Hostname: page-component-8448b6f56d-sxzjt Total loading time: 0 Render date: 2024-04-19T09:04:56.867Z Has data issue: false hasContentIssue false
  • English
  • Français

High prevalence of Leucocytozoon spp. in the endangered yellow-eyed penguin (Megadyptes antipodes) in the sub-Antarctic regions of New Zealand

Published online by Cambridge University Press:  29 January 2013

L. S. ARGILLA ,
L. HOWE ,
B. D. GARTRELL  and
M. R. ALLEY
L. S. ARGILLA
Affiliation:
New Zealand Wildlife Health Centre, Institute of Veterinary, Animal and Biomedical Sciences, Massey University, Palmerston North, New Zealand
L. HOWE
Affiliation:
New Zealand Wildlife Health Centre, Institute of Veterinary, Animal and Biomedical Sciences, Massey University, Palmerston North, New Zealand
B. D. GARTRELL*
Affiliation:
New Zealand Wildlife Health Centre, Institute of Veterinary, Animal and Biomedical Sciences, Massey University, Palmerston North, New Zealand
M. R. ALLEY
Affiliation:
New Zealand Wildlife Health Centre, Institute of Veterinary, Animal and Biomedical Sciences, Massey University, Palmerston North, New Zealand
*
*Corresponding author: New Zealand Wildlife Health Centre, Institute of Veterinary, Animal and Biomedical Sciences, Massey University, Private Bag 11 222, Palmerston North, New Zealand. Tel: 011 64 6 356 9099. Fax: 011 64 6 350 5714. E-mail: B.Gartrell@massey.ac.nz
Get access Rights & Permissions [Opens in a new window]

Summary

Yellow-eyed penguins (YEPs) have suffered major population declines over the past 30 years, with no single cause established. Leucocytozoon was first identified in yellow-eyed penguins in 2005. During the 2008/09 breeding season, a high mortality was seen in both mainland yellow-eyed penguins as well as those on Enderby Island of the Auckland Islands archipelago. A high overall prevalence of Leucocytozoon spp. in association with a high incidence of chick mortality was observed during this period on Enderby Island. One chick had histological evidence of leucocytozoonosis with megaloschizonts in multiple organs throughout its body. In addition, a high prevalence (73·7%) of Leucocytozoon was observed by PCR in the blood of adult Enderby yellow-eyed penguins taken during the 2006/07 season. These findings were different from the low prevalence detected by PCR on the coast of the South Island (11%) during the 2008/2009 breeding session and earlier on Campbell Island (21%) during the 2006/2007 breeding session. The Leucocytozoon spp. sequences detected lead us to conclude that the Leucocytozoon parasite is common in yellow-eyed penguins and has a higher prevalence in penguins from Enderby Island than those from Campbell Island and the mainland of New Zealand. The Enderby Island yellow-eyed penguins are infected with a Leucocytozoon spp. that is genetically distinct from that found in other yellow-eyed penguin populations. The role of Leucocytozoon in the high levels of chick mortality in the yellow-eyed penguins remains unclear.

Keywords

Leucocytozoonyellow-eyed penguinEnderby IslandmortalityNew Zealand
Type
Research Article
Information
Parasitology , Volume 140 , Issue 5 , April 2013 , pp. 672 - 682
Copyright
Copyright © Cambridge University Press 2013

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.)

Footnotes

†

Current address: Wellington Zoo, Newtown, Wellington, New Zealand.

References

REFERENCES

Alley, M. R. (2005). Leucocytozoonosis in yellow-eyed penguins, Megadyptes antipodes . Kokako 12, 31–32.Google Scholar
Atkinson, C. T. and van Riper, C. (1991). Pathogenicity and epizootiology of avian haematozoa: Plasmodium, Leucocytozoon, and Haemoproteus . In Bird-Parasite Interactions (ed. Loye, J. E. and Zuk, M.), pp. 19–48. Oxford University Press, Oxford, UK.Google Scholar
Baldwin, K., Bartges, J., Buffington, T., Freeman, L. M., Grabow, M., Legred, J. and Ostwald, D. (2010). AAHA nutritional assessment guidelines for dogs and cats. Journal of the American Animal Hospital Association 46, 285–296.CrossRefGoogle ScholarPubMed
Bennett, G. F., Peirce, M. A. and Ashford, R. W. (1993). Avian hematozoa – mortality and pathogenicity. Journal of Natural History 27, 993–1001.Google Scholar
Bensch, S., Hellgren, O. and Perez-Tris, J. (2009). MalAvi: a public database of malaria parasites and related haemosporidians in avian hosts based on mitochondrial cytochrome b lineages. Molecular Ecology Resources 9, 1353–1358.Google Scholar
Boessenkool, S., Star, B., Waters, J. M. and Seddon, P. J. (2009). Multilocus assignment analyses reveal multiple units and rare migration events in the recently expanded yellow-eyed penguin (Megadyptes antipodes). Molecular Ecology 18, 2390–2400.Google Scholar
Brown, L., Cat, T. and DasGupta, A. (2001). Interval estimation for a proportion. Statistical Science 16, 101–133.CrossRefGoogle Scholar
Craig, D. A. and Crosby, T. K. (2008). Gynandromorphs of New Zealand Austrosimulium spp. (Diptera: Simuliidae). Zootaxa 1811, 57–68.CrossRefGoogle Scholar
Darby, J. T. and Seddon, P. J. (1990). Breeding biology of the yellow-eyed penguin (Megadyptes antipodes). In Penguin Biology (ed. Davis, L. S. and Darby, J. T.), pp. 45–62. Academic Press, Orlando, FL, USA.Google Scholar
Desser, S. S. and Allison, F. B. (1979). Aspects of the sporogonic development of Leucocytozoon tawaki of the Fiordland crested penguin in its primary vector, Austrosimulium ungulatum: an ultrastructural study. Journal of Parasitology 65, 737–744.Google Scholar
Desser, S. S. and Bennett, G. F. (1993). The genera Leucocytozoon, Haemoproteus and Hepatocystis . In Parasitic Protozoa (ed. Kreier, J. P.). pp. 273–307. Academic Press, New York, USA.Google Scholar
Dumbleton, L. J. (1963). The classification and distribution of the Simuliidae (Diptera) with particular reference to the genus Austrosimulium. New Zealand Journal of Science 6, 320–357.Google Scholar
Dumbleton, L. J. (1973). The genus Austrosimulium Tonnoir (Diptera: Simuliidae) with particular reference to the New Zealand fauna. New Zealand Journal of Science 1, 480–584.Google Scholar
Dunbar, M. R., Torniquist, S. and Giordano, M. R. (2003). Blood parasites in sage-grouse from Nevada and Oregon. Journal of Wildlife Diseases 39, 203–208.CrossRefGoogle ScholarPubMed
Durrant, K. L., Beadell, J. S., Ishtiaq, G. R., Graves, G. R. and Olson, S. L. (2006). Avian haematozoa in South America: a comparison of temperate and tropical zones. Ornithological Monographs 60, 98–111.Google Scholar
Fallis, A. M., Bisset, S. A. and Allison, F. R. (1976). Leucocytozoon tawaki n.sp. (Eucoccida: Leucocytozoidae) from the penguin Eudyptes pachyrhynchus, and preliminary observations on its development in Austrosimulium spp. (Diptera: Simuliidae). New Zealand Journal of Zoology 3, 11–16.Google Scholar
Fallis, A. M., Desser, S. S. and Khan, R. A. (1974). On species of Leucocytozoon . Advanced Parasitology 12, 1–67.CrossRefGoogle ScholarPubMed
Garvin, M. C., Szell, C. C. and Moore, F. R. (2006). Blood parasites of nearctic-neotropical migrant passerine birds during spring trans-Gulf migration: impact on host body condition. Journal of Parasitology 92, 990–996.CrossRefGoogle ScholarPubMed
Gill, J. M. and Darby, J. T. (1993). Deaths in yellow-eyed penguins (Megadyptes antipodes) on the Otago Peninsula during the summer of 1990. New Zealand Veterinary Journal 41, 39–42.Google Scholar
Graczyk, T. K., Cranfield, M. R., Brossy, J. J., Cockrem, J. F., Jouventin, P. and Seddon, P. J. (1995). Detection of avian malaria infections in wild and captive penguins. Journal of the Helminthological Society of Washington 62, 135–141.Google Scholar
Grindstaff, J. L., Brodie, E. D. and Ketterson, E. D. (2003). Immune function across generations: integrating mechanism and evolutionary process in maternal antibody transmission. Proceedings of the Royal Society of London, B 270, 2309–2319.CrossRefGoogle ScholarPubMed
Higgins, D., Thompson, J., Gibson, T., Thompson, J. D., Higgins, D. G. and Gibson, T. J. (1994). ClustalW: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties, and weight matrix choice. Nucleic acids Research 22.Google Scholar
Hill, A. G., Howe, L., Gartrell, B. D. and Alley, M. R. (2010). Prevalence of Leucocytozoon spp. in the endangered yellow-eyed penguin Megadyptes antipodes . Parasitology 137, 1477–1485.Google Scholar
Hsu, C., Campbell, G. R. and Levine, N. D. (1973). A checklist of the species of the genus Leucocytozoon (Apicomplexa, Plasmodiidae). Journal of Protozoology 20, 195–203.Google Scholar
Hunter, D. B., Rohner, C. and Currie, D. C. (1997). Mortality in fledgling great horned owls from black fly hematophaga and leucocytozoonosis. Journal of Wildlife Diseases 33, 486–491.CrossRefGoogle ScholarPubMed
IUCN (2011). IUCN Red List of Threatened Species. Version 2011.2. www.iucnredlist.org.Google Scholar
Jarvi, S. I., Schultz, J. J. and Atkinson, C. T. (2002). PCR diagnostics underestimate the prevalence of avian malaria (Plasmodium relictum) in experimentally infected passerines. Journal of Parasitology 88, 153–158.Google Scholar
Jones, H. I. and Shellam, G. R. (1999). The occurrence of blood-inhabiting protozoa in captive and free-living penguins. Polar Biology 21, 5–10.Google Scholar
Marchant, S. E. and Higgins, P. J. E. (1990). Handbook of Australian, New Zealand, & Antarctic Birds (HANZAB). Volume 1: Ratites to Ducks, Vol 1. Oxford University Press, Melbourne, Victoria, Australia.Google Scholar
McKinlay, B. (2001). Hoiho (Megadyptes antipodes) recovery plan 2000–2025. Department of Conservation, Wellington, New Zealand.Google Scholar
Merino, S., Moreno, J., Sanz, J. J. and Arriero, E. (2000). Are avian blood parasites pathogenic in the wild? A medication experiment in blue tits (Parus caeruleus). Proceedings of the Royal Society of London, B 267, 2507–2510.Google Scholar
Moore, P. J. (1992). Breeding biology of the yellow-eyed penguin Megadyptes antipodes on Campbell Island. Emu 92, 157–162.Google Scholar
Moore, P. J., Fletcher, D. and Amey, J. (2001). Population estimates of yellow-eyed penguins, Megadyptes antipodes, on Campbell Island, 1987–98. Emu 101, 225–236.CrossRefGoogle Scholar
Moore, P. J. and Wakelin, M. D. (1997). Diet of the yellow-eyed penguin (Megadyptes antipodes), South Island, New Zealand, 1991–1993. Marine Ornithology 25, 17–29.Google Scholar
Remple, J. D. (2004). Intracellular hematozoa of raptors: a review and update. Journal of Avian Medicine and Surgery 18, 75–88.CrossRefGoogle Scholar
Richards, F. A., Sehgal, R. N. M., Jones, H. I. and Smith, T. B. (2002). A comparative analysis of PCR-based detection methods for avian malaria. Journal of Parasitology 88, 819–822.Google Scholar
Ronquist, F. and Huelsenbeck, J. P. (2003). MrBayes 3: Bayesian phylogenetic inference under mixed models. Bioinformatics 19, 1572–1574.Google Scholar
Staszewski, V. and Siitari, H. (2010). Antibody injection in the egg yolk: maternal antibodies affect humeral immune response of the offspring. Functional Ecology 24, 1333–1341.Google Scholar
Steele, E. J. and Noblet, G. P. (1992). Schizogonic development of Leucocytozoon smithi . Journal of Protozoology 39, 530–536.Google Scholar
Sturrock, H. J. W. and Tompkins, D. M. (2007). Avian malaria (Plasmodium spp.) in yellow-eyed penguins: investigating the cause of high seroprevalence but low observed infection. New Zealand Veterinary Journal 55, 158–160.Google Scholar
Swofford, D. L. (2002). PAUP*: Phylogenetic Analysis Using Parsimony (and other Methods) 4.0. Beta, Version 10. Sinauer, Sunderland, MA, USA.Google Scholar
Valkiunas, G. (2005). Avian Malaria Parasites and other Haemosporidia. CRC Press, Boca Raton, FL, USA.Google Scholar
Valkiunas, G., Iezhova, T. A., Krizanauskiene, A., Palinauskas, V., Sehgal, R. N. M. and Bensch, S. (2008). A comparative analysis of microscopy and PCR-based detection methods for blood parasites. Journal of Parasitology 94, 1395–1401.CrossRefGoogle ScholarPubMed
Valkiunas, G., Santiago-Alarcon, D., Levin, II, Iezhova, T. A. and Parker, P. G. (2010). A new Haemoproteus species (Haemosporida: Haemoproteidae) from the endemic galapagos dove Zenaida galapagoensis, with remarks on the parasite distribution, vectors, and molecular diagnostics. Journal of Parasitology 96, 783–792.Google Scholar
Vanheezik, Y. (1990 a). Patterns and variability of growth in the yellow-eyed penguin. Condor 92, 904–912.Google Scholar
Vanheezik, Y. (1990 b). Seasonal, geographical, and age-related variations in the diet of the yellow-eyed penguin (Megadyptes antipodes). New Zealand Journal of Zoology 17, 201–212.Google Scholar
Vanheezik, Y. and Davis, L. (1990). Effects of food variability on growth rates, fledging sizes and reproductive success in the yellow-eyed penguin (Megadyptes antipodes). Ibis 132, 354–365.Google Scholar