Skip to main content

Differential prevalence and diversity of haemosporidian parasites in two sympatric closely related non-migratory passerines


Haemosporidian parasites infecting birds show distinct heterogeneity in their distribution among host species. However, despite numerous studies on the prevalence and diversity of parasite communities across species, very little is known on patterns of differences between them. Such data is lacking because up to date the majority of studies explored the patterns of variation in infections in different years, different time of sampling within a year or a breeding cycle, different study sites or was based on a small sample size, all of which may affect the estimates of prevalence and parasite diversity. Here, the prevalence, richness and diversity of haemosporidian parasites from the genera Plasmodium and Haemoproteus were studied in two closely related non-migratory hole-nesting passerines: Great Tits and Blue Tits. Birds were sampled in sympatrically breeding populations during two seasons at the same stage of their breeding cycle – late nestling care. Great Tits were more prevalently infected with Plasmodium and Haemoproteus parasites (97·1 vs 71·2%), harboured a higher proportion of multiple infections (26·2 vs 3·2%) and had a more diverse parasite community (11 vs 5 parasite lineages) than Blue Tits. Observed differences between two host species are discussed with reference to their breeding densities and immunological and behavioural characteristics.

Corresponding author
*Corresponding author: Museum and Institute of Zoology, Polish Academy of Sciences, Wilcza 64, 00-679 Warszawa, Poland. Tel.: 0048 22 629 32 21. Fax: 0048 22 629 63 02. E-mail:
Hide All
Allan S. A., Bernier U. R. and Kline D. L. (2006). Laboratory evaluation of avian odors for mosquito (Diptera: Culicidae) attraction. Journal of Medical Entomology 43, 225231.
Andrade B. B., Texeira C. R., Barral A. and Barral-Netto M. (2005). Haematophagous arthropod saliva and host defense system: a tale of tear and blood. Anais da Academia Brasileira de Ciências 77, 665693.
Antonovics J., Iwasa Y. and Hassell M. P. (1995). A generalized model of parasitoid, veneral and vector-based transmission processes. American Naturalist 145, 661675.
Arriero E. and Møller A. P. (2008). Host ecology and life-history traits associated with blood parasite species richness in birds. Journal of Evolutionary Biology 21, 15041513.
Atkinson C. T. and Van Riper C. III. (1991). Pathogenecity and epizootiology of avian haematozoa: Plasmodium, Leucocytozoon, and Haemoproteus . In Bird-parasite Interactions (ed. Loye J. E. and Zuk M.), pp. 1948. Oxford University Press, Oxford, UK.
Beadell J. S., Gering E., Austin J., Dumbacher J. P., Peirce M. A., Pratt T. K., Atkinson C. T. and Fleischer R. C. (2004). Prevalence and differential host-specificity of two avian blood parasite genera in the Australo-Papuan region. Molecular Ecology 13, 38293844.
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, 112122.
Bensch S., Hellgren O. and Pérez-Tris J. (2009). MalAvi: a public database of malaria parasites and related haemosporidians in avian hosts based on mitochondrial cytochrome b lineages. Molecular Ecology Resources 9, 13531358.
Bernotienė R., Palinauskas V., Iezhova T., Murauskaitė D. and Valkiūnas G. (2016). Avian haemosporidian parasites (Haemosporida): a comparative analysis of different polymerase chain reaction assays in detection of mixed infections. Experimental Parasitology 163, 3137.
Butler D. (2009). asreml: asreml() fits the linear mixed model. R package version 3.0.
Clayton D. H. and Moore J. (1997). Host-Parasite Evolution. General Pricinples and Avian Models. Oxford University Press, Oxford, UK.
Colwell R. K. (2013). EstimateS: Statistical estimation of species richness and shared species from samples. Version 9. User's Guide and application published at:
Cosgrove C. L., Wood M. J., Day K. P. and Sheldon B. C. (2008). Seasonal variation in Plasmodium prevalence in a population of blue tits Cyanistes caeruleus . Journal of Animal Ecology 77, 540548.
Cramp S. (ed). (1985). Handbook of the Birds of Europe, the Middle East and North Africa: the Birds of the Western Palearctic, Vol. VIII. Oxford University Press, Oxford, UK.
Davies T. J. and Pedersen A. B. (2008). Phylogeny and geography predict pathogen community similarity in wild primates and humans. Proceedings of the Royal Society of London B 275, 16951701.
Dubiec A., Góźdź I. and Mazgajski T. D. (2013). Green plant material in avian nests. Avian Biology Research 6, 133146.
Ferrer E. S., García-Navas V., Sanz J. J. and Ortego J. (2012). Molecular characterization of avian malaria parasites in three Mediterranean blue tit (Cyanistes caeruleus) populations. Parasitology Research 111, 21372142.
Garvin M. C. and Greiner E. C. (2003). Epizootiology of Haemoproteus danilewskyi (Haemosporina: Haemoproteidae) in blue jays (Cyanocitta cristata) in Southcentral Florida. Journal of Wildlife Diseases 39, 19.
Hall T. (1999). BioEdit. Biological Sequence Alignment Editor for Windows. North Carolina State University, NC, USA,
Hamilton W. D. and Zuk M. (1982). Heritable true fitness and bright birds: a role for parasites? Science 218, 384387.
Hoshen M. and Morse A. (2004). A weather-driven model of malaria transmission. Malaria Journal 3, 3246.
Isaksson C., Sepil I., Baramidze V. and Sheldon B. C. (2013). Explaining variance of avian malaria infection in the wild: the importance of host density, habitat, individual life-history and oxidative stress. BMC Ecology 13, 15.
Jenkins T. and Owens I. P. F. (2011). Biogeography of avian blood parasites (Leucocytozoon spp.) in two resident hosts across Europe: phylogeographic structuring or the abundance-occupancy relationship? Molecular Ecology 20, 39103920.
Jovani R. and Tella J. L. (2006). Parasite prevalence and sample size: misconceptions and solutions. Trends in Parasitology 22, 214218.
Knowles S. C. L., Nakagawa S. and Sheldon B. C. (2009). Elevated reproductive effort increases blood parasitaemia and decreases immune function in birds: a meta-regression approach. Functional Ecology 23, 405415.
Krams I., Suraka V., Rattiste K., Āboliņš-Ābols M., Krama T., Rantala M. J., Mierauskas P., Cīrule D. and Saks L. (2012). Comparative analysis reveals a possible immunity-related absence of blood parasites in Common Gulls (Larus canus) and Black-headed Gulls (Chroicocephalus ridibundus). Journal of Ornithology 153, 12451252.
Krams I. A., Suraka V., Rantala M. J., Sepp T., Mierauskas P., Vrublevska J. and Krama T. (2013). Acute infection of avian malaria impairs concentration of haemoglobin and survival in juvenile altricial birds. Journal of Zoology 291, 3441.
Kulma K., Low M., Bensch S. and Qvarnström A. (2013). Malaria infections reinforce competitive asymmetry between two Ficedula flycatchers in a recent contact zone. Molecular Ecology 22, 45914601.
Kulma K., Low M., Bensch S. and Qvarnström A. (2014). Malaria-infected female collared flycatchers (Ficedula albicollis) do not pay the cost of late breeding. PLoS ONE 9, e85822.
Lachish S., Knowles S. C. L., Alves R., Sepil I., Davies A., Lee S., Wood M. J. and Sheldon B. C. (2012). Spatial determinants of infection risk in a multi-species avian malaria system. Ecography 35, 112.
Lafuma L., Lambrechts M. M. and Raymond M. (2001). Aromatic plants in bird nests as a protection against bloodsucking flying insects? Behavioural Processes 56, 113120.
Lee K. A., Martin L. B. II, Hasselquist D., Ricklefs R. E. and Wikelski M. (2006). Contrasting adaptive immune defenses and blood parasite prevalence in closely related Passer sparrows. Oecologia 150, 383392.
Martínez-de la Puente J., Merino S., Lobato E., Rivero-de Aguilar J., del Cerro S., Ruiz-de-Castañeda R. and Moreno J. (2009). Does weather affect biting fly abundance in avian nests? Journal of Avian Biology 40, 653657.
Marzal A., de Lope F., Navarro C. and Møller A. P. (2005). Malarial parasites decrease reproductive success: an experimental study in a passerine bird. Oecologia 142, 541545.
Marzal A., Balbontín J., Reviriego M., García-Longoria L., Relinque C., Hermosell I. G., Magallanes S., López-Calderón C., de Lope F. and Møller A. P. (2016). A longitudinal study of age-related changes in Haemoproteus infection in a passerine bird. Oikos, in press. doi: 10.1111/oik.02778.
Ortego J. and Cordero P. J. (2010). Factors associated with the geographic distribution of leucocytozoa parasitizing nestling eagle owls (Bubo bubo): a local spatial-scale analysis. Conservation Genetics 11, 14791487.
Pagenkopp K. M., Klicka J., Durrant K. L., Garvin J. C. and Fleischer R. C. (2008). Geographic variation in malarial parasite lineages in the common yellowthroat (Geothlypis trichas). Conservation Genetics 9, 15771588.
Petit C., Hossaert-McKey M., Perret P., Blondel J. and Lambrechts M. M. (2002). Blue tits use selected plants and olfaction to maintain an aromatic environment for nestlings. Ecology Letters 5, 585589.
Podmokła E., Dubiec A., Drobniak S. M., Arct A., Gustafsson L. and Cichoń M. (2014 a). Avian malaria is associated with increased reproductive investment in the blue tit. Journal of Avian Biology 45, 219224.
Podmokła E., Dubiec A., Drobniak S. M., Arct A., Gustafsson L. and Cichoń M. (2014 b). Determinants of prevalence and intensity of infection with malaria parasites in the Blue Tit. Journal of Ornithology 155, 721727.
Poulin R. (2007). Evolutionary Ecology of Parasites, 2nd Edn. Princeton University Press, Princeton, NJ.
Pérez-Tris J. and Bensch S. (2005). Diagnosing genetically diverse avian malarial infections using mixed-sequence analysis and TA-cloning. Parasitology 131, 1523.
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, 885892.
Russell C. B. and Hunter F. F. (2005). Attraction of Culex pipiens/restuans (Diptera: Culicidae) mosquitoes to bird uropygial gland odors at two elevations in the Niagara region of Ontario. Journal of Medical Entomology 42, 301305.
Scheuerlein A. and Ricklefs R. E. (2004). Prevalence of blood parasites in European passeriform birds. Proceedings of the Royal Society of London B 271, 13631370.
Schmid-Hempel P. (2011). Evolutionary Parasitology. Oxford University Press, Oxford, UK.
Scordato E. S. C. and Kardish M. R. (2014). Prevalence and beta diversity in avian malaria communities: host species is a better predictor than geography. Journal of Animal Ecology 83, 13871397.
Shannon C. E. and Weaver W. (1962). The Mathematical Theory of Information. University of Illinois Press, Urbana.
Shurulinkov P. and Chakarov N. (2006). Prevalence of blood parasites in different local populations of reed warbler (Acrocephalus scirpaceus) and great reed warbler (Acrocephalus arundinaceus). Parasitology Research 99, 588592.
Stjernman M., Råberg L. and Nilsson J.-Å. (2008). Maximum host survival at intermediate parasite infection intensities. PLoS ONE 3, e2463.
Svensson L. (1992). Identification Guide to European Passerines, 4th Edn. BTO, Stockholm, Sweden.
Svoboda A., Marthinsen G., Turčoková L., Lifjeld J. T. and Johnsen A. (2009). Identification of blood parasites in old world warbler species from the Danube River Delta. Avian Diseases 53, 634636.
Szöllősi E., Cichoń M., Eens M., Hasselquist D., Kempenaers B., Merino S., Nilsson J.-Å., Rosivall B., Rytkönen S., Török J., Wood M. J. and Garamszegi L. Z. (2011). Determinants of distribution and prevalence of avian malaria in blue tit populations across Europe: separating host and parasite effects. Journal of Evolutionary Biology 24, 20142024.
Taylor-Robinson A. W. (1995). Regulation of immunity to malaria – valuable lessons learned from murine models. Parasitology Today 11, 334342.
Tomás G., Merino S., Martínez-de la Puente J., Moreno J., Morales J., Lobato E., Rivero-de Aguilar J. and del Cerro S. (2012). Interacting effects of aromatic plants and female age on nest-dwelling ectoparasites and blood-sucking flies in avian nests. Behavioural Process 90, 246253.
Valkiūnas G. (2005). Avian Malaria Parasites and Other Haemosporidia. CRC Press, Boca Raton, FL.
Valkiūnas G., Bensch S., Iezhova T. A., Križanauskienė A., Hellgren O. and Bolshakov C. V. (2006). Nested cytochrome b polymerase chain reaction diagnostics underestimate mixed infections of avian blood haemosporidian parasites: microscopy is still essential. Journal of Parasitology 92, 418422.
Valkiūnas G., Iezhova T. A., Loiseau C. and Sehgal R. N. M. (2009). Nested cytochrome b polymerase chain reaction diagnostics detect sporozoites of hemosporidian parasites in peripheral blood of naturally infected birds. Journal of Parasitology 95, 15121515.
Van Rooyen J., Lalubin F., Glaizot O. and Christe P. (2013). Altitudinal variation in haemosporidian parasite distribution in great tit populations. Parasites & Vectors 6, 139.
Waldenström J., Bensch S., Hasselquist D. and Östman Ö. (2004). A new nested PCR method very efficient in detecting Plasmodium and Haemoproteus infections from avian blood. Journal of Parasitology 90, 191194.
Walsh P. S., Metzger D. A. and Higuchi R. (1991). Chelex® 100 as a medium for simple extraction of DNA for PCR-based typing from forensic material. Biotechniques 10, 506513.
Wiersch S. C., Lubjuhn T., Maier W. A. and Kampen H. (2007). Haemosporidian infection in passerine birds from Lower Saxony. Journal of Ornithology 148, 1724.
Wood M. J., 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, 32633273.
Yohannes E., Križanauskienė A., Valcu M., Bensch S. and Kempenaers B. (2009). Prevalence of malaria and related haemosporidian parasites in two shorebird species with different winter habitat distribution. Journal of Ornithology 150, 287291.
Zamora-Vilchis I., Williams S. E. and Johnson C. N. (2012). Environmental temperature affects prevalence of blood parasites of birds on an elevation gradient: implications for disease in a warming climate. PLoS ONE 7, e39208.
Zylberberg M., Derryberry E. P., Breuner C. W., MacDougall-Shackleton E. A., Cornelius J. M. and Hahn T. P. (2015). Haemoproteus infected birds have increased lifetime reproductive success. Parasitology 142, 10331043.
Recommend this journal

Email your librarian or administrator to recommend adding this journal to your organisation's collection.

  • ISSN: 0031-1820
  • EISSN: 1469-8161
  • URL: /core/journals/parasitology
Please enter your name
Please enter a valid email address
Who would you like to send this to? *



Altmetric attention score

Full text views

Total number of HTML views: 11
Total number of PDF views: 68 *
Loading metrics...

Abstract views

Total abstract views: 324 *
Loading metrics...

* Views captured on Cambridge Core between September 2016 - 20th January 2018. This data will be updated every 24 hours.