Hostname: page-component-8448b6f56d-xtgtn Total loading time: 0 Render date: 2024-04-24T22:26:13.744Z Has data issue: false hasContentIssue false
  • English
  • Français

Afternoon shedding of a new species of Isospora (Apicomplexa) in the endangered Regent Honeyeater (Xanthomyza phrygia)

Published online by Cambridge University Press:  28 April 2011

VICTORIA MORIN-ADELINE ,
LARRY VOGELNEST ,
NAVNEET K. DHAND ,
MICHAEL SHIELS ,
WARRICK ANGUS  and
JAN ŠLAPETA
VICTORIA MORIN-ADELINE
Affiliation:
Faculty of Veterinary Science, University of Sydney, New South Wales 2006, Australia
LARRY VOGELNEST
Affiliation:
Taronga Zoo, Taronga Conservation Society Australia, Bradleys Head Road, Mosman, New South Wales 2088, Australia
NAVNEET K. DHAND
Affiliation:
Faculty of Veterinary Science, University of Sydney, New South Wales 2006, Australia
MICHAEL SHIELS
Affiliation:
Taronga Zoo, Taronga Conservation Society Australia, Bradleys Head Road, Mosman, New South Wales 2088, Australia
WARRICK ANGUS
Affiliation:
Taronga Zoo, Taronga Conservation Society Australia, Bradleys Head Road, Mosman, New South Wales 2088, Australia
JAN ŠLAPETA*
Affiliation:
Faculty of Veterinary Science, University of Sydney, New South Wales 2006, Australia
*
*Corresponding author: McMaster Building B14, Faculty of Veterinary Science, University of Sydney, New South Wales 2006, Australia. Tel: +61 2 9251 2025. Fax: +61 2 935 17348. E-mail: jan.slapeta@sydney.edu.au
Get access Rights & Permissions [Opens in a new window]

Summary

The Regent Honeyeater (Xanthomyza phyrigia) is an endangered Australian bird species. Breeding populations have been established at Australian zoos in support of re-introduction programmes. This species is the host of a new species of Isospora (Apicomplexa). Oocysts are spherical, 25·8 (22·5–28·75) by 23·8 (20–26·25) μm with a colourless to pale yellow smooth wall undergoing rapid exogenous sporulation, 90% sporulated oocysts in 8 h at 20°C. Each oocyst contains 1 polar granule. Sporocysts are ovoid, 18·67 (17–19) by 9·49 (9–10) μm with a flat Stieda body and spherical substieda body devoid of a hyaline body. The asexual stages and sexual phase is within the enterocytes of the duodenum and jejunum. Faeces collected in the morning (AM, n=84) and in the afternoon (PM, n=90) revealed significant diurnal periodicity in oocyst shedding; 21% (18 of 84) of the AM were positive with the mean of 499 oocysts.g−1 compared to the PM with 91% (82 of 90) bird faeces positive with the mean of 129 723 oocysts.g−1. Therefore, parasite checks for these birds should be carried out in the afternoon to obtain an accurate result. The ecological significance of the high parasite burden in captive birds requires further investigation and comparison to the wild counterparts.

Keywords

coccidiaIsosporaRegent Honeyeaterhoneyeaterdiurnal sheddingoocystsrecovery programme
Type
Research Article
Information
Parasitology , Volume 138 , Issue 6 , May 2011 , pp. 713 - 724
Copyright
Copyright © Cambridge University Press 2011

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

Anwar, M. (1966). Isospora lacazei (Labbe 1893) and I. chloridis sp. n. (Protozoa - Eimeriidae) from English Sparrow (Passer domesticus) Greenfinch (Chloris chloris) and Chaffinch (Fringilla coelebs). Journal of Protozoology 13, 84–90. doi:10.1111/j.1550-7408.1966.tb01875.xGoogle Scholar
Baeta, R., Faivre, B., Motreuil, S., Gaillard, M. and Moreau, J. (2008). Carotenoid trade-off between parasitic resistance and sexual display: an experimental study in the blackbird (Turdus merula). Proceedings of the Royal Society of London, B 275, 427–434. doi:10.1098/rspb.2007.1383Google Scholar
Barta, J. R., Schrenzel, M. D., Carreno, R. and Rideout, B. A. (2005). The genus Atoxoplasma (Garnham 1950) as a junior objective synonym of the genus Isospora (Schneider 1881) species infecting birds and resurrection of Cystoisospora (Frenkel 1977) as the correct genus for Isospora species infecting mammals. Journal of Parasitology 91, 726–727. doi:10.1645/GE-3341.1Google Scholar
Belli, S. I., Smith, N. C. and Ferguson, D. J. P. (2006). The coccidian oocyst: a tough nut to crack!? Trends in Parasitology 22, 416–423. doi: 10.1016/J.Pt.2006.07.004Google Scholar
Berto, B. P., Luz, H., Flausino, W., Ferreira, I. and Lopes, C. W. G. (2009). New species of Eimeria Schneider, 1875 and Isospora Schneider, 1881 (Apicomplexa: Eimeriidae) from the short-crested flycatcher Myiarchus ferox (Gmelin) (Passeriformes: Tyrannidae) in South America. Systematic Parasitology 74, 75–80. doi:10.1007/s11230-009-9197-3CrossRefGoogle Scholar
Bird-Life-International (2008). Xanthomyza phrygia. In IUCN Red List of Threatened Species Version 2010.1. (ed. IUCN2010), www.iucnredlist.org.Google Scholar
Boughton, D. C. (1933). Diurnal gametic periodicity in avian Isospora. American Journal of Hygiene 18, 161–184.Google Scholar
Brawner, W. R. and Hill, G. E. (1999). Temporal variation in shedding of coccidial oocysts: implications for sexual-selection studies. Canadian Journal of Zoology-Revue Canadienne De Zoologie 77, 347–350. doi:10.1139/cjz-77-2-347Google Scholar
Brown, M. E., Ball, S. J. and Holman, D. (2001). The periodicity of isosporan oocyst discharge in the greenfinch (Carduelis chloris). Journal of Natural History 35, 945–948. doi: 10.1080/002229301300323875Google Scholar
Dhand, N. K. (2010). UniLogistic: A SAS macro for descriptive and univariable logistic regression analyses. Journal of Statistical Software 35, 1–15.Google Scholar
Dolnik, O. (2006). The relative stability of chronic Isospora sylvianthina (Protozoa: Apicomplexa) infection in blackcaps (Sylvia atricapilla): evaluation of a simplified method of estimating isosporan infection intensity in passerine birds. Parasitology Research 100, 155–160. doi:10.1007/s00436-006-0253-5Google Scholar
Dolnik, O. V., Palinauskas, V. and Bensch, S. (2009). Individual oocysts of Isospora (Apicomplexa: Coccidia) parasites from avian feces: from photo to sequence. Journal of Parasitology 95, 169–174. doi:10.1645/GE-1873.1CrossRefGoogle ScholarPubMed
Driskell, A. C. and Christidis, L. (2004). Phylogeny and evolution of the Australo-Papuan honeyeaters (Passeriformes, Meliphagidae). Molecular Phylogenetics and Evolution 31, 943–960. doi:10.1016/j.ympev.2003.10.017CrossRefGoogle ScholarPubMed
Duszynski, D. W. and Wilber, P. G. (1997). A guideline for the preparation of species descriptions in the Eimeriidae. The Journal of Parasitology 83, 333–336. doi:10.2307/3284470Google Scholar
Filipiak, L., Mathieu, F. and Moreau, J. (2009). Caution on the assessment of intestinal parasitic load in studying parasite-mediated sexual selection: the case of Blackbird coccidiosis. International Journal for Parasitology 39, 741–746. doi:10.1016/j.ijpara.2008.11.005Google Scholar
Franklin, D. C., Menkhorst, P. W. and Robinson, J. L. (1989). Ecology of the Regent honeyeater (Xanthomyza phrygia). Emu 89, 140–154. doi:10.1071/MU9890140Google Scholar
Garnett, S. T. and Crowley, G. M. (2000). The Action Plan for Australian Birds 2000, Environment Australia, Canberra, Australia.Google Scholar
Grulet, O., Landau, I. and Baccam, D. (1982). Les Isospora du moineau domestique: multiplicité des espéces. Annales de Parasitologie Humaine et Comparée 57, 209–235.Google Scholar
Grulet, O., Landau, I., Millet, P. and Baccam, D. (1986 a). Les Isospora du moineau I – Compléments à l’étude systématique. Annales de Parasitologie Humaine et Comparee 61, 155–160.Google Scholar
Grulet, O., Landau, I., Millet, P. and Baccam, D. (1986 b). Les Isospora du moineau II – Études sur la biologie. Annales de Parasitologie Humaine et Comparée 61, 161–192.Google Scholar
Hamilton, W. D. and Zuk, M. (1982). Heritable true fitness and bright birds: a role for parasites? Science 218, 384–387. doi: 10.1126/science.7123238Google Scholar
Higgins, P. J., Peter, J. M. and Steele, W. K. (2001). Handbook of Australian, New Zealand and Antarctic Birds: Volume Five - Tyrant-flycatchers to Chats. Oxford University Press, Melbourne, Victoria, Australia.Google Scholar
Hill, G. E. and Brawner, W. R. (1998). Melanin-based plumage coloration in the house finch is unaffected by coccidial infection. Proceedings of the Royal Society of London, B 265, 1105–1109. doi:10.1098/rspb.1998.0405CrossRefGoogle Scholar
Hõrak, P., Saks, L., Karu, U., Ots, I., Surai, P. F. and McGraw, K. J. (2004). How coccidian parasites affect health and appearance of greenfinches. Journal of Animal Ecology 73, 935–947. doi:10.1111/j.0021-8790.2004.00870.xGoogle Scholar
King, J. S., Šlapeta, J., Jenkins, D. J., Ellis, J. T. and Windsor, P. A. (2010). Australian dingoes are definitive hosts of Neospora caninum. International Journal for Parasitology 40, 945–950. doi:10.1016/j.ijpara.2010.01.008Google Scholar
Levine, N. D. (1982). Isospora passeris n. sp. from the House sparrow Passer domesticus, Isospora lacazei, and related apicomplexan protozoa. Transactions of the American Microscopical Society 101, 66–74. doi:10.2307/3225571Google Scholar
Levine, N. D. (1988). Protozoan Phylum Apicomplexa, CRC Press, Boca Raton, FL, USA.Google Scholar
Levine, N. D. and Mohan, R. N. (1960). Isospora sp. (Protozoa, Eimeriidae) from cattle and its relationship to I. lacazei of the English sparrow. Journal of Parasitology 46, 733–741. doi:10.2307/3275522Google Scholar
López, G., Figuerola, J. and Soriguer, R. (2007). Time of day, age and feeding habits influence coccidian oocyst shedding in wild passerines. International Journal for Parasitology 37, 559–564. doi:10.1016/j.ijpara.2006.12.014Google Scholar
Lozano, G. A. (2001). Carotenoids, immunity, and sexual selection: comparing apples and oranges? The American Naturalist 158, 200–203. doi:10.1086/321313Google Scholar
Martinaud, G., Billaudelle, M. and Moreau, J. (2009). Circadian variation in shedding of the oocysts of Isospora turdi (Apicomplexa) in Blackbirds (Turdus merula): An adaptative trait against desiccation and ultraviolet radiation. International Journal for Parasitology 39, 735–739. doi: 10.1016/j.ijpara.2008.11.006Google Scholar
McGraw, K. J. and Hill, G. E. (2000). Differential effects of endoparasitism on the expression of carotenoid- and melanin-based ornamental coloration. Proceedings of the Royal Society of London, B 267, 1525–1531. doi:10.1098/rspb.2000.1174Google Scholar
McGraw, K. J., MacKillop, E. A., Dale, J. and Hauber, M. E. (2002). Different colors reveal different information: how nutritional stress affects the expression of melanin- and structurally based ornamental plumage. The Journal of Experimental Biology 205, 3747–3755. doi:10.1139/z04-054Google Scholar
Misof, K. (2004). Diurnal cycle of Isospora spp. oocyst shedding in Eurasian blackbirds (Turdus merula). Canadian Journal of Zoology – Revue Canadienne De Zoologie 82, 764–768. doi:10.1139/Z04-054CrossRefGoogle Scholar
Oliver, D. L. (1988). The breeding behaviour of the endangered regent honeyeater, Xanthomyza phrygia, near Armidale, New South Wales. Australian Journal of Zoology 46, 153–170. doi:10.1071/ZO97028Google Scholar
Perrucci, S., Rossi, G. and Macchioni, G. (1998). Isospora thibetana n. sp. (Apicomplexa, Eimeriidae), a parasite of the Tibetan siskin (Serinus thibetanus=Carduelis thibetanus) (Passeriformes, Fringillidae). Journal of Eukaryotic Microbiology 45, 198–201. doi:10.1111/j.1550-7408.1998.tb04525.xCrossRefGoogle Scholar
Polley, L., Hoberg, E. and Kutz, S. (2010). Climate change, parasites and shifting boundaries. Acta Veterinaria Scandinavica 52 (Suppl. 1), S1. doi:10.1186/1751-0147-52-S1-S1Google Scholar
Rossi, G., Perrucci, S. and Macchioni, G. (1996). Isospora atrata n. sp. (Apicomplexa, Eimeriidae): A new coccidium isolated from Carduelis atrata (Passeriformes, Fringillidae). Journal of Eukaryotic Microbiology 43, 489–491. doi:10.1111/j.1550-7408.1996.tb04508.xGoogle Scholar
Schrenzel, M. D., Maalouf, G. A., Gaffney, P. M., Tokarz, D., Keener, L. L., McClure, D., Griffey, S., McAloose, D. and Rideout, B. A. (2005). Molecular characterization of isosporoid coccidia (Isospora and Atoxoplasma spp.) in passerine birds. Journal of Parasitology 91, 635–647. doi:10.1645/GE-3310Google Scholar
Sharman, P. A., Smith, N. C., Wallach, M. G. and Katrib, M. (2010). Chasing the golden egg: vaccination against poultry coccidiosis. Parasite Immunology 32, 590–598. doi: 10.1111/j.1365-3024.2010.01209.xGoogle Scholar
Stabler, R. M. and Kitzmiller, N. J. (1972). Isospora petrochelidon sp. n. (Protozoa: Eimeriidae) from Cliff swallow, Petrochelidon pyrrhonota. Journal of Protozoology 19, 248–251. doi:10.1111/j.1550-7408.1972.tb03447.xGoogle Scholar
Tamura, K., Dudley, J., Nei, M. and Kumar, S. (2007). MEGA4: Molecular Evolutionary Genetics Analysis (MEGA) software version 4.0. Molecular Biology and Evolution 24, 1596–1599. doi:10.1093/molbev/msm092Google Scholar
Thomas, R. (2009). Regent honeyeater habitat restoration project Lurg Hills, Victoria. Ecological Management & Restoration 19, 84–97. doi:10.1111/j.1442-8903.2009.00470.xGoogle Scholar
Thompson, R. C. A., Lymbery, A. J. and Smith, A. (2010). Parasites, emerging disease and wildlife conservation. International Journal for Parasitology 40, 1163–1170. doi:10.1016/j.ijpara.2010.04.009Google Scholar
Tung, K. C., Liu, J. S., Cheng, F. P., Yang, C. H., Tu, W. C., Wang, K. S., Shyu, C. L., Lai, C. H., Chou, C. C. and Lee, W. M. (2007). Study on the species-specificity of Isospora michaelbakeri by experimental infection. Acta Veterinaria Hungarica 55, 77–85. doi: 10.1556/Avet.55.2007.1.8Google Scholar
Upton, S. J., Langen, T. A. and Wright, T. F. (1995). A new species of Isospora Schneider, 1881 (Apicomplexa, Eimeriidae) from the White-Throated Magpie Jay Calocitta formosa (Passeriformes, Corvidae) from Costa-Rica. Systematic Parasitology 31, 195–199. doi:10.1007/BF00009117Google Scholar
Zahavi, A. (1975). Mate selection: a selection for a handicap. Journal of Theoretical Biology 53, 205–214. doi:10.1016/0022-5193(75)90111-3Google Scholar
Supplementary material: File

Morin-Adeline supplementary material

Morin-Adeline supplementary material

Download Morin-Adeline supplementary material(File)
File 100.9 KB