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Haemoparasites of the pied flycatcher: inter-population variation in the prevalence and community composition

Published online by Cambridge University Press:  08 November 2017

Anna Dubiec
Museum and Institute of Zoology, Polish Academy of Sciences, Wilcza 64, 00-679 Warszawa, Poland
Edyta Podmokła*
Institute of Environmental Sciences, Jagiellonian University, Gronostajowa 7, 30-387 Kraków, Poland
Iga Harnist
Museum and Institute of Zoology, Polish Academy of Sciences, Wilcza 64, 00-679 Warszawa, Poland
Tomasz D. Mazgajski
Museum and Institute of Zoology, Polish Academy of Sciences, Wilcza 64, 00-679 Warszawa, Poland
Author for correspondence: Edyta Podmokła, E-mail:


The prevalence and community composition of haemoparasites can substantially differ among avian host populations, which may lead to different selection pressures. Therefore, information about these parameters is crucial for understanding, e.g. the inter-population variation in host life history traits. Here, we molecularly screened a population of a long-distance migrant, the pied flycatcher Ficedula hypoleuca, from central Poland for the presence of three genera of blood parasites: Haemoproteus, Plasmodium and Trypanosoma. The infection rate in this population was the highest for haemosporidians (86·8%) and one of the highest for trypanosomes (39·7%) among the thus far screened breeding populations of this species. The haemosporidian community was composed of six Haemoproteus/Plasmodium lineages, and the trypanosome community – 4 species and a parasite assigned to genus level. Trypanosomes were dominated by T. culicavium, a recently described species, corroborating the prediction that insectivorous songbirds are vertebrate hosts of this parasite. Host sex and age did not explain variation in infection incidence except for the higher trypanosome infection rates in males. A comparison of the study population with three other breeding populations previously screened molecularly for haemosporidians showed some geographic differences. This study confirms the importance of examining local parasite communities across a host distribution range.

Research Article
Copyright © Cambridge University Press 2017 

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Apanius, V (1991) Avian trypanosomes as models of hemoflagellate evolution. Parasitology Today 7, 8790.Google Scholar
Baker, JR (1976) Biology of the trypanosomes of birds. In Lumsden, WHR and Evans, DA (eds). Biology of the Kinetoplastida, London: Academic Press, pp. 131174.Google Scholar
Bates, D, Mächler, M, Bolker, B and Walker, S (2015) Fitting linear mixed-effects models using lme4. Journal of Statistical Software 67, 148.Google Scholar
Bennett, GF (1961) On the specificity and transmission of some avian trypanosomes. Canadian Journal of Zoology 39, 1733.Google Scholar
Bennett, GF, Siikamäki, P, Rätti, O, Allander, K, Gustafsson, L and Squires-Parsons, D (1994) Trypanosomes of some Fennoscandian birds. Memórias do Instituto Oswaldo Cruz 89, 531537.CrossRefGoogle Scholar
Bensch, S and Åkesson, S (2003) Temporal and spatial variation of hematozoans in Scandinavian willow warblers. Journal of Parasitology 89, 388391.CrossRefGoogle ScholarPubMed
Bensch, S, Pérez-Tris, J, Waldenström, J and Hellgren, O (2004) Linkage between nuclear and mitochondrial DNA sequences in avian malaria parasites: multiple cases of cryptic speciation? Evolution 58, 16171621.Google Scholar
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.CrossRefGoogle Scholar
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.Google Scholar
Bibby, CJ and Green, RE (1980) Foraging behaviour of migrant pied flycatchers, Ficedula hypoleuca, on temporary territories. The Journal of Animal Ecology 49, 507521.Google Scholar
Bolker, BM, Brooks, ME, Clark, CJ, Geange, SW, Poulsen, JR, Stevens, MHH and White, J-SS (2009) Generalized linear mixed models: a practical guide for ecology and evolution. Trends in Ecology & Evolution 24, 127135.CrossRefGoogle ScholarPubMed
Bruford, M, Hanotte, O, Brookfield, J and Burke, T (1998) Multilocus and single-locus DNA fingerprinting. In Hoelzel, A (ed.). Molecular Genetic Analysis of Populations: A Practical Approach, Oxford, UK: IRL Press, pp. 287336.CrossRefGoogle Scholar
Canty, A and Ripley, B (2015) Boot: Bootstrap R (S-Plus) Functions. R package version 1.315.Google Scholar
Clark, P, Boardman, W and Raidal, S (2009) Atlas of Clinical Avian Hematology. Oxford: Wiley-Blackwell.Google Scholar
Cosgrove, CL, Wood, MJ, Day, KP and Sheldon, BC (2008) Seasonal variation in Plasmodium prevalence in a population of blue tits Cyanistes caeruleus. Journal of Animal Ecology 77, 540548.CrossRefGoogle Scholar
Cramp, S and Perrins, CM (1993) Handbook of the Birds of Europe, the Middle East and North Africa. The Birds of the Western Palearctic. Volume VII Flycatchers to Shrikes. Oxford, UK: Oxford University Press.Google Scholar
Dale, S, Kruszewicz, A and Slagsvold, T (1996) Effects of blood parasites on sexual and natural selection in the pied flycather. Journal of Zoology 238, 373393.CrossRefGoogle Scholar
Darriba, D, Taboada, GL, Doallo, R and Posada, D (2012) Jmodeltest 2: more models, new heuristics and parallel computing. Nature Methods 9, 772772.Google Scholar
Desser, SS, McIver, SB and Jez, D (1975) Observations on the role of simuliids and culicids in the transmission of avian and anuran trypanosomes. International Journal for Parasitology 5, 507509.Google Scholar
Deviche, P, Greiner, EC and Manteca, X (2001) Seasonal and age-related changes in blood parasite prevalence in dark-eyed juncos (Junco hyemalis, Aves, Passeriformes). Journal of Experimental Zoology 289, 456466.CrossRefGoogle ScholarPubMed
Deviche, P, Fokidis, HB, Lerbour, B and Greiner, E (2010) Blood parasitaemia in a high latitude flexible breeder, the white-winged crossbill, Loxia leucoptera: contribution of seasonal relapse versus new inoculations. Parasitology 137, 261273.Google Scholar
Dubiec, A and Mazgajski, TD (2013) Nest mass variation over the nesting cycle in the pied flycatcher (Ficedula hypoleuca). Avian Biology Research 6, 127132.Google Scholar
Dubiec, A, Podmokła, E and Gustafsson, L (2017) Intra-individual changes in haemosporidian infections over the nesting period in great tit females. Parasitology Research 116, 23852392.Google Scholar
Dufva, R (1996) Blood parasites, health, reproductive success, and egg volume in female great tits Parus major. Journal of Avian Biology 27, 8387.Google Scholar
Dyrcz, A, Wink, M, Kruszewicz, A and Leisler, B (2005) Male reproductive success is correlated with blood parasite levels and body condition in the promiscuous aquatic warbler (Acrocephalus paludicola). The Auk 122, 558565.CrossRefGoogle Scholar
Egizi, AM, Farajollahi, A and Fonseca, DM (2014) Diverse host feeding on nesting birds may limit early-season West Nile virus amplification. Vector-Borne and Zoonotic Diseases 14, 447453.CrossRefGoogle ScholarPubMed
Fallon, SM, Ricklefs, RE, Swanson, BL and Bermingham, E (2003) Detecting avian malaria: an improved polymerase chain reaction diagnostic. Journal of Parasitology 89, 10441047.Google Scholar
Ferrer, ES, García-Navas, V, Sanz, JJ and Ortego, J (2012) Molecular characterization of avian malaria parasites in three Mediterranean blue tit (Cyanistes caeruleus) populations. Parasitology Research 111, 21372142.Google Scholar
Freeman-Gallant, CR, O'Connor, KD and Breuer, ME (2001) Sexual selection and the geography of Plasmodium infection in Savannah sparrows (Passerculus sandwichensis). Oecologia 127, 517521.CrossRefGoogle ScholarPubMed
Garamszegi, LZ (2010) The sensitivity of microscopy and PCR-based detection methods affecting estimates of prevalence of blood parasites in birds. Journal of Parasitology 96, 11971203.Google Scholar
Gardener, M (2014) Community Ecology: Analytical Methods Using R and Excel. Exeter: Pelagic Publishing.Google Scholar
Griffiths, R, Double, MC, Orr, K and Dawson, RJG (1998) A DNA test to sex most birds. Molecular Ecology 7, 10711075.CrossRefGoogle ScholarPubMed
Haldane, JBS (1949) Disease and evolution. La Ricerca Scentifica Supplemento 19, 111.Google Scholar
Hall, TA (1999) Bioedit: a user-friendly biological sequence alignment editor and analysis program for windows 95/98/NT. Nucleic Acids Symposium Series 41, 9598.Google Scholar
Hellgren, O, Waldenström, J and Bensch, S (2004) A new PCR assay for simultaneous studies of Leucocytozoon, Plasmodium, and Haemoproteus from avian blood. Journal of Parasitology 90, 797802.CrossRefGoogle ScholarPubMed
Hulier, E, Pétour, P, Snounou, G, Nivez, M-P, Miltgen, F, Mazier, D and Rénia, L (1996) A method for the quantitative assessment of malaria parasite development in organs of the mammalian host. Molecular and Biochemical Parasitology 77, 127135.CrossRefGoogle ScholarPubMed
Knowles, SCL, Palinauskas, V and Sheldon, BC (2010) Chronic malaria infections increase family inequalities and reduce parental fitness: experimental evidence from a wild bird population. Journal of Evolutionary Biology 23, 557569.Google Scholar
Knowles, SCL, Wood, MJ, Alves, R, Wilkin, TA, Bensch, S and Sheldon, BC (2011) Molecular epidemiology of malaria prevalence and parasitaemia in a wild bird population. Molecular Ecology 20, 10621076.CrossRefGoogle Scholar
Krama, T, Krams, R, Cīrule, D, Moore, FR, Rantala, MJ and Krams, IA (2015) Intensity of haemosporidian infection of parids positively correlates with proximity to water bodies, but negatively with host survival. Journal of Ornithology 156, 10751084.Google Scholar
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.CrossRefGoogle Scholar
Laaksonen, T, Sirkiä, PM, Calhim, S, Brommer, JE, Leskinen, PK, Primmer, CR, Adamík, P, Artemyev, AV, Belskii, E, Both, C, Bureš, S, Burgess, MD, Doligez, B, Forsman, JT, Grinkov, V, Hoffmann, U, Ivankina, E, Král, M, Krams, I, Lampe, HM, Moreno, J, Mägi, M, Nord, A, Potti, J, Ravussin, P-A and Sokolov, L (2015) Sympatric divergence and clinal variation in multiple coloration traits of Ficedula flycatchers. Journal of Evolutionary Biology 28, 779790.CrossRefGoogle ScholarPubMed
Lachish, S, Knowles, SCL, Alves, R, Wood, MJ and Sheldon, BC (2011) Fitness effects of endemic malaria infections in a wild bird population: the importance of ecological structure. Journal of Animal Ecology 80, 11961206.Google Scholar
Martínez-de la Puente, J, Merino, S, Tomas, G, Moreno, J, Morales, J, Lobato, E, Garcia-Fraile, S and Belda, EJ (2010) The blood parasite Haemoproteus reduces survival in a wild bird: a medication experiment. Biology Letters 6, 663665.Google Scholar
McCurdy, DG, Shutler, D, Mullie, A and Forbes, MR (1998) Sex-biased parasitism of avian hosts: relations to blood parasite taxon and mating system. Oikos 82, 303312.Google Scholar
Merino, S, Moreno, J, Jose Sanz, 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 B: Biological Sciences 267, 25072510.CrossRefGoogle Scholar
Molyneux, DH (1977) Vector relationships in the Trypanosomatidae. Advances in Parasitology 15, 182.Google Scholar
Mungomba, LM, Molyneux, DH and Wallbanks, KR (1989) Host-parasite relationship of Trypanosoma corvi in Ornithomyia avicularia. Parasitology Research 75, 167174.Google Scholar
Nagata, H (2006) Reevaluation of the prevalence of blood parasites in Japanese passerines by using PCR based molecular diagnostics. Ornithological Science 5, 105112.Google Scholar
Neto, JM, Pérez-Rodríguez, A, Haase, M, Flade, M and Bensch, S (2015) Prevalence and diversity of plasmodium and haemoproteus parasites in the globally-threatened aquatic warbler Acrocephalus paludicola. Parasitology 142, 11831189.Google Scholar
Nilsson, E, Taubert, H, Hellgren, O, Huang, X, Palinauskas, V, Markovets, MY, Valkiūnas, G and Bensch, S (2016) Multiple cryptic species of sympatric generalists within the avian blood parasite Haemoproteus majoris. Journal of Evolutionary Biology 29, 18121826.CrossRefGoogle ScholarPubMed
Oakgrove, KS, Harrigan, RJ, Loiseau, C, Guers, S, Seppi, B and Sehgal, RNM (2014) Distribution, diversity and drivers of blood-borne parasite co-infections in Alaskan bird populations. International Journal for Parasitology 44, 717727.Google Scholar
Oksanen, J, Blanchet, FG, Kindt, R, Legendre, P, Minchin, PR, O'Hara, RB, Simpson, GL, Solymos, P, Stevens, MHH and Wagner, H (2016) Vegan: Community Ecology Package. R package version 2.35.Google Scholar
Ouwehand, J, Ahola, MP, Ausems, ANMA, Bridge, ES, Burgess, M, Hahn, S, Hewson, CM, Klaassen, RHG, Laaksonen, T, Lampe, HM, Velmala, W and Both, C (2016) Light-level geolocators reveal migratory connectivity in European populations of pied flycatchers Ficedula hypoleuca. Journal of Avian Biology 47, 6983.Google Scholar
Pagenkopp, KM, Klicka, J, Durrant, KL, Garvin, JC and Fleischer, RC (2008) Geographic variation in malarial parasite lineages in the common yellowthroat (Geothlypis trichas). Conservation Genetics 9, 15771588.Google Scholar
Pedersen, AB and Fenton, A (2007) Emphasizing the ecology in parasite community ecology. Trends in Ecology & Evolution 22, 133139.Google Scholar
Peev, S, Zehtindjiev, P, Ilieva, M, Träff, J, Briedis, M and Adamík, P (2016) Haemosporidian blood parasite diversity and prevalence in the semi-collared flycatcher (Ficedula semitorquata) from the eastern Balkans. Parasitology International 65, 613617.Google Scholar
Podmokła, E, Dubiec, A, Drobniak, SM, Arct, A, Gustafsson, L and Cichoń, M (2014) Determinants of prevalence and intensity of infection with malaria parasites in the blue tit. Journal of Ornithology 155, 721727.Google Scholar
Poulin, R (2003) The decay of similarity with geographical distance in parasite communities of vertebrate hosts. Journal of Biogeography 30, 16091615.Google Scholar
R Development Core Team (2014) R: A Language and Environment for Statistical Computing. Vienna, Austria: R Foundation for Statistical Computing.Google Scholar
Rätti, O, Dufva, R and Alatalo, RV (1993) Blood parasites and male fitness in the pied flycatcher. Oecologia 96, 410414.CrossRefGoogle ScholarPubMed
Ribeiro, SF, Sebaio, F, Branquinho, FCS, Marini, , Vago, AR and Braga, ÉM (2005) Avian malaria in Brazilian passerine birds: parasitism detected by nested PCR using DNA from stained blood smears. Parasitology 130, 261267.CrossRefGoogle ScholarPubMed
Ronquist, F and Huelsenbeck, JP (2003) Mrbayes 3: bayesian phylogenetic inference under mixed models. Bioinformatics 19, 15721574.Google Scholar
Sanz, JJ, Arriero, E, Moreno, J and Merino, S (2001a) Female hematozoan infection reduces hatching success but not fledging success in pied flycatchers Ficedula hypoleuca. The Auk 118, 750755.Google Scholar
Sanz, JJ, Arriero, E, Moreno, J and Merino, S (2001b) Interactions between hemoparasite status and female age in the primary reproductive output of pied flycatchers. Oecologia 126, 339344.Google Scholar
Schuurs, AHWM and Verheul, HAM (1990) Effects of gender and sex steroids on the immune response. Journal of Steroid Biochemistry 35, 157172.CrossRefGoogle ScholarPubMed
Sehgal, RNM, Jones, HI and Smith, TB (2001) Host specificity and incidence of Trypanosoma in some African rainforest birds: a molecular approach. Molecular Ecology 10, 23192327.Google Scholar
Siikamäki, P, Rätti, O, Hovi, M and Bennett, GF (1997) Association between haematozoan infections and reproduction in the pied flycatcher. Functional Ecology 11, 176183.Google Scholar
Silverin, B and Andersson, G (1984) Food composition of adult and nestling pied flycatchers, Ficedula hypoleuca, during the breeding period. Var Fagelvarld 43, 517524.Google Scholar
Soares, L, Ellis, VA and Ricklefs, RE (2016) Co-infections of haemosporidian and trypanosome parasites in a North American songbird. Parasitology 143, 19301938.Google Scholar
Sol, D, Jovani, R and Torres, J (2000) Geographical variation in blood parasites in feral pigeons: the role of vectors. Ecography 23, 307314.CrossRefGoogle Scholar
Spurgin, LG, Illera, JC, Padilla, DP and Richardson, DS (2012) Biogeographical patterns and co-occurrence of pathogenic infection across island populations of Berthelot's pipit (Anthus berthelotii). Oecologia 168, 691701.Google Scholar
Svensson, L (1994) Identification Guide to European Passerines. Stockhom: Svensson.Google Scholar
Svoboda, A, Marthinsen, G, Pavel, V, Chutný, B, Turčoková, L, Lifjeld, JT and Johnsen, A (2015) Blood parasite prevalence in the Bluethroat is associated with subspecies and breeding habitat. Journal of Ornithology 156, 371380.Google Scholar
Svobodová, M, Weidinger, K, Peške, L, Volf, P, Votýpka, J and Voříšek, P (2015a) Trypanosomes and haemosporidia in the buzzard (Buteo buteo) and sparrowhawk (Accipiter nisus): factors affecting the prevalence of parasites. Parasitology Research 114, 551560.Google Scholar
Svobodová, M, Volf, P and Votýpka, J (2015b) Trypanosomatids in ornithophilic bloodsucking Diptera. Medical and Veterinary Entomology 29, 444447.Google Scholar
Swanson, BL, Lyons, AC and Bouzat, JL (2014) Distribution, prevalence and host specificity of avian malaria parasites across the breeding range of the migratory lark sparrow (Chondestes grammacus). Genetica 142, 235249.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, 562564.Google Scholar
Szöllősi, E, Cichoń, M, Eens, M, Hasselquist, D, Kempenaers, B, Merino, S, Nilsson, J-Å, Rosivall, B, Rytkönen, S, Török, J, Wood, MJ and Garemszegi, LZ (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.CrossRefGoogle ScholarPubMed
Szöllősi, E, Garamszegi, LZ, Hegyi, G, Laczi, M, Rosivall, B and Török, J (2016) Haemoproteus infection status of collared flycatcher males changes within a breeding season. Parasitology Research 115, 46634672.Google Scholar
Valkiūnas, G, Iezhova, TA and Sehgal, RNM (2016) Deforestation does not affect the prevalence of a common trypanosome in African birds. Acta Tropica 162, 222228.CrossRefGoogle Scholar
van Oers, K, Richardson, DS, Sæther, SA and Komdeur, J (2010) Reduced blood parasite prevalence with age in the Seychelles warbler: selective mortality or suppression of infection? Journal of Ornithology 151, 6977.Google Scholar
Votýpka, J, Szabová, J, Rádrová, J, Zídková, L and Svobodová, M (2012) Trypanosoma culicavium sp. nov., an avian trypanosome transmitted by Culex mosquitoes. International Journal of Systematic and Evolutionary Microbiology 62, 745754.Google Scholar
Votýpka, J and Svobodová, M (2004) Trypanosoma avium: experimental transmission from black flies to canaries. Parasitology Research 92, 147151.Google Scholar
Votýpka, J, Lukeš, J and Oborník, M (2004) Phylogenetic relationship of Trypanosoma corvi with other avian Trypanosomes. Acta Protozoologica 43, 225231.Google Scholar
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, 191194.Google Scholar
Wiersch, SC, Lubjuhn, T, Maier, WA and Kampen, H (2007) Haemosporidian infection in passerine birds from lower Saxony. Journal of Ornithology 148, 1724.Google Scholar
Zídková, L, Cepicka, I, Szabová, J and Svobodová, M (2012) Biodiversity of avian trypanosomes. Infection, Genetics and Evolution 12, 102112.Google Scholar