Altitudinal variation in haemosporidian parasite distribution in great tit populations

Parasites and Vectors

Volumn 6, Issue 1, 2013, Pages

  Rooyen, Juan Van ^a   Lalubin, Fabrice ^a   Glaizot, Olivier ^a,b   Christe, Philippe ^a  

^a UNIVERSITY OF LAUSANNE   (Switzerland)

^b Musee de Zoologie Lausanne   (Switzerland)

Author keywords

Haemoproteus; Leucocytozoon; Lineages; Parasite prevalence; Plasmodium

Indexed keywords

ALTITUDE; ANIMAL EXPERIMENT; ARTICLE; BIRD; BLOOD PARASITE; BREEDING; ENVIRONMENTAL FACTOR; HAEMOSPORIDA; HOST PARASITE INTERACTION; MIXED INFECTION; NONHUMAN; PARASITE; PLASMODIUM; POLYMERASE CHAIN REACTION;

ANIMALS; BIODIVERSITY; BIRD DISEASES; DNA, PROTOZOAN; GENETIC VARIATION; HAEMOSPORIDA; MOLECULAR SEQUENCE DATA; PASSERIFORMES; POLYMERASE CHAIN REACTION; PREVALENCE; PROTOZOAN INFECTIONS, ANIMAL; SEQUENCE ANALYSIS, DNA; SWITZERLAND; TOPOGRAPHY, MEDICAL;

AVES; HAEMOPROTEUS; HAEMOPROTEUS SP.; LEUCOCYTOZOON; PARUS MAJOR; PLASMODIUM PARASITES; PLASMODIUM RELICTUM; PLASMODIUM SP.;

EID: 84877046617     PISSN: None     EISSN: 17563305     Source Type: Journal    
DOI: 10.1186/1756-3305-6-139     Document Type: Article

References (61)

1. Valkiunas G, Avian Malaria Parasites and Other Haemosporidia Boca Raton: CRC Press 2005
2. Avian host-selection by Culex pipiens in experimental trials. Simpson JE, Folsom-O'Keefe CM, Childs JE, Simons LE, Andreadis TG, Diuk-Wasser MA, PLoS ONE 2009 4 7861 10.1371/journal.pone.0007861 19924251
3. New species of haemosporidian parasites (Haemosporida) from African rainforest birds, with remarks on their classification. Valkiunas G, Iezhova TA, Loiseau C, Chasar A, Thomas BS, Sehgal RNM, Parasitol Res 2008 103 1213 1228 10.1007/s00436-008-1118-x 18668264
4. MalAvi: a public database of malaria parasites and related Haemosporidians in avian hosts based on mitochondrial cytochrome b lineages. Bensch S, Hellgren O, Pérez-Tris J, Mol Ecol Res 2009 9 1353 1358 10.1111/j.1755-0998.2009.02692.x
5. Hippoboscid-transmitted Haemoproteus parasites (Haemosporida) infect Galapagos Pelecaniform birds: evidence from molecular and morphological studies, with a description of Haemoproteus iwa. Levin II, Valkiunas G, Santiago-Alarcon D, Cruz LL, Iezhova TA, Hailer F, Dearborn D, Schreiber EA, Fleischer RC, Ricklefs RE, Parker PG, O'Brien SL, Int J Parasitol 2011 41 1019 1027 10.1016/j.ijpara.2011.03.014 21683082
6. Novel Haemoproteus species (Haemosporida: Haemoproteidae) from the swallow-tailed gull (Lariidae), with remarks on the host range of hippoboscid-transmitted avian hemoproteids. Levin II, Valkiunas G, Parker PG, Iezhova TA, J Parasitol 2012 98 847 854 10.1645/GE-3007.1 22324933
7. High prevalence and lineage diversity of avian malaria in wild populations of great tits (Parus major) and mosquitoes (Culex pipiens). Glaizot O, Fumagalli L, Iritano K, Lalubin F, Van Rooyen J, Christe P, PLoS ONE 2012 7 34964 10.1371/journal.pone.0034964 22506060
8. Avian malaria infections in western European mosquitoes. Ventim R, Ramos JA, Osorio H, Lopes RJ, Perez-Tris J, Mendes L, Parasitol Res 2012 111 637 645 10.1007/s00436-012-2880-3 22427023
9. The epizootiology and ecological significance of malaria in hawaiian landbirds. Van Riper C, Van Riper SG, Goff ML, Laird M, Ecol Monogr 1986 56 327 344 10.2307/1942550
10. Genetic characterization of avian malaria (protozoa) in the endangered lesser kestrel, Falco naumanni. Ortego J, Calabuig G, Cordero PJ, Aparicio JM, Parasitol Res 2007 101 1153 1156 10.1007/s00436-007-0575-y 17514379 (Pubitemid 47228810)
11. Haemosporidian infection in passerine birds from lower saxony. Wiersch SC, Lubjuhn T, Maier WA, Kampen H, J Ornithol 2007 148 17 24 (Pubitemid 46071072)
12. Within-population variation in prevalence and lineage distribution of avian malaria in blue tits, Cyanistes caeruleus. Wood MJ, Cosgrove CL, Wilkin TA, Knowles SCL, Day KP, Sheldon BC, Mol Ecol 2007 16 3263 73 10.1111/j.1365-294X.2007.03362.x 17651202 (Pubitemid 47094286)
13. Haemosporidian blood parasites in European birds of prey and owls. Krone O, Waldenström J, Lessow O, Müller K, Iezhova TA, Fickel J, Bensch S, Valkiunas G, J Parasitol 2008 94 709 715 18605786 (Pubitemid 351999778)
14. Identification of blood parasites in old world warbler species from the Danube River Delta. Svoboda A, Marthinsen G, Lifjeld JT, Johnsen A, Turčoková L, Avian Dis 2009 53 634 636 10.1637/8842-040409-Case.1 20095169
15. Genetic diversity of avian blood parasites in SE Europe: Cytochrome b lineages of the genera Plasmodium and Haemoproteus (Haemosporida) from Bulgaria. Dimitrov D, Zehtindjiev P, Bensch S, Acta Parasitol 2010 55 201 209 10.2478/s11686-010-0029-z
16. Factors associated with the geographic distribution of leucocytozoa parasitizing nestling eagle owls (Bubo bubo): a local spatial-scale analysis. Ortego J, Cordero PJ, Conserv Genet 2010 11 1479 1487 10.1007/s10592-009-9978-x
17. Determinants of distribution and prevalence of avian malaria in blue tit populations across Europe: separating host and parasite effects. Szöllosi E, Cichon M, Eens M, Hasselquist D, Kempenaers B, Merino S, Nilsson JÅ Rosivall B, Rytkönen S, Török J, Wood MJ, Garamszegi LZ, J Evol Biol 2011 24 2014 2024 10.1111/j.1420-9101.2011.02339.x 21726328
18. Cross-species infection of blood parasites between resident and migratory songbirds in Africa. Waldenström J, Bensch S, Kiboi S, Hasselquist D, Ottosson U, Mol Ecol 2002 11 1545 1554 10.1046/j.1365-294X.2002.01523.x 12144673
19. Detecting shifts of transmission areas in avian blood parasites-a phylogenetic approach. Hellgren O, Waldenström J, Pérez-Tris J, Szöllosi E, Hasselquist D, Križanauskiene A, Ottosson U, Bensch S, Mol Ecol 2007 16 1281 1290 10.1111/j.1365-294X.2007.03227.x 17391413 (Pubitemid 46354197)
20. Molecular phylogenetic and morphological analysis of haemosporidian parasites (Haemosporida) in a naturally infected European songbird, the blackcap Sylvia atricapilla, with description of Haemoproteus pallidulus sp. nov. Križanauskiene A, Pérez-Tris J, Palinauskas V, Hellgren O, Bensch S, Valkiunas G, Parasitology 2010 137 217 227 10.1017/S0031182009991235 19765350
21. Prevalence, diversity, and interaction patterns of avian Haemosporidians in a four-year study of blackcaps in a migratory divide. Santiago-Alarcon D, Bloch R, Rolshausen G, Schaefer HM, Segelbacher G, Parasitology 2011 138 824 853 10.1017/S0031182011000515
22. Environmental temperature affects prevalence of blood parasites of birds on an elevation gradient: implications for disease in a warming climate. Zamora-Vilchis I, Williams SE, Johnson CN, PLoS ONE 2012 7 39208 10.1371/journal.pone.0039208 22723966
23. Twofold cost of reproduction: an increase in parental effort leads to higher malarial parasitaemia and to a decrease in resistance to oxidative stress. Christe P, Glaizot O, Strepparava N, Devevey G, Fumagalli L, Proc R Soc B 2012 279 1142 1149 10.1098/rspb.2011.1546 21920974
24. Haemoatozoa infections in a great tit Parus major population in Central Portugal: relationships with breeding effort and health. Norte AC, Araújo PM, Sampaio HL, Sousa JP, Ramos JA, Ibis 2009 151 677 688 10.1111/j.1474-919X. 2009.00960.x
25. Blood parasites, health, reproductive success, and egg volume in female great tits Parus major. Dufva R, J Avian Biol 1996 27 83 87 10.2307/3676964
26. Paternal investment affects prevalence of malaria. Richner H, Christe P, Oppliger A, Proc Natl Acad Sci USA 1995 92 1192 1194 10.1073/pnas.92.4.1192 7862659
27. Clutch size and malaria resistance. Oppliger A, Christe P, Richner H, Nature 1996 381 565 565 8637590
28. Clutch size and malarial parasites in female great tits. Oppliger A, Christe P, Richner H, Behav Ecol 1997 8 148 152 10.1093/beheco/8.2.148
29. Reproductive effort influences the prevalence of haematozoan parasites in great tits. Norris K, Anwar M, Read AF, J Anim Ecol 1994 63 601 610 10.2307/5226
30. Biogeography of avian blood parasites(Leucocytozoon spp.) in two resident hosts across Europe: phylogeographic structuring or the abundance-occupancy relationship? Jenkins T, Owens IPF, Mol Ecol 2011 20 3910 3920 10.1111/j.1365-294X.2011.05221.x 21880082
31. Predictive mapping of alpine grasslands in Switzerland: Species versus community approach. Zimmermann NE, Kienast F, J Veg Sci 1999 10 469 482 10.2307/3237182 (Pubitemid 29463894)
32. Host specificity in avian blood parasites: a study of Plasmodium and Haemoproteus mitochondrial DNA amplified from birds. Bensch S, Stjernman M, Hasselquist D, Östman O, Hansson B, Westerdahl H, Pinheiro RT, Proc R Soc B 2000 267 1583 1589 10.1098/rspb.2000.1181 11007335 (Pubitemid 30624131)
33. A new nested polymerase chain reaction method very efficient in detecting Plasmodium and Haemoproteus infections from avian blood. Waldenström J, Bensch S, Hasselquist D, Östman O, J Parasitol 2004 90 191 4 10.1645/GE-3221RN 15040694 (Pubitemid 38280755)
34. Avian haemosporidian persistence and co-infection in great tits at the individual level. Van Rooyen J, Lalubin F, Glaizot O, Christe P, Malaria J 2013 12 40 10.1186/1475-2875-12-40
35. A restriction site to differentiate Plasmodium and Haemoproteus infections in birds: on the inefficiency of general primers for detection of mixed infections. Martínez J, Martínez-de la Puente J, Herrero J, Del Cerro S, Rivero-de Aguilar J, Vásquez RA, Merino S, Lobato E, Parasitology 2009 136 713 722 10.1017/S0031182009006118 19416554
36. R-Cran Project, version 2.15.0. [ http://www.R-project.org ]
37. lme4: Linear mixed-effects models using S4 classes.R package version 0.99875-6. Bates DM, Sarkar D, 2007
38. Package "vegan" version 2.0-2. Oksanen J, Blanchet FG, Kindt R, Legendre P, Minchin PR, O'Hara RB, Simpson GL, Solymos P, Stevens MHH, Wagner H, [ http://cran.r-project.org/web/packages/vegan/index.html ] 2011
39. Kindt R, Coe R, Tree diversity analysis. A manual and software for common statistical methods for ecological and biodiversity studies Nairobi (Kenya): World Agroforestry Centre (ICRAF) 2005 [ISBN 92-9059-179-X]
40. Comparison of mitochondrial cytochrome b lineages and morphospecies of two avian malaria parasites of the subgenera Haemamoeba and Giovannolaia (Haemosporida: Plasmodiidae). Palinauskas V, Kosarev V, Shapoval A, Bensch S, Valkiunas GN, Zootaxa 2007 1626 39 50 (Pubitemid 350074111)
41. Variation in host specificity between species of avian haemosporidian parasites: evidence from parasite morphology and cyochrome b gene sequences. Križanauskiene A, Hellgren O, Kosarev V, Sokolov L, Bensch S, Valkiunas G, J Parasitol 2006 92 1319 1324 10.1645/GE-873R.1 17304814
42. Polymerase chain reaction-based identification of Plasmodium (Huffia) elongatum, with remarks on species identity of haemosporidian lineages deposited in GenBank. Valkiunas G, Zehtindjiev P, Dimitrov D, Križanauskiene A, Iezhova TA, Bensch S, Parasitol Res 2008 102 1185 1193 10.1007/s00436-008-0892-9 18270739
43. Global phylogeographic limits of Hawaii's avian malaria. Beadell JS, Ishtiaq F, Covas R, Melo M, Warren BH, Atkinson CT, Bensch S, Graves GR, Jhala YV, Peirce MA, Rahmani AR, Fonseca DM, Fleischer RC, Proc R Soc B 2006 237 2953 2944
44. Molecular epidemiology of malaria prevalence and parasitaemia in a wild bird population. Knowles SCL, Wood MJ, Alves R, Wilkin TA, Bensch S, Sheldon BC, Mol Ecol 2011 20 1062 1076 10.1111/j.1365-294X.2010.04909.x 21073677
45. Malariaparasiten in den Vögeln. Grassi B, Feletti R, Zentralbl Bakteriol Mikrobiol Hyg [B] 1891 9 403 409
46. Prevalence of blood parasites in European passeriform birds. Scheuerlein A, Ricklefs RE, Proc R Soc B 2004 271 1363 1370 10.1098/rspb.2004.2726 15306334 (Pubitemid 38858312)
47. Occurrence of biting midges (Culicoides spp.) at three different altitudes in an alpine region of Switzerland. Tschuor AC, Kauffmann C, Schaffner F, Mathis A, SAT 2009 151 215 221
48. Prevalence of avian haemotozoa in wild birds in a high-altitude forest in Japan. Imura T, Suzuki Y, Ejiri H, Sato Y, Ishida K, Sumiyama D, Murata K, Yukawa M, Vet Parasitol 2012 183 244 248 21831523
49. Leucocytozoon simondi in emperor geese from the Yukon-Kuskokwim delta in Alaska. Hollmén TE, Franson JC, Creekmore LH, Schmutz JA, Fowler AC, Condor 1998 100 402 404 10.2307/1370286 (Pubitemid 28235459)
50. Evolution, epidemiology, and population genetics of black flies (Diptera: Simuliidae). Adler PH, Cheke RA, Post RJ, Infect Genet Evol 2010 10 846 865 10.1016/j.meegid.2010.07.003 20624485
51. The new river connection to the black fly problem in southern West Virginia. Amrine JW, W Va AFES Bull 1982 678 1 30
52. Thompson JN, The geographic mosaic of coevolution Chicago IL: University of Chicago Press 2005
53. Dispersal increases local transmission of avian malarial parasites. Pérez-Tris J, Bensch S, Ecol Lett 2005 8 838 845 10.1111/j.1461-0248. 2005.00788.x (Pubitemid 41009259)
54. Sensitive measure of prevalence and parasitaemia of haemosporidia from European blackbird (Turdus merula) populations: value of PCR-RFLP and quantitative PCR. Bentz S, Rigaud T, Barroca M, Martin-Laurent F, Bru D, Moreau J, Faivre B, Parasitology 2006 133 685 692 10.1017/S0031182006001090 16948874 (Pubitemid 44763964)
55. Temporal dynamics and diversity of avian malaria parasites in a single host species. Bensch S, Waldenström J, Jonzén N, Westerdahl H, Hansson B, Sejberg D, Hasselquist D, J Anim Ecol 2007 76 112 122 10.1111/j.1365-2656.2006.01176.x 17184359 (Pubitemid 46019706)
56. Virulence. Bull JJ, Evolution 1994 48 1423 1437 10.2307/2410237
57. Host density and the evolution of parasite virulence. Knolle H, J Theor Biol 1989 136 199 207 10.1016/S0022-5193(89)80226-7 2779267 (Pubitemid 19060233)
58. Vertebrate host specificity of two avian malaria parasites of the subgenus Novyelia: Plasmodium nucleophilum and Plasmodium vaughani. Iezhova TA, Valkiunas G, Bairlein F, J Parasitol 2005 91 472 474 10.1645/GE-3377RN 15986631 (Pubitemid 40762625)
59. Plasmodium relictum (lineage SGS1) and Plasmodium ashfordi (lineage GRW2): The effects of the co-infection on experimentally infected passerine birds. Palinauskas V, Valkiunas G, Bolshakov CV, Bensch S, Exp Parasitol 2011 127 527 33 10.1016/j.exppara.2010.10.007 21050849
60. Effects of malaria double infection in birds: one plus one is not two. Marzal A, Bensch S, Reviriego M, Balbontin J, De Lope F, J Evol Biol 2008 21 979 87 10.1111/j.1420-9101.2008.01545.x 18462316 (Pubitemid 351832280)
61. Snow DW, Perrins CM, The Birds of the Western Palearctic Volume 2-Passerines Oxford, New York: Oxford University Press 1998