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A new pathogen spillover from domestic to wild animals: Plasmodium juxtanucleare infects free-living passerines in Brazil

Published online by Cambridge University Press:  09 May 2018

Francisco C. Ferreira-Junior*
Affiliation:
Departamento de Parasitologia, Instituto de Ciências Biológicas, Universidade Federal de Minas Gerais, Belo Horizonte, MG, Brazil
Daniela de Angeli Dutra
Affiliation:
Departamento de Parasitologia, Instituto de Ciências Biológicas, Universidade Federal de Minas Gerais, Belo Horizonte, MG, Brazil
Patrícia Silveira
Affiliation:
Programa de Pós-graduação em Biologia Celular, Instituto de Ciências Biológicas, Universidade Federal de Minas Gerais, Belo Horizonte, MG, Brazil
Richard Campos Pacheco
Affiliation:
Programa de Pós-graduação em Ciências Veterinárias, Faculdade de Medicina Veterinária, Universidade Federal de Mato Grosso, Cuiabá, MT, Brazil
Rute Witter
Affiliation:
Programa de Pós-graduação em Ciências Veterinárias, Faculdade de Medicina Veterinária, Universidade Federal de Mato Grosso, Cuiabá, MT, Brazil
Dirceu Guilherme de Souza Ramos
Affiliation:
Unidade Acadêmica Especial de Ciências Agrárias, Universidade Federal de Goiás, Jataí, GO, Brazil
M. Andreína Pacheco
Affiliation:
Department of Biology/IGEM/Temple University, Philadelphia, USA
Ananias A. Escalante
Affiliation:
Department of Biology/IGEM/Temple University, Philadelphia, USA
Érika M. Braga*
Affiliation:
Departamento de Parasitologia, Instituto de Ciências Biológicas, Universidade Federal de Minas Gerais, Belo Horizonte, MG, Brazil
*
Author for correspondence: Francisco C. Ferreira-Junior and Érika M. Braga, E-mail: franciscocarlosfj@gmail.com; embraga@icb.ufmg.br
Author for correspondence: Francisco C. Ferreira-Junior and Érika M. Braga, E-mail: franciscocarlosfj@gmail.com; embraga@icb.ufmg.br

Abstract

Habitat modification may facilitate the emergence of novel pathogens, and the expansion of agricultural frontiers make domestic animals important sources of pathogen spillover to wild animals. We demonstrate for the first time that Plasmodium juxtanucleare, a widespread parasite from domestic chickens, naturally infects free-living passerines. We sampled 68 wild birds within and at the border of conservation units in central Brazil composed by Cerrado, a highly threatened biome. Seven out of 10 passerines captured in the limits of a protected area with a small farm were infected by P. juxtanucleare as was confirmed by sequencing a fragment of the parasite's cytochrome b. Blood smears from these positive passerines presented trophozoites, meronts and gametocytes compatible with P. juxtanucleare, meaning these birds are competent hosts for this parasite. After these intriguing results, we sampled 30 backyard chickens managed at the area where P. juxtanucleare-infected passerines were captured, revealing one chicken infected by the same parasite lineage. We sequenced the almost complete mitochondrial genome from all positive passerines, revealing that Brazilian and Asian parasites are closely related. P. juxtanucleare can be lethal to non-domestic hosts under captive and rehabilitation conditions, suggesting that this novel spillover may pose a real threat to wild birds.

Type
Research Article
Copyright
Copyright © Cambridge University Press 2018 

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References

Asghar, M et al. (2015) Hidden costs of infection: chronic malaria accelerates telomere degradation and senescence in wild birds. Science 347, 436438.Google Scholar
Becker, DJ, Streicker, DG and Altizer, S (2015) Linking anthropogenic resources to wildlife-pathogen dynamics: a review and meta-analysis. Ecology Letters 18, 483495.Google Scholar
Belo, NO et al. (2011) Prevalence and lineage diversity of avian Haemosporidians from three distinct Cerrado habitats in Brazil. PLoS ONE 6, e17654.Google Scholar
Bennett, GF and Warren, M (1966) Biology of the Malaysian strain of Plasmodium juxtanucleare Versiani and Gomes, 1941. I. Description of the stages in the vertebrate host. Journal of Parasitology 52, 565569.Google Scholar
Bennett, GF, Warren, M and Cheong, WH (1966) Biology of the Malaysian strain of Plasmodium juxtanucleare Versiani and Gomes, 1941. II. The sporogonic stages in Culex (Culex) sitiens Wiedmann. The Journal of Parasitology 52, 647652.Google Scholar
Bensch, S, Hellgren, O and Pérez-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, 13531358.Google Scholar
Bensch, S et al. (2000) Host specificity in avian blood parasites: a study of Plasmodium and Haemoproteus mitochondrial DNA amplified from birds. Proceedings of the Royal Society B: Biological Sciences 267, 15831589.Google Scholar
Beuchle, R et al. (2015) Land cover changes in the Brazilian Cerrado and Caatinga biomes from 1990 to 2010 based on a systematic remote sensing sampling approach. Applied Geography 58, 116127.Google Scholar
Brearley, G et al. (2013) Wildlife disease prevalence in human-modified landscapes: wildlife disease in human-modified landscapes. Biological Reviews 88, 427442.Google Scholar
Carrete, M et al. (2009) Goats, birds, and emergent diseases: apparent and hidden effects of exotic species in an island environment. Ecological Applications 19, 840853.Google Scholar
Chen, T-H et al. (2015) Avian Plasmodium infection in field-collected mosquitoes during 2012–2013 in Tarlac, Philippines. Journal of Vector Ecology 40, 386392.Google Scholar
Consoli, RAGB and de Oliveira, RL (1994) Principais Mosquitos de Importância Sanitária no Brasil. Rio de Janeiro, RJ: FIOCRUZ.Google Scholar
Daszak, P, Cunningham, AA and Hyatt, AD (2000) Emerging infectious diseases of wildlife--threats to biodiversity and human health. Science (New York, N.Y.) 287, 443449.Google Scholar
Deem, SL et al. (2012) Diseases of poultry and endemic birds in Galapagos: implications for the reintroduction of native species. Animal Conservation 15, 7382.Google Scholar
Earle, RA et al. (1991) Occurrence of Plasmodium juxtanucleare in greywing francolin: short communication. South African Journal of Wildlife Research 21, 3032.Google Scholar
Ebert, D and Herre, EA (1996) The evolution of parasitic diseases. Parasitology Today 12, 96101.Google Scholar
Ellis, VA et al. (2015) Local host specialization, host-switching, and dispersal shape the regional distributions of avian haemosporidian parasites. Proceedings of the National Academy of Sciences of the United States of America 112, 1129411299.Google Scholar
Ewen, JG et al. (2012) Parasite management in translocations: lessons from a threatened New Zealand bird. Oryx 46, 446456.Google Scholar
Fallon, SM et al. (2003) Detecting avian malaria: an improved polymerase chain reaction diagnostic. Journal of Parasitology 89, 10441047.Google Scholar
Fecchio, A et al. (2013) Structure and organization of an avian haemosporidian assemblage in a Neotropical savanna in Brazil. Parasitology 140, 181192.Google Scholar
Ferreira, FCJ et al. (2016) Searching for putative avian malaria vectors in a seasonally Dry tropical forest in Brazil. Parasites & Vectors 9, 587.Google Scholar
Ferreira, FC Jr et al. (2017) Habitat modification and seasonality influence avian haemosporidian parasite distributions in southeastern Brazil. PLoS ONE 12, e0178791.Google Scholar
Friend, M, McLean, RG and Joshua Dein, F (2001) Disease emergence in birds: challenges for the twenty-first century. The Auk 118, 290303.Google Scholar
Fuller, T et al. (2012) The ecology of emerging infectious diseases in migratory birds: an assessment of the role of climate change and priorities for future research. EcoHealth 9, 8088.Google Scholar
Garcia, SC et al. (2013) Molecular epidemiology of newcastle disease in Mexico and the potential spillover of viruses from poultry into wild bird species. Applied and Environmental Microbiology 79, 49854992.Google Scholar
Garnham, PCC (1966) Malaria Parasites and Other Haemosporidia. Oxford, England: Blackwell Scientific.Google Scholar
Gonzalez-Quevedo, C, Davies, RG and Richardson, DS (2014) Predictors of malaria infection in a wild bird population: landscape-level analyses reveal climatic and anthropogenic factors. Journal of Animal Ecology 83, 10911102.Google Scholar
Gottdenker, NL et al. (2005) Assessing the risks of introduced chickens and their pathogens to native birds in the Galápagos archipelago. Biological Conservation 126, 429439.Google Scholar
Gouy, M, Guindon, S and Gascuel, O (2010) Seaview version 4: a multiplatform graphical user interface for sequence alignment and phylogenetic tree building. Molecular Biology and Evolution 27, 221224.Google Scholar
Grim, KC et al. (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
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
Hillman, AE, Lymbery, AJ and Thompson, RCA (2015) Is Toxoplasma gondii a threat to the conservation of free-ranging Australian marsupial populations? International Journal for Parasitology: Parasites and Wildlife 5, 1727.Google Scholar
Karlsson, EA et al. (2015) Non-Human primates harbor diverse mammalian and avian Astroviruses including those associated with human infections. PLoS Pathogens 11, e1005225.Google Scholar
Knowles, SCL, Palinauskas, V and Sheldon, BC (2010) Chronic malaria infections increase family inequalities and reduce parental fitness: experimental evidence from a wild bird population. Journal of Evolutionary Biology 23, 557569.Google Scholar
Krettli, AU (1972) Plasmodium juxtanucleare in the state of Minas Gerais, Brazil. Studies on its prevalence and some aspects of its biology. Revista do Instituto de Medicina Tropical de Sao Paulo 14, 235245.Google Scholar
Kumar, S, Stecher, G and Tamura, K (2016) MEGA7: molecular evolutionary genetics analysis version 7.0 for bigger datasets. Molecular Biology and Evolution 33, 18701874.Google Scholar
Lafferty, KD (2003) Is disease increasing or decreasing, and does it impact or maintain biodiversity? Journal of Parasitology 89, s101s105.Google Scholar
Lafferty, KD and Gerber, LR (2002) Good medicine for conservation biology: the intersection of epidemiology and conservation theory. Conservation Biology 16, 593604.Google Scholar
LaPointe, DA, Atkinson, CT and Samuel, MD (2012) Ecology and conservation biology of avian malaria. Annals of the New York Academy of Sciences 1249, 211226.Google Scholar
Laurito, M, Visintin, AM and Almirón, WR (2008) Culex saltanensis morphological redescription of the immature and adult stages. Journal of the American Mosquito Control Association 24, 203210.Google Scholar
Lopes, LE et al. (2009) Aves da Chapada dos Guimarães, Mato grosso, Brasil: uma síntese histórica do conhecimento. Papéis Avulsos de Zoologia 49, 947.Google Scholar
Lourenço-de-Oliveira, R and de Castro, FA (1991). Culex saltanensis Dyar, 1928: natural vector of Plasmodium juxtanucleare in Rio de Janeiro, Brazil. Memórias do Instituto Oswaldo Cruz 86, 8794.Google Scholar
Lourenço-de-Oliveira, R et al. (1986) Alguns aspectos da ecologia dos mosquitos (Diptera, Culicidae) de uma área de planície (granjas Calábria), em Jacarepaguá, Rio de Janeiro: V. Criadouros. Memórias do Instituto Oswaldo Cruz 81, 265271.Google Scholar
Luttrell, MP et al. (2001) Mycoplasma gallisepticum in house finches (Carpodacus mexicanus) and other wild birds associated with poultry production facilities. Avian Diseases 45, 321329.Google Scholar
Massard, CL (1982) Caracterizacao do parasitismo por Plasmodium juxtanucleare (Haemosporidea:Plasmodiidae) em criacao de Gallus gallus da raca Leghorn Branca. Arquivos da Universidade Federal Rural do Rio de Janeiro 5, 141146.Google Scholar
Mennerat, A et al. (2010) Intensive farming: evolutionary implications for parasites and pathogens. Evolutionary Biology 37, 5967.Google Scholar
Mota, RA et al. (2000) Plasmodium juxtanucleare (Versiani e Gomes, 1941) em galinhas (Gallus gallus L., 1857) de criações rústicas no Estado de Pernambuco. Revista Brasileira de Ciência Veterinária 7, 188190.Google Scholar
Mukhin, A et al. (2016) The strategy to survive primary malaria infection: an experimental study on behavioural changes in parasitized birds. PLoS ONE 11, e0159216.Google Scholar
Murata, K et al. (2008) Plasmodium (Bennettinia) juxtanucleare infection in a captive white eared-pheasant (Crossoptilon crossoptilon) at a Japanese zoo. The Journal of Veterinary Medical Science 70, 203205.Google Scholar
Myers, N et al. (2000) Biodiversity hotspots for conservation priorities. Nature 403, 853858.Google Scholar
Norris, DE (2004) Mosquito-borne diseases as a consequence of land Use change. EcoHealth 1, 1924.Google Scholar
Omori, S et al. (2007) Complete nucleotide sequences of the mitochondrial genomes of two avian malaria protozoa, Plasmodium gallinaceum and Plasmodium juxtanucleare. Parasitology Research 100, 661664.Google Scholar
Pacheco, MA et al. (2011 a) Timing the origin of human malarias: the lemur puzzle. BMC Evolutionary Biology 11, 299.Google Scholar
Pacheco, MA et al. (2011 b) Haemosporidian infection in captive masked bobwhite quail (Colinus virginianus ridgwayi), an endangered subspecies of the northern bobwhite quail. Veterinary Parasitology 182, 113120.Google Scholar
Pacheco, MA et al. (2013) Malarial parasite diversity in chimpanzees: the value of comparative approaches to ascertain the evolution of Plasmodium falciparum antigens. Malaria Journal 12, 328.Google Scholar
Padilla, DP et al. (2017) Factors affecting the distribution of haemosporidian parasites within an oceanic island. International Journal for Parasitology 47, 225235.Google Scholar
Paraense, WL (1949) A survey on the occurrence of “Plasmodium juxtanucleare” in Bambuí (State of minas Gerais). Memórias do Instituto Oswaldo Cruz 47, 355359.Google Scholar
Pedersen, AB et al. (2007) Infectious diseases and extinction risk in wild mammals. Conservation Biology: The Journal of the Society for Conservation Biology 21, 12691279.Google Scholar
Podmokła, E et al. (2017) Effect of haemosporidian infections on host survival and recapture rate in the blue tit. Journal of Avian Biology 48, 796803.Google Scholar
Poulsen, J et al. (2000) Prevalence and distribution of gastro-intestinal helminths and haemoparasites in young scavenging chickens in upper eastern region of Ghana, West Africa. Preventive Veterinary Medicine 45, 237245.Google Scholar
Preece, ND et al. (2017) A guide for ecologists: detecting the role of disease in faunal declines and managing population recovery. Biological Conservation 214, 136146.Google Scholar
Prezoto, HHS et al. (2001) Aspectos do parasitismo de Plasmodium (Novyella) juxtanucleare Versiani & Gomes, 1941 em Gallus gallus L., 1758 em criação rústica no município de Santa Bárbara do Tugúrio – MG. Revista Brasileira de Ciência Veterinária 8, 6567.Google Scholar
Rambaut, A et al. (2015) Tracer v1. 6. Retrieved from Molecular evolution, phylogenetics and epidemiology website: http://tree.bio.ed.ac.uk/software/tracer/ (accessed 12 February 2018).Google Scholar
Reiter, ME and LaPointe, DA (2007) Landscape factors influencing the spatial distribution and abundance of mosquito vector Culex quinquefasciatus (Diptera: Culicidae) in a mixed residential-agricultural community in Hawai'i. Journal of Medical Entomology 44, 861868.Google Scholar
Ricklefs, RE et al. (2017) Avian migration and the distribution of malaria parasites in New World passerine birds. Journal of Biogeography 44, 11131123.Google Scholar
Robinson, RA et al. (2010) Emerging infectious disease leads to rapid population declines of common British birds. PLoS ONE 5, e12215.Google Scholar
Ronquist, F and Huelsenbeck, JP (2003) Mrbayes 3: Bayesian phylogenetic inference under mixed models. Bioinformatics (oxford, England) 19, 15721574.Google Scholar
Roos, FL et al. (2015) Prevalence and diversity of avian malaria parasites in migratory black skimmers (rynchops Niger, Laridae, charadriiformes) from the Brazilian Amazon basin. Parasitology Research 114, 39033911.Google Scholar
Sainsbury, AW and Vaughan-Higgins, RJ (2012) Analyzing disease risks associated with translocations. Conservation Biology 26, 442452.Google Scholar
Sambrook, J and Russell, DW (2001) Molecular Cloning: A Laboratory Manual. Cold Spring Harbor, New York: Cold Spring Harbor Laboratory Press.Google Scholar
Santiago-Alarcon, D, Palinauskas, V and Schaefer, HM (2012 a) Diptera vectors of avian Haemosporidian parasites: untangling parasite life cycles and their taxonomy. Biological Reviews 87, 928964.Google Scholar
Santiago-Alarcon, D et al. (2012 b) Bloodmeal analysis reveals avian Plasmodium infections and broad host preferences of Culicoides (Diptera: Ceratopogonidae) vectors. PLoS ONE 7, e31098.Google Scholar
Sehgal, RNM (2010) Deforestation and avian infectious diseases. Journal of Experimental Biology 213, 955960.Google Scholar
Sehgal, RNM (2015) Manifold habitat effects on the prevalence and diversity of avian blood parasites. International Journal for Parasitology: Parasites and Wildlife 4, 421430.Google Scholar
Sick, H (1997) Ornitologia Brasileira. Nova Fronteira, Rio de Janeiro, RJ.Google Scholar
Silveira, P, DaMatta, RA and Dagosto, M (2009) Hematological changes of chickens experimentally infected with Plasmodium (Bennettinia) juxtanucleare. Veterinary Parasitology 162, 257262.Google Scholar
Silveira, P et al. (2013) Interactions of Plasmodium juxtanucleare and chicken anaemia virus: establishing a model. Parasitology 140, 17771788.Google Scholar
Smith, KF, Acevedo-Whitehouse, K and Pedersen, AB (2009) The role of infectious diseases in biological conservation. Animal Conservation 12, 112.Google Scholar
Tattiyapong, M et al. (2016) Molecular characterization of Plasmodium juxtanucleare in Burmese red junglefowls (Gallus gallus spadiceus) in Thailand. The Journal of Protozoology Research 26, 110.Google Scholar
Tompkins, DM et al. (2015) Emerging infectious diseases of wildlife: a critical perspective. Trends in Parasitology 31, 149159.Google Scholar
Valkiūnas, G (2005) Avian Malaria Parasites and Other Haemosporidia, 1st Edition. Boca Raton, Florida: CRC Press.Google Scholar
van Riper, CI et al. (1986) The epizootiology and ecological significance of malaria in Hawaiian land birds. Ecological Monographs 56, 327344.Google Scholar
Vanstreels, RET et al. (2015) Epidemiology and pathology of avian malaria in penguins undergoing rehabilitation in Brazil. Veterinary Research 46, 30.Google Scholar
Versiani, V and Gomes, BF (1941) Sobre um novo hematozoario da galinha, Plasmodium juxtanucleare n. sp. (Nota previa). Revista Brasileira de Biologia 1, 231233.Google Scholar
Versiani, V and Gomes, BF (1943) Plasmodium juxtanucleare, parasita da galinha doméstica (Nota adicionais). Revista Brasileira de Biologia 3, 113117.Google Scholar
Vogel, HF (2014) Occurrence of the eastern slaty thrush (Turdidae) in southern Brazil during the non-breeding season. Brazilian Journal of Ornithology 22, 260264.Google Scholar
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