochondrial cytochrome oxidase c subunit I (cox 1) gene of the zoonotic parasitic nematode, Ancylostoma ceylanicum from humans, dogs and cats. Acta Tropica 128, 154157.
Nosanchuk, J., Wade, S. and Landolf, M. (1995). Case report of and description of parasite in Mammomonogamus laryngeus (human syngamosis) infection. Journal of Clinical Microbiology 33, 9981000.
Obanda, V., Iwaki, T., Mutinda, N. M. and Gakuya, F. (2011). Gastrointestinal parasites and associated lesions in starving free-ranging African elephants. South African Journal of Wildlife Research 41, 167172.
Pomajbíková, K., Petrželková, K. J., Petrášová, J., Profousová, I., Kalousová, B., Jirků, M., , R. M. and Modrý, D. (2012). Distribution of the entodiniomorphid ciliate Troglocorys cava Tokiwa, Modrý, Ito, Pomajbíková, Petrželková & Imai, 2010, (Entodiniomorphida: Blepharocorythidae) in wild and captive chimpanzees. Journal of Eukaryotic Microbiology 59, 9799.
Posada, D. and Crandall, K. A. (1998). Modeltest: testing the model of DNA substitution. Bioinformatics 14, 817818.
Poulin, R. and Keeney, D. B. (2008). Host specificity under molecular and experimental scrutiny. Trends in Parasitology 24, 2428.
Poulin, R. and Mouillot, D. (2003). Parasite specialization from a phylogenetic perspective: a new index of host specificity. Parasitology 126, 473480.
Railliet, M. A. (1899). Syngame laryngien du boeuf. Comptes Rendu des Séances de la Société de Biologie et des ses Filiales 6, 174176.
Ronquist, F. and Huelsenbeck, J. P. (2003). MrBayes 3: Bayesian phylogenetic inference under mixed models. Bioinformatics 19, 15721574.
Ryzhikov, K. M. (1948). Phylogenetic interrelationships of nematodes of the family Syngamidae and an attempt to reconstruct their systematics. Doklady Akademii Nauk SSSR 62, 733736.
Sak, B., Petrzelkova, K. J., Kvetonova, D., Mynarova, A., Shutt, K. A., Pomajbikova, K., Kalousová, B., Modrý, D., Benavides, J., Todd, A. and Kváč, M. (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, e71840.
Seneviratne, P. (1954). Syngamus mcgaughei sp. nov. in domestic cats in Ceylon. Ceylon Veterinary Journal 2, 5560.
Shutt, K. A. (2014). Wildlife tourism and conservation: an interdisciplinary evaluation of gorilla ecotourism in Dzanga-Sangha, Central African Republic. Ph.D. thesis. Durham University, Durham, UK, 252 pp. Available at Durham E-Theses Online:
Shutt, K., Heistermann, M., Kasim, A., Todd, A., Kalousová, B., Profousová, I., Petrželková, K., Fuh, T., Dicky, J.-F., Bopalanzognako, J.-B. and Setchell, J. M. (2014). Effects of habituation, research and ecotourism on feacal glucocorticoid metabolites in wild western lowland gorillas: implications for conservation management. Biological Conservation 172, 7279.
Turkalo, A. and Fay, J. M. (1996). Studying forest elephants by direct observation: preliminary results from the Dzanga Clearing, Central African Republic. Pachyderm 20, 4554.
Turkalo, A. K., Wrege, P. H. and Wittemyer, G. (2013). Long-term monitoring of Dzanga Bai forest elephants: forest clearing use patterns. PLoS ONE 8, e85154.
van den Berghe, L. (1937). Contribution à l'etude des parasites de l'okapi. Revue de Zoologie et de Botanique Africaines 29, 141150.
Vercruysse, J. (1978). La mammomonogamose des zébus en empire centrafrican. Revue d’Élevage et de Médecine Vétérinaire des Pays Tropicaux 31, 427430.
von Linstow, O. (1899). Nematoden aus der Berliner Zoologischen Sammlung. Mitteilungen aus der Zoologischen Sammlung des Museums für Naturkunde in Berlin 1, 128.
Vuylsteke, C. (1935). Etude de quelques nématodes parasites de l’éléphant. Revue de Zoologie et de Botanique Africaines 27, 319325.
Recommend this journal

Email your librarian or administrator to recommend adding this journal to your organisation's collection.

  • ISSN: 0031-1820
  • EISSN: 1469-8161
  • URL: /core/journals/parasitology
Please enter your name
Please enter a valid email address
Who would you like to send this to? *


Type Description Title
Supplementary materials

Červenà supplementary material
Tables S1-S3

 Word (19 KB)
19 KB


Altmetric attention score

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