Hostname: page-component-8448b6f56d-xtgtn Total loading time: 0 Render date: 2024-04-23T05:32:26.854Z Has data issue: false hasContentIssue false

Blood parasites of penguins: a critical review

Published online by Cambridge University Press:  13 April 2016

RALPH ERIC THIJL VANSTREELS*
Affiliation:
Laboratório de Patologia Comparada de Animais Selvagens, Departamento de Patologia, Faculdade de Medicina Veterinária e Zootecnia, Universidade de São Paulo, Av. Prof. Dr. Orlando Marques de Paiva 87, São Paulo, SP 05508-270, Brazil
ÉRIKA MARTINS BRAGA
Affiliation:
Departamento de Parasitologia, Instituto de Ciências Biológicas, Universidade Federal de Minas Gerais, Caixa Postal 486, Avenida Antônio Carlos 6627, Pampulha, Belo Horizonte, MG 31270-901, Brazil
JOSÉ LUIZ CATÃO-DIAS
Affiliation:
Laboratório de Patologia Comparada de Animais Selvagens, Departamento de Patologia, Faculdade de Medicina Veterinária e Zootecnia, Universidade de São Paulo, Av. Prof. Dr. Orlando Marques de Paiva 87, São Paulo, SP 05508-270, Brazil
*
*Corresponding author: Laboratório de Patologia Comparada de Animais Selvagens, Departamento de Patologia, Faculdade de Medicina Veterinária e Zootecnia, Universidade de São Paulo, Av. Prof. Dr. Orlando Marques de Paiva 87, São Paulo, SP 05508-270, Brazil. E-mail: ralph_vanstreels@yahoo.com.br

Summary

Blood parasites are considered some of the most significant pathogens for the conservation of penguins, due to the considerable morbidity and mortality they have been shown to produce in captive and wild populations of these birds. Parasites known to occur in the blood of penguins include haemosporidian protozoans (Plasmodium, Leucocytozoon, Haemoproteus), piroplamid protozoans (Babesia), kinetoplastid protozoans (Trypanosoma), spirochete bacteria (Borrelia) and nematode microfilariae. This review provides a critical and comprehensive assessment of the current knowledge on these parasites, providing an overview of their biology, host and geographic distribution, epidemiology, pathology and implications for public health and conservation.

Type
Review Article
Copyright
Copyright © Cambridge University Press 2016 

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

Alley, M. R., Morgan, K. J., Gill, J. M. and Hocken, A. G. (2004). Diseases and causes of mortality in yellow-eyed penguins, Megadyptes antipodes. Kokako 11, 1823.Google Scholar
Allison, F. R., Desser, S. S. and Whitten, L. K. (1978). Further observations on the life cycle and vectors of the haemosporidian Leucocytozoon tawaki and its transmission to the Fiordland crested penguin. New Zealand Journal of Zoology 5, 371374.Google Scholar
Anderson, R. C. (2000). Nematode Parasites of Vertebrates: their Development and Transmission. CABI Publishing, New York, USA.CrossRefGoogle Scholar
Argilla, L. S., Howe, L., Gartrell, D. and Alley, M. R. (2013). High prevalence of Leucocytozoon spp. in the endangered yellow-eyed penguin (Megadyptes antipodes) in the sub-Antarctic regions of New Zealand. Parasitology 140, 672682.Google Scholar
Atkinson, C. T. (2008 a). Haemoproteus. In Parasitic Diseases of Wild Birds (ed. Atkinson, C. T., Thomas, N. J. and Hunter, D. B.), pp. 1334. Wiley-Blackwell, Ames, USA.Google Scholar
Atkinson, C. T. (2008 b). Avian malaria. In Parasitic Diseases of Wild Birds (ed. Atkinson, C. T., Thomas, N. J. and Hunter, D. B.), pp. 3553. Wiley-Blackwell, Ames, USA.Google Scholar
Atkinson, C. T. and Lapointe, D. A. (2009). Introduced avian diseases, climate change, and the future of Hawaiian honeycreepers. Journal of Avian Medicine and Surgery 23, 5363.Google Scholar
Atkinson, C. T. and Van Riper, C. III (1991). Pathogenicity and epizootiology of avian haematozoa: Plasmodium, Leucocytozoon, and Haemoproteus. In Bird-Parasite Interactions: Ecology, Evolution and Behaviour (ed. Loye, J. E. and Zuk, M.), pp. 1948. Oxford University Press, New York, USA.Google Scholar
Atlas of Living Australia (ALA) (2014). Records of Hippoboscidae in the Queen Victoria Museum and Art Gallery. Queen Victoria Museum and Art Gallery, Inveresk, Australia. http://bie.ala.org.au/species/hippoboscidae/.Google Scholar
Aybar, C. A. V., Juri, M. J. D., De Grosso, M. S. L. and Spinelli, G. R. (2010). Species diversity and seasonal abundance of Culicoides biting midges in northwestern Argentina. Medical and Veterinary Entomology 24, 9598.CrossRefGoogle ScholarPubMed
Bak, U.-B., Park, J.-C. and Lim, Y.-J. (1984). An outbreak of malaria in penguins at the Farm-land Zoo. Korean Journal of Parasitology 22, 267272.CrossRefGoogle ScholarPubMed
Baker, J. R. (1956). Studies on Trypanosoma avium Danilewski 1885 – III. Life cycle in vertebrate and invertebrate hosts. Parasitology 46, 335352.Google Scholar
Baker, J. R. and Bird, R. G. (1968). Trypanosoma avium: fine structure of all developmental stages. Journal of Protozoology 15, 298308.CrossRefGoogle ScholarPubMed
Banks, K. L. (1978). Binding of Trypanosoma congolense to the walls of small blood vessels. Journal of Protozoology 25, 241245.Google Scholar
Barbosa, A., Benzal, J., Vidal, V., D'Amico, V., Coria, N., Diaz, J., Motas, M., Palacios, M. J., Cuervo, J. J., Ortiz, J. and Chitimia, L. (2011). Seabird ticks (Ixodes uriae) distribution along the Antarctic Peninsula. Polar Biology 34, 16211624.Google Scholar
Barbour, A. G. and Hayes, S. F. (1986). Biology of Borrelia species. Microbiological Review 50, 381400.CrossRefGoogle ScholarPubMed
Bartlett, C. M. (2008). Filarioid nematodes. In Parasitic Diseases of Wild Birds (ed. Atkinson, C. T., Thomas, N. J. and Hunter, D. B.), pp. 439462. Wiley-Blackwell, Ames, USA.CrossRefGoogle Scholar
Bartlett, C. M. and Anderson, R. C. (1986). Paronchocerca struthionus n.sp. (Nematoda: Filarioidea) from ostriches (Struthio camelus), with a redescription of Paronchocerca ciconiarum Peters, 1936 and a review of the genus. Canadian Journal of Zoology 64, 24802491.Google Scholar
Bataille, A., Fournié, G., Cruz, M., Cedeño, V., Parker, P. G., Cunningham, A. A. and Goodman, S. J. (2012). Host selection and parasite infection in Aedes taeniorhynchus, endemic disease vector in the Galápagos Islands. Infection, Genetics and Evolution 12, 18311841.Google Scholar
Beadell, J. S. and Fleischer, R. C. (2005). A restriction enzyme–based assay to distinguish between avian hemosporidians. Journal of Parasitolology 91, 683685.Google Scholar
Beadell, J. S., Ishtiaq, F., Covas, R., Melo, M., Warren, B. H., Atkinson, A. T., Bensch, S., Graves, G. R., Jhala, Y. V., Peirce, M. A., Rahmani, A. R., Fonseca, D. M. and Fleischer, R. C. (2006). Global phylogeographic limits of Hawaii's avian malaria. Proceedings of the Royal Society B 273, 29352944.CrossRefGoogle ScholarPubMed
Becker, D. A. and Holloway, H. L. (1968). A survey for Haematozoa in Antarctic vertebrates. Transactions of the American Microscopical Society 87, 354360.Google Scholar
Beier, J. C. and Stoskopf, M. K. (1980). The epidemiology of avian malaria in black-footed penguins (Spheniscus demersus). Journal of Zoo Animal Medicine 11, 99105.Google Scholar
Beier, J. C. and Trpis, M. (1981). Incrimination of natural culicine vectors which transmit Plasmodium elongatum to penguins at the Baltimore Zoo. Canadian Journal of Zoology 59, 470475.Google Scholar
Bennett, G. F., Earlé, R. A., Du Toit, H. and Huchzermeyer, F. W. (1992). A host-parasite catalogue of the Haematozoa of the sub-Saharan birds. Onderstepoort Journal of Veterinary Research 59, 173.Google Scholar
Borkent, A. (2013). World Species of Biting Midges (Diptera: Ceratopogonidae). Illinois Natural History Survey, Champaign, USA. http://wwx.inhs.illinois.edu/files/8413/4219/9566/CeratopogonidaeCatalog.pdf.Google Scholar
Botes, A. (2004). Immunological and epidemiological investigations in South African ostriches and penguins. Ph.D. thesis (Biochemistry). University of Stellenbosch, Stellenbosch, Republic of South Africa, 237 pp.Google Scholar
Brossy, J. J. (1992). Malaria in wild and captive jackass penguins Spheniscus demersus along the Southern African coast. Ostrich 63, 1012.Google Scholar
Brossy, J. J. (1993). Haemoparasites in the African (jackass) penguin (Spheniscus demersus). Penguin Conservation 1993, 20.Google Scholar
Brossy, J. J., Plös, A. L., Blackbeard, J. M. and Kline, A. (1999). Diseases acquired by captive penguins: what happens when they are released into the wild? Marine Ornithology 27, 185186.Google Scholar
Browne, T., Lalas, C., Mattern, T. and van Heezik, Y. (2011). Chick starvation in yellow-eyed penguins: evidence for poor diet quality and selective provisioning of chicks from conventional diet analysis and stable isotopes. Austral Ecology 36, 99108.Google Scholar
Buckle, K. N., Young, M. J. and Alley, M. R. (2014). Investigation of an outbreak of craniofacial deformity in yellow-eyed penguin (Megadyptes antipodes) chicks. New Zealand Veterinary Journal 2014, 18.Google Scholar
Bueno, M. G., Lopez, R. P. G., Menezes, R. M. T., Costa-Nascimento, M. J., Lima, G. F. M. C., Araújo, R. A. S., Guida, F. J. V. and Kirchgatter, K. (2010). Identification of Plasmodium relictum causing mortality in penguins (Spheniscus magellanicus) from São Paulo Zoo, Brazil. Veterinary Parasitology 173, 123127.Google Scholar
Cabana, A. L., Vanstreels, R. E. T., Xavier, M. O., Osório, L. G., Adornes, A. C., Leite, A. M., Soares, M. P., Silva-Filho, R. P., Catão-Dias, J. L. and Meireles, M. C. A. (2014). Lethal concurrent avian malaria and aspergillosis in Magellanic penguin (Spheniscus magellanicus). Boletín Chileno de Ornitología 20, 2832.Google Scholar
Campos, S. D. E., Pires, J. R., Nascimento, C. L., Dutra, G., Torres-Filho, R. A., Toma, H. K., Brener, B. and Almosny, N. R. P. (2014). Analysis of hematologic and serum chemistry values of Spheniscus magellanicus with molecular detection of avian malarial parasites (Plasmodium spp.). Pesquisa Veterinária Brasileira 34, 12361242.Google Scholar
Cannell, B. L., Krasnec, K. V., Campbell, K., Jones, H. I., Miller, R. D. and Stephens, N. (2013). The pathology and pathogenicity of a novel Haemoproteus spp. infection in wild Little Penguins (Eudyptula minor). Veterinary Parasitology 197, 7484.Google Scholar
Cannell, B. L., Krasnec, K. V., Campbell, K., Jones, H. I., Miller, R. D. and Stephens, N. (2014). Corrigendum to “The pathology and pathogenicity of a novel Haemoproteus spp. infection in wild Little Penguins (Eudyptula minor)” [Vet. Parasitol. 197 (1–2) (2013) 74–84]. Veterinary Parasitology 205, 416.CrossRefGoogle Scholar
Carvajal, E. R. and Alvarado, P. M. (2009). Pesquisa de Plasmodium spp. en pingüinos de Magallanes (Spheniscus magellanicus) de la Región de los Ríos: malaria aviar como nueva patología de interés en la avifauna local. Boletín Veterinario Oficial 10, 14.Google Scholar
Cereghetti, N., Wenker, C., Hoby, S., Müller, P., Marti, H. and Lengeler, C. (2012). Avian malaria and its prevention strategies in the Zoo Basel. In Proceedings of the Joint Annual Meeting of the Swiss Society for Infectious Diseases, p. 169. Swiss Society for Hospital Hygiene, Swiss Society for Microbiology and Swiss Society for Tropical Medicine and Parasitology, St. Gallen, Switzerland. http://kongress.imk.ch/sginf2012/untitled1Google Scholar
Chabaud, A. G. and Ball, G. H. (1964). Filarie cardiaque chez un Manchot des Galapagos. Annales de Parasitologie 39, 621626.Google Scholar
Chauvin, A., Moreau, E., Bonnet, S., Plantard, O. and Malandrin, L. (2009). Babesia and its hosts: adaptation to long-lasting interactions as a way to achieve efficient transmission. Veterinary Research 40, 118.CrossRefGoogle ScholarPubMed
Clarke, J. R. and Kerry, K. R. (1993). Diseases and parasites of penguins. Korean Journal of Polar Research 4, 7996.Google Scholar
Coles, J. D. W. A. (1941). An epizootic in seabirds: a visit to Dassen and Malgas Islands. Journal of the South African Veterinary Medical Association 12, 2330.Google Scholar
Colombelli-Negrél, D. and Kleindorfer, S. (2014). Penguin Monitoring and Conservation Activities in the Gulf St Vincent July 2013 – June 2014. Flinders University, Adelaide, Australia.Google Scholar
Cosgrove, C. L., Day, K. P. and Sheldon, B. C. (2006). Coamplification of Leucocytozoon by PCR diagnostic tests for avian malaria: a cautionary note. Journal of Parasitology 92, 13621365.CrossRefGoogle ScholarPubMed
Cranfield, M. R., Graczyk, T. K., Beall, F. B., Ialeggio, D. M., Shaw, M. L. and Skjoldager, M. L. (1994). Subclinical avian malaria infections in African black-footed penguins (Spheniscus demersus) and induction of parasite recrudescence. Journal of Wildlife Diseases 30, 372376.Google Scholar
Crawford, R. J. M., Altwegg, R., Barham, B. J., Durant, J. M., Dyer, B. M., Geldenhuys, D., Makhado, A. B., Pichegru, L., Ryan, P. G., Underhill, L. G., Upfold, L., Visagie, J., Waller, L. J. and Whittington, P. A. (2011). Collapse of South Africa's penguins in the early 21st century. African Journal of Marine Science 33, 139156.Google Scholar
Cunningham, M., Gibbs, P., Rogers, T., Spielman, D. and Walraven, E. (1993). Ecology and Health of the Little Penguin Eudyptula Minor Near Sydney: a Report Prepared for the Water Board. Taronga Zoo, Sydney, Australia.Google Scholar
Cutler, S. J. (2006). Possibilities for relapsing fever reemergence. Emerging Infectious Diseases 12, 369374.CrossRefGoogle ScholarPubMed
Desser, S. S. and Allison, F. (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, 737744.Google Scholar
Diamond, L. S. and Herman, C. M. (1954). Incidence of trypanosomes in the Canada Goose as revealed by bone marrow culture. Journal of Parasitology 40, 195202.Google Scholar
Dietrich, M., Gómez-Díaz, E. and McCoy, K. D. (2011). Worldwide distribution and diversity of seabird ticks: implications for the ecology and epidemiology of tick-borne pathogens. Vector Borne Zoonotic Diseases 11, 453470.Google Scholar
Dinhopl, N., Mostegl, M. M., Richter, B., Nedorost, N., Maderner, A., Fragner, K. and Weissenböck, H. (2011). Application of in-situ hybridization for the detection and identification of avian malaria parasites in paraffin wax-embedded tissues from captive penguins. Avian Pathology 40, 315320.Google Scholar
Dinhopl, N., Nedorost, N., Mostegl, M. M., Weissenbacher-Lang, C. and Weissenböck, H. (2015). In situ hybridization and sequence analysis reveal an association of Plasmodium spp. with mortalities in wild passerine birds in Austria. Parasitology Research 114, 14551462.Google Scholar
Domrow, R. (1979). Dermanyssine mites from Australian birds. Records of the Western Australian Museum 7, 403413.Google Scholar
Donovan, T. A., Schrenzel, M., Tucker, T. A., Pessier, A. P. and Stalis, I. H. (2008). Hepatic hemorrhage, hemocoelom, and sudden death due to Haemoproteus infection in passerine birds: eleven cases. Journal of Veterinary Diagnostic Investigation 20, 304313.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, 320357.Google Scholar
Earlé, R. A., Bennett, G. F. and Brossy, J. J. (1992). First African record of Leucocytozoon tawaki (Apicomplexa: Leucocytozoidae) from the jackass penguin Spheniscus demersus. South African Journal of Zoology 27, 8990.Google Scholar
Earlé, R. A., Huchzermeyer, F. W., Bennett, G. F. and Brossy, J. J. (1993). Babesia peircei sp. nov. from the jackass penguin. African Zoology 28, 8890.Google Scholar
Ejiri, H., Sato, Y., Sawai, R., Sasaki, E., Matsumoto, R., Ueda, M., Higa, Y., Tsuda, Y., Omori, S., Murata, K. and Yukawa, M. (2009). Prevalence of avian malaria parasite in mosquitoes collected at a zoological garden in Japan. Parasitology Research 105, 629633.Google Scholar
Ejiri, H., Sato, Y., Kim, K.-S., Hara, T., Tsuda, Y., Imura, T., Murata, K. and Yukawa, M. (2011). Entomological study on transmission of avian malaria parasites in a zoological garden in Japan: bloodmeal identification and detection of avian malaria parasite DNA from blood-fed mosquitoes. Journal of Medical Entomology 48, 600607.Google Scholar
Elbir, H., Raoult, D. and Drancourt, M. (2013). Review article: relapsing fever Borreliae in Africa. American Journal of Tropical Medicine and Hygene 89, 288292.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, 1116.Google Scholar
Fantham, H. B. and Porter, A. (1944). On a Plasmodium (Plasmodium relictum var. spheniscidae, n. var.), observed in four species of penguins. Proceeding of the Zoological Society of London 114, 279292.Google Scholar
Felippe-Bauer, M. L., Cáceres, A., Silva, C. S., Valderrama-Bazan, W., Gonzales-Perez, A. and Costa, J. M. (2008). New records of Culicoides Latreille (Diptera: Ceratopogonidae) from Peruvian Amazonian region. Biota Neotropica 8, 3338.Google Scholar
Fix, A. S., Waterhouse, C., Greiner, E. C. and Stoskopf, M. K. (1988). Plasmodium relictum as a cause of avian malaria in wild-caught Magellanic penguins (Spheniscus magellanicus). Journal of Wildlife Diseases 24, 610619.CrossRefGoogle ScholarPubMed
Fleischman, R. W., Squire, R. A., Sladen, W. J. L. and Moore, J. (1968 a). Pathologic confirmation of malaria (Plasmodium elongatum) in African penguins (Spheniscus demersus). Bulletin of the Wildlife Diseases Association 4, 133135.Google Scholar
Fleischman, R. W., Squire, R. A., Sladen, W. J. L. and Melby, E. C. Jr. (1968 b). Malaria (Plasmodium elongatum) in captive African penguins (Spheniscus demersus). Journal of the American Veterinary Medical Association 153, 928935.Google Scholar
Forrester, D. J. and Greiner, E. C. (2008). Leucocytozoonosis. In Parasitic Diseases of Wild Birds (ed. Atkinson, C. T., Thomas, N. J. and Hunter, D. B.), pp. 54107. Wiley-Blackwell, Ames, USA.Google Scholar
Friend, M. and Franson, J. C. (1999). Field Manual of Wildlife Diseases: General Field Procedures and Diseases of Birds. United States Geological Survey, Washington, USA.Google Scholar
Garamszegi, L. Z. (2010). The sensitivity of microscopy and PCR-based detection methods affecting estimates of prevalence of blood parasites in birds. Journal of Parasitology 96, 11971203.Google Scholar
Garamszegi, L. Z. (2011). Climate change increases the risk of malaria in birds. Global Change Biology 17, 17511759.Google Scholar
Gaston, K. J., Jones, A. G., Hänel, C. and Chown, S. L. (2003). Rates of species introduction to a remote oceanic island. Proceedings of the Royal Society B 270, 10911098.Google Scholar
Gauthier-Clerc, M., Jaulhac, B., Frenot, Y., Bachelard, C., Monteil, H., Le Maho, Y. and Handrich, Y. (1999). Prevalence of Borrelia burgdorferi (the Lyme disease agent) antibodies in king penguin Aptenodytes patagonicus in Crozet Archipelago. Polar Biology 22, 141143.Google Scholar
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, 3942.Google Scholar
González-Acuña, D., Hernández, J., Moreno, L., Herrman, B., Palma, R., Latorre, A., Medina-Vogel, G., Kinsella, M. J., Martín, N., Araya, K., Torres, I., Fernandez, N. and Olsén, B. (2013). Health evaluation of wild gentoo penguins (Pygoscelis papua) in the Antarctic Peninsula. Polar Biology 36, 17491760.Google Scholar
Gough, R. E., Drury, S. E., Welchman, D. B., Chitty, J. R. and Summerhays, G. E. S. (2002). Isolation of birnavirus and reovirus-like agents from penguins in the United Kingdom. Veterinary Record 151, 422424.CrossRefGoogle ScholarPubMed
Graczyk, T. K., Cranfield, M. R. and Shift, C. J. (1993). ELISA method for detecting anti-Plasmodium relictum and anti-Plasmodium elongatum antibody in infected duckling sera using Plasmodium falciparum antigens. Journal of Parasitology 79, 879885.Google Scholar
Graczyk, T. K., Cranfield, M. R., Mccutchan, T. F. and Bicknese, E. J. (1994 a). Characteristics of naturally acquired avian malaria infections in naive juvenile African black-footed penguins (Spheniscus demersus). Parasitology Research 80, 634637.Google Scholar
Graczyk, T. K., Cranfield, M. R., Skjoldager, M. L. and Shaw, M. L. (1994 b). An ELISA for detecting anti-Plasmodium spp. antibodies in African black-footed penguins (Spheniscus demersus). Journal of Parasitology 80, 6066.Google Scholar
Graczyk, T. K., Shaw, M. L., Cranfield, M. R. and Beall, F. B. (1994 c). Hematologic Characteristics of avian malaria cases in African black-footed penguins (Spheniscus demersus) during the first outdoor exposure season. Journal of Parasitology 80, 302308.Google Scholar
Graczyk, T. K., Cranfield, M. R., Shaw, M. L. and Craig, L. E. (1994 d). Maternal antibodies against Plasmodium spp. in African black-footed penguin (Spheniscus demersus) chicks. Journal of Wildlife Diseases 30, 365371.Google Scholar
Graczyk, T. K., Brossy, J. J., Plös, A. and Stoskopf, M. K. (1995 a). Avian malaria seroprevalence in Jackass penguins (Spheniscus demersus) in South Africa. Journal of Parasitology 81, 703707.Google Scholar
Graczyk, T. K., Cockrem, J. F., Cranfield, M. R., Darby, J. T. and Moore, P. (1995 b). Avian malaria seroprevalence in wild New Zealand penguins. Parasite 2, 401405.Google Scholar
Graczyk, T. K., Cranfield, M. R., Brossy, J. J., Cockrem, J. F., Jouventin, P. and Seddon, P. J. (1995 c). Detection of avian malaria infections in wild and captive penguins. Journal of the Helminthological Society of Washington 62, 135141.Google Scholar
Graczyk, T. K., Brossy, J. J., Sanders, M. I., Dubey, J. P., Plös, A. and Stoskopf, M. K. (1996). Immunological survey of babesiosis (Babesia peircei) and toxoplasmosis in Jackass penguins in South Africa. Parasite 4, 313319.Google Scholar
Greenberg, A. E., Schable, C. A., Sulzer, A. J., Collins, W. E. and Nguyhen-Dinh, P. (1986). Evaluation of serological cross-reactivity between antibodies to Plasmodium and HLTV-III/LAV. Lancet 2, 247249.Google Scholar
Grilo, M. L. A. (2014). Characterization of infection by malaria parasites in penguins housed in zoological collections. Master's degree dissertation (Veterinary Medicine). Lisbon University, Portugal.Google Scholar
Grim, K. C., van der Merwe, E., Sullivan, M., Parsons, N., McCutchan, T. F. and Cranfield, M. (2003). Plasmodium juxtanucleare associated with mortality in black-footed penguins (Spheniscus demersus) admitted to a rehabilitation center. Journal of Zoo and Wildlife Medicine 34, 250255.Google Scholar
Grim, K. C., McCutchan, T., Li, J., Sullivan, M., Graczyk, T. K., McConkey, G. and Cranfield, M. (2004). Preliminary results of an anticircumsporozoite DNA vaccine trial for protection against avian malaria in captive African Black-footed penguins. Journal of Zoo and Wildlife Medicine 35, 154161.Google Scholar
Griner, L. A. and Sheridan, B. W. (1967). Malaria (Plasmodium relictum) in penguins at the San Diego Zoo. Veterinary Clinical Pathology 1, 717.Google Scholar
Grünberg, W. and Kutzer, E. (1963). Infektionen mit Plasmodium praecox bei Humboldt- (Spheniscus humboldti) und Brillenpinguinen (Spheniscus magellanicus) (in German). Zentralblatt für Bakteriologie, Parasitenkunde, Infektionskrankheiten und Hygiene 189, 511520.Google Scholar
Guichard, S., Guis, H., Tran, A., Garros, C., Balenghien, T. and Kriticos, D. J. (2014). Worldwide niche and future potential distribution of Culicoides imicola, a major vector of bluetongue and african horse sickness viruses. Plos ONE 9, e112491.Google Scholar
Haag, J., O'hUigin, C. and Overath, P. (1998). The molecular phylogeny of trypanosomes- evidence for an early divergence of the Salivaria. Molecular and Biochemical Parasitology 91, 3749.Google Scholar
Hamilton, P. B., Stevens, J. R., Gaunt, M. W., Gidley, J. and Gibson, W. C. (2004). Trypanosomes are monophyletic: evidence from genes for glyceraldehyde phosphate dehydrogenase and small subunit ribosomal RNA. International Journal of Parasitology 34, 13931404.Google Scholar
Hänel, C., Chown, S. L. and Davies, L. (1998). Records of alien insect species from sub-Antarctic Marion and South Georgia Islands. African Entomology 6, 366369.Google Scholar
Harmon, W., Harbecker, A. and Clark, W. A. (1985). Report to the Charles Darwin Research Station. Charles Darwin Research Station, Puerto Ayora, Ecuador.Google Scholar
Harvey, C. and Alley, M. R. (2008). Current veterinary laboratory surveillance of avian haemoparasitic diseases in New Zealand. Kokako 15, 1519.Google Scholar
Hellgren, O., Waldenström, J. and Bensch, S. (2004). A new PCR assay for simultaneous studies of Leucocytozoon, Plasmodium, and Haemoproteus from avian blood. Journal of Parasitology 90, 797802.Google Scholar
Herman, C. M., Kocan, R. M., Snyder, E. L. and Knisley, J. O. (1968). Plasmodium elongatum from a penguin. Bulletin of the Wildlife Diseases Association 4, 132.Google Scholar
Herman, C. M., Gray, C., Knisley, J. O. Jr. and Kocan, R. M. (1974). Malarial infections in the avian collection of the National Zoo in Washington, D.C., USA and in indigenous birds. In Proceedings of the International Congress of Parasitology, Munich, Germany.Google Scholar
Hill, A. G. (2008). An investigation of Leucocytozoon in the endangered yellow-eyed penguin (Megadyptes antipodes). Master's degree dissertation (Veterinary Science). Massey University, New Zealand.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, 14771485.Google Scholar
Hocken, A. G. (2005). Necropsy findings in yellow-eyed penguins (Megadyptes antipodes) from Otago, New Zealand. New Zealand Journal of Zoology 32, 18.Google Scholar
Holder, P. (1999). The mosquitoes of New Zealand and their animal disease significance. Surveillance 26, 1215.Google Scholar
Holmstad, P. R., Anwar, A., Iezhova, T. and Skorping, A. (2003). Standard sampling techniques underestimate prevalence of avian hematozoa in willow ptarmigan (Lagopus lagopus). Journal of Wildlife Diseases 39, 354358.Google Scholar
Hornby, H. E. and Bailey, H. W. (1931). Diurnal variation in the concentration of Trypanosoma congolense in the blood-vessels of the Ox's ear. Transactions of the Royal Society of Tropical Medicine and Hygiene 24, 557564.Google Scholar
Huff, C. G. (1942). Schizogony and gametocyte development in Leucocytozoon simondi, and comparisons with Plasmodium and Haemoproteus. Journal of Infectious Diseases 71, 1832.Google Scholar
Huff, G. C. and Shiroishi, T. S. (1962). Natural infection of Humboldt's penguin with Plasmodium elongatum. Journal of Parasitology 48, 495.Google Scholar
International Union for Conservation of Nature (IUCN) (2015). The IUCN Red List of Threatened Species Version 2015-3. International Union for Conservation of Nature, Gland, Switzerland. http://www.iucnredlist.org/.Google Scholar
Jones, H. I. and Shellam, G. R. (1999 a). The occurrence of blood-inhabiting protozoa in captive and free-living penguins. Polar Biology 21, 510.Google Scholar
Jones, H. I. and Shellam, G. R. (1999 b). Blood parasites in penguins, and their potential impact on conservation. Marine Ornithology 27, 181184.Google Scholar
Jones, H. I. and Woehler, E. J. (1989). A new species of blood trypanosome from little penguins (Eudyptula minor) in Tasmania. Journal of Protozoology 36, 389390.Google Scholar
Jouventin, P., Cuthbert, R. J. and Ottvall, R. (2006). Genetic isolation and divergence in sexual traits: evidence for the northern rockhopper penguin Eudyptes moseleyi being a sibling species. Molecular Ecology 15, 34133423.Google Scholar
Kearney, M., Porter, W. P., Williams, C., Ritchie, S. and Hoffmann, A. A. (2009). Integrating biophysical models and evolutionary theory to predict climatic impacts on species’ ranges: the dengue mosquito Aedes aegypti in Australia. Functional Ecology 23, 528538.Google Scholar
Kerry, K. R., Irvine, L., Beggs, A. and Watts, J. (2009). An unusual mortality event among Adélie penguins in the vicinity of Mawson station, Antarctica. In Health of Antarctic Wildlife: a Challenge for Science and Policy (ed. Kerry, K. R. and Riddle, M. J.), pp. 107112. Springer, London, UK.Google Scholar
King, S. D., Harper, G. A., Wright, J. B., McInnes, J. C., van der Lubbe, J. E., Dobbins, M. L. and Murray, S. J. (2012). Site-specific reproductive failure and decline of a population of the endangered yellow-eyed penguin: a case for foraging habitat quality. Marine Ecology Progress Series 467, 233244.Google Scholar
Ko, K.-N., Kang, S.-C., Jung, J.-Y., Bae, J.-H. and Kim, J.-H. (2008). Avian malaria associated with Plasmodium spp. infection in a penguin in Jeju Island. Korean Journal of Veterinary Research 48, 197201.Google Scholar
Laird, M. (1950). Some blood parasites of New Zealand. Zoology Publications from Victoria University of Wellington 5, 120.Google Scholar
Laird, M. (1952). Protozoological studies at Macquarie Islands. Transactionsof the Royal Society of New Zealand 79, 583588.Google Scholar
Laird, M. (1961). A lack of avian and mammalian Haematozoa in the Antarctic and Canandian Arctic. Canadian Journal of Zoology 39, 209213.Google Scholar
Laird, M. and Van Riper, C. (1981). Questionable reports of Plasmodium from birds in Hawaii, with the recognition of P. relictum ssp. capistranoae (Russel, 1932) as the avian malaria parasite there. In Parasitological Topics: a Presentation Volume to P.C.C. Garnham, F.R.S. on the Occasion of his 80th Birthday 1981 (ed. Canning, E. U.), pp. 159165. Allen Press, Lawrence, USA.Google Scholar
Landcare Research (2015). Species in NZ: Ochlertatus (Halaedes) Australis. Landcare Research, Lincoln, New Zealand. http://www.landcareresearch.co.nz/science/plants-animals-fungi/animals/invertebrates/invasive-invertebrates/mosquitoes/species-in-nz/ochlertatus-australis.Google Scholar
Leclerc, A., Chavatte, J.-M., Landau, I., Snounou, G. and Petit, T. (2014). Morphologic and molecular study of hemoparasites in wild corvids and evidence of sequence identity with Plasmodium DNA detected in captive black-footed penguins (Spheniscus demersus). Journal of Zoo and Wildlife Medicine 45, 577588.Google Scholar
Levin, I. I. and Parker, P. G. (2011). Haemosporidian parasites: impacts on avian hosts. In Fowler's Zoo and Wild Animal Medicine – Current Therapy, Volume 7 (ed. Miller, R. E. and Fowler, M.), pp. 356363. Elsevier Saunders, St. Louis, USA.Google Scholar
Levin, I. I., Outlaw, D. C., Vargas, F. H. and Parker, P. G. (2009). Plasmodium blood parasite found in endangered Galapagos penguins (Spheniscus mendiculus). Biological Conservation 142, 31913195.Google Scholar
Levin, I. I., Valkiūnas, G., Santiago-Alarcon, D., Cruz, L. L., Iezhova, T. A., O'Brien, S. L., Hailer, F., Dearborn, D., Shcreiber, E. A., Fleischer, R. C., Ricklefs, R. E. and Parker, P. G. (2011). Hippoboscid-transmitted Haemoproteus parasites (Haemosporida) infect Galapagos pelecaniform birds: evidence from molecular and morphological studies, with a description of Haemoproteus iwa. International Journal of Parasitology 41, 10191027.Google Scholar
Levin, I. I., Valkiūnas, G., Iezhova, T. A., O'Brien, S. L. and Parker, P. G. (2012). Novel Haemoproteus species (Haemosporida: Haemoproteidae) from the swallow-tailed gull (Lariidae), with remarks on the host range of hippoboscid-transmitted avian hemoproteids. Journal of Parasitology 98, 847854.Google Scholar
Levin, I. I., Zwiers, P., Deem, S. L., Geest, E. A., Higashiguchi, J. M., Iezhova, T. A., Jiménez-Uzcátegui, G., Kim, D. H., Morton, J. P., Perlut, N. G., Renfrew, R. B., Sari, E. H. R., Valkiūnas, G. and Parker, P. G. (2013). Multiple lineages of avian malaria parasites (Plasmodium) in the Galapagos islands and evidence for arrival via migratory birds. Conservation Biology 27, 13661377.Google Scholar
Magnarelli, L. A., Anderson, J. F. and Johnson, R. C. (1987). Cross-reactivity in serological tests for Lyme disease and other spirochetal infections. Journal of Infectious Diseases 156, 183188.Google Scholar
Manrique-Saide, P., Bolio-González, M., Sauri-Arceo, C., Dzib-Florez, S. and Zapata-Peniche, A. (2008). Ochlerotatus taeniorhynchus: a probable vector of Dirofilaria immitis in coastal areas of Yucatan, Mexico. Journal of Medical Entomology 45, 169171.Google Scholar
Martinsen, E. S. and Perkins, S. L. (2013). The diversity of Plasmodium and other Haemosporidians: the interesection of taxonomy, phylogenetics and genomics. In Malaria Parasites: Comparative Genomics, Evolution and Molecular Biology (ed. Carlton, J. M., Perkins, S. L. and Deitsch, K. W.), pp. 115. Caister Academic Press, Norfolk, USA.Google Scholar
Martinsen, E. S., Perkins, S. L. and Schall, J. J. (2008). A three-genome phylogeny of malaria parasites (Plasmodium and closely related genera): evolution of life-history traits and host switches. Molecular Phylogenetics and Evolution 47, 261273.Google Scholar
Mawson, P. M., Angel, L. M. and Edmonds, S. J. (1986). A checklist of helminths from Australian birds. Records of the Australian Museum 19, 219325.Google Scholar
McConkey, G. A., Li, J., Rogers, M. J., Seeley, D. C., Graczyk, T. K., Cranfield, M. R. and McCutchan, T. C. (1996). Parasite diversity in an endemic region for avian malaria and identification of a parasite causing penguin mortality. Journal of Eukaryotic Microbiology 43, 393399.Google Scholar
McDonald, S. P. (2012). Parasitology of the yellow-eyed penguin (Megadyptes antipodes). Master's degree dissertation (Science). University of Otago, New Zealand.Google Scholar
McDowell, J. V., Tran, E., Hamilton, D., Wolfgang, J., Miller, K. and Marconi, R. T. (2003). Analysis of the ability of spirochete species associated with relapsing fever, avian borreliosis, and epizootic bovine abortion to bind factor H and cleave C3b. Journal of Clinical Microbiology 41, 39053910.Google Scholar
Medlock, J. M., Schaffner, F. and Fontenille, D. (2010). Invasive Mosquitoes in the European Associate Continental and Overseas Territories. European Centre for Disease Prevention and Control, Solna, Sweden. http://www.ecdc.europa.eu/en/activities/sciadvice/_layouts/forms/review_dispform.aspx?ID=212&List=a3216f4c-f040-4f51-9f77-a96046dbfd72.Google Scholar
Meile, R. J., Lacy, R. C., Vargas, F. H. and Parker, P. G. (2013). Modeling Plasmodium parasite arrival in the Galapagos Penguin (Spheniscus mendiculus). Auk 130, 440448.Google Scholar
Merino, S., Barbosa, A., Moreno, J. and Potti, J. (1996). Absence of Haematozoa in a wild chinstrap penguin Pygoscelis antarctica population. Polar Biology 18, 227228.Google Scholar
Merkel, J., Jones, H. I., Whiteman, N. K., Gottdenker, N., Vargas, H., Travis, E. K., Miller, R. E. and Parker, P. G. (2007). Microfilariae in Galápagos penguins (Spheniscus mendiculus) and flightless cormorants (Phalacrocorax harrisi). Journal of Parasitology 93, 495503.Google Scholar
Miller, G. D., Hofkin, B. V., Snell, H., Hahn, A. and Miller, R. D. (2001). Avian malaria and Marek's disease: potential threats to Galapagos penguins Spheniscus mendiculus. Marine Ornithology 29, 4346.Google Scholar
Molyneux, D. H. (1977). Vector relationships in the Trypanosomatidae. Advances in Parasitology 15, 182.Google Scholar
Molyneux, D. H., Cooper, J. E. and Smith, W. J. (1983). Studies on the pathology of an avian trypanosome (T. bouffardi) infection in experimentally infected canaries. Parasitology 87, 4954.Google Scholar
Muñoz-Leal, S. and González-Acuña, D. (2015). The tick Ixodes uriae (Acari: Ixodidae): hosts, geographical distribution, and vector roles. Ticks and Tick Borne Diseases 6, 843868.Google Scholar
Murray, M. D. (1975). Potential vectors of bluetongue in Australia. Australian Veterinary Journal 51, 216220.CrossRefGoogle ScholarPubMed
Naus, C. W. A., Jones, F. M., Satti, M. Z., Joseph, S., Riley, E. M., Kimani, G., Mwatha, J. K., Kariuki, C. H., Ouma, J. H., Kabatereine, N. B., Vennervald, B. J. and Dunne, D. W. (2003). Serological responses among individuals in areas where both schistosomiasis and malaria are endemic: cross-reactivity between Schistosoma mansoni and Plasmodium falciparum. Journal of Infectious Diseases 187, 12721282.Google Scholar
Oliver, W. R. B. (1953). The crested penguins of New Zealand. Emu 53, 185187.Google Scholar
Olsén, B., Jaenson, T. G. T. and Bergström, S. (1995 a). Prevalence of Borrelia burgdorferi sensu lato-infected ticks on migrating birds. Applied Environmental Microbiology 61, 30823087.Google Scholar
Olsén, B., Duffy, D. C., Jaenson, T. G. T., Gylfe, A., Bonnedahl, J. and Bergström, S. (1995 b). Transhemispheric exchange of Lyme disease spirochetes by seabirds. Journal of Clinical Microbiology 33, 32703274.Google Scholar
Olsén, B. (2007). Borrelia. In Infectious Diseases of Wild Birds (ed. Thomas, N. J., Hunter, D. B. and Atkinson, C. T.), pp. 341351. Blackwell, Ames, USA.Google Scholar
Palmer, J. L., McCutchan, T. F., Vargas, F. H., Deem, S. L., Cruz, M., Hartman, D. A. and Parker, P. G. (2013). Seroprevalence of malarial antibodies in Galapagos penguins (Spheniscus mendiculus). Journal of Parasitology 99, 770776.Google Scholar
Paperna, I. and Gill, H. (2003). Schizogonic stages of Haemoproteus from Wenyons Baghdad sparrows are also found in Passer domesticus biblicus in Israel. Parasitology Research 91, 486490.Google Scholar
Parker, P. G., Whiteman, N. K. and Miller, R. E. (2006). Conservation medicine on the Galapagos Islands: partnerships among behavioral, population and veterinary scientists. Auk 123, 625638.Google Scholar
Parsons, N. J. and Underhill, L. G. (2005). Oiled and injured African penguins Spheniscus demersus and other seabirds admitted for rehabilitation. African Journal of Marine Science 27, 289296.Google Scholar
Peirce, M. A. (2000). A taxonomic review of avian piroplasms of the genus Babesia Starcovici, 1893. Journal of Natural History 34, 317332.Google Scholar
Peirce, M. A. (2005). A checklist of the valid avian species of Babesia (Apicomplexa: Piroplasmorida), Haemoproteus, Leucocytozoon (Apicomplexa: Haemosporida), and Hepatozoon (Apicomplexa: Haemogregarinidae). Journal of Natural History 39, 36213632.Google Scholar
Peirce, M. A., Greenwood, A. G. and Stidworthy, M. F. (2005). Leucocytozoon in captive penguins. Veterinary Record 157, 819820.Google Scholar
Penrith, M.-L., Huchzermeyer, F. W., Wet, S. C. and Penrith, M. J. (1994). Concurrent infection with Clostridium and Plasmodium in a captive king penguin Aptenodytes patagonicus. Avian Pathology 23, 373380.Google Scholar
Ploeg, M., Ultee, T. and Kik, M. (2011). Disseminated toxoplasmosis in black-footed penguins (Spheniscus demersus). Avian Diseases 55, 701703.Google Scholar
Quillfeldt, P., Martínez, J., Hennicke, J., Ludynia, K., Gladbach, A., Masello, J. F., Riou, S. and Merino, S. (2010). Hemosporidian blood parasites in seabirds - a comparative genetic study of species from Antarctic to tropical habitats. Naturwissenschaften 97, 809817.Google Scholar
Raethel, H. S. (1960). Plasmodieninfektionen bei Pinguinen des Berliner Zoologischen Gartens und ihre Bedeutung für die Pinguinhaltung (in German). Kleintier-Praxis 5, 6470.Google Scholar
Ratcliffe, H. L. and Worth, C. B. (1951). Toxoplasmosis of captive wild birds and mammals. American Journal of Pathology 27, 655667.Google Scholar
Redrobe, S. (2000). Plasmodium infection in a group of captive penguins including rockhopper penguins, king penguins, gentoo penguins, Macaroni penguin. In Proceedings of the Scientific Meeting of the European Association of Zoo and Wildlife Veterinarians, Paris, France.Google Scholar
Reeves, W. K., Adler, P. H., Rätti, O., Malmqvist, B. and Strasevicius, D. (2007). Molecular detection of Trypanosoma (Kinetoplastida: Trypanosomatidae) in black flies (Diptera: Simuliidae). Comparative Parasitology 74, 171175.Google Scholar
Rewell, R. E. (1948). Report of the pathologist for the year 1947. Proceedings of the Zoological Society of London 118, 501514.Google Scholar
Rodhain, J. (1939). L'infection a Plasmodium relictum chez les pingouins (in French). Annales de Parasitologie Humaine et Comparée 17, 139157.Google Scholar
Rodhain, J. and Andrianne, V.-F. (1952). Deux nouveaux cas d'infestation par Plasmodium chez des pingouins (in French). Annales de Parasitologie Humaine et Comparée 32, 573577.Google Scholar
Rollinson, D. P., Reynolds, C. and Paijmans, D. M. (2013). Vagrant Northern rockhopper penguin at Soetwater beach, Western Cape. Ornithological Observations 4, 3638.Google Scholar
Sallaberry-Pincheira, N., González-Acuña, D., Herrera-Tello, Y., Dantas, G. P. M., Luna-Jorquera, G., Frere, E., Valdés-Velasquez, A., Simeone, A. and Vianna, J. A. (2015). Molecular epidemiology of avian malaria in wild breeding colonies of Humboldt and Magellanic penguins in South America. EcoHealth 12, 267277.Google Scholar
Sano, Y., Aoki, M., Takahashi, H., Miura, M., Komatsu, M., Abe, Y., Kakino, J. and Itagaki, T. (2005). The first record of Dirofilaria immitis infection in a Humboldt penguin, Spheniscus humboldti. Journal of Parasitology 81, 12351237.Google Scholar
Schnittger, L., Rodriguez, A. E., Florin-Christensen, M. and Morrison, D. A. (2012). Babesia: a world emerging. Infection, Genetics and Evolution 12, 17881809.Google Scholar
Schramm, F., Gauthier-Clerc, M., Fournier, J.-C., McCoy, K. D., Barthel, C., Postic, D., Handrich, Y., Le Maho, Y. and Jaulhac, B. (2014). First detection of Borrelia burgdorferi sensu lato DNA in king penguins (Aptenodytes patagonicus halli). Ticks and Tick Borne Disease 5, 939942.Google Scholar
Scott, H. H. (1927). Report on the deaths occurring in the Society's Gardens during the year 1926. Proceedings of the Zoological Society of London 97, 173198.Google Scholar
Sehgal, R. N. M., Jones, H. I. and Smith, T. B. (2001). Host specificity and incidence of Trypanosoma in some African rainforest birds: a molecular approach. Molecular Ecology 10, 23192327.Google Scholar
Sergent, N., Rogers, T. and Cunningham, M. (2004). Influence of biological and ecological factors on hematological values in wild Little Penguins, Eudyptula minor. Comparative Biochemistry and Physiology 138, 333339.Google Scholar
Sherley, R. B., Waller, L. J., Strauss, V., Geldenhuys, D., Underhill, L. G. and Parsons, N. J. (2014). Hand-rearing, release and survival of African penguin chicks abandoned before independence by moulting parents. Plos ONE 9, e110794.Google Scholar
Siers, S., Merkel, J., Batailler, A., Vargas, F. H. and Parker, P. G. (2010). Ecological correlates of microfilariae prevalence in endangered Galápagos birds. Journal of Parasitology 96, 259272.Google Scholar
Silveira, P., Damatta, R. A. and Dagosto, M. (2009). Hematological changes of chickens experimentally infected with Plasmodium (Bennettinia) juxtanucleare. Veterinary Parasitology 162, 257262.Google Scholar
Silveira, P., Belo, N. O., Lacorte, G. A., Kolesnikovas, C. K. M., Vanstreels, R. E. T., Steindel, M., Catão-Dias, J. L., Valkiūnas, G. and Braga, É. M. (2013). Parasitological and new molecular-phylogenetic characterization of the malaria parasite Plasmodium tejerai in South American penguins. Parasitology International 62, 165171.Google Scholar
Simón, F., López-Belmonte, J., Marcos-Atxutegi, C., Morchón, R. and Martín-Pacho, J. R. (2005). What is happening outside North America regarding human dirofilariasis. Veterinary Parasitology 133, 181189.Google Scholar
Sinclair, B. J. (2014). CDF checklist of Galapagos flies. In Charles Darwin Foundation Galapagos Species Checklist (ed. Bungartz, F., Herrera, H., Jaramillo, P., Tirado, N., Jiménez-Uzcátegui, G., Ruiz, D., Guézou, A. and Ziemmeck, F.). Charles Darwin Foundation, Puerto Ayora, Ecuador. http://www.darwinfoundation.org/datazone/checklists/.Google Scholar
Sladen, W. J. L., Gailey-Phipps, J. J. and Divers, B. J. (1979). Medical problems and treatment of penguins at the Baltimore Zoo. International Zoo Yearbook 19, 202209.Google Scholar
Snell, A. E. (2005). The discovery of the exotic mosquito Ochlerotatus australis and the endemic Opifex fuscus (Diptera: Culicidae) on North East Island, Snares Islands. Weta 30, 1013.Google Scholar
Spinelli, G. R. and Martinez, M. E. (1991). The genus Culicoides in Uruguay (Diptera: Ceratopogonidae). Insecta Mundi 5, 175179.Google Scholar
Stevenson, C. and Woehler, E. J. (2007). Population decreases in little penguins Eudyptula minor in southeastern Tasmania, Australia, over the past 45 years. Marine Ornithology 35, 7176.Google Scholar
Stoskopf, M. K. and Beier, J. (1979). Avian malaria in African black-footed penguins. Journal of the American Veterinary Medical Association 175, 944947.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, 158160.Google Scholar
Sturrock, H. J. W. and Tompkins, D. M. (2008). Avian malaria parasites (Plasmodium spp.) in Dunedin and on the Otago Peninsula, southern New Zealand. New Zealand Veterinary Journal 32, 98102.Google Scholar
Szöllősi, E., Hellgren, O. and Hasselquist, D. (2008). A cautionary note on the use of nested PCR for parasite screening – an example from avian blood parasites. Journal of Parasitology 94, 562564.Google Scholar
Tabachnick, W. J. (2004). Culicoides and the global epidemiology of bluetongue virus infection. Veterinaria Italiana 40, 144150.Google Scholar
Thiart, H. (2005). Immunological and epidemiological investigations into avian malaria in the African penguin during rehabilitation and in breeding colonies. Master's degree dissertation (Biochemistry). University of Stellenbosch, South Africa.Google Scholar
Tollini, J., Brocksen, A. and Sureda, N. (2000). Prevention and treatment of avian malaria in a captive penguin colony. Penguin Conservation 13, 2831.Google Scholar
Tompkins, D. M. and Gleeson, D. M. (2006). Relationship between avian malaria distribution and an exotic invasive mosquito in New Zealand. Journal of the Royal Society of New Zealand 36, 5162.Google Scholar
Valkiūnas, G. (2005). Avian Malaria Parasites and Other Haemosporidia. CRC Press, Boca Ratón, USA.Google Scholar
Valkiūnas, G., Zehtindjiev, P., Dimitrov, D., Križanauskienė, A., Iezhova, T. A. and Bensch, S. (2008). Polymerase chain reaction-based identification of Plasmodium (Huffia) elongatum, with remarks on species identity of haemosporidian lineages deposited in GenBank. Parasitology Research 102, 11851193.Google Scholar
Valkiūnas, G., Santiago-Alarcon, D., Levin, I. I., 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, 783792.Google Scholar
Valkiūnas, G., Iezhova, T. A., Evans, E., Carlson, J. S., Martínez-Gómez, J. E. and Sehgal, R. N. M. (2013). Two new Haemoproteus species (Haemosporida: Haemoproteidae) from Columbiform birds. Journal of Parasitology 99, 513521.Google Scholar
Valkiūnas, G., Palinauskas, V., Ilgūnas, M., Bukauskaitė, D., Dimitrov, D., Bernotienė, R., Zehtindjiev, P., Ilieva, M. and Iezhova, T. A. (2014). Molecular characterization of five widespread avian haemosporidian parasites (Haemosporida), with perspectives on the PCR-based detection of haemosporidians in wildlife. Parasitology Research 113, 22512263.Google Scholar
van Rensburg, M. J. (2010). Parasitism, disease and breeding ecology of little blue penguins (Eudyptula minor) on Tiritiri Matangi Island, New Zealand. Master's degree dissertation (Conservation Biology). Massey University, New Zealand.Google Scholar
Van Riper, C. III, Van Riper, S. G., Goff, M. L. and Laird, M. (1986). The epizootiology and ecological significance of malaria in Hawaiian land birds. Ecology Monographs 56, 327344.Google Scholar
Vanstreels, R. E. T., Kolesnikovas, C. K. M., Sandri, S., Silveira, P., Belo, N. O., Ferreira-Junior, F. C., Epiphanio, S., Steindel, M., Braga, É. M. and Catão-Dias, J. L. (2014 a). Outbreak of avian malaria associated to multiple species of Plasmodium in Magellanic penguins undergoing rehabilitation in Southern Brazil. PLoS ONE 9, e94994.Google Scholar
Vanstreels, R. E. T., Miranda, F. R., Ruoppolo, V., Reis, A. O. A., Costa, E. S., Pessôa, A. R. L., Torres, J. P. M., Cunha, L. S. T., Piuco, R. C., Valiati, V. H., González-Acuña, D., Labruna, M. B., Petry, M. V., Epiphanio, S. and Catão-Dias, J. L. (2014 b). Investigation of blood parasites of pygoscelid penguins at the King George and Elephant Islands, South Shetlands Archipelago, Antarctica. Polar Biology 37, 135139.Google Scholar
Vanstreels, R. E. T., Silva-Filho, R. P., Kolesnikovas, C. K. M., Bhering, R. C. C., Ruoppolo, V., Epiphanio, S., Amaku, M., Ferreira-Junior, F. C., Braga, É. M. and Catão-Dias, J. L. (2015 a). Epidemiology and pathology of avian malaria in penguins undergoing rehabilitation in Brazil. Veterinary Research 46, 30.Google Scholar
Vanstreels, R. E. T., Woehler, E. J., Ruoppolo, V., Vertigan, P., Carlile, N., Priddel, D., Finger, A., Dann, P., Vinette-Herrin, K., Thompson, P., Ferreira-Junior, F. C., Braga, É. M., Hurtado, R., Epiphanio, S. and Catão-Dias, J. L. (2015 b). Epidemiology and molecular phylogeny of Babesia sp. in little penguins Eudyptula minor in Australia. International Journal of Parasitology: Parasites and Wildlife 4, 198205.Google Scholar
Vanstreels, R. E. T., Capellino, F., Silveira, P., Braga, É. M., Rodríguez-Heredia, S. A., Loureiro, J. and Catão-Dias, J. L. (in press). Avian malaria (Plasmodium spp.) in Magellanic penguins (Spheniscus magellanicus) captive in northern Argentina. Journal of Wildlife Diseases.Google Scholar
Varney, K. (2006). Quarterly review of diagnostic cases – October to December 2005: Gribbles Veterinary Pathology. Surveillance 33, 1114.Google Scholar
Votypka, J., Oborník, M., Volf, P., Svobodová, M. and Lukes, J. (2002). Trypanosoma avium of raptors (Falconiformes): phylogeny and identification of vectors. Parasitology 125, 253263.Google Scholar
Walter Reed Biosystematics Unit (WRBU) (2014). VectorMap: know the vector, know the threat. http://www.vectormap.org/.Google Scholar
White, G. B. (1989). Malaria. In Geographical Distribution of Arthropod-borne Diseases and their Principal Vectors, pp. 722. World Health Organization Vector Biology and Control Division, Geneva, Switzerland. http://apps.who.int/iris/handle/10665/60575.Google Scholar
Wirth, W. W. and Felippe-Bauer, M. L. (1989). The Neotropical biting midges related to Culicoides paraensis (Diptera: Ceratopogonidae). Memórias Instituto Oswaldo Cruz 84, 551565.Google Scholar
Woods, R., Jones, H. I., Watts, J., Miller, G. D. and Shellam, G. R. (2009). Diseases of Antarctic seabirds. In Health of Antarctic Wildlife: a Challenge for Science and Policy (ed. Kerry, K. R. and Riddle, M. J.), pp. 3556. Springer, London, UK.Google Scholar
Yabsley, M. J., Parsons, N. J., Horne, E. C., Shock, B. C. and Purdee, M. (2012). Novel relapsing fever Borrelia detected in African penguins (Spheniscus demersus) admitted to two rehabilitation centers in South Africa. Parasitology Research 110, 11251130.Google Scholar
Yoshio, T., Yukiko, H., Kyoko, S., Koichi, M., Yukita, S., Rei, M., Miya, U. and Nobuyuki, N. (2006). Research on infection vector and its control: survey on infectious mosquitoes for penguin malaria in zoos and aquariums. Kansensho Baikai Bekuta no Jittai, Seisoku Boshi Taisaku ni kansuru Kenkyu Heisei 17 Nendo Sokatsu, Buntan Kenkyu Hokokusho 2006, 4149.Google Scholar
Zídková, L., Cepicka, I., Szabová, J. and Svobodová, M. (2012). Biodiversity of avian trypanosomes. Infection, Genetics and Evolution 12, 102112.Google Scholar