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Trichomonad parasite infection in four species of Columbidae in the UK

Published online by Cambridge University Press:  19 July 2013

School of Biology, Irene Manton Building, University of Leeds, Leeds LS9 2JT, UK
Centre for Conservation Science, Royal Society for the Protection of Birds, The Lodge, Potton Road, Sandy SG19 2DL, UK
School of Biology, Irene Manton Building, University of Leeds, Leeds LS9 2JT, UK Cardiff School of Biosciences, The Sir Martin Evans Building, Museum Avenue, Cardiff CF10 3AX, UK
School of Biology, Irene Manton Building, University of Leeds, Leeds LS9 2JT, UK
Centre for Conservation Science, Royal Society for the Protection of Birds, The Lodge, Potton Road, Sandy SG19 2DL, UK
School of Biology, Irene Manton Building, University of Leeds, Leeds LS9 2JT, UK
*Corresponding author: School of Biology, Irene Manton Building, University of Leeds, Leeds LS9 2JT, UK. E-mail:
*Corresponding author: RSPB, The Lodge, Potton Road, Sandy SG19 2DL, UK. E-mail:


Trichomonas gallinae is an emerging pathogen in wild birds, linked to recent declines in finch (Fringillidae) populations across Europe. Globally, the main hosts for this parasite are species of Columbidae (doves and pigeons); here we carry out the first investigation into the presence and incidence of Trichomonas in four species of Columbidae in the UK, through live sampling of wild-caught birds and subsequent PCR. We report the first known UK cases of Trichomonas infection in 86% of European Turtle Doves Streptopelia turtur sampled, along with 86% of Eurasian Collared Doves Streptopelia decaocto, 47% of Woodpigeons Columba palumbus and 40% of Stock Doves Columba oenas. Birds were more likely to be infected if the farm provided supplementary food for gamebirds. We found three strains of T. gallinae and one strain clustering within the Trichomonas tenax clade, not previously associated with avian hosts in the UK. One T. gallinae strain was identical at the ITS/5.8S/ITS2 ribosomal region to that responsible for the finch trichomonosis epizootic. We highlight the importance of increasing our knowledge of the diversity and ecological implications of Trichomonas parasites in order further to understand the sub-clinical impacts of parasite infection.

Research Article
Copyright © Cambridge University Press 2013 

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Al-Bakry, H. S. (2009). Prevalence of avian trichomoniasis in different species of pigeons in Mosul. Iraqi Journal of Veterinary Sciences 23, 105109.CrossRefGoogle Scholar
Altschul, S. F., Madden, T. L., Schäffer, A. A., Zhang, J., Zhang, Z., Miller, W. and Lipman, D. J. (1997). Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Research 25, 33893402.CrossRefGoogle ScholarPubMed
Anderson, N. L., Grahn, R. A., Van Hoosear, K. and BonDurant, R. H. (2009). Studies of trichomonad protozoa in free ranging songbirds: prevalence of Trichomonas gallinae in house finches (Carpodacus mexicanus) and corvids and a novel trichomonad in mockingbirds (Mimus polyglottos). Veterinary Parasitology 161, 178186. doi: 10.1016/j.vetpar.2009.01.023.CrossRefGoogle Scholar
Appleby, B. M., Anwar, M. A. and Petty, S. J. (1999). Short-term and long-term effects of food supply on parasite burdens in Tawny Owls, Strix aluco. Functional Ecology 13, 315321. doi: 10.1046/j.1365-2435.1999.00319.x.CrossRefGoogle Scholar
Baker, K. (1993). Identification Guide to European Non-Passerines. BTO Guides 24. British Trust for Ornithology, Thetford, UK.Google Scholar
Bartón, K. (2012). MuMIn: Multi-model inference. R package version 1.7.7. Scholar
Boal, C. W., Mannan, R. W. and Hudelson, K. S. (1998). Trichomoniasis in Cooper's Hawks from Arizona. Journal of Wildlife Diseases 34, 590593.CrossRefGoogle ScholarPubMed
Browne, S. J. and Aebischer, N. J. (2003). Habitat use, foraging ecology and diet of Turtle Doves Streptopelia turtur in Britain. Ibis 145, 572582. doi: 10.1046/j.1474-919X.2003.00185.x.CrossRefGoogle Scholar
Bunbury, N., Bell, D., Jones, C., Greenwood, A. and Hunter, P. (2005). Comparison of the InPouch TF culture system and wet-mount microscopy for diagnosis of Trichomonas gallinae infections in the Pink Pigeon Columba mayeri. Journal of Clinical Microbiology 43, 10051006. doi: 10.1128/JCM.43.2.1005-1006.2005.CrossRefGoogle ScholarPubMed
Bunbury, N., Jones, C. G., Greenwood, A. G. and Bell, D. J. (2007). Trichomonas gallinae in Mauritian columbids: implications for an endangered endemic. Journal of Wildlife Diseases 43, 399407.CrossRefGoogle ScholarPubMed
Bunbury, N., Jones, C. G., Greenwood, A. G. and Bell, D. J. (2008). Epidemiology and conservation implications of Trichomonas gallinae infection in the endangered Mauritian Pink Pigeon. Biological Conservation 141, 153161. doi: 10.1016/j.biocon.2007.09.008.CrossRefGoogle Scholar
Burnham, K. P. and Anderson, D. R. (2002). Model Selection and Multi-Model Inference: A Practical Information-Theoretic Approach, 2nd Edn. Springer-Verlag, New York.Google Scholar
Cielecka, D., Borsuk, P., Grytner-Ziecina, B. and Turkowicz, M. (2000). First detection of Trichomonas tenax in dog and cat by PCR-RFLP. Acta Parasitologica 45, 350352.Google Scholar
Clinchy, M., Zanette, L., Boonstra, R., Wingfield, J. C. and Smith, J. N. M. (2004). Balancing food and predator pressure induces chronic stress in songbirds. Proceedings of the Royal Society of London: Series B 271, 24732479. doi: 10.1098/rspb.2004.2913.CrossRefGoogle ScholarPubMed
Cover, A. J., Harmon, W. M. and Thomas, M. W. (1994). A new method for the diagnosis of Trichomonas gallinae infection by culture. Journal of Wildlife Diseases 30, 457459.CrossRefGoogle ScholarPubMed
Crespo, R., Walker, R. L., Nordhausen, R., Sawyer, S. J. and Manalac, R. B. (2001). Salpingitis in Pekin Ducks associated with concurrent infection with Tetratrichomonas sp. and Escherichia coli. Journal of Veterinary Diagnostic Investigation 13, 240245. doi: 10.1177/104063870101300309.CrossRefGoogle ScholarPubMed
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 Viscogliosi, 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.CrossRefGoogle ScholarPubMed
Dunn, J. C. and Morris, A. J. (2012). Which features of UK farmland are important in retaining territories of the rapidly declining Turtle Dove Streptopelia turtur? Bird Study 59, 394402. doi: 10.1080/00063657.2012.725710.CrossRefGoogle Scholar
Felleisen, R. S. J. (1997). Comparative sequence analysis of 5.8S rRNA genes and internal transcribed spacer (ITS) regions of trichomonadid protozoa. Parasitology 115, 111119.CrossRefGoogle ScholarPubMed
Gaspar Da Silva, D., Barton, E., Bunbury, N., Lunness, P., Bell, D. J. and Tyler, K. M. (2007). Molecular identity and heterogeneity of trichomonad parasites in a closed avian population. Infection Genetics and Evolution 7, 433440. doi: 10.1016/j.meegid.2007.01.002.CrossRefGoogle Scholar
Gerhold, R. W., Yabsley, M. J., Smith, A. J., Ostergaard, E., Mannan, W., Cann, J. D. and Fischer, J. R. (2008). Molecular characterization of the Trichomonas gallinae morphologic complex in the United States. Journal of Parasitology 94, 13351341.CrossRefGoogle ScholarPubMed
Grabensteiner, E., Bilic, I., Kolbe, T. and Hess, M. (2010). Molecular analysis of clonal trichomonad isolates indicate the existence of heterogenic species present in different birds and within the same host. Veterinary Parasitology 172, 5364. doi:10.1016/j.vetpar.2010.04.015.CrossRefGoogle ScholarPubMed
Hall, T. (2005). BioEdit: biological sequence alignment editor for Win95/98/NT/2K/XP. Ibis Biosciences, Carlsbad, CA, USA. Scholar
Höfle, U., Gortazar, C., Ortíz, J. A., Knispel, B. and Kaleta, E. F. (2004). Outbreak of trichomoniasis in a woodpigeon (Columba palumbus) wintering roost. European Journal of Wildlife Research 50, 7377. doi: 10.1007/s10344-004-0043-2.CrossRefGoogle Scholar
Kleina, P., Bettim-Bandinelli, J., Bonatto, S. L., Benchimol, M. and Bogo, M. R. (2004). Molecular phylogeny of Trichomonadidae family inferred from ITS-1, 5.8S rRNA and ITS-2 sequences. International Journal for Parasitology 34, 963970. doi: 10.1016/j.ijpara.2004.04.004.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle ScholarPubMed
Lawson, B., Robinson, R. A., Neimanis, A., Handeland, K., Isomursu, M., Agren, E. O., Hamnes, I. S., Tyler, K. M., Chantry, J., Hughes, L. A., Pennycott, T. W., Simpson, V. R., John, S. K., Peck, K. M., Toms, M. P., Bennett, M., Kirkwood, J. K. and Cunningham, A. A. (2011 a). Evidence of spread of the emerging infectious disease finch trichomonosis, by migrating birds. EcoHealth 8, 143153. doi: 10.1007/s10393-011-0696-8.CrossRefGoogle ScholarPubMed
Lawson, B., Cunningham, A. A., Chantrey, J., Hughes, L. A., John, S. K., Bunbury, N., Bell, D. J. and Tyler, K. M. (2011 b). A clonal strain of Trichomonas gallinae is the aetiologic agent of an emerging avian epidemic disease. Infection, Genetics and Evolution 11, 16381645. doi: 10.1016/j.meegid.2011.06.007.CrossRefGoogle ScholarPubMed
Lawson, B., Robinson, R. A., Colville, K. M., Peck, K. M., Chantrey, J., Pennycott, T. W., Simpson, V. R., Toms, M. P. and Cunningham, A. A. (2012). The emergence and spread of finch trichomonosis in the British Isles. Philosophical Transactions of the Royal Society of London: Series B 367, 28522863. doi: 10.1098/rstb.2012.0130.CrossRefGoogle ScholarPubMed
Lindström, K. M., Hawley, D. M., Davis, A. K. and Wikelski, M. (2005). Stress responses and disease in three wintering house finch (Carpodacus mexicanus) populations along a latitudinal gradient. General and Comparative Endocrinology 143, 231239. doi: 10.1016/j.ygcen.2005.04.005.CrossRefGoogle ScholarPubMed
Muñoz, E. (1995). Estudio de la prevalencia y susceptibilidad a la infección por Trichomonas gallinae en aves domésticas y silvestres. Valoración de la sensibilidad del protozoo a diferentes derivados imidazólicos. Universitat Autónoma de Barcelona, Cerdanyola, Catalonia, Spain.Google Scholar
Murton, R. K., Westwood, N. J. and Isaacson, A. J. (1964). The feeding habits of the woodpigeon Columba palumbus, stock dove C. oenas and turtle dove Streptopelia turtur. Ibis 106, 174188.CrossRefGoogle Scholar
Pennycott, T. (1998). Carriage of trichomonads, Hexamita species and Blastocystis species by adult pheasants. Veterinary Record 143, 142143. doi: 10.1136/vr.143.5.142.CrossRefGoogle ScholarPubMed
R Core Development Team. (2012). R: A Language and Environment for Statistical Computing. R Foundation for Statistical Computing, Vienna, Austria. ISBN 3-900051-07-0. Scholar
Redfern, C. and Clark, J. (2001). Ringers’ Manual. British Trust for Ornithology, Thetford, UK.Google Scholar
Reinmann, K., Müller, N., Kuhnert, P., Campero, C. M., Leitsch, D., Hess, M., Henning, K., Fort, M., Müller, J., Gottstein, B. and Frey, C. F. (2012). Tritrichomonas foetus isolates from cats and cattle show minor genetic differences in unrelated loci ITS-2 and EF-1α. Veterinary Parasitology 185, 138144. doi: 10.1016/j.vetpar.2011.09.032.CrossRefGoogle ScholarPubMed
Riley, D. E., Roberts, M. C., Takayama, T. and Kreiger, J. N. (1992). Development of a polymerase chain reaction-based diagnosis of Trichomonas vaginalis. Journal of Clinical Microbiology 30, 465472.CrossRefGoogle ScholarPubMed
Risely, K., Massimino, D., Johnston, A., Newson, S. E., Eaton, M. A., Musgrove, A. J., Noble, D. G., Procter, D. and Baillie, S. R. (2012). The Breeding Bird Survey 2011. BTO Research Report 624. British Trust for Ornithology, Thetford, UK.Google Scholar
Robinson, R. A., Lawson, B., Toms, M. P., Peck, K. M., Kirkwood, J. K., Chantry, J., Clatworthy, I. R., Evans, A. D., Hughes, L. A., Hutchinson, O. C., John, S. K., Pennycott, T. W., Perkins, M. W., Rowley, P. S., Simpson, V. R., Tyler, K. M. and Cunningham, A. A. (2010). Emerging infectious disease leads to rapid population declines of common British birds. PLoS ONE 5, 8. doi: 10.1371/journal.pone.0012215.CrossRefGoogle ScholarPubMed
Romagosa, C. M. and Labisky, R. F. (2000). Establishment and dispersal of the Eurasian Collared-Dove in Florida. Journal of Field Ornithology 71, 159166. doi: 10.1648/0273-8570-71.1.159.CrossRefGoogle Scholar
Sansano-Maestre, J., Garijo-Toledao, M. M. and Gómez-Muñoz, M. T. (2009). Prevalence and genotyping of Trichomonas gallinae in pigeons and birds of prey. Avian Pathology 38, 201207.CrossRefGoogle ScholarPubMed
Stabler, R. M. (1948). Protection in pigeons against virulent Trichomonas gallinae acquired by infection with milder strains. Journal of Parasitology 34, 150153.CrossRefGoogle ScholarPubMed
Stabler, R. M. (1954). Trichomonas gallinae: a review. Parasitological Reviews 3, 368402.Google ScholarPubMed
Stimmelmayr, R., Stefani, L. M., Thrall, M. A., Landers, K., Revan, F., Miller, A., Beckstead, R. and Gerhold, R. (2012). Trichomonosis in free-ranging Eurasian Collared Doves (Streptopelia decaocto) and African Collared Dove Hybrids (Streptopelia risoria) in the Caribbean and description of ITS-1 region genotypes. Avian Diseases 56, 441445. doi: 10.1637/9905-082311-Case.1.CrossRefGoogle ScholarPubMed
Tamura, K., Peterson, D., Peterson, N., Stecher, G., Nei, M. and Kumar, S. (2011). MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Molecular Biology and Evolution 28, 27312739. doi: 10.1093/molbev/msr121.CrossRefGoogle ScholarPubMed
Thompson, J. D., Higgins, D. G. and Gibson, T. J. (1994). CLUSTAL W: improving the sensitivity of progressive multiple sequence alignments through sequence weighting, position specific gap penalties and weight matrix choice. Nucleic Acids Research 22, 46734680. doi: 10.1093/nar/22.22.4673.CrossRefGoogle ScholarPubMed
Veterinary Laboratories Agency (2009). Wildlife Diseases in the UK Reported in the Years 2002–2009. VLA on behalf of the Department for Environment, Food and Rural Affairs (Defra) and the World Organisation for Animal Health, Weybridge, UK.Google Scholar
Villanúa, D., Höfle, U., Pérez-Rodríguez, L. and Gortázar, C. (2006). Trichomonas gallinae in wintering Common Wood Pigeons Columba palumbus in Spain. Ibis 148, 641648. doi: 10.1111/j.1474-919X.2006.00561.x.CrossRefGoogle Scholar
Walker, R. L., Hayes, D. C., Sawyer, S. J., Nordhausen, R. W., van Hoosear, K. A. and BonDurant, R. H. (2003). Comparison of the 5.8S rRNA Gene and internal transcribed spacer regions of trichomonadid protozoa recovered from the bovine preputial cavity. Journal of Veterinary Diagnostic Investigation 15, 1420. doi: 10.1177/104063870301500104.CrossRefGoogle ScholarPubMed
Xiao, J. C., Xie, L. F., Fang, S. L., Gao, M. Y., Zhu, Y., Song, L. Y., Zhong, H. M. and Lun, Z. R. (2006). Symbiosis of Mycoplasma hominis in Trichomonas vaginalis may link metronidazole resistance in vitro. Parasitology Research 100, 123130.CrossRefGoogle ScholarPubMed