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Do blood parasites infect Magellanic penguins (Spheniscus magellanicus) in the wild? Prospective investigation and climatogeographic considerations

Published online by Cambridge University Press:  11 January 2017

RALPH ERIC THIJL VANSTREELS Open the ORCID record for RALPH ERIC THIJL VANSTREELS [Opens in a new window] ,
MARCELA UHART ,
VIRGINIA RAGO ,
RENATA HURTADO ,
SABRINA EPIPHANIO  and
JOSÉ LUIZ CATÃO-DIAS
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, Avenida Prof. Dr. Orlando Marques de Paiva 87, São Paulo, SP 05508-270, Brazil
MARCELA UHART
Affiliation:
Karen C. Drayer Wildlife Health Center, School of Veterinary Medicine, University of California Davis. One Shields Avenue, Davis, CA 95616, USA Wildlife Conservation Society (WCS), Amenabar 1595, Ciudad de Buenos Aires C1426AKC, Argentina
VIRGINIA RAGO
Affiliation:
Wildlife Conservation Society (WCS), Amenabar 1595, Ciudad de Buenos Aires C1426AKC, Argentina Consejo Nacional de Investigaciones Científicas y Técnicas (CONICET). Av. Rivadavia 1917, Ciudad de Buenos Aires C1033AAJ, Argentina
RENATA HURTADO
Affiliation:
Institute of Research and Rehabilitation of Marine Animals (IPRAM). Rodovia BR-262 Km 0, Cariacica, ES 29140-130, Brazil
SABRINA EPIPHANIO
Affiliation:
Laboratório de Imunopatologia Celular e Molecular da Malária, Departamento de Análises Clínicas e Toxicológicas, Faculdade de Ciências Farmacêuticas, Universidade de São Paulo. Avenida Prof. Lineu Prestes 580, Cidade Universitária, São Paulo, SP 05508-000, 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, Avenida Prof. Dr. Orlando Marques de Paiva 87, São Paulo, SP 05508-270, Brazil
*
*Corresponding author. 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
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Summary

Magellanic penguins (Spheniscus magellanicus) are native to Argentina, Chile and the Falkland Islands. Magellanic penguins are highly susceptible to blood parasites such as the mosquito-borne Plasmodium spp., which have been documented causing high morbidity and mortality in zoos and rehabilitation centres. However, to date no blood parasites have been detected in wild Magellanic penguins, and it is not clear whether this is reflective of their true absence or is instead related to an insufficiency in sampling effort or a failure of the diagnostic methods. We examined blood smears of 284 Magellanic penguins from the Argentinean coast and tested their blood samples with nested polymerase chain reaction tests targeting Haemoproteus, Plasmodium, Leucocytozoon and Babesia. No blood parasites were detected. Analysing the sampling effort of previous studies and the climatogeography of the region, we found there is strong basis to conclude that haemosporidians do not infect wild Magellanic penguins on the Argentinean coast. However, at present it is not possible to determine whether such parasites occur on the Chilean coast and at the Falkland Islands. Furthermore, it is troubling that the northward distribution expansion of Magellanic penguins and the poleward distribution shift of vectors may lead to novel opportunities for the transmission of blood parasites.

Keywords

avian malariaclimate changediseaseHaemosporidahealthvector-borne pathogenPiroplasmidaseabird

Information

Type
Research Article
Information
Parasitology , Volume 144 , Issue 5 , April 2017 , pp. 698 - 705
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Copyright © Cambridge University Press 2017 

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References

REFERENCES

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, 371–374.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, 672–682.CrossRefGoogle ScholarPubMed
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, 1621–1624.CrossRefGoogle Scholar
BirdLife International (2012). Spheniscus magellanicus. The IUCN Red List of Threatened Species 2012: e.T22697822A37820611. http://dx.doi.org/10.2305/IUCN.UK.2012-1.RLTS.T22697822A37820611.en CrossRefGoogle Scholar
Boersma, P. D., Frere, E., Kane, O., Pozzi, L. M., Pütz, K., Raya-Rey, A., Rebstock, G. A., Simeone, A., Smith, J., Van Buren, A., Yorio, P. and García-Borboroglu, P. (2014). Magellanic penguin (Spheniscus magellanicus). In Penguins: Natural History and Conservation (ed. García-Borboroglu, P. and Boersma, P. D.), pp. 145–152. Washington University Press, Seattle, USA.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, 123–127.CrossRefGoogle 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, 28–32.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, 1236–1242.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, 1–4.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
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, 88–90.CrossRefGoogle 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.CrossRefGoogle 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, 610–619.CrossRefGoogle ScholarPubMed
Fontannaz, C. C. (2001). Estadística Climatología. Dirección Meterológica de Chile, Climatología y Meteorología Aplicada, Santiago, Chile.Google Scholar
Garamszegi, L. Z. (2011). Climate change increases the risk of malaria in birds. Global Change Biology 17, 1751–1759.CrossRefGoogle Scholar
Gómez-Laich, A., Wilson, R. P., Sala, J. E., Luzenti, A. and Quintana, F. (2015). Moving northward: comparison of the foraging effort of Magellanic penguins from three colonies of northern Patagonia. Marine Biology 162, 1451–1461.CrossRefGoogle Scholar
Gubbels, J. M., de Vos, A. P., van der Weide, M., Viseras, J. and Schouls, L. M. (1999). Simultaneous detection of bovine Theileria and Babesia species by reverse line blot hybridization. Journal of Clinical Microbiology 37, 1782–1789.CrossRefGoogle ScholarPubMed
Hajek, E. R. and Di Castri, F. (1975). Bioclimatografia de Chile. Universidad Católica de Chile, Santiago, Chile.Google Scholar
Harvell, C. D., Mitchell, C. E., Ward, J. R., Altizer, S., Dobson, A. P., Ostfeld, R. S. and Samuel, M. D. (2002). Climate warming and disease risks for terrestrial and marine biota. Science 296, 2158–2162.CrossRefGoogle ScholarPubMed
Hawkey, C. M., Horsley, D. T. and Keymer, I. F. (1989). Haematology of wild penguins (Sphenisciformes) in the Falkland islands. Avian Pathology 18, 495–502.CrossRefGoogle 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, 797–802.CrossRefGoogle ScholarPubMed
Hijmans, R. J., Cameron, S. E., Parra, J. L., Jones, P. G. and Jarvis, A. (2005). Very high resolution interpolated climate surfaces for global land areas. International Journal of Climatology 25, 1965–1978.CrossRefGoogle 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.CrossRefGoogle ScholarPubMed
Jovani, R., Tella, J. L., Forero, M. G., Bertellotti, M., Blanco, G., Ceballos, O. and Donázar, J. Á. (2001). Apparent absence of blood parasites in the Patagonian seabird community: is it related to the marine environment? Waterbirds 24, 430–433.CrossRefGoogle Scholar
Keymer, I. F., Malcolm, H. M., Hunt, A. and Horsley, D. T. (2001). Health evaluation of penguins (Sphenisciformes) following mortality in the Falklands (South Atlantic). Diseases of Aquatic Organisms 45, 159–166.CrossRefGoogle 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, 197–201.Google Scholar
Medlin, L., Elwood, H. J., Stickel, S. and Sogin, M. L. (1988). The characterization of enzymatically amplified eukaryotic 16-like rRNA-coding regions. Gene 71, 491–499.CrossRefGoogle 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
Merino, S., Moreno, J., Vásquez, R. A., Martínez, J., Sánchez-Monsálvez, I., Estades, C. F., Ippi, S., Sabat, P., Rozzi, R. and McGehee, S. (2008). Haematozoa in forest birds from southern Chile: latitudinal gradients in prevalence and parasite lineage richness. Austral Ecology 33, 329–340.CrossRefGoogle Scholar
Montero, E., González, L. M., Chaparro, A., Benzal, J., Bertellotti, M., Masero, J. A., Colominas-Ciuró, R., Vidal, V. and Barbosa, A. (2016). First record of Babesia sp. in Antarctic penguins. Ticks and Tick Borne Diseases 7, 498–501.CrossRefGoogle ScholarPubMed
Moreno, J., Yorio, P., Garcia-Borboroglu, P., Potti, J. and Villar, S. (2002). Health state and reproductive output in Magellanic penguins (Spheniscus magellanicus). Ethology, Ecology and Evolution 14, 19–28.CrossRefGoogle Scholar
Municipalidad de Puerto Madryn (MPM) (2009). Dengue. http://www.madryn.gov.ar/dengue/ Google Scholar
Municipalidad de Puerto Madryn (MPM) (2016). Comienzan las fumigaciones por moscas y mosquitos. http://lu17.com/destacado/comienzan-las-fumigaciones-por-moscas-y-mosquitos 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, 843–868.CrossRefGoogle ScholarPubMed
Pozzi, L. M., García-Borboroglu, P., Boersma, P. D. and Pascual, M. A. (2015). Population regulation in Magellanic penguins: what determines changes in colony size. PLoS ONE 10, e0119002.CrossRefGoogle ScholarPubMed
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. Naturwissenshcaften 97, 809–817.CrossRefGoogle ScholarPubMed
Ramos, A. M., Santos, L. A. R. and Fortes, L. T. G. (2009). Normais Climatológicas do Brasil 1961–1990. Instituto Nacional de Meteorologia, Brasília.Google Scholar
Reiczigel, J., Földi, J. and Ózsvári, L. (2010). Exact confidence limits for prevalence of a disease with an imperfect diagnostic test. Epidemiology & Infection 138, 1674–1678.CrossRefGoogle ScholarPubMed
Richard, 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.CrossRefGoogle ScholarPubMed
Rogers, D. J. and Randolph, S. E. (2000). The global spread of malaria in a future, warmer world. Science 289, 1763–1766.CrossRefGoogle Scholar
Rosenfeld, G. (1947). Corante pancrômico para hematologia e citologia clínica: nova combinação dos componentes do May-Grunwald e do Giemsa num só corante de emprego rápido. Memórias do Instituto Butantan 20, 329–335.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, 267–277.CrossRefGoogle ScholarPubMed
Sergeant, E. S. G. (2016). Epitools epidemiological calculators. AusVet Animal Health Services and Australian Biosecurity Cooperative Research Centre for Emerging Infectious Disease. http://epitools.ausvet.com.au/ 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, 165–171.CrossRefGoogle ScholarPubMed
Servicio Meteorológico Nacional (SMN) (2016). Atlas Climático. http://www.smn.gov.ar/serviciosclimaticos/?mod=elclima&id=1 Google Scholar
Tella, J. L., Forero, M. G., Bertellotti, M., Donázar, J. A., Blanco, G. and Ceballos, O. (2001). Offspring body condition and immunocompetence are negatively affected by high breeding densities. Proceedings of the Royal Society of London B 268, 1455–1461.CrossRefGoogle ScholarPubMed
Tollini, J., Brocksen, A. and Sureda, N. (2000). Prevention and treatment of avian malaria in a captive penguin colony. Penguin Conservation 13, 28–31.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. Parasitological Research 102, 1185–1193.CrossRefGoogle ScholarPubMed
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). Outbreak of avian malaria associated to multiple species of Plasmodium in Magellanic penguins undergoing rehabilitation in Southern Brazil. PLoS ONE 9, e94994.CrossRefGoogle ScholarPubMed
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). Epidemiology and pathology of avian malaria in penguins undergoing rehabilitation in Brazil. Veterinary Research 46, 30.CrossRefGoogle ScholarPubMed
Vanstreels, R. E. T., Braga, É. M. and Catão-Dias, J. L. (2016 a). Blood parasites of penguins: a critical review. Parasitology 143, 931–956.CrossRefGoogle ScholarPubMed
Vanstreels, R. E. T., Capellino, F., Silveira, P., Braga, É. M., Rodríguez-Heredia, S. A., Loureiro, J. and Catão-Dias, J. L. (2016 b). Avian malaria (Plasmodium spp.) in Magellanic penguins (Spheniscus magellanicus) captive in northern Argentina. Journal of Wildlife Diseases 52, 734–737.CrossRefGoogle ScholarPubMed
Waldenström, J., Bensch, S., Hasslequist, D. and Östman, Ö. (2004). A new nested polymerase chain reaction method very efficient in detecting Plasmodium and Haemoproteus infections from avian blood. Journal of Parasitology 90, 191–194.CrossRefGoogle ScholarPubMed
Walter Reed Biosystematics Unit (WRBU) (2016). VectorMap: know the vector, know the threat. http://www.vectormap.org/ Google Scholar
Wilson, R. P., Scolaro, J. A., Grémillet, D., Kierspel, M. A. M., Laurenti, S., Upton, J., Gallelli, H., Quintana, F., Frere, E., Müller, G., Straten, M. T., and Zimmer, I. (2005). How do Magellanic penguins cope with variability in their access to prey? Ecological Monographs 75, 379–401.CrossRefGoogle Scholar