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Correlates of blood parasitism in a threatened marshland passerine: infection by kinetoplastids of the genus Trypanosoma is related to landscape metrics of habitat edge

Published online by Cambridge University Press:  08 May 2019

Justyna Kubacka Open the ORCID record for Justyna Kubacka [Opens in a new window] ,
Alina Gerlée ,
Julien Foucher ,
Judith Korb  and
Edyta Podmokła
Justyna Kubacka*
Affiliation:
Museum and Institute of Zoology, Polish Academy of Sciences, Wilcza 64, 00-679 Warsaw, Poland
Alina Gerlée
Affiliation:
Department of Geoecology, Faculty of Geography and Regional Studies, University of Warsaw, Krakowskie Przedmieście 30, 00-927 Warsaw, Poland
Julien Foucher
Affiliation:
Association pour la Connaissance et la Recherche Ornithologique Loire et Atlantique (ACROLA), 10 rue de la Paix, 44480 Donges, France
Judith Korb
Affiliation:
Evolutionary Biology and Ecology, Institute of Biology I (Zoology), Hauptstrasse 1, D-79104 Freiburg, Germany
Edyta Podmokła
Affiliation:
Department of Comparative Anatomy, Institute of Zoology and Biomedical Research, Jagiellonian University, Gronostajowa 9, 30-387 Kraków, Poland
*
Author for correspondence: Justyna Kubacka, E-mail: [email protected]
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Abstract

In birds, vector-borne parasites invading the bloodstream are important agents of disease, affect fitness and shape population viability, thus being of conservation interest. Here, we molecularly identified protozoan blood parasites in two populations of the threatened Aquatic Warbler Acrocephalus paludicola, a migratory passerine nesting in open marsh. We explored whether prevalence and lineage diversity of the parasites vary by population and whether infection status is explained by landscape metrics of habitat edge and individual traits (body mass, fat score, wing length and sex). Aquatic Warblers were infected by genera Plasmodium, Leucocytozoon and Trypanosoma, with seven, one and four lineages, and 29.9, 0.7 and 12.5% prevalence, respectively. No Haemoproteus infections were detected. Prevalence did not vary between the populations, but lineage diversity was higher in Polesie than in Biebrza for all the lineages pooled and for Plasmodium. Infection by Trypanosoma decreased with patch core area and increased with density of habitat edge. Infection status was not predicted by the individual traits. Our study is the first to show an association between edge-related landscape features and blood parasitism in an open habitat bird. This finding will support informed conservation measures for avian species of the globally shrinking marshland and other treeless habitats.

Keywords

Aquatic Warbleravian malariablood parasitesbody conditionedge effectsHaemoproteusLeucocytozoonPlasmodiumsex effects
Type
Research Article
Information
Parasitology , Volume 146 , Issue 8 , July 2019 , pp. 1036 - 1046
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Copyright
Copyright © Cambridge University Press 2019 

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References

Altschul, SF, Gish, W, Miller, W, Myers, EW and Lipman, DJ (1990) Basic local alignment search tool. Journal of Molecular Biology 215, 403–410.Google Scholar
Apanius, V (1991) Avian trypanosomes as models of hemoflagellate evolution. Parasitology Today 7, 87–90.Google Scholar
Aquatic Warbler Conservation Team (1999) World population, trends and conservation status of the Aquatic Warbler Acrocephalus paludicola. Die Vogelwelt 2, 12–32.Google Scholar
Arriero, E and Møller, AP (2008) Host ecology and life-history traits associated with blood parasite species richness in birds. Journal of Evolutionary Biology 21, 1504–1513.Google Scholar
Atkinson, CT, Forrester, DJ and Greiner, EC (1988) Pathogenicity of Haemoproteus meleagridis (Haemosporina: Haemoproteidae) in experimentally infected domestic turkeys. The Journal of Parasitology 74, 228–239.Google Scholar
Atkinson, CT, Thomas, NJ and Hunter, DB (eds) (2008) Parasitic Diseases of Wild Birds. Ames, IA, USA: John Wiley & Sons, Inc.Google Scholar
Bates, D, Mächler, M, Bolker, B and Walker, S (2015) Fitting linear mixed-effects models using lme4. Journal of Statistical Software 67, 1–48.Google Scholar
Beaudoin, RL, Applegate, JE, Davis, DE and McLean, RG (1971) A model for the ecology of avian malaria. Journal of Wildlife Diseases 7, 5–14.Google Scholar
Belo, NO, Pinheiro, RT, Reis, ES, Ricklefs, RE and Braga, ÉM (2011) Prevalence and lineage diversity of avian haemosporidians from three distinct cerrado habitats in Brazil. PLoS ONE 6, e17654.Google Scholar
Bennett, GF, Montgomerie, R and Seutin, G (1992) Scarcity of Haematozoa in birds breeding on the Arctic tundra of North America. The Condor 94, 289–292.Google Scholar
Bensch, S, Stjernman, M, Hasselquist, D, Ostman, O, Hansson, B, Westerdahl, H and Pinheiro, RT (2000) Host specificity in avian blood parasites: a study of Plasmodium and Haemoproteus mitochondrial DNA amplified from birds. Proceedings of the Royal Society B: Biological Sciences 267, 1583–1589.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, 112–122.Google 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, 1353–1358.Google Scholar
Benson, DA, Cavanaugh, M, Clark, K, Karsch-Mizrachi, I, Lipman, DJ, Ostell, J and Sayers, EW (2013) Genbank. Nucleic Acids Research 41, D36–D42.Google Scholar
Biedrzycka, A, Migalska, M and Bielański, W (2015) A quantitative PCR protocol for detecting specific Haemoproteus lineages: molecular characterization of blood parasites in a Sedge Warbler population from southern Poland. Journal of Ornithology 156, 201–208.Google Scholar
BirdLife International (2017) Acrocephalus paludicola (amended version of 2016 assessment). The IUCN Red List of Threatened Species 2017: e.T22714696A110042215.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, 127–135.Google Scholar
Bonneaud, C, Sepil, I, Mila, B, Buermann, W, Pollinger, J, Sehgal, RNM, Valkiūnas, G, Iezhova, TA, Saatchi, S and Smith, TB (2009) The prevalence of avian Plasmodium is higher in undisturbed tropical forests of Cameroon. Journal of Tropical Ecology 25, 439–447.Google Scholar
Briedis, M and Keišs, O (2016) Extracting historical population trends using archival ringing data – an example: the globally threatened Aquatic Warbler. Journal of Ornithology 157, 419–425.Google Scholar
Burnham, KP and Anderson, DR (2002) Model Selection and Multimodel Inference: A Practical Information-Theoretic Approach, 2nd Edn. New York, USA: Springer-Verlag.Google Scholar
Burnham, KP and Anderson, DR (2004) Multimodel inference: understanding AIC and BIC in model selection. Sociological Methods and Research 33, 261–304.Google Scholar
Canty, A and Ripley, B (2017) boot: Bootstrap R (S-Plus) functions. R package version 1.3-20. CRAN R Project. doi: 10.1093/gerona/glq232.Google Scholar
Dawson, RD and Bortolotti, GR (2000) Effects of hematozoan parasites on condition and return rates of American Kestrels. The Auk 117, 373–381.Google Scholar
Dawson, RD and Bortolotti, GR (2001) Sex-specific associations between reproductive output and hematozoan parasites of American Kestrels. Oecologia 126, 193–200.Google Scholar
Dimitrov, D, Zehtindjiev, P and Bensch, S (2010) Genetic diversity of avian blood parasites in SE Europe: cytochrome b lineages of the genera Plasmodium and Haemoproteus (Haemosporida) from Bulgaria. Acta Parasitologica 55, 201–209.Google Scholar
Dimitrov, D, Ilieva, M, Ivanova, K, Brlik, V and Zehtindjiev, P (2018) Detecting local transmission of avian malaria and related haemosporidian parasites (Apicomlexa, Haemosporida) at a Special Protection Area of Natura 2000 network. Parasitology 117, 2187–2199.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, 558–565.Google Scholar
Fecchio, A, Pinheiro, R, Felix, G, Faria, IP, Pinho, JB, Lacorte, GA, Braga, EM, Farias, IP, Aleixo, A, Tkach, VV, Collins, MD, Bell, JA and Weckstein, JD (2018) Host community similarity and geography shape the diversity and distribution of haemosporidian parasites in Amazonian birds. Ecography 41, 505–515.Google Scholar
Fernández, M, Rojo, MÁ, Casanueva, P, Carrión, S, Hernández, MÁ and Campos, F (2010) High prevalence of haemosporidians in Reed Warbler Acrocephalus scirpaceus and Sedge Warbler Acrocephalus schoenobaenus in Spain. Journal of Ornithology 151, 27–32.Google Scholar
Ferraguti, M, Martínez-de la Puente, J, Bensch, S, Roiz, D, Ruiz, S, Viana, DS, Soriguer, RC and Figuerola, J (2018) Ecological determinants of avian malaria infections: an integrative analysis at landscape, mosquito and vertebrate community levels. Journal of Animal Ecology 87, 727–740.Google Scholar
Flade, M, Malashevich, U, Krogulec, J, Poluda, A, Preiksa, Z, Végvári, Z and Lachmann, L (2018) World distribution, population, and trends. In Tanneberger, F and Kubacka, J (eds), The Aquatic Warbler Conservation Handbook. Potsdam, Germany: Brandenburg State Office for Environment (LfU), pp. 22–35.Google Scholar
Fredeen, FJ and Mason, PG (1991) Meteorological factors influencing host-seeking activity of female Simulium luggeri (Diptera: Simuliidae). Journal of Medical Entomology 28, 831–840.Google Scholar
Gardener, M (2014) Community Ecology: Analytical Methods Using R and Excel. Exeter, UK: Pelagic Publishing.Google Scholar
Gonzalez-Quevedo, C, Davies, RG and Richardson, DS (2014) Predictors of malaria infection in a wild bird population: landscape-level analyses reveal climatic and anthropogenic factors. Journal of Animal Ecology 83, 1091–1102.Google Scholar
Gudex-Cross, D, Barraclough, RK, Brunton, DH and Derraik, JGB (2015) Mosquito communities and avian malaria prevalence in Silvereyes (Zosterops lateralis) within forest edge and interior habitats in a New Zealand regional park. EcoHealth 12, 432–440.Google Scholar
Hakkarainen, H, Ilmonen, P, Koivunen, V and Korpimäki, E (1998) Blood parasites and nest defense behaviour of Tengmalm's Owls. Oecologia 114, 574–577.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. doi: citeulike-article-id:691774.Google Scholar
Hatchwell, BJ, Wood, MJ, Anwar, MA, Chamberlain, DE and Perrins, CM (2001) The haematozoan parasites of Common Blackbirds Turdus merula: associations with host condition. Ibis 143, 420–426.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, 797–802.Google Scholar
Hellgren, O, Wood, MJ, Waldenström, J, Hasselquist, D, Ottosson, U, Stervander, M and Bensch, S (2013) Circannual variation in blood parasitism in a sub-Saharan migrant passerine bird, the Garden Warbler. Journal of Evolutionary Biology 26, 1047–1059.Google Scholar
Herse, MR, With, KA and Boyle, WA (2018) The importance of core habitat for a threatened species in changing landscapes. Journal of Applied Ecology 55, 2241–2252.Google Scholar
Holmes, JC (1996) Parasites as threats to biodiversity in shrinking ecosystems. Biodiversity and Conservation 5, 975–983.Google Scholar
Kaiser, A (1993) A new multi-category classification of subcutaneous fat deposits of songbirds. Journal of Field Ornithology 64, 246–255.Google Scholar
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, 557–569.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, 1062–1076.Google 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, 1075–1084.Google Scholar
Kubacka, J, Oppel, S, Dyrcz, A, Lachmann, L, Barros Da Costa, JPD, Kail, U and Zdunek, W (2014) Effect of mowing on productivity in the endangered Aquatic Warbler Acrocephalus paludicola. Bird Conservation International 24, 45–58.Google Scholar
Kučera, J (1982) Blood parasites of birds in Central Europe. 4. Trypanosoma, “Atoxoplasma”, microfilariae and other rare haematozoa. Folia Parasitologica 29, 107–113.Google Scholar
Laurance, SGW, Jones, D, Westcott, D, Mckeown, A, Harrington, G and Hilbert, DW (2013) Habitat fragmentation and ecological traits influence the prevalence of avian blood parasites in a tropical rainforest landscape. PLoS ONE 8, e76227.Google Scholar
Li, Z, Roux, E, Dessay, N, Girod, R, Stefani, A, Nacher, M, Moiret, A and Seyler, F (2016) Mapping a knowledge-based malaria hazard index related to landscape using remote sensing: application to the cross-border area between French Guiana and Brazil. Remote Sensing 8, 319.Google Scholar
Lillie, TH, Kline, DL and Hall, DW (1988) Host-seeking activity of Culicoides spp. (Diptera: Ceratopogonidae) near Yankeetown, Florida. Journal of the American Mosquito Control Association 4, 485–493.Google Scholar
Loiseau, C, Iezhova, T, Valkiūnas, G, Chasar, A, Hutchinson, A, Buermann, W, Smith, TB and Sehgal, RNM (2010) Spatial variation of haemosporidian parasite infection in African rainforest bird species. Journal of Parasitology 96, 21–29.Google Scholar
Loye, J and Carroll, S (1995) Birds, bugs and blood: avian parasitism and conservation. Trends in Ecology & Evolution 10, 232–235.Google Scholar
Lyles, AM and Dobson, AP (1993) Infectious disease and intensive management: population dynamics, threatened hosts, and their parasites. Journal of Zoo and Wildlife Medicine 24, 315–326.Google Scholar
Martin, F, McCreadie, J and Colbo, M (1994) Effect of trap site, time of day, and meteorological factors on abundance of host-seeking mammalophilic black flies (Diptera: Simuliidae). The Canadian Entomologist 126, 283–289.Google Scholar
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, 653–657.Google Scholar
Marzal, A (2012) Malaria parasites. In Okwa, DO (ed.), Rijeka, Chroatia: InTech, pp. 135–159. doi: 10.5772/33730.Google Scholar
Marzal, A, de Lope, F, Navarro, C and Møller, AP (2005) Malarial parasites decrease reproductive success: an experimental study in a passerine bird. Oecologia 142, 541–545.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, 303–312.Google Scholar
McGarigal, K, Cushman, SA, Neel, MC and Ene, E (2012) FRAGSTATS v4: Spatial Pattern Analysis Program for Categorical and Continuous Maps. University of Massachusettes, Amherst, MA. URL . doi: citeulike-article-id:287784.Google Scholar
Merino, S, Moreno, J, Sanz, JJ 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. Series B: Biological Sciences 267, 2507–2510.Google Scholar
Molyneux, DH (1977) Vector relationships in the Trypanosomatidae. Advances in Parasitology 15, 1–82.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, 1183–1189.Google Scholar
Oksanen, J, Blanchet, FG, Friendly, M, Kindt, R, Legendre, P, McGlinn, D, Minchin, PR, O'Hara, RB, Simpson, GL, Solymos, P, Henry, M, Stevens, H, Szoecs, E and Wagner, H (2019) vegan: Community Ecology Package. R package version 2.5-4.Google Scholar
Oppliger, A, Clobert, J, Lecomte, J, Lorenzon, P, Boudjemadi, K and John-Alder, HB (1998) Environmental stress increases the prevalence and intensity of blood parasite infection in the common lizard Lacerta vivipara. Ecology Letters 1, 129–138.Google Scholar
Pérez-Rodríguez, A, Khimoun, A, Ollivier, A, Eraud, C, Faivre, B and Garnier, S (2018) Habitat fragmentation, not habitat loss, drives the prevalence of blood parasites in a Caribbean passerine. Ecography 41, 1835–1849.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, 721–727.Google Scholar
Polish Society for the Protection of Birds (2014) Raport monitoringów w projekcie LIFE+ „Wodniczka i biomasa” (lata 2011-2014) wraz z oceną działań projektu. Marki, Poland: OTOP.Google Scholar
QGIS Development Team (2018) QGIS Geographic Information System. Open Source Geospatial Foundation Project.Google Scholar
Rätti, O, Dufva, R and Alatalo, RV (1993) Blood parasites and male fitness in the pied flycatcher. Oecologia 96, 410–414.Google Scholar
R Core Team (2018) R: A Language and Environment for Statistical Computing.Google Scholar
Reinoso-Pérez, MT, Canales-Delgadillo, JC, Chapa-Vargas, L and Riego-Ruiz, L (2016) Haemosporidian parasite prevalence, parasitemia, and diversity in three resident bird species at a shrubland dominated landscape of the Mexican highland plateau. Parasites and Vectors 9, 307.Google Scholar
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.Google Scholar
Ries, L, Fletcher, RJ, Battin, J and Sisk, TD (2004) Ecological responses to habitat edges: mechanisms, models, and variability explained. Annual Review of Ecology, Evolution, and Systematics 35, 491–522.Google Scholar
Sambrook, J and Russell, DW (2001) Molecular Cloning: A Laboratory Manual, 3rd Edn. New York, USA: Cold Spring Harbor.Google Scholar
Schaefer, HM, Naef-Daenzer, B, Leisler, B, Schmid, V, Muller, JK and Schulze-Hagen, K (2000) Spatial behaviour in the Aquatic Warbler (Acrocephalus paludicola) during mating and breeding. Journal fur Ornithologie 141, 418–424.Google Scholar
Scordato, ESC and Kardish, MR (2014) Prevalence and beta diversity in avian malaria communities: host species is a better predictor than geography. Journal of Animal Ecology 83, 1387–1397.Google Scholar
Sebaio, F, Braga, ÉM, Branquinho, F, Manica, LT and Marini, MÂ (2010) Blood parasites in Brazilian Atlantic Forest birds: effects of fragment size and habitat dependency. Bird Conservation International 20, 432–439.Google Scholar
Sehgal, RNM (2015) Manifold habitat effects on the prevalence and diversity of avian blood parasites. International Journal for Parasitology: Parasites and Wildlife 4, 421–430.Google Scholar
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, 2319–2327.Google Scholar
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, 588–592.Google Scholar
Shurulinkov, P, Chakarov, N and Daskalova, G (2012) Blood parasites, body condition, and wing length in two subspecies of yellow wagtail (Motacilla flava) during migration. Parasitology Research 110, 2043–2051.Google Scholar
Shurulinkov, P, Spasov, L, Stoyanov, G and Chakarov, N (2018) Blood parasite infections in a wild population of ravens (Corvus corax) in Bulgaria. Malaria Journal 17, 33.Google Scholar
Shutler, D, Clark, RG, Rutherford, ST and Mullie, A (1999) Blood parasites, clutch volume, and condition of Gadwalls and Mallards. Journal of Avian Biology 30, 295–301.Google Scholar
Šlapeta, J, Morin-Adeline, V, Thompson, P, McDonell, D, Shiels, M, Gilchrist, K, Votýpka, J and Vogelnest, L (2016) Intercontinental distribution of a new trypanosome species from Australian endemic Regent Honeyeater (Anthochaera phrygia). Parasitology 143, 1012–1025.Google Scholar
Svensson, L (1992) Identification Guide to European Passerines, 4th Edn. Norfolk, UK: British Trust for Ornithology.Google Scholar
Svoboda, A, Marthinsen, G, Turčoková, L, Lifjeld, JT and Johnsen, A (2009) Identification of blood parasites in Old World warbler species from the Danube River Delta. Avian Diseases Digest 53, 634–636.Google Scholar
Svobodová, M, Dolnik, OV, Čepička, I and Rádrová, J (2017) Biting midges (Ceratopogonidae) as vectors of avian trypanosomes. Parasites and Vectors 10, 224.Google Scholar
Tella, JL, Blanco, G, Forero, MG, Gajon, A, Donazar, JA and Hiraldo, F (1999) Habitat, world geographic range, and embryonic development of hosts explain the prevalence of avian hematozoa at small spatial and phylogenetic scales. Proceedings of the National Academy of Sciences 96, 1785–1789.Google Scholar
Thomson, RL, Tomás, G, Forsman, JT, Broggi, J and Mönkkönen, M (2010) Predator proximity as a stressor in breeding flycatchers: mass loss, stress protein induction, and elevated provisioning. Ecology 91, 1832–1840.Google Scholar
Valkiūnas, G (2005) Avian Malaria Parasites and Other Haemosporidia. Boca Raton, FL, USA: CRC Press.Google Scholar
Valkiūnas, G, Z̆ic̆kus, T, Shapoval, AP and Iezhova, TA (2006) Effect of Haemoproteus belopolskyi (Haemosporida: Haemoproteidae) on body mass of the Blackcap Sylvia atricapilla. Journal of Parasitology 92, 1123–1125.Google Scholar
van Riper, C, van Riper, SG, Goff, ML and Laird, M (1986) The epizootiology and ecological significance of malaria in Hawaiian land birds. Ecological Monographs 56, 327–344.Google Scholar
Ventim, R, Morais, J, Pardal, S, Mendes, L, Ramos, JA and Pérez-Tris, J (2012) Host-parasite associations and host-specificity in haemoparasites of reed bed passerines. Parasitology 139, 310–316.Google Scholar
Verhulst, S and Nilsson, JÅ (2008) The timing of birds’ breeding seasons: a review of experiments that manipulated timing of breeding. Philosophical Transactions of the Royal Society B: Biological Sciences 363, 399–410.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, 745–754.Google Scholar
Waldenström, 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.Google Scholar
Wood, MJ, Cosgrove, CL, Wilkin, TA, Knowles, SCL, Day, KP and Sheldon, BC (2007) Within-population variation in prevalence and lineage distribution of avian malaria in blue tits, Cyanistes caeruleus. Molecular Ecology 16, 3263–3273.Google Scholar
Zehtindjiev, P, Ilieva, M, Westerdahl, H, Hansson, B, Valkiunas, G and Bensch, S (2008) Dynamics of parasitemia of malaria parasites in a naturally and experimentally infected migratory songbird, the great reed warbler Acrocephalus arundinaceus. Experimental Parasitology 119, 99–110.Google Scholar
Zehtindjiev, P, Ilieva, M, Krizanauskiene, A, Oparina, O, Oparin, M and Bensch, S (2009) Occurrence of haemosporidian parasites in the paddyfield warbler, Acrocephalus agricola (Passeriformes, Sylviidae). Acta Parasitologica 54, 295–300.Google Scholar
Zídková, L, Cepicka, I, Szabová, J and Svobodová, M (2012) Biodiversity of avian trypanosomes. Infection, Genetics and Evolution 12, 102–112. doi: 10.1016/j.meegid.2011.10.022.Google Scholar
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