Skip to main content
SpringerLink
Log in

Temporal patterns of occurrence and transmission of the blood parasite Haemoproteus payevskyi in the great reed warbler Acrocephalus arundinaceus

  • Original Article
  • Published:
Journal of Ornithology Aims and scope Submit manuscript

Abstract

We studied the prevalence and intensity of the haemosporidian blood parasite Haemoproteus payevskyi in great reed warblers at Lake Kvismaren (6 years) and Lake Segersjö (3 years) in Sweden. Based on microscopic inspection of slides from 282 adult birds, 20.6% showed infection of H. payevskyi in circulating red blood cells in at least 1 year. For parasite prevalence, there was no difference between years, sex, and age classes. However, parasite intensity was higher in females than in males, and this was most pronounced in 1-year-old birds. Individuals scored to carry parasites in yearn were more likely to show parasite infection yearn + 1 than birds scored to be parasite-free in yearn. None of 99 juvenile birds examined at the breeding site in late summer, 4–9 weeks after hatching, showed infection of H. payevskyi. Parasite intensity in infected adult birds decreased in the course of the breeding season and no new or relapse infections were observed during this period. Thus, our data imply that in the great reed warbler, a long-distance migrant to tropical Africa, transmission of H. payevskyi occurs on wintering sites or at stopover sites during migration.

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

Similar content being viewed by others

References

  • Allander K, Bennett GF (1994) Prevalence and intensity of haematozoan infection in a population of great tits, Parus major, from Gotland, Sweden. J Avian Biol 25:69–74

    Google Scholar 

  • Allander K, Sundberg J (1997) Temporal variation and reliability of blood parasite levels in captive yellowhammer males Emberiza citrinella. J Avian Biol 28:325–330

    Google Scholar 

  • Ashford RW (1971) Blood parasites and migratory fat at Lake Chad. Ibis 113:100–101

    Google Scholar 

  • Atkinson CT, van Riper C III (1991) Pathogenicity and epizootiology of avian haematozoa: Plasmodium, Leucocytozoon and Haemoproteus. In: Loye JE, Zuk M (eds) Bird–parasite interactions: ecology, evolution and behaviour. Oxford University Press, Oxford, pp 19–48

    Google Scholar 

  • Bennett GF, Sikamaki P, Jokimaki J, Hovi M, Huhta E (1995) Leucocytozoon muscicapa n. sp. (Leucocytozoidae: Apicomplexa) from the pied flycatcher Ficedula hypoleuca (Pallas) (Passeriformes: Muscicapinae). Syst Parasitol 31:33–36

    Google Scholar 

  • Bensch S (1996) Female mating status and reproductive success in the great reed warbler: is there a potential cost of polygyny that requires compensation? J Anim Ecol 65:283–296

    Google Scholar 

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

    PubMed  Google Scholar 

  • Bensch S, Hasselquist D (1991) Territory infidelity in the polygynous great reed warbler, Acrocephalus arundinaceus: the effect on variation in territory attractiveness. J Anim Ecol 60:857–871

    Google Scholar 

  • Bensch S, Hasselquist D (1994) Higher rate of nest loss among primary than secondary females: infanticide in the great reed warbler? Behav Ecol Sociobiol 35:309–317

    Google Scholar 

  • 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

    PubMed  Google Scholar 

  • Bensch S, Stjernman M, Hasselquist D, Östman Ö, Hansson B, Westerdahl H, Torres Pinheiro R (2000) Host specificity and host switching in avian haematozoa: a study of Plasmodium and Haemoproteus mtDNA amplified from avian blood. Proc R Soc Lond B 267:1583–1589

    CAS  Google Scholar 

  • Bensch S, Waldenström J, Jonzén N, Westerdahl H, Hansson B, Sejberg D, Hasselquist D (2007) Temporal dynamics and diversity of avian malaria parasites in a single host species. J Anim Ecol 76:112–122

    PubMed  Google Scholar 

  • Cramp S (1992) Handbook of the birds of Europe the Middle East and North Africa, vol 6. Oxford University Press, Oxford

    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

    Google Scholar 

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

    Google Scholar 

  • Dawson RD, Bortolotti GR (2000) Effects of haematozoan parasites on condition and return rates of American kestrels. Auk 117:373–380

    Google Scholar 

  • De Roo A, DeHeegher J (1969) Ecology of the great reed warbler, Acrocephalus arundinaceus (L), wintering in the southern Congo savannah. Gerfaut 59:260–275

    Google Scholar 

  • Desser SS, Bennet GF (1993) The genera Leucocytozoon, Haemoproteus and Hepatocystis. In: Kreier JP (ed) Parasitic protozoa, vol 4. Academic press, New York, pp 273–307

    Google Scholar 

  • Dyrcz A (1986) Factors affecting facultative polygyny and breeding results in the great reed warbler, Acrocephalus arundinaceus. J Ornithol 127:447–461

    Google Scholar 

  • Dyrcz A (1988) Mating systems in European marsh-nesting Passeriformes, vol 2. Acta XIX Congress Internationalis Ornithologie, Ottawa, pp 2613–2623

    Google Scholar 

  • Folstad I, Karter AJ (1992) Parasites, bright males, and the immunocompetence handicap. Am Nat 139:602–622

    Google Scholar 

  • Freeman-Gallant C, O’Connor KD, Breuer ME (2001) Sexual selection and the geography of Plasmodium infection in Savannah sparrows (Passerculus sandwichensis). Oecologia 127:517–521

    PubMed  Google Scholar 

  • Gregory RD, Montgomery SSJ, Montgomery WI (1992) Population biology of Heligmosomoides polygyrus (Nematoda) in the wood mouse. J Anim Ecol 61:749–757

    Google Scholar 

  • Gylfe Å, Bergström S, Lundström J, Olsen B (2000) Reactivation of Borrelia infection in birds. Nature 403:724–725

    CAS  PubMed  Google Scholar 

  • Hall S (1996) The timing of post-juvenile moult and fuel deposition in relation to the onset of autumn migration in reed warblers Acrocephalus scirpaceus and sedge warblers Acrocephalues schoenobaenus. Ornis Svec 6:89–96

    Google Scholar 

  • Hasselquist D (1995) Demography and lifetime reproductive success in the polygynous great reed warbler. Jpn J Ornithol 44:181–194

    Google Scholar 

  • Hasselquist D (1998) Polygyny in great reed warblers: a long-term study of factors contributing to male fitness. Ecology 79:2376–2390

    Google Scholar 

  • Hasselquist D, Bensch S, Ottosson U (1993) Diurnal song pattern in the great reed warbler. Ornis Svec 3:125–136

    Google Scholar 

  • Hasselquist D, Bensch S, von Schantz T (1996) Correlation between song repertoire, extra-pair paternity and offspring survival in the great reed warbler. Nature 381:229–232

    CAS  Google Scholar 

  • Hasselquist D, Lindström Å, Jenni-Eiermann S, Koolhaas A, Piersma T (2007) Long flights do not influence the immune responses of a long-distance migrant bird. J exp Biol 210:1123–1131

    PubMed  Google Scholar 

  • Hedenström A, Bensch S, Hasselquist D, Lockwood M, Ottosson U (1993) Migration, stopover and moult of the great reed warbler Acrocephalus arundinaceus in Ghana, West Africa. Ibis 135:177–180

    Google Scholar 

  • Hellgren O, Waldenström J, Perez-Tris J, Szöllösi E, Hasselquist D, Krizanauskiene A, Ottosson U, Bensch S (in press) Detecting shifts of transmission areas in avian blood parasites—a phylogenetic approach. Mol Ecol 16:1281–1290

  • Korpimäki E, Tolonen P, Bennett GF (1995) Blood parasites, sexual selection and reproductive success of European Kestrels. Ecosciénce 2:335–343

    Google Scholar 

  • Lessells CM, Boag PT (1987) Unrepeatable repeatabilities: a common mistake. Auk 104:116–121

    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 

  • Møller AP, Erritzøe J (1998) Host immune defence and migration in birds. Evol Ecol 12:945–953

    Google Scholar 

  • Nelson RJ, Demas GE (1996) Seasonal changes in immune function. Q Rev Biol 71:511–548

    CAS  PubMed  Google Scholar 

  • Olsen NJ, Kovacs WJ (1996) Gonadal steroids and immunity. Endocr Rev 17:369–384

    CAS  PubMed  Google Scholar 

  • Oppliger A, Christe P, Richner H (1997) Clutch size and malarial parasites in female great tits. Behav Ecol 8:148–152

    Google Scholar 

  • Peirce MA, Mead CJ (1978) Haematozoa of British birds III. Spring incidence of blood parasites of birds from Hertfordshire, especially returning migrants. J Nat Hist 12:337–340

    Google Scholar 

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

    Google Scholar 

  • Råberg L, Grahn M, Hasselquist D, Svensson E (1998) On the adaptive significance of stress-induced immunosuppression. Proc R Soc Lond B 265:1637–1641

    Google Scholar 

  • Richner H, Christe P, Oppliger A (1995) Paternal investment affects prevalence of malaria. Proc Natl Acad Sci USA 92:1192–1194

    CAS  PubMed  Google Scholar 

  • Ricklefs RE, Fallon SM, Bermingham E (2004) Evolutionary relationships, cospeciation, and host switching in avian malaria parasites. Syst Biol 53:111–119

    PubMed  Google Scholar 

  • Rintamäki PT, Halonen M, Kilpimaa J, Lundberg A (1997) Blood parasites found in three passerine species during spring migration. Ornis Fenn 74:195–200

    Google Scholar 

  • Rogers D, Randolph SE (2000) The global spread of malaria in a future, warmer world. Science 289:1763–1766

    CAS  PubMed  Google Scholar 

  • Sejberg D, Bensch S, Hasselquist D (2000) Nestling provisioning in polygynous great reed warblers: do males bring larger prey to compensate for fewer nest visits? Behav Ecol Sociobiol 47:213–219

    Google Scholar 

  • Sokal RR, Rohlf JF (1981) Biometry. Freeman, New York

    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

    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 

  • SPSS Inc (2000) SYSTAT 10.0 for windows. SPSS Inc, Evanston

  • Sturkie PD, Benzo CA (1986) Avian physiology. Springer, Berlin

    Google Scholar 

  • Valkiūnas G (1993) The role of seasonal migrations in the distribution of Haemosporidia of birds in North Palaearctic. Ekologija (Vilnius) 2:57–67

    Google Scholar 

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

    Google Scholar 

  • Valkiūnas G, Iezhova TA (2001) A comparison of blood parasites in three subspecies of the yellow wagtail Motacilla flava. J Parasitol 87:930–934

    PubMed  Google Scholar 

  • Valkiūnas G, Zehtindjiev P, Hellgren O, Ilieva M, Iezhova TA, Bensch S (2007) Linkage between mitochondrial cytochrome b lineages and morphospecies of two avian malaria parasites, with a description of Plasmodium (Novyella) ashfordi sp. nov. Parasitol Res (in press)

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

    PubMed  Google Scholar 

  • Waldenström J, Bensch S, Hasselquist D, Östman Ö (2004) A new nested polymerase chain reaction method very efficient in detecting Plasmodium and Haemoproteus infections from avian blood. J Parasitol 90:191–194

    PubMed  Google Scholar 

  • Weatherhead PJ, Bennett GF (1991) Ecology of red-winged blackbird parasitism by haematozoa. Can J Zool 69:2352–2359

    Google Scholar 

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

    Google Scholar 

  • Wedekind C, Folstad I (1994) Adaptive or non-adaptive immunosuppression by sex hormones? Am Nat 143:936–938

    Google Scholar 

  • Westerdahl H, Waldenström J, Hansson B, Hasselquist D, von Schantz T, Bensch S (2005) Association between malaria and MHC in a migratory songbird. Proc R Soc Lond B 272:1511–1518

    CAS  Google Scholar 

  • Westneat DF, Birkhead TR (1998) Adapative hypotheses linking the immune system and mate choice. Proc R Soc Lond B 265:1065–1073

    Google Scholar 

  • Zuk M (1990) Reproductive strategies and disease susceptibility: an evolutionary viewpoint. Parasitol Today 6:231–233

    CAS  PubMed  Google Scholar 

  • Zuk M, McKean KA (1996) Sex differences in parasite infections: patterns and processes. Int J Parasitol 26:1009–1024

    CAS  PubMed  Google Scholar 

Download references

Acknowledgements

We wish to thank Bo Nielsen, Anna-Karin Olsson, Bengt Hansson, Helena Westerdahl, Martin Stervander, Douglas Sejberg for extensive help with data collection in the field. This study was financially supported by the Swedish Research Council (NFR/VR), Swedish Research Council for Environment, Agricultural Sciences and Spatial Planning (Formas), Royal Swedish Academy of Sciences (Ahlstrands, Hierta-Retzius), Crafoord Foundation, Carl Tryggers Foundation, Lunds Djurskyddsfond. This is report no.149 from the Kvismare Bird Observatory.

Author information

Authors and Affiliations

  1. Department of Animal Ecology, Lund University, Ecology Building, 223 62, Lund, Sweden

    Dennis Hasselquist, Jonas Waldenström & Staffan Bensch

  2. Department of Ecology and Evolution, Uppsala University, Norbyvägen 18D, 752 36, Uppsala, Sweden

    Örjan Östman

  3. Section for Zoonotic Ecology and Epidemiology, Department of Biology and Environmental Science, Kalmar University, 391 82, Kalmar, Sweden

    Jonas Waldenström

Authors
  1. Dennis Hasselquist
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Örjan Östman
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Jonas Waldenström
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Staffan Bensch
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Dennis Hasselquist.

Additional information

Communicated by F. Bairlein.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Hasselquist, D., Östman, Ö., Waldenström, J. et al. Temporal patterns of occurrence and transmission of the blood parasite Haemoproteus payevskyi in the great reed warbler Acrocephalus arundinaceus . J Ornithol 148, 401–409 (2007). https://doi.org/10.1007/s10336-007-0144-2

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10336-007-0144-2

Keywords

Search

Navigation