Description and molecular characterization of Plasmodium (Novyella) unalis sp. nov. from the Great Thrush (Turdus fuscater) in highland of Colombia

Parasitology Research

Volumn 112, Issue 12, 2013, Pages 4193-4204

  Mantilla, Juan S ^a   González, Angie D ^a   Valkiūnas, Gediminas ^b   Moncada, Ligia I ^a   Matta, Nubia E ^a  

^a UNIVERSIDAD NACIONAL DE COLOMBIA   (Colombia)

^b VILNIUS UNIVERSITY   (Lithuania)

Author keywords

[No Author keywords available]

Indexed keywords

CYTOCHROME B; PROTOZOAL DNA;

ARTICLE; AVIAN MALARIA; BLOOD SMEAR; BRAZIL; CHILE; COLOMBIA; CONTROLLED STUDY; COSTA RICA; CYTOCHROME B GENE; GAMETOCYTE; GENETIC DIFFERENCE; GENETIC DISTANCE; GENOME SIZE; GEOGRAPHIC AND GEOLOGICAL PHENOMENA; HIGHLAND; HOST PARASITE INTERACTION; MOLECULAR GENETICS; MORPHOLOGY; NEW SPECIES; NONHUMAN; NUCLEOTIDE SEQUENCE; PARASITE EXAMINATION; PARASITE TRANSMISSION; PHYLOGENY; PLASMODIUM; PLASMODIUM UNALIS; PLASMODIUM VAUGHANI; POLYMERASE CHAIN REACTION; PRIORITY JOURNAL; SCHIZONT; SEQUENCE HOMOLOGY; SPECIES COMPARISON; TROPHOZOITE; TURDIDAE FUSCATER; TURDUS; UNITED STATES;

AVES; PASSERIFORMES; TURDIDAE; TURDUS FUSCATER;

ALTITUDE; ANIMALS; COLOMBIA; CYTOCHROMES B; ERYTHROCYTES; GENES, MITOCHONDRIAL; GENES, PROTOZOAN; MALARIA, AVIAN; PHYLOGENY; PLASMODIUM; SONGBIRDS;

EID: 84890224405     PISSN: 09320113     EISSN: 14321955     Source Type: Journal    
DOI: 10.1007/s00436-013-3611-0     Document Type: Article

References (59)

1. Angel L, Ramírez A, Dominguez E (2010) Heat island and temperature spatiotemporal changes in Bogotá City. Rev Acad Colomb Cienc Exact Fis Nat 34:173-183
2. Asociacion Bogotana de Ornitologia (ed) (2000) Aves de la Sabana de Bogota, guia de campo. ABO CAR, Bogota
3. Bensch S, Stjernman M, Hasselquist D, Ostman O, Hannson B, Westerdahl H, Pinheiro RT (2000) Host specificity in avian blood parasites: a study of Plasmodium and Haemoproteus mitochondrial DNA amplified from birds. Proc R Soc Lond B Biol Sci 267:1583-1589. doi: 10.1098/rspb.2000.1181 (Pubitemid 30624131)
4. Bensch S, Hellgren O, Pérez-Tris J (2009) MalAvi: a public database of malaria parasites and related haemosporidians in avian hosts based on mitochondrial cytochrome b lineages. Mol Ecol Resour 9:1353-1358. doi: 10.1111/j.1755-0998.2009.02692.x
5. Bensch S, Pérez-Tris J, Waldenström J, Hellgren O (2004) Linkage between nuclear and mitochondrial DNA sequences in avian malaria parasites: multiple cases of cryptic speciation? Evolution 58:1617-1621. doi: 10.1111/j.0014-3820.2004.tb01742.x (Pubitemid 39033469)
6. Chavatte JM, Uzbekov R, Paperna I, Richard-Lenoble D, Landau I (2010) Ultrastructure of erythrocytic stages of avian Plasmodium spp. of the sub-genus Novyella and its "globule". Parasite 17:123-127. doi: 10.1051/parasite/2010172123
7. Corradetti A, Garnham PCC, Laird M (1963) New classification of the avian malaria parasites. Parassitologia 5:1-4
8. Corradetti A, Scanga M (1965) Notes on Plasmodium (Giovannolaia) polare and its transmission with Culiseta longiareolata. Parassitologia 7:61-64
9. Darriba D, Taboada GL, Doallo R, Posada D (2012) jModelTest 2: more models, new heuristics and parallel computing. Nat Methods 9:772. doi: 10.1038/nmeth.2109
10. Department of Geosciences Universidad Nacional de Colombia (2011) Boletín del análisis de las variables obtenidas en la estación meteorológica de la Universidad Nacional. http://www.geociencias.unal.edu.co/?niv=not¬=545&dep=12. Accessed 30 Apr 2013
11. Dodge M, Guers SL, Sekercioǧlu ÇH, Sehgal RNM (2013) North American transmission of hemosporidian parasites in the Swainson's thrush (Catharus ustulatus), a migratory songbird. J Parasitol 99:548-553. doi: 10.1645/GE-3134.1
12. Freed LA, Cann RL, Goff ML, Kuntz WA, Bodner GR (2005) Increase in avian malaria at upper elevation in Hawai'i. Condor 107:753-764. doi: 10.1650/7820.1 (Pubitemid 41698143)
13. Glaizot O, Fumagalli L, Iritano K, Lalubin F, Van Rooyen J, Christe P (2012) High prevalence and lineage diversity of avian malaria in wild populations of Great Tits (Parus major) and mosquitoes (Culex pipiens). PLoS ONE 7:e34964. doi: 10.1371/journal.pone.0034964
14. Grimm NB, Faeth SH, Golubiewski NE, Redman CL, Wu J, Bai X, Briggs JM (2008) Global change and the ecology of cities. Science 319:756-760. doi: 10.1126/science.1150195 (Pubitemid 351225834)
15. Hall TA (1999) BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucleic Acids Symp Ser 41:95-98
16. Hellgren O, Krizanauskiene A, Valkiunas G, Bensch S (2007) Diversity and phylogeny of mitochondrial cytochrome B lineages from six morphospecies of avian Haemoproteus (Haemosporida: Haemoproteidae). J Parasitol 93:889-896. doi: 10.1645/GE-1051R1.1 (Pubitemid 47502204)
17. Hellgren O, Waldenström J, Bensch S (2004) A new PCR assay for simultaneous studies of Leucocytozoon spp., Plasmodium spp. and Haemoproteus spp. from avian blood. J Parasitol 90:797-802. doi: 10.1645/GE-184R1 (Pubitemid 39128736)
18. Higgs S, Beaty BJ (2004) Natural cycles of vector-borne pathogens. In: Marquardt WC, Black WC, Freier JE, Hagedorn HH, Hemingway J, Higgs S, James AA, Kondratieff B, Moore CG (eds) Biology of disease vectors, 2nd edn. Elsevier Academic, San Diego, pp 167-186
19. Howe L, Castro IC, Schoener ER, Hunter S, Barraclough RK, Alley MR (2012) Malaria parasites (Plasmodium spp.) infecting introduced, native and endemic New Zealand birds. Parasitol Res 110:913-923. doi: 10.1007/s00436-011-2577-z
20. Inci A, Yildirim A, Njabo KY, Duzlu O, Biskin Z, Ciloglu A (2012) Detection and molecular characterization of avian Plasmodium from mosquitoes in central Turkey. Vet Parasitol 188:179-184. doi: 10.1016/j.vetpar.2012.02.012
21. Kim KS, Tsuda Y (2010) Seasonal changes in the feeding pattern of Culex pipiens pallens govern the transmission dynamics of multiple lineages of avian malaria parasites in Japanese wild bird community. Mol Ecol 19:5545-5554. doi: 10.1111/j.1365-294X.2010.04897.x
22. Kimura M, Darbro JM, Harrington LC (2010) Avian malaria parasites share congeneric mosquito vectors. J Parasitol 96:144-151. doi: 10.1645/GE-2060.1
23. Lacorte GA, Felix GM, Pinheiro RR, Chaves AV, Almeida-Neto G, Neves FS, Leite LO, Santos FR, Braga EM (2013) Exploring the diversity and distribution of neotropical avian malaria parasites - a molecular survey from southeast Brazil. PLoS ONE 8:e57770. doi: 10.1371/journal.pone.0057770
24. Landau I, Chavatte JM, Peters W, Chabaud A (2010) The sub-genera of avian Plasmodium. Parasite 17:3-7. doi: 10.1051/parasite/2010171003
25. LaPointe DA, Goff ML, Atkinson CT (2010) Thermal constraints to the sporogonic development and altitudinal distribution of avian malaria Plasmodium relictum in Hawai'i. J Parasitol 96:318-324. doi: 10.1645/GE-2290.1
26. Larkin MA, Blackshields G, Brown NP, Chenna R, McGettigan PA, McWilliam H, Valentin F, Wallace IM, Wilm A, Lopez R, Thompson JD, Gibson TJ, Higgins DG (2007) Clustal W and Clustal X version 2.0. Bioinformatics 23:2947-2948. doi: 10.1093/bioinformatics/btm404 (Pubitemid 350162903)
27. Leica Microsystems Switzerland Limited (2012) Software Leica Application Suite, LAS EZ Version 2.1.0. http://www.leica-microsystems.com/products/ microscope-software/educational/details/product/leica-las-ez/downloads/. Accessed 30 Sep 2012
28. Loiseau C, Harrigan RJ, Robert A, Bowie RC, Thomassen HA, Smith TB, Sehgal RN (2012) Host and habitat specialization of avian malaria in Africa. Mol Ecol 21:431-441. doi: 10.1111/j.1365-294X.2011.05341.x
29. Lotta IA, Matta NE, Torres RD, Moreno de Sandino M, Moncada LI (2013) Leucocytozoon fringillinarum and Leucocytozoon dubreuili in Turdus fuscater from a Colombian Páramo ecosystem. J Parasitol 99:359-362. doi: 10.1645/GE-3156.1
30. Mantilla JS, Matta NE, Pacheco MA, Escalante AA, Gonzalez AD, Moncada LI (2013) Identification of Plasmodium (Haemamoeba) lutzi (Lucena, 1939) from Turdus fuscater (Great Thrush) in Colombia. J Parasitol 99:662-668. doi: 10.1645/12-138.1
31. Martinsen ES, Paperna I, Schall JJ (2006) Morphological versus molecular identification of avian Haemosporidia: an exploration of three species concepts. Parasitology 133:279-288. doi: 10.1017/S0031182006000424 (Pubitemid 44214942)
32. Martinsen ES, Perkins SL, Schall JJ (2008) A three-genome phylogeny of malaria parasites (Plasmodium and closely related genera): evolution of life-history traits and host switches. Mol Phylogenet Evol 47:261-273. doi: 10.1016/j.ympev.2007.11.012
33. Merino S, Moreno J, Vásquez RA, Martínez J, Sánchez-Monsálvez 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 Ecol 33:329-340. doi: 10.1111/j.1442-9993.2008.01820.x (Pubitemid 351533700)
34. Miller MA, Pfeiffer W, Schwartz T (2010) Creating the CIPRES Science Gateway for inference of large phylogenetic trees. Proc Gatew Comput Environ Workshop (GCE) 1-8. doi: 10.1109/gce.2010.5676129
35. Molina LF, Osorio J, Uribe E (1997) Cerros, humedales y areas rurales: Santa Fe de Bogota. DAMA, Bogota
36. Møller AP, Erritzøe J, Karadas F (2010) Levels of antioxidants in rural and urban birds and their consequences. Oecologia 163:35-45. doi: 10.1007/s00442-009-1525-4
37. Pacheco MA, Escalante AA, Garner MM, Bradley GA, Aguilar RF (2011) Haemosporidian infection in captive masked bobwhite quail (Colinus virginianus ridgwayi), an endangered subspecies of the northern bobwhite quail. Vet Parasitol 182:113-120. doi: 10.1016/j.vetpar.2011.06.006
38. Rambaut A (2006) FigTree: tree figure drawing too, version1.3.1. Institute of Evolutionary Biology, University of Edinburgh. http://tree.bio.ed. ac.uk/software/figtree/. Accessed 12 May 2013
39. Rambaut A, Drummond AJ (2007) Tracer v1.5. http://tree.bio.ed.ac.uk/ software/tracer/. Accessed 12 May 2013
40. Remsen JV, Cadena CD, Jaramillo A, Nores M, Pacheco JF, Pérez-Emán J, Robbins MB, Stiles FG, Stotz DF, Zimmer KJ (2012) A classification of the bird species of South America. American Ornithologists' Union, version 7 December 2012. http://www.museum.lsu.edu/~Remsen/SACCBaseline. html. Accessed 7 Dec 2012
41. Ricklefs RE, Fallon SM (2002) Diversification and host switching in avian malaria parasites. Proc R Soc Lond B Biol Sci 269:885-892. doi: 10.1098/rspb.2001.1940 (Pubitemid 34518130)
42. Ricklefs RE, Outlaw DC (2010) A molecular clock for malaria parasites. Science 329:226-229. doi: 10.1126/science.1188954
43. Ridgely RS, Allnutt TF, Brooks T, McNicol DK, Mehlman DW, Young BE, Zook JR, International Birdlife (2012) Digital distribution maps of the birds of the western hemisphere, version 5.0. In BirdLife International and NatureServe. Bird species distribution maps of the world. Turdus fuscater. In: IUCN Red List of Threatened Species. Version 2012.2. http://maps.iucnredlist.org/map.html?id= 106006415. Accessed 12 May 2013
44. Rodríguez OA, Moya H, Matta NE (2009) Avian blood parasites in the National Natural Park Chingaza: high Andes of Colombia. Hornero 24:1-6
45. Ronquist F, Huelsenbeck JP (2003) MrBayes 3: Bayesian phylogenetic inference under mixed models. Bioinformatics 19:1572-1574. doi: 10.1093/bioinformatics/btg180 (Pubitemid 37038874)
46. Salazar MJ, Moncada LI (2004) Life cycle of Culex quinquefasciatus Say (Diptera: Culicidae) under uncontrolled conditions. Biomedica 24:385-392
47. Sambrook J, Fritsch EF, Maniatis T (1989) Chapter 6 Preparation and analysis of eukaryotic genomic DNA. In: Molecular cloning a laboratory manual, 2nd edn. Cold Spring Harbor Laboratory, New York, pp 6.4-6.12
48. Santiago-Alarcon D, Palinauskas V, Schaefer HM (2012) Diptera vectors of avian haemosporidian parasites: untangling parasite life cycles and their taxonomy. Biol Rev Camb Philos Soc 87:928-964. doi: 10.1111/j.1469-185X.2012. 00234.x
49. Schmidt KA, Ostfeld RS (2001) Biodiversity and the dilution effect in disease ecology. Ecology 82:609-619. doi: 10.1890/0012-9658(2001)082[0609: BATDEI]2.0.CO;2 (Pubitemid 32175310)
50. Schneider CA, Rasband WS, Eliceiri KW (2012) NIH Image to ImageJ: 25 years of image analysis. Nat Methods 9:671-675. doi: 10.1038/nmeth.2089
51. Shahabuddin M, Costero A (2001) Spatial distribution of factors that determine sporogonic development of malaria parasites in mosquitoes. Insect Biochem Mol Biol 31:231-240 (Pubitemid 32194778)
52. Tamura K, Peterson D, Peterson N, Stecher G, Nei M, Kumar S (2011) MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol Biol Evol 28:2731-2739. doi: 10.1093/molbev/msr121
53. Valkiunas G (2005) Avian malaria parasites and other haemosporidia. CRC, Boca Raton
54. Valkiunas G, Iezhova TA, Krizanauskiene A, Palinauskas V, Bensch S (2008a) In vitro hybridization of Haemoproteus spp.: an experimental approach for direct investigation of reproductive isolation of parasites. J Parasitol 94:1385-1394. doi: 10.1645/GE-1569.1
55. Valkiunas G, Iezhova TA, Loiseau C, Smith TB, Sehgal RN (2009) New malaria parasites of the subgenus Novyella in African rainforest birds, with remarks on their high prevalence, classification and diagnostics. Parasitol Res 104:1061-1077. doi: 10.1007/s00436-008-1289-5
56. Valkiunas G, Zehtindjiev P, Dimitrov D, Krizanauskiene A, Iezhova TA, Bensch S (2008b) Polymerase chain reaction-based identification of Plasmodium (Huffia) elongatum, with remarks on species identity of haemosporidian lineages deposited in GenBank. Parasitol Res 102:1185-1193. doi: 10.1007/s00436-008-0892- 9
57. Zamora-Vilchis I, Williams SE, Johnson CN (2012) Environmental temperature affects prevalence of blood parasites of birds on an elevation gradient: implications for disease in a warming climate. PLoS ONE 7:e39208. doi: 10.1371/journal.pone.0039208
58. Zehtindjiev P, Krizanauskiene A, Bensch S, Palinauskas V, Asghar M, Dimitrov D, Scebba S, Valkiunas G (2012a) A new morphologically distinct avian malaria parasite that fails detection by established polymerase chain reaction-based protocols for amplification of the cytochrome B gene. J Parasitol 98:657-665. doi: 10.1645/GE-3006.1
59. Zehtindjiev P, Križanauskiene A, Scebba S, Dimitrov D, Valkiunas G, Hegemann A, Tieleman BI, Bensch S (2012b) Haemosporidian infections in skylarks (Alauda arvensis): a comparative PCR-based and microscopy study on the parasite diversity and prevalence in southern Italy and the Netherlands. Eur J Wildl Res 58:335-344. doi: 10.1007/s10344-011-0586-y