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Type: Article
Published: 2019-04-15
Page range: 478–488
Abstract views: 140
PDF downloaded: 2

Intestinal ciliates (Alveolata, Ciliophora) in Brazilian domestic horses (Equus caballus L.) and a review on the ciliate communities associated with horses around the world

Laboratório de Protozoologia, Programa de Pós-graduação em Ciências Biológicas - Comportamento e Biologia Animal, Instituto de Ciências Biológicas, Universidade Federal de Juiz de Fora, Campus Universitário, CEP 36036-330, Juiz de Fora, Minas Gerais, Brazil
Laboratório de Protozoologia, Programa de Pós-graduação em Ciências Biológicas - Comportamento e Biologia Animal, Instituto de Ciências Biológicas, Universidade Federal de Juiz de Fora, Campus Universitário, CEP 36036-330, Juiz de Fora, Minas Gerais, Brazil
Laboratório de Protozoologia, Programa de Pós-graduação em Ciências Biológicas - Comportamento e Biologia Animal, Instituto de Ciências Biológicas, Universidade Federal de Juiz de Fora, Campus Universitário, CEP 36036-330, Juiz de Fora, Minas Gerais, Brazil
Laboratório de Protozoologia, Programa de Pós-graduação em Ciências Biológicas - Comportamento e Biologia Animal, Instituto de Ciências Biológicas, Universidade Federal de Juiz de Fora, Campus Universitário, CEP 36036-330, Juiz de Fora, Minas Gerais, Brazil
Echinodermata Entodiniomorphida Suctoria symbiotic ciliates Trichostomatia

Abstract

The aims of this study were to identify and quantify the gastrointestinal ciliates from Brazilian domestic horses, to compare the data obtained with previous studies and to review data on ciliate communities associated with horses around the world. We used eight domestic horses, kept under extensive management. Fecal samples were obtained immediately after defecation of animals and fixed in 18.5% formaldehyde. We identify 24 species of endosymbiotic ciliates, distributed in two subclasses, two orders, five families and 13 genera. The ciliate composition was similar among the animals analyzed. The family Blepharocorythidae presented the higher prevalence and the family Buetschliidae was observed in greater abundance and density. Among the species identified, Cycloposthium dentiferum was observed for the first time in Central and South America and Bundleia elongata, B. inflata, B. piriformis, B. vorax and Cycloposthium psicauda, were observed for the first time in the American continent. In addition, the species Buissonella tapiri, which was originally discovered in fecal contents of the American tapir (Tapirus terrestris) in Brazil was observed for the first time associated to Equus caballus. The review on the ciliate communities associated with horses around the world demonstrated that the equine ciliates are a very diversified group with representatives in two subclasses, Suctoria and Trichostomatia, totaling 78 species distributed in three orders and six families, having been registered in different equine hosts (Equus asinus, Equus caballus and Equus quagga) and geographic locations (USA, China, Russia, Taiwan, Mexico, Cyprus, Turkey, Kyrgyzstan and Brazil).

 

References

  1. Aladro-Lubel, M.A., Mayén-Estrada, R., Reyes-Santos, M. (2006) Lista dos faunísticos de México XI Registro actualizado de ciliados (agosto 2004). Instituto de Biología, Universidad Nacional Autónoma de México, acultad de Ciencias, México, 99 pp.

    Belzecki, G., Miltko, R., Michalowski, T. & McEwan, N.R. (2016) Methods for the cultivation of ciliated protozoa from the large intestine of horses. FEMS Microbiology Letters, 363 (2), 1–4.

    Buisson, J. (1923) Les infusoires ciliés du tube digestif de l'homme et des mammiferes. These, Amedee Legrand, Paris, 200 pp. [Paris Le Gall]

    Bundle, A. (1895) Ciliate infusorian im coecum des Pferdes. Zeitschrift für wissenschaftliche Zoologie, 60, 284–350.

    Bush, A.O., Laffert, K.D., Lotz, J.M. & Shostak, A.W. (1997) Parasitology meets ecology on its own terms: Margolis et al. reviseted. Journal of Parasitology, 83, 575–583.

    https://doi.org/10.2307/3284227

    Chavarria, M. (1933) Estudios protistológicos. II. Ochoterenaia appendiculata gen. n., sp. n., nuevo infusorio del intestino del caballo (Equus caballus Linn) de Mexico. Anales del Instituto Biología, Universidad Nacional Autónoma de México, 4, 191–196.

    Collin, G. (1854) Traité de physiologie comparée des animaux; consideré dans ses rapports avec les sciences naturelles, la medicine, la zootechnie, et l’economie rurale. J.-B. Baillière, Paris, 667 pp.

    Cunha, A.M. & Muniz, J. (1925) contribuição para o conhecimento dos ciliados parasitos dos mamíferos do Brasil. Sciencia Medica, 3, 732–747.

    D’Agosto, M. & Carneiro, M.E. (1999) Evaluation of lugol sulution used for counting rumen ciliates. Revista Brasileira de Zoologia, 85, 725–729.

    https://doi.org/10.1590/S0101-81751999000300011

    Dehority, B.A. (1984) Evaluation of subsampling and fixation procedures used for counting rumen protozoa. Applied and Environmental Microbiology, 48, 182–185.

    Dehority, B.A. (1986) Protozoa of the digestive tract of herbivorous mammals. Insect Science and its Application, 7, 279–296.

    https://doi.org/10.1017/S1742758400009346

    Dovgal, I.V. (2002) Evolution, phylogeny and classification of Suctorea (Ciliophora). Protistology, 2, 194–270.

    Fernández-Galiano, D. (1959) La infraciliación en Cycloposthium edentatum Strelkow. Boletín Real de la Sociedad Española de Historia Natural, Biologica, 57, 139–150.

    Fiorentini, A. (1890) Intorno ai protisti dell’intestino degli equi. Bolletin des Siences 12, 7–17.

    French, R.A., Meier, W.A. & Zachary, J.F. (1996) Eosinophilic colitis and hepatitis in a horse with colonic intramucosal ciliated protozoa. Veterinary Pathology, 33, 235–238.

    Gassovksy, G. (1919) On the microfauna of intestine of the horse. Travaux de la Société des Naturalistes de Petrograd, 49, 20–37.

    https://doi.org/10.1177/030098589603300215

    Göçmen, B., Gürelli, G. & Dehority, B. (2012) Fecal ciliate composition of Cypriot domestic horses (Equus caballus Linnaeus, 1758). Turkish Journal of Zoology, 36 (2), 163–141.

    Gruby, D. & Delafond, O. (1843) Recherches sur des animalcules se devéloppant en grand nombre dans l’estomac et l’istestins, pendant la digestion des animaux herbivores et carnivores. Compte rendus hebdomadaires des séances de l’Academie des Sciences, 17, 1304–1308.

    Güiris, A.D.M., Rojas, H.N.M., Berovides, A.V., Sosa, P.J., Pérez, E.M.E., Cruz, A.E., Chávez, H.C., Moguel, A.J.A., Jiménez-Coello, M. & Ortega-Pacheco, A. (2010) Biodiversity and distribution of helminths and protozoa in naturally infected horses from the biosphere reserve “La Sierra Madre de Chiapas”, México. Veterinary Parasitology, 170, 268–277.

    https://doi.org/10.1016/j.vetpar.2010.02.016

    Gürelli, G. (2012) Comparative study of hindgut ciliates in horses, mules and donkeys in Turkey. Global Veterinaria, 9 (6), 700–705.

    Gürelli, G. (2016) Intestinal ciliate fauna of the Asian elephant from Gaziantep, Turkey and the description of Brevitentaculum antebum n. g., n. sp. European Journal of Protistology, 56, 26–31.

    https://doi.org/10.1016/j.ejop.2016.05.001

    Gürelli, G. & Göçmen, B. (2010) The occurence of the hindgut ciliate Hemiprorodon Gymnoposthium (Ciliophora: Buetschliidae) from domestic horses in Cyprus. Türkiye Parazitoloji Dergisi, 34 (3), 206–208.

    Gürelli, G. & Göçmen, B. (2011) Intestinal ciliate composition found in the feces of the Turk rahvan horse Equus caballus, Linnaeus, 1758. European Journal of Protistology, 47, 245–255.

    https://doi.org/10.1016/j.ejop.2011.04.005

    Gürelli, G. & Göçmen, B. (2012) Intestinal ciliate composition in the feces of racing horses from Izmir, Turkey. European Journal of Protistology, 48, 215–226.

    https://doi.org/10.1016/j.ejop.2012.01.002

    Gürelli, G., Canbulat, S. & Aldayarov, N. (2015) Fecal ciliate composition of domestic horses (Equus caballus Linnaeus, 1758) living in Kyrgyzstan. Zootaxa, 4039 (1), 145–156.

    Hsiung, T.-S. (1930) A monograph on the protozoa of the large intestine of the horse. Iowa State College Journal of Science, 4, 359–423.

    Hsiung, T.-S. (1935a) Notes on the known species of Triadinium with the description of a new species. Bulletin of the Fan Memorial Institute of Biology, 6, 21–32.

    Hsiung, T.-S. (1935b) On some new species from the mule, with the description of a new genus. Bulletin of the Fan Memorial Institute of Biology, 6, 81–94.

    Hsiung, T.-S. (1936) A survey of the ciliates of Chinese equines. Bulletin of the Fan Memorial Institute of Biology, 6, 289–304.

    Ike, K., Imai, S. & Ishii, T. (1985) Establishment of intestinal ciliates in new-born horses. Japanese Journal of Veterinary Science, 47, 39–43.

    https://doi.org/10.1292/jvms1939.47.39

    Ike, K., Nuruki, R., Imai, S. & Ishii, T. (1981) Composition of intestinal ciliates excreted in feces of the light horse. Bulletin of the Nippon Veterinary Zootechnical College, 30, 91–100.

    Ike, K., Nuruki, R., Imai, S. & Ishii, T. (1983a) Composition of intestinal ciliates and bacteria excreted in feces of the race-horse. Japanese Journal of Veterinary Science, 45, 157–163.

    https://doi.org/10.1292/jvms1939.45.157

    Ike, K., Nuruki, R., Nomoto, Y., Imai, S. & Ishii, T. (1983b) Comparative studies on the intestinal ciliate fauna excreted in the feces of yearlings, bloodmares, riding horses and racehorses. Bulletin of Equine Research Institute, 20, 63–70.

    Imai, S., Inami, K., Morita, T., Ike, K. & Ito, A. (1999) Intestinal ciliate composition found in the feces of Japanese native kiso horse. Bulletin of the Nippon Veterinary and Animal Science University, 48, 33–38.

    Ito, A., Imai, S., Ogimito, K. & Nakahara, M. (1996) Intestinal ciliates found in the feces of Japanese native Tokara pony, with the description of a new genus and a new species. Journal of Veterinary and Medical Science, 58, 103–108.

    https://doi.org/10.1292/jvms.58.103

    Ito, A., Ishihara, M. & Imai, S. (2014) Bozasella gracilis n. sp. (Ciliophora, Entodiniomorphida) from Asian elephant and phylogenetic analysis of entodiniomorphids and vestibuliferids. European Journal Protistology, 50, 134–152.

    https://doi.org/10.1016/j.ejop.2014.01.003

    Ito, A., Imai, S. & Ogimoto, K. (1994) Rumen ciliate composition and diversity of Japanese beef black cattle in comparison with those Holstein-Friesien cattle. The Journal of the Veterinary and Medical Science, 56, 707–714.

    https://doi.org/10.1292/jvms.56.707

    Kornilova, O.A. (2003) The fauna of ciliates from the intestine of Asiatic wild ass (kulan). Tessa Press, St-Petersburg, 215 pp.

    Kornilova, O.A. (2006) Ciliates from the intestine of Yakut Horse (Equus caballus). Parazitologiia, 40, 472–478

    Levine, N.D. (1961) Protozoan parasites of domestic animals and of man. Burgess Publishing Co., Minneapolis, 412 pp.

    https://doi.org/10.5962/bhl.title.7000

    Lynn, D.H. (2008) The ciliated Protozoa: characterization, classification and guide to the literature. Springer, New York, 605 pp.

    Mishima, T., Katamoto, H., Hori, Y., Kakengi, V.A.M. & Ito, A. (2009) Rumen ciliates from Tanzanian short horn zebu cattle Bos taurus indicus and the infraciliature of Entodinium palmare n. sp. and Enoploplastron stokyi (Buisson, 1924). European Journal of Protistology, 45, 77–86.

    https://doi.org/10.1016/j.ejop.2008.07.002

    Moon-van der Staay, S.Y., van der Staay, G.W.M., Michalowski, T., Jouany, J.-P., Pristas, P., Javorsky, P., Kisidayovà, S., Varadyova, Z., McEwan, N.R., Newbold, C.J., van Alen, T., Graaf, R. de, Schmid, M., Huynen, M.A. & Hackstein, J.H.P. (2014) The symbiotic intestinal ciliates and the evolution of their hosts. European Journal of Protistology, 50, 166–173.

    https://doi.org/10.1016/j.ejop.2014.01.004

    Snelling, T., Pinloche, E., Worgan, H.J., Newbold, J. & McEwan, N.R. (2011) Molecular phylogeny of Spirodinium equi, Triadinium caudatum and Blepharocorys sp. from the equine hindgut. Acta Protozoologica, 50, 319–326.

    Strelkow, A. (1939) Parasitical infusoria from the intestine of Ungulata belonging to the family Equidae. Urchen Zap. Uchenye Zapiski Leningrad Pedagog Institute Gertsena, 17, 262–374.

    Strüder-Kypke, M.C., Kornilova, O.A. & Lynn, D.H. (2007) Phylogeny of trichostomes ciliates (Ciliophora, Litostomatea) endosymbiotic in the Yakut horse (Equus caballus). European Journal of Protistology, 43, 319–328.

    https://doi.org/10.1016/j.ejop.2007.06.005

    Tung, K.-C. (1992) Analysis of the composition and morphology of intestinal ciliates excreted in feces of the riding horses in middle Taiwan. Bulletin of the Facult of Agriculture and National Chung-Hsing Univervisty, 41, 53–56.

    Wolska, M. (1969) Triadinium minimum Gassovsky. Its phylogenetic significance. Revista de la Sociedad Mexicana de Historia Natural, 30, 65–78.

    Wolska, M. (1971) Studies on the family Blepharocorythidae Hsiung. V. A review of genera and species. Acta Protozoologica, 9, 23–43.

    Wolska, M. (1978a) Light and electron microscope studies on Ochoterenaia appendiculata Chavarria (Ciliata, Blepharocorythina). Acta Protozoologica, 17, 483–492.

    Wolska, M. (1978b) Triadinium caudatum Fiorent. electron microscope observations. Acta Protozoologica, 17, 445–454.

    Wolska, M. (1979) Circodinium minimum (Gassovsky, 1918), electron-microscope investigations. Acta Protozoologica, 18, 223–229.

    Wolska, M. (1980) Tetratoxum unifasciculatum (Fiorent.) (Ciliata, Entodiniomorphida). 1. Somatic and adoral infra- ciliature. Acta Protozoologica, 19, 15–20.

    Wolska, M. (1981) Studies on the genus Triadinium Fior. (Ciliata, Entodiniomorphida). Comparison of Triadinium galea Gass. and Triadinium caudatum Fior. Acta Protozoologica, 20, 357–365.

    Wolska, M. & Piechaczek, H. (1970) Some intestinal ciliates of American tapir. Acta Protozoologica, 15, 221–229.