Biogeographical patterns and co-occurrence of pathogenic infection across island populations of Berthelot's pipit (Anthus berthelotii)

Oecologia

Volumn 168, Issue 3, 2012, Pages 691-701

  Spurgin, Lewis G ^a   Illera, Juan Carlos ^b,c   Padilla, David P ^a,b   Richardson, David S ^a  

^a UNIVERSITY OF EAST ANGLIA   (United Kingdom)

^b INSTITUTO DE PRODUCTOS NATURALES Y AGROBIOLOGÍA   (Spain)

^c UNIVERSITY OF OVIEDO   (Spain)

Author keywords

Bird; Island; Malaria; Pox; Species area relationship

Indexed keywords

BLOOD; COEXISTENCE; COLONIZATION; DISEASE INCIDENCE; DISEASE PREVALENCE; DISEASE TRANSMISSION; DISPERSAL; HOST-PATHOGEN INTERACTION; ISLAND; MALARIA; MIGRATION; MOLECULAR ANALYSIS; PASSERINE; PREDICTION; PROTIST; SELECTION; SPATIOTEMPORAL ANALYSIS; SPECIES-AREA RELATIONSHIP; VIRAL DISEASE; ZOOGEOGRAPHY;

ANIMAL; ARTICLE; ATLANTIC ISLANDS; AVIAN MALARIA; BIRD DISEASE; BODY COMPOSITION; FOWLPOX VIRUS; HAEMOSPORIDA; ISOLATION AND PURIFICATION; PARASITOLOGY; PHYLOGEOGRAPHY; PLASMODIUM; POPULATION DYNAMICS; POXVIRUS INFECTION; PROTOZOAL INFECTION; SONGBIRD;

ANIMALS; ATLANTIC ISLANDS; AVIPOXVIRUS; BIRD DISEASES; BODY COMPOSITION; HAEMOSPORIDA; MALARIA, AVIAN; PASSERIFORMES; PHYLOGEOGRAPHY; PLASMODIUM; POPULATION DYNAMICS; POXVIRIDAE INFECTIONS; PROTOZOAN INFECTIONS;

ATLANTIC OCEAN; ATLANTIC OCEAN (NORTH);

ANTHUS BERTHELOTII; AVES; LEUCOCYTOZOON; TRYPANOSOMA;

EID: 84856800623     PISSN: 00298549     EISSN: None     Source Type: Journal    
DOI: 10.1007/s00442-011-2149-z     Document Type: Article

References (93)

1. Acevedo-Whitehouse K, Gulland F, Greig D, Amos W (2003) Inbreeding: disease susceptibility in California sea lions. Nature 422: 35.
2. Akey BL, Nayar JK, Forrester DJ (1981) Avian pox in Florida wild turkeys: Culex nigripalpus and Wyeomyia vanduzeei as experimental vectors. J Wildl Dis 17: 597.
3. Alcaide M et al (2010) MHC diversity and differential exposure to pathogens in kestrels (aves: Falconidae). Mol Ecol 19: 691-705.
4. Anderson RM, May RM (1979) Population biology of infectious diseases: part I. Nature 280: 361-367.
5. Anderson RM, May RM (1981) The population dynamics of microparasites and their invertebrate hosts. Philos Trans R Soc B Biol Sci 291: 451-524.
6. Apanius V (1991) Avian trypanosomes as models of hemoflagellate evolution. Parasitol Today 7: 87-90.
7. Apanius V, Yorinks N, Bermingham E, Ricklefs RE (2000) Island and taxon effects in parasitism and resistance of Lesser Antillean birds. Ecology 81: 1959-1969.
8. Atkinson CT, Dusek RJ, Lease JK (2001) Serological responses and immunity to superinfection with avian malaria in experimentally infected Hawaii amakihi. J Wildl Dis 37: 20-27.
9. Atkinson CT, Lease JK, Dusek RJ, Samuel MD (2005) Prevalence of pox-like lesions and malaria in forest bird communities on leeward Mauna Loa Volcano, Hawaii. Condor 107: 537-546.
10. Balmer O, Stearns SC, Schötzau A, Brun R (2009) Intraspecific competition between co-infecting parasite strains enhances host survival in African trypanosomes. Ecology 90: 3367-3378.
11. Beadell JS et al (2004) Prevalence and differential host-specificity of two avian blood parasite genera in the Australo-Papuan region. Mol Ecol 13: 3829-3844.
12. Bensch S, Åkesson S (2003) Temporal and spatial variation of hematozoans in Scandinavian willow warblers. J Parasitol 89: 388-391.
13. 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.
14. 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 Resour 9: 1353-1358.
15. 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.
16. Carrete M et al (2009) Goats, birds, and emergent diseases: apparent and hidden effects of exotic species in an island environment. Ecol Appl 19: 840-853.
17. Cornell HV (1986) Oak species attributes and host size influence cynipine wasp species richness. Ecology 67: 1582-1592.
18. Cosgrove CL, Wood MJ, Day KP, Sheldon BC (2008) Seasonal variation in Plasmodium prevalence in a population of blue tits Cyanistes caeruleus. J Anim Ecol 77: 540-548.
19. Coulson JC (1956) Mortality and egg production of the Meadow Pipit with special reference to altitude. Bird Study 3: 119-132.
20. Cox FE (2001) Concomitant infections, parasites and immune responses. Parasitology 122: S23-S28.
21. Cramp S (1985) The birds of the western palearctic. Oxford University Press, London.
22. Crawley MJ (2007) The R book. Wiley, Chichester.
23. Dale S, Kruszewicz A, Slagsvold T (1996) Effects of blood parasites on sexual and natural selection in the pied flycatcher. J Zool 238: 373-393.
24. Dobson AP (1988) Restoring island ecosystems: the potential of parasites to control introduced mammals. Conserv Biol 2: 31-39.
25. Dritschilo W, Cornell H, Nafus D, O'Connor B (1975) Insular biogeography: of mice and mites. Science 190: 467-469.
26. Dufva R (1996) Blood parasites, health, reproductive success, and egg volume in female Great Tits Parus major. J Avian Biol 27: 83-87.
27. Eggert LS, Terwilliger LA, Woodworth BL, Hart PJ, Palmer D, Fleischer RC (2008) Genetic structure along an elevational gradient in Hawaiian honeycreepers reveals contrasting evolutionary responses to avian malaria. Bmc Evol Biol 8: 315.
28. Fallon SM, Bermingham E, Ricklefs RE (2003) Island and taxon effects in parasitism revisited: avian malaria in the Lesser Antilles. Evolution 57: 606-615.
29. Fallon SM, Ricklefs RE, Latta SC, Bermingham E (2004) Temporal stability of insular avian malarial parasite communities. Proc R Soc Lond B Biol Sci 271: 493-500.
30. Freed LA, Cann RL (2006) DNA quality and accuracy of avian malaria PCR diagnostics: a review. Condor 108: 459-473.
31. Freeman S, Jackson WM (1990) Univariate metrics are not adequate to measure avian body size. Auk 107: 69-74.
32. Green AJ (2001) Mass/length residuals: measures of body condition or generators of spurious results? Ecology 82: 1473-1483.
33. Griffiths R, Double M, Orr K, Dawson RJG (1998) A DNA test to sex most birds. Mol Ecol 7: 1071-1075.
34. Guégan JF, Kennedy CR (1996) Parasite richness/sampling effort/host range: the fancy three-piece jigsaw puzzle. Parasitol Today 12: 367-369.
35. Gulland FMD (1995) The impact of infectious diseases on wild animal populations: a review. In: Grenfell BT, Dobson A (eds) Ecology of infectious diseases in natural populations. Cambridge University Press, Cambridge, pp 20-51.
36. Hall TA (1999) BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucleic Acid Symp Ser 41: 95-98.
37. Hamilton WD, Zuk M (1982) Heritable true fitness and bright birds: a role for parasites? Science 218: 384-387.
38. Haukisalmi V, Henttonen H (1993) Coexistence in helminths of the bank vole Clethrionomys glareolus. I. Patterns of co-occurrence. J Anim Ecol 62: 221-229.
39. Hellgren O, Bensch S, Malmqvist B (2008) Bird hosts, blood parasites and their vectors-associations uncovered by molecular analyses of blackfly blood meals. Mol Ecol 17: 1605-1613.
40. Hockin DC (1981) The environmental determinants of the insular butterfly faunas of the British Isles. Biol J Linn Soc 16: 63-70.
41. Hudson PJ, Dobson AP, Newborn D (1998) Prevention of population cycles by parasite removal. Science 282: 2256-2258.
42. Illera JC (2007) Bisbita Caminero Anthus berthelotii. In: Lorenzo JA (ed) Atlas de las aves nidificantes en el archipiélago Canario (1997-2003). General de Conservación de la Naturaleza-Sociedad Española de Ornitología, Madrid, pp 344-347.
43. Illera JC, Emerson BC, Richardson DS (2007) Population history of Berthelot's pipit: colonization, gene flow and morphological divergence in Macaronesia. Mol Ecol 16: 4599-4612.
44. Illera JC, Emerson BC, Richardson DS (2008) Genetic characterization, distribution and prevalence of avian pox and avian malaria in the Berthelot's pipit (Anthus bertheloti) in Macaronesia. Parasitol Res 103: 1435-1443.
45. Ishtiaq F et al (2008) Avian haematozoan parasites and their associations with mosquitoes across Southwest Pacific Islands. Mol Ecol 17: 4545-4555.
46. Ishtiaq F, Clegg SM, Phillimore AB, Black RA, Owens IPF, Sheldon BC (2010) Biogeographical patterns of blood parasite lineage diversity in avian hosts from southern Melanesian islands. J Biogeogr 37: 120-132.
47. Jarvi SI, Triglia D, Giannoulis A, Farias M, Bianchi K, Atkinson CT (2008) Diversity, origins and virulence of Avipoxviruses in Hawaiian forest birds. Conserv Genet 9: 339-348.
48. Johnson PTJ, Stanton DE, Preu ER, Forshay KJ, Carpenter SR (2008) Dining on disease: how interactions between infection and environment affect predation risk. Ecology 87: 1973-1980.
49. Kilpatrick AM et al (2006) Effects of chronic avian malaria (Plasmodium relictum) infection on reproductive success of Hawaii Amakihi (Hemignathus virens). Auk 123: 764-774.
50. Kleindorfer S, Dudaniec RY (2006) Increasing prevalence of avian poxvirus in Darwin's finches and its effect on male pairing success. J Avian Biol 37: 69-76.
51. Knowles SCL, Palinauskas V, Sheldon BC (2010) Chronic malaria infections increase family inequalities and reduce parental fitness: experimental evidence from a wild bird population. J Evol Biol 23: 557-569.
52. Kuris AM, Blaustein AR, Alio JJ (1980) Hosts as islands. Am Nat 116: 570-586.
53. Lee LH, Lee KH (1997) Application of the polymerase chain reaction for the diagnosis of fowl poxvirus infection. J Virol Methods 63: 113-119.
54. Lindström KM, Foufopoulos J, Pärn H, Wikelski M (2004) Immunological investments reflect parasite abundance in island populations of Darwin's finches. Proc R Soc Lond B Biol Sci 271: 1513-1519.
55. MacArthur RH, Wilson EO (1967) The theory of island biogeography. Princeton Univ Press, Princeton.
56. Marghoob AB (1995) Prevalence of a malarial parasite over time and space: Plasmodium mexicanum in its vertebrate host, the western fence lizard Sceloporus occidentalis. J Anim Ecol 64: 177-185.
57. Marzal A, Bensch S, Reviriego M, Balbontin J, de Lope F (2008) Effects of malaria double infection in birds: one plus one is not two. J Evol Biol 21: 979-987.
58. Maslov DA, Lukes J, Jirku M, Simpson L (1996) Phylogeny of trypanosomes as inferred from the small and large subunit rRNAs: implications for the evolution of parasitism in the trypanosomatid protozoa. Mol Biochem Parasitol 75: 197-205.
59. McCurdy DG, Shutler D, Mullie A, Forbes MR (1998) Sex-biased parasitism of avian hosts: relations to blood parasite taxon and mating system. Oikos 82: 303-312.
60. Møller AP, Nielsen JT (2007) Malaria and risk of predation: a comparative study of birds. Ecology 88: 871-881.
61. Mondal SP, Lucio-Martinez B, Buckles EL (2008) Molecular characterization of a poxvirus isolated from an American Flamingo (Phoeniconais ruber rubber). Avian Dis 52: 520-525.
62. Mougeot F, Redpath SM (2004) Sexual ornamentation relates to immune function in male red grouse Lagopus lagopus scoticus. J Avian Biol 35: 425-433.
63. Njabo KY et al (2011) Nonspecific patterns of vector, host and avian malaria parasite associations in a central African rainforest. Mol Ecol 20: 1049-1061.
64. Ortego JIN, Aparicio JM, Calabuig G, Cordero PJ (2007) Risk of ectoparasitism and genetic diversity in a wild lesser kestrel population. Mol Ecol 16: 3712-3720.
65. Pérez-Tris J, Hasselquist D, Hellgren O, Krizanauskiene A, Waldenström J, Bensch S (2005) What are malaria parasites? Trends Parasitol 21: 209-211.
66. R Development Core Team (2008) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna.
67. Richardson DS, Jury FL, 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.
68. Ricklefs RE (2010) Evolutionary diversification, coevolution between populations and their antagonists, and the filling of niche space. Proc Natl Acad Sci USA 107: 1265-1272.
69. Ricklefs RE et al (2008) Community relationships of avian malaria parasites in southern Missouri. Ecol Monogr 75: 543-559.
70. Ritchie BW (1995) Avian viruses: function and control. Wingers, Lake Worth.
71. Saito K et al (2009) Avian poxvirus infection in a white-tailed sea eagle (Haliaeetus albicilla) in Japan. Avian Pathol 38: 485-489.
72. Sehgal RNM, Jones HI, Smith TB (2001) Host specificity and incidence of Trypanosoma in some African rainforest birds: a molecular approach. Mol Ecol 10: 2319-2327.
73. Smits JE, Tella JL, Carrete M, Serrano D, Lopez G (2005) An epizootic of avian pox in endemic short-toed larks (Calandrella rufescens) and Berthelot's pipits (Anthus berthelotii) in the Canary Islands, Spain. Vet Pathol 42: 59-65.
74. Sokal RR, Rohlf FJ (1995) Biometry: the principles and practice of statistics in biological research. WH Freeman, New York.
75. Sol D, Jovani R, Torres J (2003) Parasite mediated mortality and host immune response explain age-related differences in blood parasitism in birds. Oecologia 135: 542-547.
76. Sorci G (1996) Patterns of haemogregarine load, aggregation and prevalence as a function of host age in the lizard Lacerta vivipara. J Parasitol 82: 676-678.
77. Spurgin LG, Richardson DS (2010) How pathogens drive genetic diversity: MHC, mechanisms and misunderstandings. Proc R Soc Lond B Biol Sci 277: 979-988.
78. Staats CM, Schall JJ (1996) Malarial parasites (Plasmodium) of Anolis lizards: Biogeography in the lesser Antilles. Biotropica 28: 388-393.
79. Tarello W (2008) Prevalence and clinical signs of avipoxvirus infection in falcons from the Middle East. Vet Dermatol 19: 101-104.
80. Tompkins DM, Dunn AM, Smith MJ, Telfer S (2010) Wildlife diseases: from individuals to ecosystems. J Anim Ecol 80: 19-38.
81. Valkiunas G (2005) Avian malaria parasites and other haemosporidia. CRC Press, Boca Raton.
82. Valkiunas G, Zickus T, Shapoval AP, Iezhova TA (2006) Effect of Haemoproteus belopolskyi (Haemosporida: Haemoproteidae) on body mass of the blackcap Sylvia atricapilla. J Parasitol 92: 1123-1125.
83. van Oers K, Richardson DS, Saether SA, Komdeur J (2010) Reduced blood parasite prevalence with age in the Seychelles Warbler: selective mortality or suppression of infection? J Ornithol 151: 69-77.
84. van Riper C, Forrester DJ (2007) Avian pox. In: Thomas N, Hunter B, and Atkinson CT (eds) Infectious and parasitic diseases of wild birds. Blackwell, Ames, pp 131-176.
85. van Riper C, van Riper SG, Goff ML, Laird M (1986) The epizootiology and ecological significance of malaria in Hawaiian land birds. Ecol Monogr 56: 327-344.
86. van Riper C, van Riper SG, Hansen WR (2002) Epizootiology and effect of avian pox on Hawaiian forest birds. Auk 119: 929-942.
87. Vögeli M, Lemus JA, Serrano D, Blanco G, Tella JL (2011) An island paradigm on the mainland: host population fragmentation impairs the community of avian pathogens. Proc R Soc Lond B Biol Sci. doi: 10. 1098/rspb. 2010. 1227.
88. Waldenstrom J, Bensch S, Hasselquist D, Ostman O (2004) A new nested polymerase chain reaction method very efficient in detecting Plasmodium and Haemoproteus infections from avian blood. J Parasitol 90: 191-194.
89. Walther BA, Cotgreave P, Price RD, Gregory RD, Clayton DH (1995) Sampling effort and parasite species richness. Parasitol Today 11: 306-310.
90. Westerdahl H, Waldenstrom J, Hansson B, Hasselquist D, von Schantz T, Bensch S (2005) Associations between malaria and MHC genes in a migratory songbird. Proc R Soc Lond B Biol Sci 272: 1511-1518.
91. Whittaker RJ (1998) Island biogeography. ecology, evolution, and conservation. Oxford University Press, New York.
92. Wiehn J, Korpimaki E, Pen I (1999) Haematozoan infections in the Eurasian kestrel: effects of fluctuating food supply and experimental manipulation of parental effort. Oikos 84: 87-98.
93. Wood MJ, Cosgrove CL, Wilkin TA, Knowles SCL, Day KP, Sheldon BC (2007) Within-population variation in prevalence and lineage distribution of avian malaria in blue tits, Cyanistes caeruleus. Mol Ecol 16: 3263-3273.