, Volume 168, Issue 3, pp 691–701 | Cite as

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

  • Lewis G. Spurgin
  • Juan Carlos Illera
  • David P. Padilla
  • David S. Richardson
Population ecology - Original Paper


Pathogens can exert strong selective forces upon host populations. However, before we can make any predictions about the consequences of pathogen-mediated selection, we first need to determine whether patterns of pathogen distribution are consistent over spatiotemporal scales. We used molecular techniques to screen for a variety of blood pathogens (avian malaria, pox and trypanosomes) over a three-year time period across 13 island populations of the Berthelot’s pipit (Anthus berthelotii). This species has only recently dispersed across its range in the North Atlantic, with little subsequent migration, providing an ideal opportunity to examine the causes and effects of pathogenic infection in populations in the early stages of differentiation. We screened 832 individuals, and identified two strains of Plasmodium, four strains of Leucocytozoon, and one pox strain. We found strong differences in pathogen prevalence across populations, ranging from 0 to 65%, and while some fluctuations in prevalence occurred, these differences were largely stable over the time period studied. Smaller, more isolated islands harboured fewer pathogen strains than larger, less isolated islands, indicating that at the population level, colonization and extinction play an important role in determining pathogen distribution. Individual-level analyses confirmed the island effect, and also revealed a positive association between Plasmodium and pox infection, which could have arisen due to dual transmission of the pathogens by the same vectors, or because one pathogen lowers resistance to the other. Our findings, combined with an effect of infection on host body condition, suggest that Berthelot’s pipits are subject to different levels of pathogen-mediated selection both across and within populations, and that these selective pressures are consistent over time.


Malaria Pox Island Bird Species–area relationship 



The Canary and Madeiran governments kindly gave permission to work in Macaronesia. Laura García and Felipe Rodríguez-Godoy provided invaluable assistance in the field. Kirsty Hodgson, Sarah Holmes and David Wright assisted with the molecular work, and James Kitson helped with the figures. The local governments of Fuerteventura, La Gomera, La Palma and El Hierro provided accommodation. José Ramón Rodríguez-Delgado provided accommodation in Lanzarote. Staff from the Natural Park of Madeira provided logistical support in the Madeiran and Selvagens archipelagos, and the Portuguese Navy helped with transport to Selvagem Grande and Deserta Grande. We thank two anonymous reviewers for comments on the manuscript. This work was funded by a Ph.D. Grant from the Natural Environment Research Council to DSR and LGS, and a Spanish fellowship (Ramón y Cajal program) to JCI.

Supplementary material

442_2011_2149_MOESM1_ESM.doc (35 kb)
Supplementary material 1 (DOC 35 kb)


  1. Acevedo-Whitehouse K, Gulland F, Greig D, Amos W (2003) Inbreeding: disease susceptibility in California sea lions. Nature 422:35PubMedCrossRefGoogle Scholar
  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 17:597PubMedGoogle Scholar
  3. Alcaide M et al (2010) MHC diversity and differential exposure to pathogens in kestrels (aves: Falconidae). Mol Ecol 19:691–705PubMedCrossRefGoogle Scholar
  4. Anderson RM, May RM (1979) Population biology of infectious diseases: part I. Nature 280:361–367PubMedCrossRefGoogle Scholar
  5. Anderson RM, May RM (1981) The population dynamics of microparasites and their invertebrate hosts. Philos Trans R Soc B Biol Sci 291:451–524CrossRefGoogle Scholar
  6. Apanius V (1991) Avian trypanosomes as models of hemoflagellate evolution. Parasitol Today 7:87–90PubMedCrossRefGoogle Scholar
  7. Apanius V, Yorinks N, Bermingham E, Ricklefs RE (2000) Island and taxon effects in parasitism and resistance of Lesser Antillean birds. Ecology 81:1959–1969CrossRefGoogle Scholar
  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 37:20–27PubMedGoogle Scholar
  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 107:537–546CrossRefGoogle Scholar
  10. Balmer O, Stearns SC, Schötzau A, Brun R (2009) Intraspecific competition between co-infecting parasite strains enhances host survival in African trypanosomes. Ecology 90:3367–3378PubMedCrossRefGoogle Scholar
  11. Beadell JS et al (2004) Prevalence and differential host-specificity of two avian blood parasite genera in the Australo-Papuan region. Mol Ecol 13:3829–3844PubMedCrossRefGoogle Scholar
  12. Bensch S, Åkesson S (2003) Temporal and spatial variation of hematozoans in Scandinavian willow warblers. J Parasitol 89:388–391PubMedCrossRefGoogle Scholar
  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 58:1617–1621PubMedGoogle Scholar
  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 9:1353–1358PubMedCrossRefGoogle Scholar
  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 60:383–389PubMedGoogle Scholar
  16. Carrete M et al (2009) Goats, birds, and emergent diseases: apparent and hidden effects of exotic species in an island environment. Ecol Appl 19:840–853PubMedCrossRefGoogle Scholar
  17. Cornell HV (1986) Oak species attributes and host size influence cynipine wasp species richness. Ecology 67:1582–1592CrossRefGoogle Scholar
  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 77:540–548PubMedCrossRefGoogle Scholar
  19. Coulson JC (1956) Mortality and egg production of the Meadow Pipit with special reference to altitude. Bird Study 3:119–132CrossRefGoogle Scholar
  20. Cox FE (2001) Concomitant infections, parasites and immune responses. Parasitology 122:S23–S28PubMedCrossRefGoogle Scholar
  21. Cramp S (1985) The birds of the western palearctic. Oxford University Press, LondonGoogle Scholar
  22. Crawley MJ (2007) The R book. Wiley, ChichesterCrossRefGoogle Scholar
  23. Dale S, Kruszewicz A, Slagsvold T (1996) Effects of blood parasites on sexual and natural selection in the pied flycatcher. J Zool 238:373–393CrossRefGoogle Scholar
  24. Dobson AP (1988) Restoring island ecosystems: the potential of parasites to control introduced mammals. Conserv Biol 2:31–39CrossRefGoogle Scholar
  25. Dritschilo W, Cornell H, Nafus D, O’Connor B (1975) Insular biogeography: of mice and mites. Science 190:467–469PubMedCrossRefGoogle Scholar
  26. Dufva R (1996) Blood parasites, health, reproductive success, and egg volume in female Great Tits Parus major. J Avian Biol 27:83–87Google Scholar
  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 8:315PubMedCrossRefGoogle Scholar
  28. Fallon SM, Bermingham E, Ricklefs RE (2003) Island and taxon effects in parasitism revisited: avian malaria in the Lesser Antilles. Evolution 57:606–615PubMedGoogle Scholar
  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 271:493–500CrossRefGoogle Scholar
  30. Freed LA, Cann RL (2006) DNA quality and accuracy of avian malaria PCR diagnostics: a review. Condor 108:459–473CrossRefGoogle Scholar
  31. Freeman S, Jackson WM (1990) Univariate metrics are not adequate to measure avian body size. Auk 107:69–74Google Scholar
  32. Green AJ (2001) Mass/length residuals: measures of body condition or generators of spurious results? Ecology 82:1473–1483CrossRefGoogle Scholar
  33. Griffiths R, Double M, Orr K, Dawson RJG (1998) A DNA test to sex most birds. Mol Ecol 7:1071–1075PubMedCrossRefGoogle Scholar
  34. Guégan JF, Kennedy CR (1996) Parasite richness/sampling effort/host range: the fancy three-piece jigsaw puzzle. Parasitol Today 12:367–369PubMedCrossRefGoogle Scholar
  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 20–51CrossRefGoogle Scholar
  36. Hall TA (1999) BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucleic Acid Symp Ser 41:95–98Google Scholar
  37. Hamilton WD, Zuk M (1982) Heritable true fitness and bright birds: a role for parasites? Science 218:384–387PubMedCrossRefGoogle Scholar
  38. Haukisalmi V, Henttonen H (1993) Coexistence in helminths of the bank vole Clethrionomys glareolus. I. Patterns of co-occurrence. J Anim Ecol 62:221–229Google Scholar
  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 17:1605–1613PubMedCrossRefGoogle Scholar
  40. Hockin DC (1981) The environmental determinants of the insular butterfly faunas of the British Isles. Biol J Linn Soc 16:63–70CrossRefGoogle Scholar
  41. Hudson PJ, Dobson AP, Newborn D (1998) Prevention of population cycles by parasite removal. Science 282:2256–2258PubMedCrossRefGoogle Scholar
  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 344–347Google Scholar
  43. Illera JC, Emerson BC, Richardson DS (2007) Population history of Berthelot’s pipit: colonization, gene flow and morphological divergence in Macaronesia. Mol Ecol 16:4599–4612PubMedCrossRefGoogle Scholar
  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 103:1435–1443PubMedCrossRefGoogle Scholar
  45. Ishtiaq F et al (2008) Avian haematozoan parasites and their associations with mosquitoes across Southwest Pacific Islands. Mol Ecol 17:4545–4555PubMedCrossRefGoogle Scholar
  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 37:120–132CrossRefGoogle Scholar
  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 9:339–348CrossRefGoogle Scholar
  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 87:1973–1980CrossRefGoogle Scholar
  49. Kilpatrick AM et al (2006) Effects of chronic avian malaria (Plasmodium relictum) infection on reproductive success of Hawaii Amakihi (Hemignathus virens). Auk 123:764–774CrossRefGoogle Scholar
  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 37:69–76Google Scholar
  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 23:557–569PubMedCrossRefGoogle Scholar
  52. Kuris AM, Blaustein AR, Alio JJ (1980) Hosts as islands. Am Nat 116:570–586CrossRefGoogle Scholar
  53. Lee LH, Lee KH (1997) Application of the polymerase chain reaction for the diagnosis of fowl poxvirus infection. J Virol Methods 63:113–119CrossRefGoogle Scholar
  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 271:1513–1519CrossRefGoogle Scholar
  55. MacArthur RH, Wilson EO (1967) The theory of island biogeography. Princeton Univ Press, PrincetonGoogle Scholar
  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 64:177–185CrossRefGoogle Scholar
  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 21:979–987PubMedCrossRefGoogle Scholar
  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 75:197–205PubMedCrossRefGoogle Scholar
  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 82:303–312CrossRefGoogle Scholar
  60. Møller AP, Nielsen JT (2007) Malaria and risk of predation: a comparative study of birds. Ecology 88:871–881PubMedCrossRefGoogle Scholar
  61. Mondal SP, Lucio-Martinez B, Buckles EL (2008) Molecular characterization of a poxvirus isolated from an American Flamingo (Phoeniconais ruber rubber). Avian Dis 52:520–525PubMedCrossRefGoogle Scholar
  62. Mougeot F, Redpath SM (2004) Sexual ornamentation relates to immune function in male red grouse Lagopus lagopus scoticus. J Avian Biol 35:425–433CrossRefGoogle Scholar
  63. Njabo KY et al (2011) Nonspecific patterns of vector, host and avian malaria parasite associations in a central African rainforest. Mol Ecol 20:1049–1061PubMedCrossRefGoogle Scholar
  64. Ortego JIN, Aparicio JM, Calabuig G, Cordero PJ (2007) Risk of ectoparasitism and genetic diversity in a wild lesser kestrel population. Mol Ecol 16:3712–3720PubMedCrossRefGoogle Scholar
  65. Pérez-Tris J, Hasselquist D, Hellgren O, Krizanauskiene A, Waldenström J, Bensch S (2005) What are malaria parasites? Trends Parasitol 21:209–211PubMedCrossRefGoogle Scholar
  66. R Development Core Team (2008) R: a language and environment for statistical computing. R Foundation for Statistical Computing, ViennaGoogle Scholar
  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 10:2263–2273PubMedCrossRefGoogle Scholar
  68. Ricklefs RE (2010) Evolutionary diversification, coevolution between populations and their antagonists, and the filling of niche space. Proc Natl Acad Sci USA 107:1265–1272PubMedCrossRefGoogle Scholar
  69. Ricklefs RE et al (2008) Community relationships of avian malaria parasites in southern Missouri. Ecol Monogr 75:543–559CrossRefGoogle Scholar
  70. Ritchie BW (1995) Avian viruses: function and control. Wingers, Lake WorthGoogle Scholar
  71. Saito K et al (2009) Avian poxvirus infection in a white-tailed sea eagle (Haliaeetus albicilla) in Japan. Avian Pathol 38:485–489PubMedCrossRefGoogle Scholar
  72. Sehgal RNM, Jones HI, Smith TB (2001) Host specificity and incidence of Trypanosoma in some African rainforest birds: a molecular approach. Mol Ecol 10:2319–2327PubMedCrossRefGoogle Scholar
  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 42:59–65PubMedCrossRefGoogle Scholar
  74. Sokal RR, Rohlf FJ (1995) Biometry: the principles and practice of statistics in biological research. WH Freeman, New YorkGoogle Scholar
  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 135:542–547PubMedGoogle Scholar
  76. Sorci G (1996) Patterns of haemogregarine load, aggregation and prevalence as a function of host age in the lizard Lacerta vivipara. J Parasitol 82:676–678PubMedCrossRefGoogle Scholar
  77. Spurgin LG, Richardson DS (2010) How pathogens drive genetic diversity: MHC, mechanisms and misunderstandings. Proc R Soc Lond B Biol Sci 277:979–988CrossRefGoogle Scholar
  78. Staats CM, Schall JJ (1996) Malarial parasites (Plasmodium) of Anolis lizards: Biogeography in the lesser Antilles. Biotropica 28:388–393CrossRefGoogle Scholar
  79. Tarello W (2008) Prevalence and clinical signs of avipoxvirus infection in falcons from the Middle East. Vet Dermatol 19:101–104PubMedCrossRefGoogle Scholar
  80. Tompkins DM, Dunn AM, Smith MJ, Telfer S (2010) Wildlife diseases: from individuals to ecosystems. J Anim Ecol 80:19–38PubMedCrossRefGoogle Scholar
  81. Valkiunas G (2005) Avian malaria parasites and other haemosporidia. CRC Press, Boca RatonGoogle Scholar
  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 92:1123–1125PubMedCrossRefGoogle Scholar
  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 151:69–77CrossRefGoogle Scholar
  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 131–176Google Scholar
  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 56:327–344CrossRefGoogle Scholar
  86. van Riper C, van Riper SG, Hansen WR (2002) Epizootiology and effect of avian pox on Hawaiian forest birds. Auk 119:929–942CrossRefGoogle Scholar
  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 90:191–194PubMedCrossRefGoogle Scholar
  89. Walther BA, Cotgreave P, Price RD, Gregory RD, Clayton DH (1995) Sampling effort and parasite species richness. Parasitol Today 11:306–310PubMedCrossRefGoogle Scholar
  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 272:1511–1518CrossRefGoogle Scholar
  91. Whittaker RJ (1998) Island biogeography. ecology, evolution, and conservation. Oxford University Press, New YorkGoogle Scholar
  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 84:87–98CrossRefGoogle Scholar
  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 16:3263–3273PubMedCrossRefGoogle Scholar

Copyright information

© Springer-Verlag 2011

Authors and Affiliations

  • Lewis G. Spurgin
    • 1
  • Juan Carlos Illera
    • 2
    • 3
  • David P. Padilla
    • 1
    • 2
  • David S. Richardson
    • 1
  1. 1.Centre for Ecology, Evolution and Conservation, School of Biological SciencesUniversity of East AngliaNorwichUK
  2. 2.Island Ecology and Evolution Research Group, (IPNA-CSIC)TenerifeSpain
  3. 3.Research Unit of Biodiversity (UO/CSIC/PA), Departamento de Biología de Organismos y SistemasOviedo UniversityOviedoSpain

Personalised recommendations