Hostname: page-component-cd9895bd7-gbm5v Total loading time: 0 Render date: 2024-12-26T04:08:41.813Z Has data issue: false hasContentIssue false

Mammomonogamus nematodes in felid carnivores: a minireview and the first molecular characterization

Published online by Cambridge University Press:  21 May 2018

Barbora Červená*
Affiliation:
Department of Pathology and Parasitology, Faculty of Veterinary Medicine, University of Veterinary and Pharmaceutical Sciences Brno, Palackého tř. 1946/1, 61242, Brno, Czech Republic
Kristýna Hrazdilová
Affiliation:
Central European Institute for Technology (CEITEC), University of Veterinary and Pharmaceutical Sciences, Palackého tř. 1946/1, 612 42 Brno, Czech Republic Department of Virology, Veterinary Research Institute, Hudcova 296/70, 621 00, Brno, Czech Republic
Peter Vallo
Affiliation:
Institute of Vertebrate Biology, Czech Academy of Sciences, Květná 8, 603 65, Brno, Czech Republic Evolutionary Ecology and Conservation Genomics, University of Ulm, Albert Einstein Allee 11, 89069, Ulm, Germany
Jennifer Ketzis
Affiliation:
Department of Biomedical Sciences, Ross University School of Veterinary Medicine, P.O. Box 334, Basseterre, Saint Kitts, West Indies
Pompei Bolfa
Affiliation:
Department of Biomedical Sciences, Ross University School of Veterinary Medicine, P.O. Box 334, Basseterre, Saint Kitts, West Indies
Edgar Tudor
Affiliation:
Animal Island Paradise Hospital, Saipan, Northern Mariana Islands, USA
Estevam G. Lux-Hoppe
Affiliation:
Faculdade de Ciências Agrárias e Veterinárias da Universidade Estadual Paulista (UNESP) – Câmpus de Jaboticabal, Via de Acesso Prof. Paulo Donato Castelane, S/N – Vila Industrial, Jaboticabal – SP, 14884-900, Brazil
Caroline Blanvillain
Affiliation:
Société d'Ornithologie de Polynésie, BP 7023–98719 Taravao, Tahiti, Polynésie Française
David Modrý
Affiliation:
Department of Pathology and Parasitology, Faculty of Veterinary Medicine, University of Veterinary and Pharmaceutical Sciences Brno, Palackého tř. 1946/1, 61242, Brno, Czech Republic Central European Institute for Technology (CEITEC), University of Veterinary and Pharmaceutical Sciences, Palackého tř. 1946/1, 612 42 Brno, Czech Republic Institute of Parasitology, Biology Centre of the Czech Academy of Sciences, Branišovská 31, 370 05, České Budějovice, Czech Republic
*
Author for correspondence: Barbora Červená, E-mail: bara.cervena@gmail.com

Abstract

Five of the 13 known species of Mammomonogamus have been described in members of the family Felidae, including domestic cats, making felids the most frequent hosts of Mammomonogamus. The occurrence of Mammomonogamus in felids is geographically scattered and information on the life cycle and other aspects of infections is lacking. The paucity of data opens the questions on possible conspecificity of some of the described species of Mammomonogamus and on the existence of possible reservoirs for infections in domestic cats in geographically isolated endemic foci of infection. To test such hypotheses, we compared sequences of mitochondrial and nuclear markers obtained from Mammomonogamus adults or eggs collected from domestic cats in three geographically distant localities. Based on morphology, geographic origin and site of infection, the worms examined can be referred to as Mammomonogamus ierei and Mammomonogamus auris. Phylogenetic analyses of both mitochondrial and ribosomal DNA markers showed monophyly of the genus Mammomonogamus and suggested the existence of at least two species in cats. Review of the literature, the existence of several species and the discontinuous geographic distribution of Mammomonogamus infections in domestic cats suggest an historical spillover of infection from wild reservoirs, presumably wild felids.

Type
Research Article
Copyright
Copyright © Cambridge University Press 2018 

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Anderson, RC (2000) Nematode Parasites of Vertebrates. Their Development and Transmission, 2nd Edn. Wallingford, Oxon, UK: CAB International Publishing.Google Scholar
Asato, R et al. (1986) Prevalence of helminthic infections in cats on Okinawa Island, Japan. Japanese Journal of Parasitology 35, 209214.Google Scholar
Baruš, V and Tenora, F (1972) Notes on the systematics and taxonomy of the nematodes belonging to the family Syngamidae Leiper, 1912. Acta Universitatis Agriculturae et Silviculturae Mendelianae Brunensis 20, 275286.Google Scholar
Bowman, DD et al. (2002) The nematodes. In Bowman, DD, Hendrix, CM, Lindsay, DS and Barr, SC (eds), Feline Clinical Parasitology. Ames, USA: Iowa State University Press, pp. 233354.Google Scholar
Buckley, JJC (1934) On Syngamus ierei sp. nov. from domestic cats, with some observations on its life-cycle. Journal of Helminthology 12, 8998.Google Scholar
Cameron, WM (1931) On some lungworms of the Malay tiger. Journal of Helminthology 9, 147152.Google Scholar
Červená, B et al. (2017) Host specificity and basic ecology of Mammomonogamus (Nematoda, Syngamidae) from lowland gorillas and forest elephants in Central African Republic. Parasitology 144, 10161025.Google Scholar
Červená, B et al. (2018) Diversity of Mammomonogamus (Nematoda: Syngamidae) in large African herbivores. Parasitology Research 117, 10131024.Google Scholar
Chilton, NB, Huby-Chilton, F and Gasser, RB (2003) First complete large subunit ribosomal RNA sequence and secondary structure for a parasitic nematode: phylogenetic and diagnostic implications. Molecular and Cellular Probes 17, 3339.Google Scholar
Chilton, NB et al. (2006) The evolutionary origins of nematodes within the order Strongylida are related to predilection sites within hosts. Molecular Phylogenetics and Evolution 40, 118128.Google Scholar
Cuadrado, R, Maldonado-Moll, JF and Segarra, J (1980) Gapeworm infection of domestic cats in Puerto Rico. Journal of the American Veterinary Medical Association 176, 996997.Google Scholar
Diesing, CM (1857) Sechzehn Arten von Nematoideen (Mit IV Tafeln). XIII Bande der Denkschriften der mathematisch-naturwissenschaftlichen Classe der Kaiserlichen Akademie der Wissenschaften in Wien 1–28.Google Scholar
Faust, EC and Tang, Ch-Ch (1934) A new species of Syngamus (S. auris) from the middle ear of the cat in Foochow, China. Parasitology 26, 455459.Google Scholar
Folmer, O et al. (1994) DNA primers for amplification of mitochondrial cytochrome c oxidase subunit I from diverse metazoan invertebrates. Molecular Marine Biology and Biotechnology 3, 294299.Google Scholar
Gattenuo, T, Ketzis, J and Shell, L (2014) Fenbendazole treatment for Mammomonogamus species infection of a domestic cat on St. Kitts, West Indies. Journal of Feline Medicine and Surgery 16, 864866.Google Scholar
Gedoelst, L (1924) Un syngame parasite de l'hippopotame. Annales de Parasitologie Humaine et Comparée 2, 307311.Google Scholar
Gerichter, CB (1949) Studies on nematodes parasitic in the lungs of Felidae in Palestine. Parasitology 39, 251262.Google Scholar
Graber, M et al. (1971) La mammomonogamose des ruminants domestiques et sauvages. Revue d’Élevage et de Médecine Vétérinaire des Pays Tropicaux 24, 525541.Google Scholar
Guilbride, PDL (1953) Syngamus ierei, Physaloptera praeputialis and Platynosomum fastosum from a cat in Jamaica. The Veterinary Record 65, 220.Google Scholar
Hall, TA (1999) Bioedit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucleic Acids Symposium Series 41, 9598.Google Scholar
Hasegawa, H (1992) Parasites of the Iriomote cat, Felis iriomotensis (III). Island Studies in Okinawa 10, 124.Google Scholar
Hastings, WK (1970) Monte Carlo sampling methods using Markov chains and their applications. Biometrika 57, 97109.Google Scholar
Hu, Y et al. (2014) Earliest evidence for commensal processes of cat domestication. Proceedings of the National Academy of Sciences 111, 116120.Google Scholar
Kearse, M et al. (2012) Geneious basic: an integrated and extendable desktop software platform for the organization and analysis of sequence data. Bioinformatics (oxford, England) 28, 16471649.Google Scholar
Krecek, RC et al. (2010) Parasites of stray cats (Felis domesticus L., 1758) on St. Kitts, West Indies. Veterinary Parasitology 172, 147149.Google Scholar
Larkin, MA et al. (2007) Clustal W and ClustalX version 2.0. Bioinformatics (Oxford, England) 23, 29472948.Google Scholar
Lindquist, DW and Austin, ER (1981) Exotic parasitism in a Siamese cat. Feline Practice 11, 910.Google Scholar
Magnaval, J-F and Magdeleine, J (2004) La mammomonogamose humaine. Médecine Tropicale 64, 2122.Google Scholar
Mönnig, HO (1932) Syngamus indicus. 18th Report of Director of Veterinary Services and Animal Industry, Union of South Africa, p. 173.Google Scholar
Murray, JL and Gardner, GL (1997) Leopardus pardalis. Mammalian Species 548, 110.Google Scholar
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.Google Scholar
O'Brian, SJ and Johnson, WE (2007) The evolution of cats. Scientific American 297, 6875.Google Scholar
Patton, S and Rabinowitz, AR (1994) Parasites of wild Felidae in Thailand: a coprological survey. Journal of Wildlife Diseases 30, 472475.Google Scholar
Posada, D and Crandall, KA (1998) Modeltest: testing the model of DNA substitution. Bioinformatics (Oxford, England) 14, 817818.Google Scholar
Railliet, MA (1899) Syngame laryngien du boeuf. Comptes Rendus des Séances de la Société de Biologie et de ses Filiales 6, 174176.Google Scholar
Ronquist, F and Huelsenbeck, JP (2003) Mrbayes 3: Bayesian phylogenetic inference under mixed models. Bioinformatics (Oxford, England) 19, 15721574.Google Scholar
Ryzhikov, KM (1949) Syngamidy domašnych i dikich životnych. Osnovy Nematodologii 1, 1164 (in Russian).Google Scholar
Sakamoto, T, Kaneda, H and Nakagawa, S (1971) Ten species of parasites from leopard Panthera pardus (Linnaeus). Japanese Journal of Parasitology 20, 59 (Suppl.).Google Scholar
Seneviratne, P (1954) Syngamus mcgaughei sp. nov. in domestic cats in Ceylon. Ceylon Veterinary Journal 2, 5560.Google Scholar
Sugiyama, E et al. (1982) A new record of Mammomonogamus auris from the middle ear of the domestic cats in Japan. Japanese Journal of Parasitology 31, 471476.Google Scholar
Tudor, EG et al. (2008) Mammomonogamus auris infection in the middle ear of a domestic cat in Saipan, Northern Mariana Islands, USA. Journal of Feline Medicine and Surgery 10, 501504.Google Scholar
van den Berghe, L (1937) Contribution à l'etude des parasites de l'okapi. Revue de Zoologie et de Botanique Africaines 29, 141150.Google Scholar
Vigne, J-D et al. (2016) Earliest ‘domestic’ cats in China identified as leopard cat (Prionailurus bengalensis). PLoS ONE 11, e0147295.Google Scholar
von Linstow, O (1899) Nematoden aus der Berliner Zoologischen Sammlung. Mitteilungen aus der Zoologischen Sammlung des Museums für Naturkunde in Berlin 1, 128.Google Scholar
Vuylsteke, C (1935) Etude de quelques nématodes parasites de l’éléphant. Revue de Zoologie et de Botanique Africaines 27, 319325.Google Scholar
Supplementary material: Image

Červená et al. supplementary material

Figure S3

Download Červená et al. supplementary material(Image)
Image 1.1 MB
Supplementary material: Image

Červená et al. supplementary material

Figure S4

Download Červená et al. supplementary material(Image)
Image 1 MB
Supplementary material: File

Červená et al. supplementary material

Table S1

Download Červená et al. supplementary material(File)
File 16.6 KB
Supplementary material: File

Červená et al. supplementary material

Table S2

Download Červená et al. supplementary material(File)
File 13.4 KB