You have full text access to this OnlineOpen article

Temporal dynamics and diversity of avian malaria parasites in a single host species

  1. STAFFAN BENSCH,
  2. JONAS WALDENSTRÖM,
  3. NICLAS JONZÉN,
  4. HELENA WESTERDAHL,
  5. BENGT HANSSON,
  6. DOUGLAS SEJBERG,
  7. DENNIS HASSELQUIST

Article first published online: 20 DEC 2006

DOI: 10.1111/j.1365-2656.2006.01176.x

Issue

Journal of Animal Ecology

Journal of Animal Ecology

Volume 76, Issue 1, pages 112–122, January 2007

Additional Information

How to Cite

BENSCH, S., WALDENSTRÖM, J., JONZÉN, N., WESTERDAHL, H., HANSSON, B., SEJBERG, D. and HASSELQUIST, D. (2007), Temporal dynamics and diversity of avian malaria parasites in a single host species. Journal of Animal Ecology, 76: 112–122. doi: 10.1111/j.1365-2656.2006.01176.x

Author Information

  1. Department of Animal Ecology, Ecology Building, Lund University, S-223 62 Lund Sweden; Department of Theoretical Ecology, Ecology Building, Lund University, S-223 62 Lund Sweden

* S. Bensch, Department of Animal Ecology, Ecology Building, Lund University, S-223 62 Lund, Sweden. Tel.: +46 46 2224292; Fax: +46 46 2224716; E-mail: staffan.bensch@zooekol.lu.se

Publication History

  1. Issue published online: 20 DEC 2006
  2. Article first published online: 20 DEC 2006
  3. Received 21 April 2006; accepted 6 September 2006

SEARCH

SEARCH BY CITATION

ARTICLE TOOLS

View Full Article (HTML) Get PDF (210K)

References

  • Andersson, M. (1994) Sexual Selection. Princeton University Press, Princeton, NJ.
  • Arlt, D., Hansson, B., Bensch, S., Von Schantz, T. & Hasselquist, D. (2004) Breeding synchrony does not affect extra-pair paternity in great reed warblers. Behaviour, 141, 863–880.
  • Atkinson, C.T. & Van Riper, C. III (1991) Pathogenicity and epizootiology of avian haematozoa: Plasmodium, Leucocytozoon, and Haemoproteus. Bird–Parasite Interactions (eds J.E.Loye & M.Zuk), pp. 19–48. Oxford University Press, Oxford.
  • Atkinson, C.T., Dusek, R.J. & Lease, J.K. (2001) Serological responses and immunity to superinfection with avian malaria in experimentally-infected Hawaii Amakihi. Journal of Wildlife Diseases, 37, 20–27.
  • Beadell, J.S., Gering, E., Austin, J., Dumbacher, J.P., Peirce, M.A., Pratt, T.K., Atkinson, C.T. & Fleischer, R.C. (2004) Prevalence and differential host-specificity of two avian blood parasite genera in the Australo-Papuan region. Molecular Ecology, 13, 3829–3844.
    Direct Link:
  • Beadell, J.S., Ishtiaq, F., Covas, R., Melo, M., Warren, B.H., Atkinson, C.T., Bensch, S., Graves, G.R., Jhala, Y.V., Peirce, M.A., Rahmani, A.R., Fonseca, D.M. & Fleischer, R.C. (2006) Global Phylogeographic limits of Hawaii's avian malaria. Proceedings of the Royal Society of London B, Biology Sciences, 273, 2935 –2944.
  • Bensch, S. (1996) Female mating status and reproductive success in the great reed warbler: is there a potential cost of polygyny that requires compensation? Journal of Animal Ecology, 65, 283–296.
  • Bensch, S. & Åkesson, S. (2003) Temporal and spatial variation of Hematozoans in Scandinavian willow warblers. Journal of Parasitology, 89, 388–391.
  • Bensch, S. & Hasselquist, D. (1992) Evidence for active female choice in a polygynous warbler. Animal Behaviour, 44, 301–311.
  • Bensch, S., Hasselquist, D., Nielsen, B. & Hansson, B. (1998) Higher fitness for philopatric than for immigrant males in a semi-isolated population of great reed warblers. Evolution, 52, 877–883.
  • Bensch, S., Stjernman, M., Hasselquist, D., Östman, Ö., Hansson, B., Westerdahl, H. & Torres-Pinheiro, R. (2000) Host specificity in avian blood parasites: a study of Plasmodium and Haemoproteus mitochondrial DNA amplified from birds. Proceedings of the Royal Society of London B, Biology Sciences, 267, 1583–1589.
  • 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.
  • Bonneaud, C., Pérez-Tris, J., Federici, P., Chastel, O. & Sorci, G. (2006) Mhc alleles associated with local resistance to malaria in a passerine. Evolution, 60, 383–389.
  • Bruce, M.C., Donnelly, C.A., Alpers, M.P., Galinski, M.R., Barnwell, J.W., Walliker, D. & Day, K.P. (2000) Cross-species interactions between malaria parasites in humans. Science, 287, 845–848.
  • Burnham, K.P. & Anderson, D.R. (1998) Model selection and inference: a practical information-theoretic approach. Springer Verlag, New York.
  • Catchpole, C.K. (1986) Song repertoires and reproductive success in the great reed warbler Acrocephalus arundinaceus. Behavioral Ecology Sociobiology, 91, 439–445.
  • Chatfield, C. (1999) The Analysis of Time Series: an Introduction, 5th edn. Chapman & Hall, Boca Raton, FL.
  • Clark, C.W. & Rosenzweig, M.L. (1994) Extinction and colonization processes: parameter estimates from sporadic surveys. American Naturalist, 143, 583–596.
  • Edler, R., Klump, G.M. & Friedl, T.W.P. (2004) Do blood parasites affect reproductive performance in male red bishops (Euplectes orix)? A test of the Hamilton-Zuk hypothesis. Ethology Ecology and Evolution, 16, 315–328.
  • Escalante, A.A., Freeland, D.E., Collins, W.E. & Lal, A.A. (1998) The evolution of primate malaria parasites based on the gene encoding cytochrome b from the linear mitochondrial genome. Proceedings of the National Academy of Sciences of the USA, 95, 8124–8129.
  • Eshel, I. & Hamilton, W.D. (1984) Parent-offspring correlation in fitness under fluctuating selection. Proceedings of the Royal Society of London B, Biology Sciences, 122, 1–14.
  • Fallon, S.M., Ricklefs, R.E., Latta, S.C. & Bermingham, E. (2004) Temporal stability of insular avian malarial parasite communities. Proceedings of the Royal Society of London B, Biology Sciences, 271, 493–500.
  • Fallon, S.M., Bermingham, E. & Ricklefs, R.E. (2005) Host specialization and geographic localization of avian malaria parasites: a regional analysis in the Lesser Antilles. American Naturalist, 165, 466–480.
  • Gupta, S. & Galvani, A. (1999) The effects of host heterogeneity on pathogen population structure. Philosophical Transactions of the Royal Society of London B, 354, 711–719.
  • Gupta, S., Swinton, J. & Anderson, R.M. (1994) Theoretical studies of the effects of heterogeneity in the parasite population on the transmission dynamics of malaria. Proceedings of The Royal Society of London Series B-Biology Sciences, 256, 231–238.
  • Hamilton, W.D. & Zuk, M. (1982) Heritable true fitness and bright birds: a role for parasites? Science, 218, 384–387.
  • Hansson, B., Bensch, S., Hasselquist, D. & Nielsen, B. (2002) Restricted dispersal in a long-distance migrant bird with patchy distribution, the great reed warbler. Oecologia, 130, 536–542.
  • Hasselquist, D. (1998) Polygyny in great reed warblers: a long-term study of factors contributing to male fitness. Ecology, 79, 2376–2390.
  • Hasselquist, D. & Bensch, S. (1991) Trade-off between mate guarding and mate attraction in the polygynous great reed warbler. Behavioral Ecology Sociobiology, 28, 187–193.
  • Hasselquist, D., Bensch, S. & Von Schantz, T. (1995) Low frequency of extra-pair paternity in the polygynous great warbler. Behavioral Ecology, 6, 27–38.
  • Hasselquist, D., Bensch, S. & Von Schantz, T. (1996) Correlation between male song repertoire, extra-pair paternity and offspring survival in the great reed warbler. Nature, 381, 229–232.
  • Hellgren, O. (2005) The occurrence of haemosporidean parasites in the Fennoscandian bluethroat (Luscinia svecica) population. Journal of Ornithology, 146, 55–60.
  • Hilborn, R. & Mangel, M. (1997) The Ecological Detective: Confronting Models with Data. Princeton University Press, Princeton, NJ.
  • Hudson, P.J., Dobson, A.P. & Newborn, D. (1998) Prevention of population cycles by parasite removal. Science, 282, 2256–2258.
  • Ishtiaq, F., Beadell, J.S., Baker, A.J., Rahmani, A.R., Jhala, Y.V. & Fleischer, R.C. (2006) Prevalence and evolutionary relationships of haematozoan parasites in native versus introduced populations of common myna Acridotheres tristis. Proceedings of the Royal Society of London B, Biology Sciences, 273, 587–594.
  • Jarvi, S.I., Farias, M.E.M., Baker, H., Freifeld, H.B., Baker, P.E., Van Gelder, E., Massey, J.G. & Atkinson, C.T. (2003) Detection of avian malaria (Plasmodium spp.) in native land birds of American Samoa. Conservation Genetics, 4, 629–637.
  • Lack, D. (1954) The Natural Regulation of Animal Numbers. Clarendon Press, Oxford.
  • Lively, C.M. & Dybdahl, M.F. (2000) Parasite adaptation to locally common host genotypes. Nature, 405, 679–681.
  • Martin, M.J., Rayner, J.C., Gagneux, P., Barnwell, J.W. & Varki, A. (2005) Evolution of human-chimpanzee differences in malaria susceptibility: relationship to human genetic loss of N-glycolylneuraminic acid. Proceedings of the National Academy of Sciences of the USA, 102, 12819–12824.
  • Marzal, A., De Lope, F., Navarro, C. & Møller, A.P. (2005) Malarial parasites decrease reproductive success: an experimental study in a passerine bird. Oecologia, 142, 541–545.
  • McCullagh, P. & Nelder, J.A. (1989) Generalized Linear Models. Chapman & Hall, London.
  • McCutchan, T.F., Grim, K.C., Li, J., Weiss, W., Rathore, D., Sullivan, M., Graczyk, T.K., Kumar, S. & Cranfield, M.R. (2004) Measuring the effects of an ever-changing environment on malaria control. Infection and Immunity, 72, 2248–2253.
  • Merino, S., Moreno, J., Sanz, J.J. & Arriero, E. (2000) Are avian blood parasites pathogenic in the wild? A medication experiment in blue tits (Parus caeruleus). Proceedings of the Royal Society of London B, Biology Sciences, 267, 2507–2510.
  • Milinski, M. & Bakker, T.C.M. (1990) Female sticklebacks use male coloration in mate choice and hence avoid parasitized males. Nature, 344, 330–333.
  • Molineaux, L. (1988) The epidemiology of human malaria as an explanaition of its distribution, including some implications for its control. Malaria: Principles and Practices of Malariology (eds W.H.Wernsdorfer & I.McGregor), pp. 913–998. Churchill Livingstone, Edinburgh.
  • Møller, A.P. (1990) Effects of haematophagous mite on the barn swallow (Hirundo rustica): a test of the Hamilton and Zuk hypothesis. Evolution, 44, 771–784.
  • Møller, A.P. & Erritzoe, J. (1998) Host immune defence and migration in birds. Evolutionary Ecology, 12, 945–953.
  • Nowicki, S., Hasselquist, D., Bensch, S. & Peters, S. (2000) Nestling growth and song repertoire size in great reed warblers: evidence for song learning as an indicator mechanism in mate choice. Proceedings of the Royal Society of London B, Biology Sciences, 267, 2419–2424.
  • Pérez-Tris, J. & Bensch, S. (2005a) Diagnosing genetically diverse avian malaria infections using mixed-sequence analysis and TA-cloning. Parasitology, 131, 1–9.
  • Pérez-Tris, J. & Bensch, S. (2005b) Dispersal increases local transmission of avian malarial parasites. Ecology Letters, 8, 838–845.
    Direct Link:
  • Pérez-Tris, J., Hasselquist, D., Hellgren, O., Krizanauskiene, A., Waldenström, J. & Bensch, S. (2005) What are malaria parasites? Trends in Parasitology, 21, 209–211.
  • Quinn, G.P. & Keough, M.J. (2002) Experimental Design and Data Analysis for Biologists. Cambridge University Press, Cambridge.
  • Read, A.F. (1987) Comparative evidence supports the Hamilton and Zuk hypothesis on parasites and sexual selection. Nature, 327, 68–70.
  • Read, A.F. & Harvey, P.H. (1989) Reassessment of comparative evidence for Hamilton and Zuk theory on the evolution of secondary sexual characters. Nature, 339, 618–620.
  • Reullier, J., Pérez-Tris, J., Bensch, S. & Secondi, J. (2006) Diversity, distribution and exchange of blood parasites meeting at an avian moving contact zone. Molecular Ecology, 15, 753–763.
    Direct Link:
  • Richie, T.L. (1988) Interactions between malaria parasites infecting the same vertebrate host. Parasitology, 96, 607–639.
  • Ricklefs, R.E. (1992) Embryonic development period and the prevalence of avian malaria parasites. Proceedings of the National Academy of Sciences of the USA, 89, 4722–4725.
  • Ricklefs, R.E. & Fallon, S.M. (2002) Diversification and host switching in avian malaria parasites. Proceedings of the Royal Society of London B, Biology Sciences, 269, 885–892.
  • Ricklefs, R.E., Fallon, S.M. & Bermingham, E. (2004) Evolutionary relationships, cospeciation, and host switching in avian malaria parasites. Systematic Biology, 53, 111–119.
  • Ricklefs, R.E., Swanson, B.L., Fallon, S.M., Martínez-Abraín, A., Scheuerlein, A., Gray, J. & Latta, S.C. (2005) Community relationships of avian malaria parasites in southern Missouri. Ecological Monographs, 75, 543–559.
  • Van Riper, C. III, Van Riper, S.G., Goff, M.L. & Laird, M. (1986) The epizootiology and ecological significance of malaria in Hawaiian land birds. Ecological Monographs, 56, 327–344.
  • De Roode, J.C., Pansini, R., Cheesman, S.J., Helinski, M.E.H., Huijben, S., Wargo, A.R., Bell, A.S., Chan, B.H.K., Walliker, D. & Read, A.F. (2005) Virulence and competitive ability in genetically diverse malaria infections. Proceedings of the National Academy of Sciences of the USA, 102, 7624–7628.
  • SAS (1990) SAS/STAT User's Guide. SAS Institute Inc., Cary, NC.
  • Schall, J.J. & Marghoob, A.B. (1995) Prevalence of a malarial parasite over time and space: Plasmodium mexicanum in its vertebrate host, the western fence lizard Sceloporus occidentalis. Journal of Animal Ecology, 64, 177–185.
  • Scheuerlein, A. & Ricklefs, R.E. (2004) Prevalence of blood parasites in European passerine birds. Proceedings of the Royal Society of London B, Biology Sciences, 271, 1363–1370.
  • Spencer, K.A., Buchanan, K.L., Leitner, S., Goldsmith, A.R. & Catchpole, C.K. (2005) Parasites affect song complexity and neural development in a songbird. Proceedings of the Royal Society of London B, Biology Sciences, 272, 2037–2043.
  • Stenseth, N.C. (1999) Population cycles in voles and lemmings: density dependence and phase dependence in a stochastic world. Oikos, 87, 427–461.
  • Stjernman, M., Råberg, L. & Nilsson, J.-Å. (2004) Survival costs of reproduction in the blue tit (Parus caeruleus): a role for parasites? Proceedings of the Royal Society of London B, Biology Sciences, 271, 2387–2394.
  • Topolska, A.E., Wang, L., Black, C.G. & Coppel, R.L. (2004) Merozoite cell biology. Malaria Parasites (eds A.P.Waters & C.J.Janse), Caister Academic Press, Norfolk.
  • Valkiûnas, G. (1993) Pathogenic influence of haemosporidians and trypanosomes on wild birds in the field conditions: facts and hypotheses. Ekologija, Vilnius, 1, 47–60.
  • Valkiûnas, G. (2005) Avian Malaria Parasites and Other Haemosporidia. CRC Press, Boca Raton, FL.
  • Valkiûnas, G., Bensch, S., Iezhova, T.A., Kripanauskienë, A., Hellgren, O. & Bolshakov, C.V. (2006) Nested cytochrome b PCR diagnostics underestimate mixed infections of avian blood Haemosporidian parasites: microscopy is still essential. Journal of Parasitology, 92, 418–422.
  • Waldenström, J., Bensch, S., Kiboi, S., Hasselquist, D. & Ottosson, U. (2002) Cross-species infection of blood parasites between resident and migratory songbirds in Africa. Molecular Ecology, 11, 1545–1554.
    Direct Link:
  • Waldenström, J., Bensch, S., Hasselquist, D. & Östman, Ö. (2004) A new nested PCR method very efficient in detecting Plasmodium and Haemoproteus infections from avian blood. Journal of Parasitology, 90, 191–194.
  • Weatherhead, P.J. (1990) Secondary sexual traits, parasites, and polygyny in red-winged blackbirds, Agelaius phoeniceus. Behavioral Ecology, 1, 125–130.
  • Westerdahl, H., Waldenström, J., Hansson, B., Hasselquist, D., Von Schantz, T. & Bensch, S. (2005) Associations between malaria and MHC genes in a migratory songbird. Proceedings of the Royal Society of London B, Biology Sciences, 272, 1511–1518.
  • Woolhouse, M.E.J., Taylor, L.H.T. & Haydon, D.T. (2001) Population biology of multihost pathogens. Science, 292, 1109–1112.
  • Woolhouse, M.E.J., Haydon, D.T. & Antia, R. (2005) Emerging pathogens: the epidemiology and evolution of species jumps. Trends in Ecology and Evolution, 20, 238–244.
View Full Article (HTML) Get PDF (210K)