Hostname: page-component-cd9895bd7-fscjk Total loading time: 0 Render date: 2024-12-23T20:20:27.357Z Has data issue: false hasContentIssue false
  • English
  • Français

Prevalence, diversity, and interaction patterns of avian haemosporidians in a four-year study of blackcaps in a migratory divide

Published online by Cambridge University Press:  26 April 2011

D. SANTIAGO-ALARCON ,
R. BLOCH ,
G. ROLSHAUSEN ,
H. M. SCHAEFER  and
G. SEGELBACHER
D. SANTIAGO-ALARCON*
Affiliation:
Department of Evolutionary Biology and Animal Ecology, Faculty of Biology, University of Freiburg, Hauptstrasse 1, D-79104 Freiburg, Germany
R. BLOCH
Affiliation:
Department of Evolutionary Biology and Animal Ecology, Faculty of Biology, University of Freiburg, Hauptstrasse 1, D-79104 Freiburg, Germany
G. ROLSHAUSEN
Affiliation:
Department of Evolutionary Biology and Animal Ecology, Faculty of Biology, University of Freiburg, Hauptstrasse 1, D-79104 Freiburg, Germany
H. M. SCHAEFER
Affiliation:
Department of Evolutionary Biology and Animal Ecology, Faculty of Biology, University of Freiburg, Hauptstrasse 1, D-79104 Freiburg, Germany
G. SEGELBACHER
Affiliation:
Department of Wildlife Ecology and Management, University of Freiburg, Tennenbacher Strasse 4, D-79106 Freiburg
*
*Corresponding author. Department of Evolutionary Biology and Animal Ecology, Faculty of Biology, University of Freiburg, Hauptstrasse 1, D-79104 Freiburg, Germany. Tel: +49 0761 203 2545. Fax: +49 0761 203 2544. E-mail: [email protected]
Get access Rights & Permissions [Opens in a new window]

Summary

Migratory birds contribute to the movement of avian parasites between distant locations, thereby influencing parasite distribution and ecology. Here we analyse the prevalence, diversity and interaction patterns of Haemosporida parasites infecting Blackcap (Sylvia atricapilla) populations in a recently established migratory divide of southwestern Germany across 4 years. We hypothesize that the temporal and spatial isolation provided by 2 sympatric Blackcap breeding populations (migratory divide) might modify ecological interactions and thus create differences in the structure of the parasite community according to migratory route. We used a fragment of the mitochondrial DNA cytochrome b gene to determine haemosporidian haplotypes. We detected an overall infection prevalence of 70·3% (348 out of 495 blackcaps sampled from 2006 to 2009), and prevalence rates were significantly different among years and seasons. We observed a total of 27 parasite haplotypes infecting blackcaps, from them 6 new rare Haemoproteus haplotypes were found in 2 mixed infections. H. parabelopolskyi haplotypes SYAT01 (35·7%) and SYAT02 (20·8%) comprised most of the infections. An association analysis suggests that SYAT01 and SYAT02 are interacting negatively, implying that they are either competing directly for host resources, or indirectly by eliciting a cross-immune response. Molecular data show no clear difference between the parasite communities infecting blackcaps with different migratory routes, despite some temporal and spatial isolation between the two sympatric blackcap populations.

Keywords

HaemosporidaHaemoproteusSylvia atricapillacontact zonemigration
Type
Research Article
Information
Parasitology , Volume 138 , Issue 7 , June 2011 , pp. 824 - 835
Copyright
Copyright © Cambridge University Press 2011

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

REFERENCES

Atkinson, C. T., Dusek, R. J., Woods, K. L. and Iko, W. M. (2000). Pathogenicity of avian malaria in experimentally infected Hawaii Amakihi. Journal of Wildlife Diseases 36, 197–204.CrossRefGoogle ScholarPubMed
Bearhop, S., Fiedler, W., Furness, R. W., Votier, S. C., Waldron, S., Newton, J., Bowen, G. J., Berthold, P. and Farnsworth, K. (2005). Assortative mating as a mechanism for rapid evolution of a migratory divide. Science 310, 502–504.CrossRefGoogle ScholarPubMed
Bearhop, S., Furness, R. W., Hilton, G. M., Votier, S. C. and Waldron, S. (2003). A forensic approach to understanding diet and habitat use from stable isotope analysis of (avian) claw material. Functional Ecology 17, 270–275.CrossRefGoogle Scholar
Bensch, S. and Åkesson, S. (2003). Temporal and spatial variation of hematozoans in Scandinavian Willow warblers. Journal of Parasitology 89, 388–391.CrossRefGoogle ScholarPubMed
Bensch, S., Hellgren, O. and Pérez-Tris, J. (2009). A public database of malaria parasites and related haemosporidians in avian hosts based on mitochondrial cytochrome b lineages. Molecular Ecology Resources 9, 1353–1358.CrossRefGoogle ScholarPubMed
Berthold, P., Helbig, A. J., Mohr, G. and Querner, U. (1992). Rapid microevolution of migratory behavior in a wild bird species. Nature, London 360, 668–670.CrossRefGoogle Scholar
Cheesman, S. J., de Roode, J. C., Read, A. F. and Carter, R. (2003). Real-time quantitative PCR for analysis of genetically mixed infections of malaria parasites: technique validation and applications. Molecular and Biochemical Parasitology 131, 83–91.CrossRefGoogle ScholarPubMed
de Roode, J. C., Culleton, R., Cheesman, S. J., Carter, R. and Read, A. F. (2004). Host heterogeneity is a determinant of competitive exclusion or coexistence in genetically diverse malaria infections. Proceedings of the Royal Society of London, B 271, 1073–1080.CrossRefGoogle ScholarPubMed
de Roode, J. C., Helinski, M. E. H., Anwar, M. A. and Read, A. F. (2005). Dynamics of multiple infection and within-host competition in genetically diverse malaria infections. American Naturalist 166, 531–542.CrossRefGoogle ScholarPubMed
de Roode, J. C., Read, A. F., Chan, B. H. K. and Mackinnon, M. J. (2003). Rodent malaria parasites suffer from the presence of conspecific clones in three-clone Plasmodium chabaudi infections. Parasitology 127, 411–418.CrossRefGoogle ScholarPubMed
Elfving, K., Olsen, B., Bergström, S., Waldenström, J., Lundkvist, A., Sjöstedt, A., Mejlon, H. and Nilsson, K. (2010). Dissemination of spotted fever rickettsia agents in Europe by migrating birds. PLOSOne 5, e8572.CrossRefGoogle ScholarPubMed
Fiedler, W. (2005). Ecomorphology of the external flight apparatus of blackcaps (Sylvia atricapilla) with different migration behavior. Annals of the New York Academy of Sciences 1046, 253–263.CrossRefGoogle ScholarPubMed
Freed, L. A. and Cann, R. L. (2006). DNA quality and accuracy of avian malaria PCR diagnostics: A review. Condor 108, 459–473.CrossRefGoogle Scholar
Guindon, S. and Gascuel, O. (2003). A simple, fast, and accurate algorithm to estimate large phylogenies by maximum likelihood. Systematic Biology 52, 696–704.CrossRefGoogle ScholarPubMed
Hall, T. A. (1999). BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucleic Acids Symposium Series 41, 95–98.Google Scholar
Hasselquist, D., Östman, Ö., Waldenström, J. and Bensch, S. (2007). Temporal patterns of occurrence and transmission of the blood parasite Haemoproteus payevskyi in the great reed warbler Acrocephalus arundinaceus. Journal of Ornithology 148, 401–409.CrossRefGoogle Scholar
Hellgren, O., Pérez-Tris, J., Waldenström, J., Szöllosi, E., Križanauskienė, A., Hasselquist, D., Ottosson, U. and Bensch, S. (2007). Detecting shifts of transmission areas in avian blood parasites – a phylogenetic approach. Molecular Ecology 16, 1281–1290.CrossRefGoogle ScholarPubMed
Hood, G. (2009). PopTools v. 3.1.0. http://www.cse.csiro.au/poptools/Google Scholar
Huelsenbeck, J. P. and Ronquist, F. (2001). MRBAYES: Bayesian inference of phylogeny. Bioinformatics 17, 754–755.CrossRefGoogle Scholar
Križanauskienė, A., Pérez-Tris, J., Palinauskas, V., Hellgren, O., Bensch, S. and Valkiūnas, G. (2010). Molecular phylogenetic and morphological analysis of haemosporidian parasites (Haemosporida) in a naturally infected European songbird, the Blackcap Sylvia atricapilla, with description of Haemoproteus pallidulus sp. nov. Parasitology 137, 217–227.CrossRefGoogle Scholar
Kumar, S., Tamura, K. and Nei, M. (2004). MEGA 3: Integrated software for molecular evolutionary genetics analysis and sequence alignment. Briefings in Bioinformatics 5, 150–163.CrossRefGoogle Scholar
Marzal, A., deLope, F., Navarro, C. and Møller, A. P. (2005). Malaria parasites decrease reproductive success: an experimental study in a passerine bird. Oecologia 142, 541–545.CrossRefGoogle Scholar
Mazerolle, D. F. and Hobson, K. A. (2005). Estimating origins of short distance migrant songbirds in North America: contrasting inferences from hydrogen isotope measurements of feathers, claws, and blood. Condor 107, 280–288.CrossRefGoogle Scholar
Merino, S., Moreno, J., Sanz, J. J. and 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 267, 2507–2510.CrossRefGoogle Scholar
McCoy, K. D. (2003). Sympatric speciation in parasites – what is sympatry? Trends in Parasitology 19, 400–404.CrossRefGoogle ScholarPubMed
McCoy, K. D., Boulinier, T., Tirard, C. and Michalakis, Y. (2001). Host specificity of a generalist parasite: genetic evidence of sympatric host races in the seabird tick Ixodes uriae. Journal of Evolutionary Biology 14, 395–405.CrossRefGoogle Scholar
McCoy, K. D., Boulinier, T., Tirard, C. and Michalakis, Y. (2003). Host-dependent genetic structure of parasite populations: differential dispersal of seabird tick host races. Evolution 57, 288–296.Google ScholarPubMed
McCoy, K. D., Chapuis, E., Tirard, C., Boulinier, T., Michalakis, Y., Le Bohec, C., Le Maho, Y. and Gauthier-Clerc, M. (2005). Recurrent evolution of host-specialized races in a globally distributed parasite. Proceedings of the Royal Society of London, B 272, 2389–2395.Google Scholar
Miura, O., Kuris, A. M., Torchin, M. E., Hechinger, R. F. and Chiba, S. (2006). Parasites alter host phenotype and may create a new ecological niche for snail hosts. Proceedings of the Royal Society of London, B 273, 1323–1328.Google ScholarPubMed
Mouritsen, K. N. and Poulin, R. (2005). Parasites boosts biodiversity and changes animal community structure by trait-mediated indirect effects. Oikos 108, 344–350.CrossRefGoogle Scholar
Ostfeld, R. S., Keesing, F. and Eviner, V. T. (2008). Infectious Disease Ecology – Effects of Ecosystems on Disease and of Disease on Ecosystems. Princeton University Press, Princeton, NJ, USA.Google Scholar
Palinauskas, V., Valkiūnas, G., Bolshakov, C. V. and Bensch, S. (2008). Plasmodium relictum (lineage P-SGS1): effects on experimentally infected passerine birds. Experimental Parasitology 120, 372–380.CrossRefGoogle ScholarPubMed
Paul, R. E. L., Nu, V. A. T., Krettli, A. U. and Brey, P. T. (2002). Interspecific competition during transmission of two sympatric malaria parasite species to the mosquito vector. Proceedings of the Royal Society of London, B 269, 2551–2557.CrossRefGoogle Scholar
Pérez-Tris, J. and Bensch, S. (2005 a). Diagnosing genetically diverse avian malarial infections using mixed-sequence analysis and TA-cloning. Parasitology 131, 15–23.CrossRefGoogle ScholarPubMed
Pérez-Tris, J. and Bensch, S. (2005 b). Dispersal increases local transmission of avian malaria parasites. Ecology Letters 8, 838–845.CrossRefGoogle Scholar
Pérez-Tris, J., Bensch, S., Carbonell, R., Helbig, A. J. and Tellería, J. L. (2004). Historical diversification of migration patterns in a passerine bird. Evolution 58, 1819–1832.CrossRefGoogle Scholar
Pérez-Tris, J., Hellgren, O., Križanauskienė, A., Waldenström, J., Secondi, J., Bonneaud, C., Fjeldså, J., Hasselquist, D. and Bensch, S. (2007). Within-Host speciation of malaria parasites. PLOSOne 2, e235.CrossRefGoogle ScholarPubMed
Pérez-Tris, J. and Tellería, J. L. (2002). Migratory and sedentary blackcaps in sympatric non-breeding grounds: implications for the evolution of avian migration. Journal of Animal Ecology 71, 211–224.CrossRefGoogle Scholar
Perkins, S. L. (2000). Species concepts and malaria parasites: detecting a cryptic species of Plasmodium. Proceedings of the Royal Society of London, B 267, 2345–2350.CrossRefGoogle ScholarPubMed
Posada, D. (2008). jModelTest: Phylogenetic Model Averaging. Molecular Biology and Evolution 25, 1253–1256.CrossRefGoogle ScholarPubMed
Pulido, F. and Berthold, P. (2010). Current selection for lower migratory activity will drive the evolution of residency in a migratory bird population. Proceedings of the National Academy of Sciences, USA 107, 7341–7346.CrossRefGoogle Scholar
Råberg, L., de Roode, J. C., Bell, A. S., Stamou, P., Gray, D. and Read, A. F. (2006). The role of immune-mediated apparent competition in genetically diverse malaria infections. American Naturalist 168, 41–53.CrossRefGoogle ScholarPubMed
Reullier, J., Pérez-Tris, J., Bensch, S. and Secondi, J. (2006). Diversity, distribution and exchange of blood parasites meeting at an avian moving contact zone. Molecular Ecology 15, 753–763.CrossRefGoogle ScholarPubMed
Richie, T. L. (1988). Interactions between malaria parasites infecting the same vertebrate host. Parasitology 96, 607–639.CrossRefGoogle ScholarPubMed
Ricklefs, R. E. and Fallon, S. M. (2002). Diversification and host switching in avian malaria parasites. Proceedings of the Royal Society of London, B 269, 885–892.CrossRefGoogle Scholar
Ricklefs, R. E., Fallon, S. M., Latta, S. C., Swanson, B. L. and Bermingham, E. (2005). Migrants and their parasites: a bridge between two worlds. In Birds of Two Worlds: the Ecology and Evolution of Migrants (ed. Greenberg, R. and Marra, P. P.), pp. 210–221. The Johns Hopkins University Press, Baltimore, MD, USA.Google Scholar
Rolshausen, G., Hobson, K. A. and Schaefer, H. M. (2010). Spring arrival along a migratory divide of sympatric blackcaps (Sylvia atricapilla). Oecologia 162, 175–183.CrossRefGoogle ScholarPubMed
Rolshausen, G., Segelbacher, G., Hobson, K. A. and Schaefer, H. M. (2009). Contemporary evolution of reproductive isolation and phenotypic divergence in sympatry along a migratory divide. Current Biology 19, 1–5.CrossRefGoogle ScholarPubMed
Schall, J. J. and Bromwich, C. R. (1994). Interspecific interactions tested: two species of malarial parasite in a West African lizard. Oecologia 97, 326–332.CrossRefGoogle Scholar
Schall, J. J. and Vardo, A. M. (2007). Identification of microsatellite markers in Plasmodium mexicanum, a lizard malaria parasite that infects nucleated erythrocytes. Molecular Ecology Notes 7, 227–229.CrossRefGoogle Scholar
Schluter, D. (1984). A variance test for detecting species associations, with some examples. Ecology 65, 998–1005.CrossRefGoogle Scholar
Shirihai, H., Gargallo, G. and Helbig, A. J. (2001). Sylvia Warblers. Princeton University Press, Princeton, NJ, USA.Google Scholar
Stournaras, K. (2009). Vergleich von Gesang und Territorienwahl zwischen Mönchsgrasmücken (Sylvia atricapilla) verschiedener Zugrichtungen. Diploma thesis, Albert-Ludwigs-Universität Freiburg im Breisgau, Germany.Google Scholar
Svensson, L. M. E., Ruegg, K. C., Sekercioglu, C. H. and Sehgal, R. N. M. (2007). Widespread and structured distributions of blood parasite haplotypes across a migratory divide of the Swainson's thrush (Catharus ustulatus). Journal of Parasitology 93, 1488–1495.CrossRefGoogle ScholarPubMed
Szöllősi, E., Hellgren, O. and Hasselquist, D. (2008). A cautionary note on the use of nested PCR for parasite screening – an example from avian blood parasites. Journal of Parasitology 94, 562–564.CrossRefGoogle Scholar
Tellería, J. L. and Pérez-Tris, J. (2003). Seasonal distribution of a migratory bird: effects of local and regional resource tracking. Journal of Biogeography 30, 1583–1591.CrossRefGoogle Scholar
Valkiūnas, G. (2005). Avian Malaria Parasites and other Haemosporidia. CRC Press, Boca Raton, FL, USA.Google Scholar
Valkiūnas, G., Bairlein, F., Iezhova, T. A. and Dolnik, O. V. (2004). Factors affecting the relapse of Haemoproteus belopolskyi infections and the parasitemia of Trypanosoma spp. in a naturally infected European songbird, the Blackcap, Sylvia atricapilla. Parasitology Research 93, 218–222.CrossRefGoogle Scholar
Valkiūnas, G., Bensch, S., Iezhova, T. A., Križanauskienė, A., Hellgren, O. and Bolshakov, C. (2006 b). Nested cytochrome b polymerase chain reaction diagnostics underestimate mixed infections of avian blood haemosporidian parasites: microscopy is still essential. Journal of Parasitology 92, 418–422.CrossRefGoogle ScholarPubMed
Valkiūnas, G. and Iezhova, T. A. (2004 a). Detrimental effects of Haemoproteus infections on the survival of biting midge Culicoides impunctatus (Diptera: Ceratopogonidae). Journal of Parasitology 90, 194–196.CrossRefGoogle ScholarPubMed
Valkiūnas, G. and Iezhova, T. A. (2004 b). The transmission of Haemoproteus belopolskyi (Haemosporida: Haemoproteidae) of Blackcap by Culicoides impunctatus (Diptera: Ceratopogonidae). Journal of Parasitology 90, 196–198.CrossRefGoogle ScholarPubMed
Valkiūnas, G., Iezhova, T. A., Križanauskienė, A., Palinauskas, V., Sehgal, R. N. M. and Bensch, S. (2008). A comparative analysis of microscopy and PCR-based detection methods for blood parasites. Journal of Parasitology 94, 1395–1401.CrossRefGoogle ScholarPubMed
Valkiūnas, G., Iezhova, T. A., Loiseau, C. and Sehgal, R. N. M. (2009). Nested cytochrome b polymerase chain reaction diagnostics detect sporozoites of haemosporidian parasites in peripheral blood of naturally infected birds. Journal of Parasitology 95, 1512–1515.CrossRefGoogle ScholarPubMed
Valkiūnas, G., Križanauskienė, A., Iezhova, T. A., Hellgren, O. and Bensch, S. (2007). Molecular phylogenetic analysis of circumnuclear hemoproteids (Haemosporida: Haemoproteidae) of sylviid birds, with a description of Haemoproteus parabelopolskyi sp. nov. Journal of Parasitology 93, 680–687.CrossRefGoogle ScholarPubMed
Valkiūnas, G., Liutkevičius, G. and Iezhova, T. A. (2002). Complete development of three species of Haemoproteus (Haemosporida, Haemoproteidae) in the biting midge Culicoides impunctatus (Diptera, Ceratopogonidae). Journal of Parasitology 88, 864–868.CrossRefGoogle ScholarPubMed
Valkiūnas, G., Žičkus, T., Shapoval, A. P. and Iezhova, T. A. (2006 a). Effect of Haemoproteus belopolskyi (Haemosporida: Haemoproteidae) on body mass of the Blackcap Sylvia atricapilla. Journal of Parasitology 92, 1123–1125.CrossRefGoogle ScholarPubMed
Vardo, A. M. and Schall, J. J. (2007). Clonal diversity of a lizard malaria parasite, Plasmodium mexicanum, in its vertebrate host, the western fence lizard: role of variation in transmission intensity over time and space. Molecular Ecology 16, 2712–2720.CrossRefGoogle ScholarPubMed
Vardo-Zalik, A. M., Ford, A. F. and Schall, J. J. (2009). Detecting number of clones, and their relative abundance, of a malaria parasite (Plasmodium mexicanum) infecting its vertebrate host. Parasitology Research 105, 209–215.CrossRefGoogle ScholarPubMed
Vardo-Zalik, A. M. and Schall, J. J. (2008). Clonal diversity within infections and the virulence of a malaria parasite, Plasmodium mexicanum. Parasitology 135, 1363–1372.CrossRefGoogle ScholarPubMed
Vardo-Zalik, A. M. and Schall, J. J. (2009). Clonal diversity alters the infection dynamics of a malaria parasite (Plasmodium mexicanum) in its vertebrate host. Ecology 90, 529–536.CrossRefGoogle ScholarPubMed
Vorsprach, B., Meiser, C. K., Werner, D., Balczun, C. and Schaub, G. A. (2009). Monitoring of Ceratopogonidae in southwest Germany. Parasitology Research 105, 337–344.CrossRefGoogle ScholarPubMed
Waldenström, J., Bensch, S., Hasselquist, D. and Östman, Ö. (2004). A new nested polymerase chain reaction method very efficient in detecting Plasmodium and Haemoproteus infections from avian blood. Journal of Parasitology 90, 191–194.CrossRefGoogle ScholarPubMed
Waldeström, J., Bensch, S., Kiboi, S., Hasselquist, D. and Ottosson, U. (2002). Cross-species infection of blood parasites between resident and migratory songbirds in Africa. Molecular Ecology 11, 1545–1554.CrossRefGoogle Scholar
Wiersch, S. C., Lubjuhn, T., Maier, W. A. and Kampen, H. (2007). Haemosporidian infection in passerine birds from Lower Saxony. Journal of Ornithology 148, 17–24.CrossRefGoogle Scholar
Wood, J. M., Cosgrove, C. L., Wilkin, T. A., Knowles, S. C. L., Day, K. P. and Sheldon, B. C. (2007). Within-population variation in prevalence and lineage distribution of avian malaria in blue tits, Cyanistes caeruleus. Molecular Ecology 16, 3263–3273.CrossRefGoogle ScholarPubMed
Yorinks, N. and Atkinson, C. T. (2000). Effects of malaria on activity budgets of experimentally infected juvenile Apapane (Himatione sanguinea). Auk 117, 731–738.CrossRefGoogle Scholar
Supplementary material: PDF

Santiago-Alarcon Supplementary Material

Santiago-Alarcon Supplementary Material

Download Santiago-Alarcon Supplementary Material(PDF)
PDF 153.8 KB