Hostname: page-component-8448b6f56d-tj2md Total loading time: 0 Render date: 2024-04-17T01:01:31.749Z Has data issue: false hasContentIssue false

Molecular characterization of Trichomonas gallinae isolates recovered from the Canadian Maritime provinces’ wild avifauna reveals the presence of the genotype responsible for the European finch trichomonosis epidemic and additional strains

Published online by Cambridge University Press:  25 March 2015

SCOTT MCBURNEY
Affiliation:
Department of Pathology & Microbiology, Atlantic Veterinary College, University of Prince Edward Island, 550 University Avenue, Charlottetown, PE, C1A 4P3, Canada Prince Edward Island, Canada Canadian Wildlife Health Cooperative, Atlantic Region, Atlantic Veterinary College, University of Prince Edward Island, 550 University Avenue, Charlottetown, PE, C1A 4P3, Canada Prince Edward Island, Canada
WHITNEY K. KELLY-CLARK
Affiliation:
Department of Pathology & Microbiology, Atlantic Veterinary College, University of Prince Edward Island, 550 University Avenue, Charlottetown, PE, C1A 4P3, Canada Prince Edward Island, Canada Canadian Wildlife Health Cooperative, Atlantic Region, Atlantic Veterinary College, University of Prince Edward Island, 550 University Avenue, Charlottetown, PE, C1A 4P3, Canada Prince Edward Island, Canada
MARÍA J. FORZÁN
Affiliation:
Department of Pathology & Microbiology, Atlantic Veterinary College, University of Prince Edward Island, 550 University Avenue, Charlottetown, PE, C1A 4P3, Canada Prince Edward Island, Canada Canadian Wildlife Health Cooperative, Atlantic Region, Atlantic Veterinary College, University of Prince Edward Island, 550 University Avenue, Charlottetown, PE, C1A 4P3, Canada Prince Edward Island, Canada
BECKI LAWSON
Affiliation:
Institute of Zoology, Zoological Society of London, Regents Park, London NW1 4RY, UK
KEVIN M. TYLER
Affiliation:
Norwich Medical School, University of East Anglia, Norwich NR4 7TJ, UK
SPENCER J. GREENWOOD*
Affiliation:
Department of Biomedical Sciences, Atlantic Veterinary College, University of Prince Edward Island, 550 University Avenue, Charlottetown, PE, C1A 4P3, Canada Prince Edward Island, Canada
*
*Corresponding author: Department of Biomedical Sciences, Atlantic Veterinary College, University of Prince Edward Island, 550 University Avenue, Charlottetown, PE, C1A 4P3, Canada Prince Edward Island, Canada. E-mail: sgreenwood@upei.ca

Summary

Finch trichomonosis, caused by Trichomonas gallinae, emerged in the Canadian Maritime provinces in 2007 and has since caused ongoing mortality in regional purple finch (Carpodacus purpureus) and American goldfinch (Carduelis tristis) populations. Trichomonas gallinae was isolated from (1) finches and rock pigeons (Columbia livia) submitted for post-mortem or live-captured at bird feeding sites experiencing trichomonosis mortality; (2) bird seed at these same sites; and (3) rock pigeons live-captured at known roosts or humanely killed. Isolates were characterized using internal transcribed spacer (ITS) region and iron hydrogenase (Fe-hyd) gene sequences. Two distinct ITS types were found. Type A was identical to the UK finch epidemic strain and was isolated from finches and a rock pigeon with trichomonosis; apparently healthy rock pigeons and finches; and bird seed at an outbreak site. Type B was obtained from apparently healthy rock pigeons. Fe-hyd sequencing revealed six distinct subtypes. The predominant subtype in both finches and the rock pigeon with trichomonosis was identical to the UK finch epidemic strain A1. Single nucleotide polymorphisms in Fe-hyd sequences suggest there is fine-scale variation amongst isolates and that finch trichomonosis emergence in this region may not have been caused by a single spill-over event.

Type
Research Article
Copyright
Copyright © Cambridge University Press 2015 

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

REFERENCES

Anderson, N., Grahn, R., Van Hoosear, K. and BonDurant, B. (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.Google Scholar
Amin, A., Bilic, I., Liebhart, D. and Hess, M. (2014). Trichomonads in birds–a review. Parasitology 141, 733747.Google Scholar
Boal, C. and Mannan, R. (1999). Comparative breeding ecology of Cooper's hawks in urban and exurban areas of southeastern Arizona. Journal of Wildlife Management 63, 7784.Google Scholar
Bunbury, N., Jones, C., Greenwood, A. and Bell, D. (2007). Trichomonas gallinae in Mauritian columbids: implications for an endangered endemic. Journal of Wildlife Diseases 43, 399407.Google Scholar
Chi, J. F., Lawson, B., Durrant, C., Beckmann, K., John, S., Alrefaei, A. F., Kirkbride, K., Bell, D. J., Cunningham, A. A. and Tyler, K. M. (2013). The finch epidemic strain of Trichomonas gallinae is predominant in British non-passerines. Parasitology 140, 12341245.Google Scholar
Felleisen, R. (1997). Comparative sequence analysis of 5·8S rDNA genes and internal transcribed spacer (ITS) regions of trichomonadid protozoa. Parasitology 115, 111119.Google Scholar
Felsenstein, J. (1985). Confidence limits on phylogenies: an approach using the bootstrap. Evolution 39, 783791.Google Scholar
Forzán, M., Vanderstichel, R., Melekhovets, Y. and McBurney, S. (2010). Trichomoniasis in finches from the Canadian Maritime provinces – An emerging disease. Canadian Veterinary Journal 51, 391396.Google Scholar
Ganas, P., Jaskulska, B., Lawson, B., Zadravec, M., Hess, M. and Bilic, I. (2014). Multi-locus sequence typing confirms the clonality of Trichomonas gallinae isolates circulating in European finches. Parasitology 141, 652661.Google Scholar
Gerhold, R. (2009). Trichomonosis in songbirds. SCWDS Briefs from Southeastern Cooperative Wildlife Disease Study College of Veterinary Medicine 25, 67.Google Scholar
Gerhold, R., Yablsey, M., Smith, A., Ostergaard, E., Mannan, W. and Fischer, J. R. (2008). Molecular characterization of the Trichomonas gallinae morphologic complex in the United States. Journal of Parasitology 94, 13351341.Google Scholar
Gerhold, R. W., Maestas, L. P. and Harnage, P. M. (2013). Persistence of two Trichomonas gallinae isolates in chlorinated and distilled water with or without organic material. Avian Diseases 57, 681683.Google Scholar
Girard, Y. A., Rogers, K. H., Woods, L. W., Chouicha, N., Miller, W. A. and Johnson, C. K. (2014). Dual-pathogen etiology of avian trichomonosis in a declining band-tailed pigeon population. Infection, Genetics and Evolution 24, 146156.CrossRefGoogle Scholar
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.Google Scholar
Hall, T. (1999). BioEdit: a user friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucleic Acids Symposium 41, 9598.Google Scholar
Hernandez, S. M., Keel, K., Sanchez, S., Trees, E., Gerner-Smidt, P., Adams, J. K., Cheng, Y., Ray, A., Martin, G., Presotto, A., Ruder, M. G., Brown, J., Blehert, D. S., Cottrell, W., Maurer, J. J. (2013). Epidemiology of a Salmonella enterica subsp. enterica serovar Typhimurium strain associated with a songbird outbreak. Applied Environmental Microbiology 78, 72907298.Google Scholar
Jukes, T. H. and Cantor, C. R. (1969). Evolution of protein molecules. In Mammalian Protein Metabolism (ed. Munro, H. N.), pp. 21132. Academic Press, New York, USA.Google Scholar
Kocan, R. (1969). Various grains and liquid as potential vehicles of transmission for Trichomonas gallinae . Bulletin of the Wildlife Disease Association 5, 148149.Google Scholar
Lawson, B., Cunningham, A., Chantrey, J., Hughes, L., Kirkwood, J., Pennycott, T. and Simpson, V. (2006). Epidemic finch mortality. Veterinary Record 159, 367.Google Scholar
Lawson, B., Robinson, R., Neimanis, A., Handeland, K., Isomursu, M., Agren, E. O., Hamnes, I. S., Tyler, K. M., Chantrey, 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.Google Scholar
Lawson, B., Cunningham, 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.Google Scholar
Lawson, B., Robinson, R. A., Colvile, 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 B 367, 28522863.Google Scholar
National Wildlife Health Center (2002) Quarterly Wildlife Mortality Report October 2002–December 2002. United States Geological Survey. National Wildlife Heath Center, U.S.A. Available: http://www.nwhc.usgs.gov/publications/quarterly_reports/2002_qtr_4.jsp.Google Scholar
Nei, M. and Kumar, S. (2000). Molecular Evolution and Phylogenetics. Oxford University Press, New York.Google Scholar
Neimanis, A., Handeland, K., Isomursu, M., Agren, E., Mattsson, R., Hamnes, I. S., Bergsjø, B. and Hirvelä-Koski, V. (2010). First report of epizootic trichomoniasis in wild finches (Family Fringillidae) in Southern Fennoscandia. Avian Diseases 54, 136141.Google Scholar
Pennycott, T., Lawson, B., Cunningham, A., Simpson, V. and Chantrey, J. (2005). Necrotic ingluvitis in wild finches. Veterinary Record 157, 360.Google Scholar
Peters, M., Kilwinski, J., Reckling, D., Henning, K. (2009). Geha¨ufte Todesfa¨lle von wild lebenden Gru¨nfinken an Futterstellen infolge Trichomonas-gallinae-Infektionen—ein aktuelles problem in Norddeutschland. Kleintierpraxis 54, 433438.Google Scholar
Robinson, R., Lawson, B., Toms, M., Peck, K. M., Kirkwood, J. K., Chantrey, 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 8, e12215.Google Scholar
Robinson, R. A. and Clark, J. A. (2013) The Online Ringing Report: Bird ringing in Britain & Ireland in 2012 BTO, Thetford (http://www.bto.org/ringing-report.Google Scholar
Simpson, V. and Molenaar, F. (2006). Increase in trichomonosis in finches. Veterinary Record 159, 606.Google Scholar
Tamura, K., Stecher, G., Peterson, D., Filipski, A. and Kumar, S. (2013). MEGA6: molecular evolutionary genetics analysis version 6.0. Molecular Biology and Evolution 30, 27252729.Google Scholar