Circannual variation in blood parasitism in a sub-Saharan migrant passerine bird, the garden warbler

Journal of Evolutionary Biology

Volumn 26, Issue 5, 2013, Pages 1047-1059

  Hellgren, O ^a   Wood, M J ^b,c   Waldenstrom J ^d   Hasselquist, D ^b   Ottosson, U ^e   Stervander, M ^a   Bensch, S ^a  

^a LUND UNIVERSITY   (Sweden)

^b UNIVERSITY OF OXFORD   (United Kingdom)

^c UNIVERSITY OF GLOUCESTERSHIRE   (United Kingdom)

^d LINNAEUS UNIVERSITY   (Sweden)

^e UNIVERSITY OF JOS   (Nigeria)

Author keywords

Annual prevalence; Bird migration; Haemoproteus; Leucocytozoon; Plasmodium; Sylvia borin

Indexed keywords

BREEDING SITE; CIRCADIAN RHYTHM; HEMOPARASITE; HOST-PARASITE INTERACTION; MIGRATION; MIGRATORY SPECIES; PARASITE PREVALENCE; PARASITE TRANSMISSION; PHYLOGENY; PROTOZOAN; SONGBIRD; TAXONOMY;

ANIMAL; ARTICLE; BIRD DISEASE; COMPARATIVE STUDY; EVOLUTION; PARASITOLOGY; POPULATION MIGRATION; PREVALENCE; SONGBIRD;

ANIMAL MIGRATION; ANIMALS; BIOLOGICAL EVOLUTION; BIRD DISEASES; PREVALENCE; SONGBIRDS;

CAMPANIA [ITALY]; CAPRI; FENNOSCANDIA; ITALY; NAPOLI [CAMPANIA]; SWEDEN; WEST AFRICA;

AVES; HAEMOPROTEUS; HAEMOSPORIDA; LEUCOCYTOZOON; PASSERI; PASSERIFORMES; PLASMODIUM (APICOMPLEXA); SYLVIA BORIN;

EID: 84876962130     PISSN: 1010061X     EISSN: 14209101     Source Type: Journal    
DOI: 10.1111/jeb.12129     Document Type: Article

References (54)

1. Alerstam, T. 1990. Bird Migration. Cambridge University Press, Cambridge.
2. Applegate, J.E. 1971. Spring relapse of Plasmodium relictum infections in an experimental field population of English sparrows (Passer domesticus). J. Wildl. Dis. 7: 37-42.
3. Applegate, J.E., Beaudoin, R.L. & Seeley, D.C. 1971. The effect of spring relapse in English sparrows on infectivity of malaria to mosquitoes. J. Wildl. Dis. 7: 91-92.
4. Atkinson, C.T. & van Riper, C. III. 1991. Pathogenicity and epizootiology of avian haematozoa: Plasmodium, Leucocytozoon, and Haemoproteus. In Bird-parasite Interactions (Greenberg, J.E., Loye & M. Zuk, eds.). pp. 19-48. Oxford University Press, Oxford, U.K.
5. Beadell, J.S., Gering, E., Austin, J., Dumbacher, J.P., Peirce, M.A., Pratt, T.K. et al. 2004. Prevalence and differential host-specificity of two avian blood parasite genera in the Australo-Papuan region. Mol. Ecol. 13: 3829-3844.
6. Beadell, J.S., Ishtiaq, F., Covas, R., Melo, M., Warren, B.H., Atkinson, C.T. et al. 2006. Global phylogeographic limits of Hawaii's avian malaria. Proc. Biol. Sci. 273: 2935-2944.
7. Bensch, S., Perez-Tris, J., Waldenstrom, J. & Hellgren, O. 2004. Linkage between nuclear and mitochondrial DNA sequences in avian malaria parasites: multiple cases of cryptic speciation? Evolution 58: 1617-1621.
8. Bensch, S., Bengtsson, G. & Akesson, S. 2006a. Patterns of stable isotope signatures in willow warbler Phylloscopus trochilus feathers collected in Africa. J. Avian Biol. 37: 323-330.
9. Bensch, S., Waldenström, J., Jonzen, N., Westerdahl, H., Hansson, B., Sejberg, D. et al. 2006b Temporal dynamics and diversity of avian malaria parasites in a single host species. J. Animal Ecol. 76: 112-122.
10. 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. Mol. Ecol. Res. 9: 1353-1358.
11. Bonneaud, C., Perez-Tris, J., Federici, P., Chastel, O. & Sorci, G. 2006. Major histocompatibility alleles associated with local resistance to malaria in a passerine. Evolution 60: 383-389.
12. Cosgrove, C.L., Wood, M.J., Day, K.P. & Sheldon, B.C. 2008. Seasonal variation in Plasmodium prevalence in a population of blue tits Cyanistes caeruleus. J. Animal Ecol. 77: 540-548.
13. Cramp, S. 1980. Handbook of the Birds of Europe, the Middle East and North Africa: The Birds of the Western Palearctic. Oxford University Press, Oxford Eng., New York.
14. Cramp, S. 1988. Handbook of the Birds of Europe the Middle East and North Africa: The Birds of Western Palearctic. Oxford University Press, Oxford.
15. Crawley, M.J. 2007. The R Book. Wiley, Chichester.
16. Gylfe, A., Bergstrom, S., Lunstrom, J. & Olsen, B. 2000. Epidemiology - reactivation of Borrelia infection in birds. Nature 403: 724-725.
17. Hasselquist, D. 2007. Comparative immunoecology in birds: hypotheses and tests. J. Ornithol. 148: 571-582.
18. Hatchwell, B.J., Wood, M.J. & Anwar, M. 2000 The prevalence and ecology of the haematozoan parasites of European blackbirds Turdus merula. Can. J. Wild Dis. 78: 684-687.
19. Hellgren, O. 2005. The occurrence of haemosporidian parasites in the Fennoscandian bluethroat (Luscinia svecica) population. J. Ornithol. 146: 55-60.
20. Hellgren, O., Waldenstrom, J. & Bensch, S. 2004. A new PCR assay for simultaneous studies of Leucocytozoon, Plasmodium, and Haemoproteus from avian blood. J. Parasitol. 90: 797-802.
21. Hellgren, O., Waldenstrom, J., Perez-Tris, J., Szollosi, E., Hasselquist, D., Krizanauskiene, A. et al. 2007. Detecting shifts of transmission areas in avian blood parasites - a phylogenetic approach. Mol. Ecol. 16: 1281-1290.
22. Hellgren, O., Perez-Tris, J. & Bensch, S. 2009. A jack-of-all-trades and still a master of some: prevalence and host range in avian malaria and related blood parasites. Ecology 90: 2840-2849.
23. Ishiguro, F., Takada, N. & Masuzawa, T. 2005. Molecular evidence of the dispersal of Lyme disease Borrelia from the Asian continent to Japan via migratory birds. Japanese Journal of Infectious Diseases 58: 184-186.
24. Iwajomo, S.B., Ottosson, U., Barshep, Y., Helseth, A., Hulme, M.F., Stevens, M. et al. 2011. The stopover behaviour of the Garden Warbler Sylvia borin in Obudu, southeast Nigeria. Ornis Svecica 21: 29-36.
25. Knowles, S.C., Wood, M.J., Alves, R., Wilkin, T.A., Bensch, S. & Sheldon, B.C. 2011. Molecular epidemiology of malaria prevalence and parasitaemia in a wild bird population. Mol. Ecol. 20: 1062-1076.
26. Krizanauskiene, A., Hellgren, O., Kosarev, V., Sokolov, L., Bensch, S. & Valkiunas, G. 2006. Variation in host specificity between species of avian haemosporidian parasites: evidence from parasite morphology and cytochrome b gene sequences. J. Parasitol. 92: 1319-1324.
27. Latorre-Margalef, N., Gunnarsson, G., Munster, V.J., Fouchier, R.A.M., Osterhaus, A.D.M.E., Elmberg, J. et al. 2009. Effects of influenza A virus infection on migrating mallard ducks. Proc. Biol. Sci. 276: 1029-1036.
28. Loiseau, C., Zoorob, R., Garnier, S., Birard, J., Federici, P., Julliard, R. et al. 2008. Antagonistic effects of a MHC class I allele on malaria-infected house sparrows. Ecol. Lett. 11: 258-265.
29. Mackenzie, J.S., Gubler, D.J. & Petersen, L.R. 2004. Emerging flaviviruses: the spread and resurgence of Japanese encephalitis, West Nile and dengue viruses. Nat. Med. 10: S98-S109.
30. Møller, A.P. & Erritzøe, J. 1998. Host immune defence and migration in birds. Evol. Ecol. 12: 945-953.
31. Munster, V.J., Baas, C., Lexmond, P., Waldenstrom, J., Wallensten, A., Fransson, T. et al. 2007. Spatial, temporal, and species variation in prevalence of influenza A viruses in wild migratory birds. PLoS Pathog. 3: 630-638.
32. Olias, P., Wegelin, M., Zenker, W., Freter, S., Gruber, A.D. & Klopfleisch, R. 2011. Avian malaria deaths in parrots, Europe. Emerging Infect. Dis. 17: 950-952.
33. Olsen, B., Munster, V.J., Wallensten, A., Waldenstrom, J., Osterhaus, A.D.M.E. & Fouchier, R.A.M. 2006. Global patterns of influenza A virus in wild birds. Science 312: 384-388.
34. Ottosson, U., Waldenström, J., Hjort, C. & McGregor, R. 2005. Garden Warbler Sylvia borin migration in sub-Saharan West Africa: phenology and body mass changes. Ibis 147: 750-757.
35. Perez-Tris, J. & Bensch, S. 2005a. Diagnosing genetically diverse avian malarial infections using mixed-sequence analysis and TA-cloning. Parasitology 131: 15-23.
36. Perez-Tris, J. & Bensch, S. 2005b. Dispersal increases local transmission of avian malarial parasites. Ecol. Lett. 8: 838-845.
37. Perez-Tris, J., Hellgren, O., Krizanauskiene, A., Waldenstrîm, J., Secondi, J., Bonneaud, C. et al. 2007 Within-host speciation of malaria parasites. PLoS ONE.
38. Reullier, J., Perez-Tris, J., Bensch, S. & Secondi, J. 2006. Diversity, distribution and exchange of blood parasites meeting at an avian moving contact zone. Mol. Ecol. 15: 753-763.
39. Richardson, D.S., Jury, F.L., Blaakmeer, K., Komdeur, J. & Burke, T. 2001. Parentage assignment and extra-group paternity in a cooperative breeder: the Seychelles warbler (Acrocephalus sechellensis). Mol. Ecol. 10: 2263-2273.
40. Ricklefs, R.E. & Fallon, S.M. 2002. Diversification and host switching in avian malaria parasites. Proc. Biol. Sci. 269: 885-892.
41. Ricklefs, R.E., Fallon, S.M., Latta, S.C., Swanson, B.L. & Bermingham, E. 2005. Migrants and their parasites; a bridge between two worlds In: Birds of Two Worlds; The Ecology and Evolution of Migration, Vol. 1 (Greenberg, R., Marra & P.P, eds.). pp. 210-221. The Johns Hopkins University Press, Baltimore.
42. Sambrook, J., Fritch, F.J. & Maniatis, T. 2002. Molecular Cloning, A Laboratory Manual. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY.
43. Smith, R.P., Rand, P.W., Lacombe, E.H., Morris, S.R., Holmes, D.W. & Caporale, D.A. 1996. Role of bird migration in the long-distance dispersal of Ixodes dammini, the vector of Lyme disease. J. Infect. Dis. 174: 221-224.
44. Stenseth, N.C., Atshabar, B.B., Begon, M., Belmain, S.R., Bertherat, E., Carniel, E. et al. 2008. Plague: past, present, and future. Plos Medicine 5: 9-13.
45. Valkiunas, G. 2005 Avian Malaria Parasites and other Haemosporidia. CRC, Boca Raton, Florida.
46. Valkiūnas, G., Bensch, S., Iezhova, T.A., Krizanauskiene, A., Hellgren, O. & Bolshakov, C.V. 2006. Nested cytochrome b polymerase chain reaction diagnostics underestimate mixed infections of avian blood haemosporidian parasites: microscopy is still essential. J. Parasitol. 92: 418-422.
47. Waldenström, J., Bensch, S., Kiboi, S., Hasselquist, D. & Ottosson, U. 2002. Cross-species infection of blood parasites between resident and migratory songbirds in Africa. Mol. Ecol. 11: 1545-1554.
48. (Wernham, C.V. et al., eds) 2002. The Migration Atlas: Movement of the Birds of Britain and Ireland. T. & A.D. Poyser, London.
49. Westerdahl, H., Waldenstrom, J., Hansson, B., Hasselquist, D. & Schantz, von, T. & Bensch, S., 2005. Associations between malaria and MHC genes in a migratory songbird. Proc. Biol. Sci. 272: 1511-1518.
50. Westerdahl, H., Asghar, M., Hasselquist, D. & Bensch, S. 2012. Quantitative disease resistance: to better understand parasite-mediated selection on major histocompatibility complex. Proc. Biol. Sci. 279: 577-584.
51. Wood, S.N. 2004. Stable and efficient multiple smoothing parameter estimation for generalized additive models. Journal of the American Statistical Association 99: 673-686.
52. Wood, S.N. 2006 Generalized Additive Models: An Introduction with R. Chapman & Hall/CRC, London.
53. Wood, S.N. 2012. "mgcv". website accessed 9 Nov 2012: http://people.bath.ac.uk/sw283/mgcv/
54. Wood, M.J., Cosgrove, C.L., Wilkin, T.A., Knowles, S.C.L., Day, K.P. & Sheldon, B.C. 2007. Within-population variation in prevalence and lineage distribution of avian malaria in blue tits, Cyanistes caeruleus. Mol. Ecol. 16: 3263-3273.