Skip to main content

Advertisement

SpringerLink
Log in

Geographic variation in malarial parasite lineages in the common yellowthroat (Geothlypis trichas)

  • Research Article
  • Published:
Conservation Genetics Aims and scope Submit manuscript

Abstract

Our current understanding of migration routes of many birds is limited and researchers have employed various methods to determine migratory patterns. Recently, parasites have been used to track migratory birds. The objective of this study was to determine whether haemosporidian parasite lineages detect significant geographic structure in common yellowthroats (Geothlypis trichas). We examined liver tissue or blood from 552 birds sampled from multiple locations throughout the continental United States, southern Canada, and the Bahamas. We found a 52.7% overall prevalence of haematozoan infection. We identified 86.1% of these infections to genus: 81% were Plasmodium; 5% were Haemoproteus; and 0.1% were Leucocytozoon. There were significant differences in the prevalence of different parasite genera among regions (χ2 = 36.82, P < 0.0001) and in the proportion of Plasmodium infections versus other parasites among regions (χ2 = 35.52, P < 0.0001). Sequence information identified three Haemoproteus lineages, two Leucocytozoon lineages, and thirteen Plasmodium lineages. Due to the low number of Haemoproteus and Leucocytozoon, only Plasmodium lineages were used in the geographic comparison of lineages. Six Plasmodium lineages were found in eight or more birds and the prevalence of these varied significantly among regions (χ2 = 172.33, P < 0.0001). Additionally, 45 juvenile birds were sampled to determine what parasites could be obtained in the breeding grounds and we found only one lineage. In conclusion, parasite lineages show some geographic structure, with some lineages being more geographically specific than others, but are not useful for determining migratory connectivity in this species.

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

Access this article

Log in via an institution

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

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3

Similar content being viewed by others

References

  • Alavi Y, Arai M, Mendoza J et al (2003) The dynamics of interactions between Plasmodium and the mosquito: a study of the infectivity of Plasmodium berghei and Plasmodium gallinaceum, and their transmission by Anopheles stephensi, Anopheles gambiae and Aedes aegypti. Int J Parasitol 33:933–943

    Article  PubMed  CAS  Google Scholar 

  • Atkinson CT, van Riper C III (1991) Pathogenicity and epizootiology of avian hematozoa: plasmodium, leucocytozoon, and haemoproteus. In: Loye JE, Zuk M (eds) Bird-parasite interactions. Oxford University Press, Oxford, pp 19–48

    Google Scholar 

  • Atkinson C, Forrester D, Greiner E (1988) Epizootiology of Haemoproteus meleagridis (Protozoa: Haemosporina) in Florida: seasonal transmission and vector abundance. J Med Entomol 25:45–51

    PubMed  CAS  Google Scholar 

  • Ball RM Jr, Avise J (1992) Mitochondrial DNA phylogeographic differentiation among avian populations and the evolutionary significance of subspecies. Auk 109:626–636

    Google Scholar 

  • Ballard G, Geupei G, Nur N et al (2003) Long-term declines and decadal patterns in population trends of songbirds in western North America, 1979–1999. Condor 105:737–755

    Article  Google Scholar 

  • Beadell J, Fleischer R (2005) A restriction enzyme-based assay to distinguish between avian hemosporidians. J Parasitol 91:683–685

    Article  CAS  Google Scholar 

  • Beadell J, Gering E, Austin J 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 

  • Beadell JS, Ishtiaq F, Covas R et al (2006) Global phylogeographic limits in Hawaii’s avian malaria. Proc R Soc Lond B 273:2935–2944

    Article  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, Stjernman M, Hasselquist D et al (2000) Host specificity in avian blood parasites: a study of Plasmodium and Haemoproteus mitochondrial DNA amplified from birds. Proc R Soc Lond B 267:1583–1589

    Article  CAS  Google Scholar 

  • Bensch S, Perez-Tris J, Waldenström J et al (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, Waldenström J, Jonzén N et al (2007) Temporal dynamics and diversity of avian malaria parasites in a single host species. J Anim Ecol 76:112–122

    Article  PubMed  Google Scholar 

  • Biek R, Drummond A, Poss M (2006) A virus reveals populations structure and recent demographic history of its carnivore host. Science 311:538–541

    Article  PubMed  CAS  Google Scholar 

  • Blouin M, Yowell C, Courtney C et al (1995) Host movement and the genetic structure of populations of parasitic nematodes. Genetics 141:1007–1014

    PubMed  CAS  Google Scholar 

  • Booth C, Elliott P (2003) Hematological responses to hematozoa in North America and neotropical songbirds. Comp Biochem Physiol 133:451–467

    Google Scholar 

  • Chamberlain CP, Blum JD, Holmes RT et al (1997) The use of stable isotope tracers for identifying populations of migratory birds. Oecologia 109:132–141

    Article  Google Scholar 

  • Cosgrove CL, Knowles SCL, Day KP et al (2006) No evidence for avian malaria infection during the nestling phase in a passerine bird. J Parasitol 92:1302–1304

    Article  PubMed  CAS  Google Scholar 

  • Criscione C, Blouin M (2004) Life cycles shape parasite evolution: comparative population genetics of salmon trematodes. Evolution 58:198–202

    PubMed  Google Scholar 

  • Davidar P, Morton E (1993) Living with parasites: prevalence of a blood parasite and its effect on survivorship in the Purple Martin. Auk 110:109–116

    Google Scholar 

  • Dumbacher J, Pratt T, Fleischer R (2003) Phylogeny of the owlet-nightjars (Aves: Aegothelidae) based on mitochondrial DNA sequence. Mol Phylogenet Evol 29:540–549

    Article  PubMed  CAS  Google Scholar 

  • Durrant KL, Beadell JS, Ishtiaq F et al (2006) Avian Hematozoa in South America: a comparison of temperate and tropical zones. Ornithol Monogr 60:98–111

    Article  Google Scholar 

  • Escalante A, Freeland D, Collins W et al (1998) The evolution of primate malaria parasites based on the gene encoding cytochrome b from the linear mitochondrial genome. Proc R Soc Lond B 95:8124–8129

    CAS  Google Scholar 

  • Fallon SM, Ricklefs RE, Swanson BL, Bermingham E (2003) Detecting avian malaria: an improved polymerase chain reaction diagnostic. J Parasitol 89:1044–1047

    Article  PubMed  CAS  Google Scholar 

  • Fallon S, Fleischer R, Graves G (2006) Malarial parasites as geographical markers in migratory birds? Biol Lett 2:213–216

    Article  PubMed  Google Scholar 

  • Falush D, Wirth T, Linz B et al (2003) Traces of human migrations in helicobacter pylori populations. Science 299:1582–1585

    Article  PubMed  CAS  Google Scholar 

  • Greiner E, Bennett G, White E et al (1975) Distribution of the avian hematozoa of North America. Can J Zool 53:1762–1787

    Article  PubMed  CAS  Google Scholar 

  • Gylfe A, Bergström S, Lundström J et al (2000) Reactivation of Borrelia infection in birds. Nature 403:724–725

    Article  PubMed  CAS  Google Scholar 

  • Haig SM, Gratto-Trevor CL, Mullins TD et al (1997) Population identification of western hemisphere shorebirds throughout the annual cycle. Mol Ecol 6:413–427

    Article  CAS  Google Scholar 

  • Hasselquist D, Östman Ö, Waldenström J et al (2007) Temporal patterns of occurrence and transmission of the blood parasite Haemoproteus payevskyi in the great reed warbler Acrocephalus arundinaceus. J Ornithol. Early Online Publishing

  • Hellgren O, Waldenström J, Peréz-Tris J et al (2007) Detecting shifts of transmission in avian blood parasites – a phylogenetic approach. Mol Ecol 16:1281–1290

    Article  PubMed  Google Scholar 

  • Hobson K, Wassenaar L (1997) Linking breeding and wintering grounds of Neotropical migrant songbirds using stable isotopic analysis of feathers. Oecologia 109:142–148

    Article  Google Scholar 

  • Hobson K, McFarland K, Wassenaar L et al (2001) Linking breeding and wintering grounds of Bicknell’s thrushes using stable isotope analyses of feathers. Auk 118:16–23

    Article  Google Scholar 

  • Hobson K, Aubry Y, Wassenaar L (2004) Migratory connectivity in Bicknell’s thrush: locating missing populations with hydrogen isotopes. Condor 106:905–909

    Article  Google Scholar 

  • Hubalek Z (2004) An annotated checklist of pathogenic microorganisms associated with migratory birds. J Wildl Dis 40:639–659

    PubMed  Google Scholar 

  • Ishtiaq F, Beadell JS, Baker AJ et al (2006) Prevalence and evolutionary relationships of haemotozoan parasites in native versus introduced populations of common myna Acridotheres tristis. Proc R Soc B: Biol Sci 273:587–594

    Article  Google Scholar 

  • Jarvi S, Atkinson CT, Fleischer RC (2001) Immunogenetics and resistance to avian malaria in Hawaiian honeycreepers (Drepanidinae). Stud Avian Biol 22:254–263

    Google Scholar 

  • Kimura M, Clegg SM, Lovette IJ et al. (2002) Phylogeographical approaches to assessing demographic connectivity between breeding and overwintering regions in the Nearctic-Neotropical warbler (Wilsonia pusilla). Mol Ecol 11:1605–1616

    Article  PubMed  CAS  Google Scholar 

  • Klei T, DeGiusti D (1975) Seasonal occurrence of Haemoproteus columbae Kruse and its vector Pseudolynchia canariensis Bequaert. J Wildl Dis 11:130–134

    PubMed  CAS  Google Scholar 

  • Latta SC, Baltz ME (1997) Population limitation in neotropical migratory birds: comments on Rappole and McDonald (1994). Auk 114:754–762

    Google Scholar 

  • Lovette IJ, Clegg SM, Smith TB (2004) Limited utility of mtDNA markers for determining connectivity among breeding and overwintering locations in three neotropical migrant birds. Conserv Biol 18:156–166

    Article  Google Scholar 

  • Marra P, Hobson K, Holmes RT (1998) Linking winter and summer events in a migratory bird by using stable-carbon isotopes. Science 282:1884–1886

    Article  PubMed  CAS  Google Scholar 

  • Martell MS, Henny C, Nye P et al (2001) Fall migration routes, timing, and wintering sites of North American Ospreys as determined by satellite telemetry. Condor 103:715–724

    Article  Google Scholar 

  • Merino S, Potti J (1995) High prevalence of Hematozoa in Nestlings of a Passerine Species, the Pied Flycatcher (Ficedula hypoleuca). Auk 112:1041–1043

    Google Scholar 

  • Merino S, Potti J (1995) High prevalence of hematozoa in nestlings of a passerine species, the Pied Flycatcher (Ficedula hypoleuca). Auk 112:1041–1043

    Google Scholar 

  • Milot E, Gibbs HL, Hobson K (2000) Phylogeography and genetic structure of northern populations of the yellow warbler (Dendroica petechia). Mol Ecol 9:667–681

    Article  PubMed  CAS  Google Scholar 

  • Paul R, Nu VAT, Krettli AU et al (2002) Interspecific competition during transmission of two sympatric malaria parasite species to the mosquito vector. Proc R Soc Lond B 269:2551–2557

    Article  Google Scholar 

  • Pérez-Tris J, Bensch S (2005) Dispersal increases local transmission of avian malarial parasites. Ecol Lett 8:838–845

    Article  Google Scholar 

  • Peterson AT, Vieglais DA, Andreasen JK (2003) Migratory birds modeled as critical transport agents for West Nile virus in North America. Vector-Borne Zoonotic Dis 3:27–37

    Article  PubMed  Google Scholar 

  • Pitra C, D’Aloia MA, Lieckfeldt D et al (2004) Genetic variation across the current range of the Asian houbara bustard (Chlamydotis undulate macqueeni), Conserv Genet 5:205–215

    Article  CAS  Google Scholar 

  • Richard FA, Sehgal RNM, Jones HI et al (2002) A comparative analysis of PCR-based detection methods for avian malaria. J Parasitol 88:819–822

    PubMed  CAS  Google Scholar 

  • Ricklefs RE, Fallon SM (2002) Diversification and host switching in avian malaria parasites. Proc R Soc Lond B 269:885–892

    Article  Google Scholar 

  • Rintamäki PT, Ojanen O, Pakkala H et al (1998) Blood parasites of migrating Willow Warblers (Phylloscopus trochilus) at a stopover site. Can J Zool 76:984–988

    Article  Google Scholar 

  • Robbins CS, Sauer JR, Greenberg RS et al (1989) Population declines in North American birds that migrate to the neotropics. Proc Natl Acad Sci USA 86:7658–7662

    Article  PubMed  CAS  Google Scholar 

  • Robinson S, Thompson F III, Donovan T et al (1995) Regional forest fragmentation and the nesting success of migratory birds. Science 267:1987–1990

    Article  PubMed  CAS  Google Scholar 

  • Rubenstein DR, Chamberlain CP, Holmes RT et al (2002) Linking breeding and wintering ranges of a migratory songbird using stable isotopes. Science 295:1062–1065

    Article  PubMed  CAS  Google Scholar 

  • Sillett TS, Holmes RT (2002) Variation in survivorship of a migratory songbird throughout its annual cycle. J Anim Ecol 71:296–308

    Article  Google Scholar 

  • Slatkin M (2004) Gene flow and the geographic structure of natural populations. Science 236:787–792

    Article  Google Scholar 

  • Sol D, Jovani R, Torres J (2000) Geographical variation in blood parasites in feral pigeons: the role of vectors. Ecography 23:307–314

    Article  Google Scholar 

  • Super P, van Riper C III (1995) A comparison of avian hematozoan epizootiology in two California coastal scrub communities. J Wildl Dis 31:447–461

    PubMed  CAS  Google Scholar 

  • Swofford DL (1999) paup*: Phylogenetic analysis using parsimony (*and other methods). Sinauer, Sunderland, MA

    Google Scholar 

  • Szymanski MM, Lovette IJ (2005) High lineage diversity and host sharing of malarial parasites in a local avian assemblage. J Parasitol 91:768–774

    Article  PubMed  CAS  Google Scholar 

  • Tankersley R, Orvis K (2003) Modeling the geography of migratory pathways and stopover habitats for neotropical migratory birds. Conserv Ecol 7(1):7

    Google Scholar 

  • Valkiunas G (2004) Avian malarial parasites and other haemosporidians. CRC Press

  • Waldenström J, Bensch S, Kiboi S et al (2002) Cross-species infection of blood parasites between resident and migratory songbirds in Africa. Mol Ecol 11:1545–1554

    Article  PubMed  Google Scholar 

  • Waldenström J, Bensch S, Hasselquist D et al (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  Google Scholar 

  • Wassenaar L, Hobson K (2000) Stable-carbon and hydrogen isotope ratios reveal breeding origins of red-winged blackbirds. Ecol Appl 10:911–916

    Article  Google Scholar 

  • Weatherhead P, Bennet G (1992) Ecology of parasitism of brown-headed cowbirds by haematozoa. Can J Zool 70:1–7

    Article  Google Scholar 

  • Webster MS, Marra PP, Haig SM et al (2002) Links between worlds: unraveling migratory connectivity. Trends Ecol Evol 17:76–83

    Article  Google Scholar 

  • Wennerberg L, Klaassen M, Lindstrom A (2002) Geographical variation and population structure in the white-rumped sandpiper Calidris fuscicollis as shown by morphology, mitochondrial DNA and carbon isotope ratios. Oecoloiga 131:390–390

    Google Scholar 

  • Wiersch SC, Maier WA, Kampen H (2005) Plasmodium (Haemamoeba) cathemerium gene sequences for phylogenetic analysis of malaria parasites. Parasitol Res 95:90–94

    Article  Google Scholar 

  • Wirth T, Meyer A, Achtman M (2005) Deciphering host migrations and origins by means of their microbes. Mol Ecol 14:3289–3306

    Article  PubMed  CAS  Google Scholar 

  • Woodworth B, Atkinson CT, LaPointe D et al (2005) Host population persistence in the face of introduced vector-borne diseases: Hawaii amakihi and avian malaria. Proc Natl Acad Sci USA 102:1531–1536

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgments

We would like to thank committee members, Catherine Schaeff and Kiho Kim, for intellectual insight and guidance. We would also like to thank two anonymous reviewers for their helpful comments. A small number of additional samples were contributed by Brian Olsen, Irby Lovette, and Rebecca Holberton. We would like to thank the various organizations that allowed us to sample common yellowthroats on their land: Aroostook National Wildlife Refuge, Iroquois National Wildlife Refuge, Paul Smith College of the Adirondacks, and the Pfeiffer Nature Center. We especially thank Daryl and Leslie Boness, who not only allowed us to sample on their beautiful property but also fed us well. We thank Carl McIntosh, Danielle Palmer, Farah Ishtiaq and Jon Beadell for help with various lab techniques. Funding was provided by the NIH (1R01GM063258) and an American University Mellon Grant.

Author information

Author notes

  1. K. M. Pagenkopp

    Present address: Department of Environmental and Aquatic Animal Health, Virginia Institute of Marine Science, The College of William and Mary, P.O. Box 1346, Gloucester Point, VA, 23062, USA

Authors and Affiliations

  1. Genetics Program, National Museum of Natural History and National Zoological Park, Smithsonian Institution, 3001 Connecticut Ave NW, Washington, DC, 20008, USA

    K. M. Pagenkopp, K. L. Durrant & R. C. Fleischer

  2. Department of Biology, American University, 4400 Massachusetts Ave NW, Washington, DC, 20016, USA

    K. M. Pagenkopp & R. C. Fleischer

  3. Marjorie Barrick Museum of Natural History, University of Nevada Las Vegas, 4505 Maryland Parkway, Box 454012, Las Vegas, NV, 89154, USA

    J. Klicka

  4. Department of Biological Sciences, University of Wisconsin-Milwaukee, P.O. Box 413, Milwaukee, WI, 53201, USA

    J. C. Garvin

Authors
  1. K. M. Pagenkopp
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. J. Klicka
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. K. L. Durrant
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. J. C. Garvin
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. R. C. Fleischer
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to K. M. Pagenkopp.

Additional information

The U.S. Government’s right to retain a non-exclusive, royalty-free license in and to any copyright is acknowledged.

Electronic supplementary material

Rights and permissions

Reprints and permissions

About this article

Cite this article

Pagenkopp, K.M., Klicka, J., Durrant, K.L. et al. Geographic variation in malarial parasite lineages in the common yellowthroat (Geothlypis trichas). Conserv Genet 9, 1577–1588 (2008). https://doi.org/10.1007/s10592-007-9497-6

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10592-007-9497-6

Keywords

Search

Navigation