Skip to main content
Log in

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

  • Population ecology - Original Paper
  • Published:
Oecologia Aims and scope Submit manuscript

Abstract

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.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3a–b

Similar content being viewed by others

References

  • Acevedo-Whitehouse K, Gulland F, Greig D, Amos W (2003) Inbreeding: disease susceptibility in California sea lions. Nature 422:35

    Article  PubMed  CAS  Google Scholar 

  • 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

    PubMed  CAS  Google Scholar 

  • Alcaide M et al (2010) MHC diversity and differential exposure to pathogens in kestrels (aves: Falconidae). Mol Ecol 19:691–705

    Article  PubMed  CAS  Google Scholar 

  • Anderson RM, May RM (1979) Population biology of infectious diseases: part I. Nature 280:361–367

    Article  PubMed  CAS  Google Scholar 

  • Anderson RM, May RM (1981) The population dynamics of microparasites and their invertebrate hosts. Philos Trans R Soc B Biol Sci 291:451–524

    Article  Google Scholar 

  • Apanius V (1991) Avian trypanosomes as models of hemoflagellate evolution. Parasitol Today 7:87–90

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    PubMed  CAS  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  PubMed  Google Scholar 

  • 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

    Article  PubMed  Google Scholar 

  • Bensch S, Åkesson S (2003) Temporal and spatial variation of hematozoans in Scandinavian willow warblers. J Parasitol 89:388–391

    Article  PubMed  Google Scholar 

  • 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

    PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  Google Scholar 

  • 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

    PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  Google Scholar 

  • Cornell HV (1986) Oak species attributes and host size influence cynipine wasp species richness. Ecology 67:1582–1592

    Article  Google Scholar 

  • 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

    Article  PubMed  Google Scholar 

  • Coulson JC (1956) Mortality and egg production of the Meadow Pipit with special reference to altitude. Bird Study 3:119–132

    Article  Google Scholar 

  • Cox FE (2001) Concomitant infections, parasites and immune responses. Parasitology 122:S23–S28

    Article  PubMed  Google Scholar 

  • Cramp S (1985) The birds of the western palearctic. Oxford University Press, London

    Google Scholar 

  • Crawley MJ (2007) The R book. Wiley, Chichester

    Book  Google Scholar 

  • 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

    Article  Google Scholar 

  • Dobson AP (1988) Restoring island ecosystems: the potential of parasites to control introduced mammals. Conserv Biol 2:31–39

    Article  Google Scholar 

  • Dritschilo W, Cornell H, Nafus D, O’Connor B (1975) Insular biogeography: of mice and mites. Science 190:467–469

    Article  PubMed  CAS  Google Scholar 

  • Dufva R (1996) Blood parasites, health, reproductive success, and egg volume in female Great Tits Parus major. J Avian Biol 27:83–87

    Google Scholar 

  • 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

    Article  PubMed  Google Scholar 

  • Fallon SM, Bermingham E, Ricklefs RE (2003) Island and taxon effects in parasitism revisited: avian malaria in the Lesser Antilles. Evolution 57:606–615

    PubMed  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • Freed LA, Cann RL (2006) DNA quality and accuracy of avian malaria PCR diagnostics: a review. Condor 108:459–473

    Article  Google Scholar 

  • Freeman S, Jackson WM (1990) Univariate metrics are not adequate to measure avian body size. Auk 107:69–74

    Google Scholar 

  • Green AJ (2001) Mass/length residuals: measures of body condition or generators of spurious results? Ecology 82:1473–1483

    Article  Google Scholar 

  • Griffiths R, Double M, Orr K, Dawson RJG (1998) A DNA test to sex most birds. Mol Ecol 7:1071–1075

    Article  PubMed  CAS  Google Scholar 

  • Guégan JF, Kennedy CR (1996) Parasite richness/sampling effort/host range: the fancy three-piece jigsaw puzzle. Parasitol Today 12:367–369

    Article  PubMed  Google Scholar 

  • 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

    Chapter  Google Scholar 

  • 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

    CAS  Google Scholar 

  • Hamilton WD, Zuk M (1982) Heritable true fitness and bright birds: a role for parasites? Science 218:384–387

    Article  PubMed  CAS  Google Scholar 

  • 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

    Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • Hockin DC (1981) The environmental determinants of the insular butterfly faunas of the British Isles. Biol J Linn Soc 16:63–70

    Article  Google Scholar 

  • Hudson PJ, Dobson AP, Newborn D (1998) Prevention of population cycles by parasite removal. Science 282:2256–2258

    Article  PubMed  CAS  Google Scholar 

  • 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

    Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  Google Scholar 

  • Ishtiaq F et al (2008) Avian haematozoan parasites and their associations with mosquitoes across Southwest Pacific Islands. Mol Ecol 17:4545–4555

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • Kuris AM, Blaustein AR, Alio JJ (1980) Hosts as islands. Am Nat 116:570–586

    Article  Google Scholar 

  • Lee LH, Lee KH (1997) Application of the polymerase chain reaction for the diagnosis of fowl poxvirus infection. J Virol Methods 63:113–119

    Article  CAS  Google Scholar 

  • 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

    Article  Google Scholar 

  • MacArthur RH, Wilson EO (1967) The theory of island biogeography. Princeton Univ Press, Princeton

    Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • Møller AP, Nielsen JT (2007) Malaria and risk of predation: a comparative study of birds. Ecology 88:871–881

    Article  PubMed  Google Scholar 

  • 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

    Article  PubMed  Google Scholar 

  • Mougeot F, Redpath SM (2004) Sexual ornamentation relates to immune function in male red grouse Lagopus lagopus scoticus. J Avian Biol 35:425–433

    Article  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • Pérez-Tris J, Hasselquist D, Hellgren O, Krizanauskiene A, Waldenström J, Bensch S (2005) What are malaria parasites? Trends Parasitol 21:209–211

    Article  PubMed  Google Scholar 

  • R Development Core Team (2008) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • Ricklefs RE et al (2008) Community relationships of avian malaria parasites in southern Missouri. Ecol Monogr 75:543–559

    Article  Google Scholar 

  • Ritchie BW (1995) Avian viruses: function and control. Wingers, Lake Worth

  • Saito K et al (2009) Avian poxvirus infection in a white-tailed sea eagle (Haliaeetus albicilla) in Japan. Avian Pathol 38:485–489

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • Sokal RR, Rohlf FJ (1995) Biometry: the principles and practice of statistics in biological research. WH Freeman, New York

    Google Scholar 

  • 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

    PubMed  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • Spurgin LG, Richardson DS (2010) How pathogens drive genetic diversity: MHC, mechanisms and misunderstandings. Proc R Soc Lond B Biol Sci 277:979–988

    Article  CAS  Google Scholar 

  • Staats CM, Schall JJ (1996) Malarial parasites (Plasmodium) of Anolis lizards: Biogeography in the lesser Antilles. Biotropica 28:388–393

    Article  Google Scholar 

  • Tarello W (2008) Prevalence and clinical signs of avipoxvirus infection in falcons from the Middle East. Vet Dermatol 19:101–104

    Article  PubMed  Google Scholar 

  • Tompkins DM, Dunn AM, Smith MJ, Telfer S (2010) Wildlife diseases: from individuals to ecosystems. J Anim Ecol 80:19–38

    Article  PubMed  Google Scholar 

  • Valkiunas G (2005) Avian malaria parasites and other haemosporidia. CRC Press, Boca Raton

    Google Scholar 

  • 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

    Article  PubMed  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

  • 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

    Article  Google Scholar 

  • van Riper C, van Riper SG, Hansen WR (2002) Epizootiology and effect of avian pox on Hawaiian forest birds. Auk 119:929–942

    Article  Google Scholar 

  • 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

  • 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

    Article  PubMed  CAS  Google Scholar 

  • Walther BA, Cotgreave P, Price RD, Gregory RD, Clayton DH (1995) Sampling effort and parasite species richness. Parasitol Today 11:306–310

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • Whittaker RJ (1998) Island biogeography. ecology, evolution, and conservation. Oxford University Press, New York

    Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgments

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.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Lewis G. Spurgin.

Additional information

Communicated by Oliver Love.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (DOC 35 kb)

Rights and permissions

Reprints and permissions

About this article

Cite this article

Spurgin, L.G., Illera, J.C., Padilla, D.P. et al. Biogeographical patterns and co-occurrence of pathogenic infection across island populations of Berthelot’s pipit (Anthus berthelotii). Oecologia 168, 691–701 (2012). https://doi.org/10.1007/s00442-011-2149-z

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00442-011-2149-z

Keywords

Navigation