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Molecular Epidemiology of Avian Malaria in Wild Breeding Colonies of Humboldt and Magellanic Penguins in South America

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Abstract

Avian malaria is a disease caused by species of the genera Haemoproteus, Leucocytozoon, and Plasmodium. It affects hundreds of bird species, causing varied clinical signs depending on the susceptibility of the host species. Although high mortality has been reported in captive penguins, limited epidemiological studies have been conducted in wild colonies, and isolated records of avian malaria have been reported mostly from individuals referred to rehabilitation centers. For this epidemiological study, we obtained blood samples from 501 adult Humboldt and 360 adult Magellanic penguins from 13 colonies throughout South America. To identify malaria parasitaemia, we amplified the mtDNA cytochrome b for all three parasite genera. Avian malaria was absent in most of the analyzed colonies, with exception of the Punta San Juan Humboldt penguin colony, in Peru, where we detected at least two new Haemoproteus lineages in three positive samples, resulting in a prevalence of 0.6% for the species. The low prevalence of avian malaria detected in wild penguins could be due to two possible causes: A low incidence, with high morbidity and mortality in wild penguins or alternatively, penguins sampled in the chronic stage of the disease (during which parasitaemia in peripheral blood samples is unlikely) would be detected as false negatives.

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References

  • Alamo A, Bouchon M (1987) Changes in the food and feeding of the sardine (Sardinops sagax sagax) during the years 1980-1984 off the Peruvian coast. Journal of Geophysical 497 Research 92: 14411-14415.

    Article  Google Scholar 

  • Araya B, Garland D, Espinoza G, Sanhueza A, Simeone AR, Teare A (2000) Population and habitat viability assessment for the Humboldt penguin (Spheniscus humboldti), Final Report. IUCN/SSC Conservation Breeding Specialist Group, Apple Valley, MN.

  • Asghar M, Westerdahl H, Zehtindjiev P, Ilieva M, Hasselquist D, Bensch S (2012) Primary peak and chronic malaria infection levels are correlated in experimentally infected great reed warblers. Parasitology 139: 1246-1252.

    Article  PubMed  Google Scholar 

  • Atkinson CT, Woods KL, Dusek RJ, Sileo LS, Iko WM (1995) Wildlife disease and conservation in Hawaii: Pathogenicity of avian malaria (Plasmodium relictum) in experimentally infected Iiwi (Vestiaria coccinea). Parasitology 111: S59-S69.

    Article  PubMed  Google Scholar 

  • Barber RT, Chávez FP (1983) Biological consequences of El Niño. Science 222: 1203-1210.

    Article  CAS  PubMed  Google Scholar 

  • Beadell JS, Gering E, Austin J, Dumbacher JP, Peirce MA, Pratt TK, Atkinson CT, Fleischer RC (2004) Prevalence and differential host-specificity of two avian blood parasite genera in the Australo-Papuan region. Molecular Ecology 13: 3829-3844.

    Article  PubMed  Google Scholar 

  • Bennett GF, Garnham PCC, Fallis AM (1965) On the status of the genera Leucocytozoon Zieman, 1893 and Haemoproteus Kruse, 1890 (Haemosporidiida: Leucocytozoidae and Haemoproteidae). Canadian Journal of Zoology 43(6): 927-932.

    Article  CAS  PubMed  Google Scholar 

  • Bensch S, Hellgren O, 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.

    Article  PubMed  Google Scholar 

  • Boersma PD, Frere E, Kane O, Pozzi LM, Pütz K, Rey AR, Rebstock GA, Simeone A, Smith J, Van Buren A, Yorio P, Garcia-Borboroglu P (2013) Magellanic penguin (Spheniscus magellanicus). In: Penguins: Natural History and Conservation, Garcia-Borboroglu P, Boersma PD (editors), Seattle, WA: University of Washington Press, pp 233-263.

    Google Scholar 

  • Boersma PD, Rebstock GA (2014) Climate change increases reproductive failure of Magellanic penguins. Plos one 9(1): 1-13.

    Article  Google Scholar 

  • Bouzat JL, Walker BG, Boersma PD (2009) Regional Genetic Structure in the Magellanic penguin (Spheniscus magellanicus) suggests metapopulation dynamics. The Auk 126(2):326-334.

    Article  Google Scholar 

  • Braga EM, Silveira P, Belo NO, Valkunas G (2011) Recent advances in the study of avian malaria: an overview with an emphasis on the distribution of Plasmodium spp in Brazil. Memorias do Instituto Oswaldo Cruz 106(1): 3-11.

    PubMed  Google Scholar 

  • Brody JR, Kern SE (2004) Sodium boric acid: a Tris-free, cooler conductive medium for DNA electrophoresis. Biotechniques 36:214-216.

    CAS  PubMed  Google Scholar 

  • Brossy J-J (1992) Malaria in wild and captive Jackass Penguins Spheniscus demersus along the Southern African Coast. Ostrich 63:10-12.

    Article  Google Scholar 

  • Cannell BL, Krasnec KV, Campbell K, Jones HI, Miller RD, Stephens N (2013) The pathology and pathogenicity of a novel Haemoproteus spp. Infection in wild Little Penguins (Eudyptula minor). Veterinary Parasitology 197: 74-84.

    Article  CAS  PubMed  Google Scholar 

  • CCAMLR (2004) Commission for the conservation of antarctic marine living resources: CCAMLR ecosystem monitoring program: Standard methods. North Hobart, Tasmania, Australia.

    Google Scholar 

  • Clarke JR, Kerry KR (1993) Diseases and parasites of penguins. Korean Journal of Polar Research 4: 79-96.

    Google Scholar 

  • Cranfield MR, Grackzyk TK, Beall FB, Laleggio DM, Shaw ML, Skjoldager ML (1991) Subclinical Avian Malaria Infection in African Black-footed penguin (Spheniscus demersus) and induction of parasite recrudescence. Journal of Wildlife Disease 30: 372-376.

    Article  Google Scholar 

  • Cranfield MR, Graczyk TK, Beall FB, Iallegio DM, Shaw ML, Skjoldager MT (1994) Subclinical avian malaria infection and induction of parasite recrudescence. Journal of Wildlife Diseases 30: 372-376.

    Article  CAS  PubMed  Google Scholar 

  • Cunningham AA, Daszak P, Rodriguez JP (2003) Pathogen pollution: Defining a parasitological threatto biodiversity conservation. Journal of Parasitology 89: S78-S83.

    Google Scholar 

  • Daszak P, Cunningham AA, Hyatt AS (2003) Infectious disease and amphibian population declines. Diversity and Distributions 9:141-150.

    Article  Google Scholar 

  • Daszak P, Tabor GM, Kilpatrick AM, Epsteein J, Plowright R (2004) Conservation medicine and a new agenda for emerging diseases. New York Academy of Sciences 1026:1-11.

    Article  Google Scholar 

  • Deem SL, Spelman LH, Yates RA, Montal RJ (2000) Canine distemper in terrestrial carnivores: a Review. Journal of Zoo and Wildlife Medicine 31(4): 441-451.

    Article  CAS  PubMed  Google Scholar 

  • De Guisti DL, Sterling CR, Dobrzechowski (1973) Transmission of the chelonian haemoproteid Haemoproteus metchnikovi by a tabanoid fly Chrysops callidus. Nature 242: 50-51.

    Article  Google Scholar 

  • De la Puente S, Bussalleu A, Cardeña M, Valdés-Velasquez A, Majluf P, Simeone A (2013) Humboldt penguin (Spheniscus humboldi). In: Penguins: Natural History and Conservation, Garcia-Borboroglu P, Boersma PD (editors), Seattle, WA: University of Washington Press, pp 265-283.

    Google Scholar 

  • Ejiri H, Sato Y, Sawai R, Sasaki E, Matsumoto R, Ueda M, Higa Y, Tsuda Y, Omori S, Murata K, Yukawa M (2009) Prevalence of avian malaria parasite in mosquitoes collected at a zoological garden in Japan. Parasitological Research 105:629–633

  • Fisher MC, Garner TWJ (2007) The relationship between the emergence of Batrachoochytrium dendrobatidis, the international trade in amphibians and introduced amphibian species. Fungal Biology Reviews 21: 2-9.

    Article  Google Scholar 

  • Fix AS, Waterhouse C, Greiner EC, Stoskopf MK (1988) Plasmodium relictum as a cause of avian malaria in wild-caught magellanic penguins (Spheniscus magellanicus). Journal of Wildlife Disease 24(4): 610-619.

    Article  CAS  Google Scholar 

  • Forrester DJ, Greiner EC, McFarlane RW (1977) Blood Parasites of some Columbiform and Passeriform Birds from Chile. Journal of Wildlife Disease 13: 94-96.

    Article  CAS  Google Scholar 

  • Forrester DJ, Foster GW, Morrison JL (2001) Leucocytozoon toddi and Haemoproteus tinnunculi (Protozoa: Haemosporina) in the Chimango Caracara (Milvago chimango) in Southern Chile. Memorias do Instituto Oswaldo Cruz 96(7): 1023-1024.

    Article  CAS  PubMed  Google Scholar 

  • Gill JM, Darby JT (1993) Deaths in yellow-eyed penguins (Megadyptes antipodes) on the Otago Peninsula during the summer of 1990. New Zealand Veterinary Journal 41: 39-42.

    Article  CAS  PubMed  Google Scholar 

  • Graczyk TK, Cockrem JF, Cranfield MR, Darby JT, Moore P (1995) Avian malaria seroprevalence in wild New Zealand penguins. Parasite 2: 401-405.

    Google Scholar 

  • Grim KC, Van der Merwe E, Sullivan M, Parsons N, McCutchan TF, Cranfield M (2003) Plasmodium juxtanucleare Associated with Mortality in Black-Footed Penguins (Spheniscus demersus) Admitted to a Rehabilitation Centers. Journal of Zoo and Wildlife Medicine 34(3): 250-255.

    Article  PubMed  Google Scholar 

  • Harrell FE Jr, with contributions from Charles Dupont and many others (2013) Hmisc: Harrell Miscellaneous. R package version 3.12-2. http://CRAN.R-project.org/package=Hmisc.

  • Hellgren O, Waldenstrom J, Bensch S (2004) A new PCR assay for simultaneous studies of Leucocytozoon, Plasmodium, and Haemoproteus from avian blood. The Journal of Parasitology 90:797–802.

    Article  CAS  PubMed  Google Scholar 

  • Hiriart-Bertrand L, Simeone A, Reyes-Arriagada R, Riquelme V, Pütz K, Lüthi B (2010) Description of a mixed-species colony of Humboldt (Spheniscus humboldti) and Magellanic Penguin (S. magellanicus) at Metalqui Island, Chiloe, southern Chile. Boletín Chileno de Ornitología 16:42–47.

    Google Scholar 

  • Huelsenbeck JP, Ronquist F (2001). MRBAYES: Bayesian inference of phylogenetic trees. Bioinformatics (Oxford, England) 17(8):754–755.

    Article  CAS  Google Scholar 

  • Huff CG, Shiroishi T (1962) Natural infection of Humboldt’s penguins with Plasmodium elongatum. The Journal of Parasitology 48:495.

    Article  Google Scholar 

  • IUCN (2014) The IUCN Red List of Threatened Species. Version 2014.2. www.iucnredlist.org. Downloaded on 12 September 2014.

  • Jarvi SI, Schultz JJ, Atkinson CT (2002) PCR diagnostics underestimate the prevalence of avian malaria (Plasmodium relictum) in experimentally-infected passerines. American Society of Parasitologies 88(1):153–158.

    Google Scholar 

  • Jones MR, Cheviron ZA, Carling MD (2013) Spatial patterns of avian malaria prevalence in Zonotrichia capensis on the western slope of the peruvian Andes. The Journal of Parasitology 99(5):903–905.

    Article  CAS  PubMed  Google Scholar 

  • Knowles SCL, Wood MJ, Alves R, Wilken TA, Bensch S, Sheldon BC (2011) Molecular epidemiology of malaria prevalence and parasitaemia in a wild bird population. Molecular Ecology 20: 1062-1076.

    Article  PubMed  Google Scholar 

  • Larkin MA, Blackshields G, Brown NP, Chenna R, McGettigan P, McWilliam H, Higgins DG (2007) Clustal W and Clustal X version 2.0. Bioinformatics (Oxford, England) 23(21): 2947-8.

    Article  CAS  Google Scholar 

  • Levin II, Outlaw DC, Vargas FH, Parker PG (2009) Plasmodium blood parasite found in endangered Galapagos penguins (Spheniscus mendiculus). Biological Conservation 142: 3191-3195.

    Article  Google Scholar 

  • Martínez D, González G (2005) Las Aves de Chile. Nueva guía de campo. Ediciones del Naturalista, Santiago, Chile, pp 620

  • McDonald SP (2003) Parasitology of the yellow-eyed penguin (Megadyptes antipodes). Unpublished MSc thesis, University of Otago, Dunedin, New Zealand

  • Merino S, Moreno J, Vasquez RA, Martinez J, Sanchez-Monsalvez I, Estades CF, Ippi S, Sabat P, Rozzi R, McGehee S (2008) Haematozoa in forest birds from southern Chile: Latitudinal gradients in prevalence and parasite lineage richness. Austral Ecology 33: 329-340.

    Article  Google Scholar 

  • Miller GD, Hofkin BV, Snell H, Hahn A, Miller RD (2001) Avian malaria and marek’s disease: potential threats to Galapagos Penguins Spheniscus mendiculus. Marine Ornithology 29:43-46.

    Google Scholar 

  • Omori S, Sato Y, Hirakawa S, Isobe T, Yukawa M, Murata K (2008) Two extra chromosomal genomes of Leucocytozoon caulleryi; complete nucleotide sequences of the mitochondrial genome and existence of the apicoplast genome. Parasitology Research 103: 953-957.

    Article  PubMed  Google Scholar 

  • Orkun Ö, Güven E (2013) A New species of Haemoproteus from a tortoise (Testudo graeca) in Turkey, with remarks on molecular phylogenetic and morphological analysis. The Journal of Parasitology 99(1): 112-117.

    Article  PubMed  Google Scholar 

  • Outlaw DC & Ricklefs RE (2010) Comparative gene evolution in Haemosporidian (Apicomplexa) parasites of birds and mammals. Molecular Biology and Evolution 27(3): 537-542.

    Article  CAS  PubMed  Google Scholar 

  • Palinauskas V, Valkiūnas G, Bensch S, Bolshakov VC (2011) Plasmodium relictum (lineage SGS1) and Plasmodium ashfordi (lineage GRW2): the effects of the co-infection on experimentally infected passerine birds. Experimental Parasitology 127:527–533.

    Article  PubMed  Google Scholar 

  • Palmer JL, McCutchan TF, VargasFH, Deem SL, Cruz M, Hartman DA, Parker, PG (2013) Seroprevalence of malarial antibodies in Galapagos penguins (Spheniscus mendiculus). The Journal of Parasitology 99(5): 770-776.

    Article  PubMed  Google Scholar 

  • Paredes R, Zavalaga CB, Battistini G, Majluf P, Mc Gill P (2003) Status of the Humboldt Penguin in Peru, 1999-2000. Waterbirds 26: 129-138.

    Article  Google Scholar 

  • Penguin Taxon Advisory Group. 2005. Penguin Husbandry Manual, third edition. American Zoo and Aquarium Association. Pg 142.

    Google Scholar 

  • Perkins SL, Schall JJ (2002) A molecular phylogeny of malarial parasites recovered from cytochrome b gene sequences. The Journal of Parasitology 88(5): 972-978.

    Article  CAS  PubMed  Google Scholar 

  • Posada D (2008) jModelTest: phylogenetic model averaging. Molecular Biology and Evolution 25(7): 1253-1256.

    Article  CAS  PubMed  Google Scholar 

  • Raffo EC, Muñoz PA (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 

  • Rambaut A (2009) FigTree v1.4.0: Tree Figure Drawing Tool. Available: http://tree.bio.ed.ac.uk/software/figtree/. Accesed February 2014

  • R Core Team (2013) R: A Language and Environment for Statistical Computing. Vienna, Austria: R Foundation for Statistical Computing. URL http://www.R-project.org/

  • Sambrook J, Fritsch EF, Maniatis T (1989) Molecular cloning: a laboratory Manual, vol. 3. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, N.Y.

    Google Scholar 

  • Scheurlein A, Ricklefs RE (2004) Prevalence of blood parasites in European passeriform birds. Proceedings of he Royal Society of London 271(1546): 1363-1370.

    Article  Google Scholar 

  • Simeone A, Wallace R (2014) Evidence of philopatry and natal dispersal in Humboldt penguins. Emu 114:69-73.

    Article  Google Scholar 

  • Santiago-Alarcon D, Outlaw DC, Ricklefs RE, Parker PG (2010) Phylogenetic relationships of haemosporidian parasites in New World Columbiformes, with emphasis on the endemic Galapagos dove. International Journal for Parasitology 40: 463-470.

    Article  CAS  PubMed  Google Scholar 

  • Schlosser JA, Dubach JM, Garner TWJ, Araya B, Bernal M, Simeone A, Smith KA, Wallace RS (2009) Evidence for gene flow differs from observed dispersal patterns in the Humboldt penguin, Spheniscus humboldti. Conservation Genetics 10: 839-849.

    Article  CAS  Google Scholar 

  • Silveira P, Belo NO, Lacorte GA, Kolesnikovas CK, Vanstreels RE, Steindel M, Catão-Dias JL, Valkiūnas G, Braga EM (2013) Parasitological and new molecular-phylogenetic characterization of the malaria parasite Plasmodium tejerai in South American penguins. Parasitology International 62(2): 165-171.

    Article  CAS  PubMed  Google Scholar 

  • Teare JA, Diebold EN, Grybowski K, Michaels MG, Wallace RS Willis MJ (1998) Nest site fidelity in Humboldt penguins at Algarrobo, Chile. Penguin Conservation 11: 22-23.

    Google Scholar 

  • Tovar H, Guillén V (1987) Reproduction and population levels of Peruvian guano birds, 1980 to1986. Journal of Geophysical Research 92: 14445-14448.

    Article  Google Scholar 

  • Valkiūnas G (2005) Avian malaria parasites and other haemosporidia. Boca Raton: CRC Press. 932 p.

    Google Scholar 

  • Valkiūnas G, Santiago-Alarcon D, Levin II, Iezhova TA, Parker PG (2010) A new Haemoproteus species (Haemosporida: Haemoproteidae) from the endemic Galapagoes dove Zenaida galapagoensis, with remarks on the parasite distribution, vector, and molecular diagnostics. Journal of Parasitology 96(4):783–792.

  • Valle CA, Cruz F, Cruz JB, Merlen G, Coulter MC (1987) The impact of the 1982-1983 El Niño-Southern Oscillation on seabirds in the Galápagos Islands, Ecuador. Journal of Geophysical Research 92: 14437-14444.

    Article  Google Scholar 

  • Vanstreel RET, Kolesnikovas CKM, Sandri S, Silveira P, Belo NO, Ferreira FC Jr, Epiphanio S, Steindel M, Braga EM, Catão-Dias L (2014) Outbreak of Avian Malaria Associated to Multiple Species of Plasmodium in Magellanic Penguins Undergoing Rehabilitation in Southern Brazil. Plos one 9(4): 1-11.

    Google Scholar 

  • Williams ES, Yuill T, Artois M, Fischer J, Haigh SA (2002) Emerging infectious diseases in wildlife. Revue Scientifique et Technique de L’Office International des Epizooties 21(1): 139-157.

    CAS  Google Scholar 

  • Williams RB (2005) Avian malaria: clinical and chemical pathology of Plasmodium gallinaceum in the domesticated fowl Gallus gallus. Avian Pathology 34(1): 29-47.

    Article  CAS  PubMed  Google Scholar 

  • Woodworth BL, Atkinson CT, LaPointe DA, Hart PJ, Spiegel CS, Tweed EJ, Henneman C, LeBrun J, Denette T, DeMots R, Kozar KL, Triglia D, Lease D, Gregor A, Smith T, Duffy D (2005) Host population persistence in the face of introduced vector-borne diseases: Hawaii amakihi and avian malaria. PNAS 102(5): 1531-1536.

    Article  PubMed Central  CAS  PubMed  Google Scholar 

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Acknowledgments

This study was financed by FONDECYT 11110060; FONDECYT 1010250; FONDECYT 1100695; CNPq 490403/2008-5; FAPESP 2009/08624-8; Sea World and Busch Gardens Conservation Fund and CONICYT. Many thanks to Patricia Majluf, Angela Guajardo, Cayetano Espinosa-Miranda, Rocio Alvarez, Barbara Ramos, Marco Cardeña, Sebastian Llanos, Matias Portflitt, Fernanda Norambuena, and David Morales for their help in the field, laboratory and data analysis. Samples were obtained under Subpesca (110), CONAF, and DGFFS-minag permits. Thanks to the Chilean Navy and Pan de Azucar CONAF Park Rangers for their assistance in fieldwork.

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Sallaberry-Pincheira, N., Gonzalez-Acuña, D., Herrera-Tello, Y. et al. Molecular Epidemiology of Avian Malaria in Wild Breeding Colonies of Humboldt and Magellanic Penguins in South America. EcoHealth 12, 267–277 (2015). https://doi.org/10.1007/s10393-014-0995-y

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