Hostname: page-component-78c5997874-dh8gc Total loading time: 0 Render date: 2024-11-19T02:13:21.065Z Has data issue: false hasContentIssue false
  • English
  • Français

Sensitive measure of prevalence and parasitaemia of haemosporidia from European blackbird (Turdus merula) populations: value of PCR-RFLP and quantitative PCR

Published online by Cambridge University Press:  04 September 2006

S. BENTZ ,
T. RIGAUD ,
M. BARROCA ,
F. MARTIN-LAURENT ,
D. BRU ,
J. MOREAU  and
B. FAIVRE
S. BENTZ
Affiliation:
Equipe Ecologie Evolutive, UMR CNRS 5561 Biogéosciences, Université de Bourgogne, 6 Bd Gabriel, 21000 Dijon, France
T. RIGAUD
Affiliation:
Equipe Ecologie Evolutive, UMR CNRS 5561 Biogéosciences, Université de Bourgogne, 6 Bd Gabriel, 21000 Dijon, France
M. BARROCA
Affiliation:
Equipe Ecologie Evolutive, UMR CNRS 5561 Biogéosciences, Université de Bourgogne, 6 Bd Gabriel, 21000 Dijon, France
F. MARTIN-LAURENT
Affiliation:
Microbiologie et Géochimie des Sols, UMR 1229 INRA/Université de Bourgogne, 17 rue Sully, BP 86510, 21065 Dijon cedex, France
D. BRU
Affiliation:
Service de Séquençage et de Génotypage, Service Commun de Biologie, 17 Rue Sully, BP 86510, 21065 Dijon Cedex, France
J. MOREAU
Affiliation:
Equipe Ecologie Evolutive, UMR CNRS 5561 Biogéosciences, Université de Bourgogne, 6 Bd Gabriel, 21000 Dijon, France
B. FAIVRE
Affiliation:
Equipe Ecologie Evolutive, UMR CNRS 5561 Biogéosciences, Université de Bourgogne, 6 Bd Gabriel, 21000 Dijon, France
Get access Rights & Permissions [Opens in a new window]

Abstract

Haemosporidian parasites are common in birds in which they act as an important selective pressure. While most studies so far have focused on the effect of their prevalence on host life-history traits, no study has measured the effect of parasitaemia. We developed molecular methods to detect, identify and quantify haemosporidia in 2 natural populations of the Blackbird Turdus merula. Three different parasite genotypes were found – 1 Haemoproteus and 2 Plasmodium. A PCR-RFLP screening revealed that only approximately 3% of blackbirds were free of parasites, compared to the 34% of uninfected birds estimated by blood smear screening. A quantitative PCR (q-PCR) assay revealed a weaker parasitaemia in microscopically undetected parasites compared to microscopically detected ones. Large parasitaemia differences were found between parasite species, suggesting either differing parasite life-histories or host resistance. Parasitaemias were also weaker in male hosts, and in urban habitats, suggesting that both host factors (e.g. immunity) and habitat characteristics (e.g. vector availability) may modulate parasite density. Interestingly, these differences in parasitaemia were comparable to differences in parasite prevalence estimated by smear screening. This suggests that previous results obtained by smear screening should be reinterpreted in terms of parasitaemia instead of parasite prevalence.

Keywords

PlasmodiumHaemoproteusTurdus merulareal-time PCRPCR-RFLPfield populationsparasitaemiaprevalence
Type
Research Article
Information
Parasitology , Volume 133 , Issue 6 , December 2006 , pp. 685 - 692
Copyright
2006 Cambridge University Press

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

Allander, K. and Bennett, G. F. ( 1994). Prevalence and intensity of haematozoan infection in a population of great tits Parus major from Gotland, Sweden. Journal of Avian Biology 25, 69–74.CrossRefGoogle Scholar
Apanius, V., Yorinks, N., Bermingham, E. and Ricklefs, R. E. ( 2000). Island and taxon effects in parasitism and resistance of lesser antillean birds. Ecology 81, 1959–1969.CrossRefGoogle Scholar
Atkinson, C. T. and Van Riper III, C. ( 1991). Pathogenicity and epizootiology of avian haematozoa: Plasmodium, Leucocytozoon and Haemoproteus. In Bird-Parasite Interactions: Ecology, Evolution and Behaviour ( ed. Loye, J. E. and Zuk, M.), pp. 19–48. Oxford University Press, Oxford.
Beadell, J. S. and Fleischer, R. C. ( 2005). A restriction enzyme–based assay to distinguish between avian hemosporidians. Journal of Parasitology 91, 683–685.CrossRefGoogle Scholar
Bensch, S. and Åkesson, S. ( 2003). Temporal and spatial variation of Hematozoans in scandinavian willow warblers. Journal of Parasitology 89, 391–393.CrossRefGoogle Scholar
Bonneaud, C., Pérez-Tris, J., Chastel, O., Federici, P. and Sorci, G. ( 2006). Mhc allele associated with local resistance to malaria in passerine. Evolution 60, 383–389.CrossRefGoogle Scholar
Buchanan, K. L., Catchpole, C. K., Lewis, J. W. and Lodge, A. ( 1999). Song as an indicator of parasitism in the sedge warbler. Animal Behaviour 57, 307–314.CrossRefGoogle Scholar
Campbell, T. W. and Dein, J. F. ( 1984). Avian hematology. The basics. Veterinary Clinics of North America, Small Animal Practice 14, 223–248.CrossRefGoogle Scholar
Contini, C., Seraceni, S., Cultrera, R., Incorvaia, C., Sebastiani, A. and Picot, S. ( 2005). Evaluation of a real-time PCR-based assay using the lightcycler system for detection of Toxoplasma gondii bradyzoite genes in blood specimens from patients with toxoplasmic retinochoroiditis. International Journal for Parasitology 35, 275–283.CrossRefGoogle Scholar
Davidar, P. and Morton, E. S. ( 1993). Living with parasites: prevalence of a blood parasite and its effects on survivorship in the Purple Martin. Auk 110, 109–116.Google Scholar
Dawson, R. D. and Bortolotti, G. R. ( 2000). Effects of hematozoan parasites on condition and return rates of american kestrels. Auk 117, 373–380.Google Scholar
Fallon, S. M., Ricklefs, R. E., Swanson, B. L. and Bermingham, E. ( 2003). Detecting avian malaria: an improved polymerase chain reaction diagnostic. Journal of Parasitology 89, 1044–1047.CrossRefGoogle Scholar
Grégoire, A., Faivre, B., Heeb, P. and Cézilly, F. ( 2002). A comparison of infestation patterns by Ixodes ticks in urban and rural populations of the Common Blackbird Turdus merula. Ibis 144, 640–645.CrossRefGoogle Scholar
Hatchwell, B. J., Wood, M. J., Anwar, M. and Perrins, C. M. ( 2000). The prevalence and ecology of the hematozoan parasites of European blackbirds, Turdus merula. Canadian Journal of Zoology 78, 684–687.CrossRefGoogle Scholar
Hatchwell, B. J., Wood, M. J., Anwar, M. A., Chamberlain, D. E. and Perrins, C. M. ( 2001). The haematozoan parasites of Common Blackbirds Turdus merula: associations with host condition. Ibis 143, 420–426.CrossRefGoogle Scholar
Mackinnon, M. J. and Read, A. F. ( 2004). Immunity promotes virulence evolution in a malaria model. PLoS Biology 2, e230.CrossRefGoogle Scholar
Marzal, A., de Lope, F., Navarro, C. and Moller, A. P. ( 2005). Malarial parasites decrease reproductive success: an experimental study in a passerine bird. Oecologia 142, 541–545.CrossRefGoogle Scholar
Matsuu, A., Ono, S., Ikadai, H., Uchide, T., Imamura, S., Onuma, M., Okano, S. and Higuchi, S. ( 2005). Development of a SYBR green real-time polymerase chain reaction assay for quantitative detection of Babesia gibsoni (Asian genotype) DNA. Journal of Veterinary Diagnostic Investigation 17, 569–573.CrossRefGoogle Scholar
Merilä, J., Bjorklund, M. and Bennett, G. F. ( 1995). Geographic and individual variation in haematozoan infections in the greenfinch, Carduelis chloris. Canadian Journal of Zoology 73, 1798–1804.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
Mouton, L., Henri, H., Boulétreau, M. and Vavre, F. ( 2003). Strain-specific regulation of intracellular Wolbachia density in multiply infected insects. Molecular Ecology 12, 3459–3465.CrossRefGoogle Scholar
Pérez-Tris, J., Hasselquist, D., Hellgren, O., Krizanauskiene, A., Waldenström, J. and Bensch, S. ( 2005). What are malaria parasites? Trends in Parasitology 21, 209–211.Google Scholar
Perkins, S. L. and Schall, J. J. ( 2002). A molecular phylogeny of malarial parasites recovered from cytochrome b gene sequences. Journal of Parasitology 88, 972–978.CrossRefGoogle Scholar
Richard, F. A., Sehgal, R. N. M., Jones, H. I. and Smith, T. B. ( 2002). A comparative analysis of PCR-based detection methods for avian malaria. Journal of Parasitology 88, 819–822.CrossRefGoogle Scholar
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. and Bermingham, E. ( 2004). Evolutionary relationships, cospeciation, and host switching in avian malaria parasites. Systematic Biology 53, 111–119.CrossRefGoogle Scholar
Sambrook, J., Fritsch, E. F. and Maniatis, T. ( 1989). Molecular Cloning. A Laboratory Manual. Cold Spring Harbor Laboratory Press, New York.
Scheuerlein, A. and Ricklefs, R. E. ( 2004). Prevalence of blood parasites in European passeriform birds. Proceedings of the Royal Society of London, B 271, 1363–1370.CrossRefGoogle Scholar
Scopel, K. K. G., Fontes, C. J. F., Nunes, A. C., Horta, M. D. and Braga, E. M. ( 2004). High prevalence of Plamodium malariae infections in a Brazilian Amazon endemic area (Apiacas-Mato Grosso State) as detected by polymerase chain reaction. Acta Tropica 90, 61–64.CrossRefGoogle Scholar
Seutin, G., White, B. N. and Boag, P. T. ( 1991). Preservation of avian blood and tissue samples for DNA analyses. Canadian Journal of Zoology 69, 82–90.CrossRefGoogle Scholar
Sol, D., Jovani, R. and Torres, J. ( 2000). Geographical variation in blood parasites in feral pigeons: the role of vectors. Ecography 23, 307–314.CrossRefGoogle Scholar
Sol, D., Jovani, R. and Torres, J. ( 2003). Parasite mediated mortality and host immune response explain age-related differences in blood parasitism in birds. Oecologia 135, 542–547.CrossRefGoogle Scholar
Szymanski, M. M. and Lovette, I. J. ( 2005). High lineage diversity and host sharing of malarial parasites in a local avian assemblage. Journal of Parasitology 91, 768–774.CrossRefGoogle Scholar
Tham, J. M., Lee, S. H., Tan, T. M. C., Ting, R. C. Y. and Kara, U. A. K. ( 1999). Detection and species determination of malaria parasites by PCR: Comparison with microscopy and with ParaSight-F and ICT malaria Pf tests in a clinical environment. Journal of Clinical Microbiology 37, 1269–1273.Google Scholar
Tschirren, B., Fitze, P. S. and Richner, H. ( 2003). Sexual dimorphism in susceptibility to parasites and cell-mediated immunity in great tit nestlings. Journal of Animal Ecology 72, 839–845.CrossRefGoogle Scholar
Valkiunias, G. ( 1997). Avian Malaria Parasites and other Haemosporidia. CRC Press, Boca Raton.
Waldenström, J., Bensch, S., Hasselquist, D. and Ostman, O. ( 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 Scholar
Zuk, M. and McKean, K. A. ( 1996). Sex difference in parasite infections: patterns and processes. International Journal for Parasitology 26, 1009–1024.CrossRefGoogle Scholar