Abstract
The prevalence and intensity of avian haemosporian infections (genera Haemoproteus and Plasmodium) were investigated using molecular techniques and microscopy in nine passerine species at three Portuguese reed beds along a small latitudinal gradient. The effect of age, sex, season, site and year in the infection prevalence was evaluated for some of these host species. Of the sampled birds, 34.5% were infected, all with low level parasitemias. Haemoproteus spp. was only present in migrant species and was not locally transmitted, while Plasmodium spp. infected more species and reached a higher overall prevalence. Prevalence differed among bird species and was affected by different variables for each species: it was associated with age in the Reed Warbler Acrocephalus scirpaceus, with season in the Cetti’s Warbler Cettia cetti and with year in the House Sparrow Passer domesticus. Site did not influence prevalence for any species at this small geographical scale. Reed Warbler adults had already migrated to Africa and contacted with two different parasite faunas, whereas juveniles had not, thereby explaining the importance of age to explain parasitemia in this species. For the resident Cetti’s Warbler, prevalence varied significantly with season, perhaps due to lower food availability in autumn and winter, making birds weaker and more prone to infection.
Zusammenfassung
Charakterisierung von Haemosporida Infektionen in Grasmücken und Sperlingen in Röhrichtgebieten in SW-Europa
Wir untersuchten die Prävalenz und die Intensität des Vorkommens von Haemosporidien (Gattungen Haemoproteus und Plasmodium) in neun Singvogelarten in drei Portugiesischen Röhrichtgebieten entlang eines geringen Nord-Süd Gradienten. Wir evaluierten die Effekte von Alter, Geschlecht, Jahreszeit, Gebiet und Jahr auf die Prävalenz der Infektionen für einige der Arten. 34,5% der beprobten Vögel waren infiziert, alle mit geringer Parasitämie. Haemoproteus ssp. war nur in Zugvogelarten präsent und wurde nicht lokal übertragen, während Plasmodium ssp. mehrere Arten infizierte und insgesamt eine höhere Prävalenz erreichte. Die Prävalenz zwischen verschiedenen Arten war unterschiedlich hoch, und wurde durch für jede Art verschiedene Variablen beeinflusst: In Teichrohrsängern (Acrocephalus scirpaceus) war die Prävalenz mit dem Alter assoziiert, in Seidensängern (Cetti cetti) mit der Jahreszeit und in Haussperlingen (Passer domesticus) variierte die Prävalenz von Jahr zu Jahr. Auf dieser relativ kleinräumigen Skala hatte das Gebiet keinen Einfluss auf die Prävalenz, in keiner der Arten. Der Effekt des Alters auf die Prävalenz in Teichrohrsängern kann damit erklärt werden, dass adulte Teichrohrsänger bereits in Afrika waren und dort Kontakt mit einer anderen Parasiten Fauna hatten, während Jungtiere noch nicht dieser diversen Umgebung ausgesetzt waren. Für residente Seidensänger dagegen kann eine geringere Verfügbarkeit von Nahrungsmitteln im Herbst und Winter der Grund sein warum hier die Prävalenz saisonal variiert, welche die Vögel schwacher und damit empfänglicher für Infektionen macht.
Similar content being viewed by others
References
Atkinson CT, van Riper C III (1991) Pathogenicity and epizootiology of avian hematozoa: Plasmodium, Leucocytozoon and Haemoproteus. In: Loye J, Zuk M (eds) Bird-parasite interactions: ecology, evolution, and behavior. Oxford University Press, New York, pp 19–48
Bennett GF, Caines JR, Bishop MA (1988) Influence of blood parasites on the body mass of passeriform birds. J Wildl Dis 24(2):339–343
Bennett GF, Squiresparsons D, Siikamaki P, Huhta E, Allander K, Hillstrom L (1995) A comparison of the blood parasites of three Fenno-Scandian populations of the pied flycatcher Ficedula hypoleuca. J Avian Biol 26(1):33–38
Bensch S, Akesson A (2003) Temporal and spatial variation of hematozoans in Scandinavian willow warblers. J Parasitol 89(2):388–391
Bensch S, Stjernman M, Hasselquist D, Ostman O, Hansson B, Westerdahl H, Pinheiro RT (2000) Host specificity in avian blood parasites: a study of Plasmodium and Haemoproteus mitochondrial DNA amplified from birds. Proc R Soc Lond B 267:1583–1589
Bensch S, Waldenstrom J, Jonzen N, Westerdahl H, Hansson B, Sejberg D, Hasselquist D (2007) Temporal dynamics and diversity of avian malaria parasites in a single host species. J Anim Ecol 76(1):112–122. doi:10.1111/j.1365-2656.2006.01176.x
Bensch S, Hellgren O, Pérez-Tris J (2009) MalAvi: a public database of malaria parasites and related haemosporidians in avian hosts based on mitochondrial cytochrome b lineages. Mol Ecol Resour 9(5):1353–1358. doi:10.1111/j.1755-0998.2009.02692.x
Bonneaud C, Pérez-Tris J, Federici P, Chastel O, Sorci G (2006) Major histocompatibility alleles associated with local resistance to malaria in a passerine. Evolution 60(2):383–389
Clayton HD, Moore J (eds) (1997) Host-parasite evolution: general principles and avian models, 1st edn. Oxford University Press, Oxford
Dimitrov D, Zehtindjiev P, 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 Parasitol 55(3):201–209. doi:10.2478/s11686-010-0029-z
Edler R, Klump GM, Friedl TWP (2004) Do blood parasites affect reproductive performance in male red bishops (Euplectes orix)? A test of the Hamilton-Zuk hypothesis. Ethol Ecol Evol 16(4):315–328
Fernandez M, Rojo MA, Casanueva P, Carrion S, Hernandez MA, Campos F (2010) High prevalence of haemosporidians in reed warbler Acrocephalus scirpaceus and sedge warbler Acrocephalus schoenobaenus in Spain. J Ornithol 151(1):27–32. doi:10.1007/s10336-009-0417-z
Freeman-Gallant CR, O’Connor KD, Breuer ME (2001) Sexual selection and the geography of Plasmodium infection in savannah sparrows (Passerculus sandwichensis). Oecologia 127(4):517–521
Garvin MC, Homer BL, Greiner EC (2003) Pathogenicity of Haemoproteus danilewskyi, Kruse, 1890, in blue jays (Cyanocitta cristata). J Wildl Dis 39(1):161–169
Hall TA (1999) BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucleic Acids Symp Ser 41:95–98
Hellgren O, Krizanauskiene A, Valkiunas G, Bensch S (2007a) Diversity and phylogeny of mitochondrial cytochrome B lineages from six morphospecies of avian Haemoproteus (Haemosporida: Haemoproteidae). J Parasitol 93:889–896
Hellgren O, Waldenstrom J, Pérez-Tris J, Szollosi E, Hasselquist D, Krizanauskiene A, Ottosson U, Bensch S (2007b) Detecting shifts of transmission areas in avian blood parasites—a phylogenetic approach. Mol Ecol 16(6):1281–1290. doi:10.1111/j.1365-294X.2007.03277.x
Loiseau C, Iezhova T, Valkiunas G, Chasar A, Hutchinson A, Buermann W, Smith TB, Sehgal RNM (2010) Spatial variation of haemosporidian parasite infection in African rainforest bird species. J Parasitol 96(1):21–29. doi:10.1645/ge-2123.1
Mendes L, Piersma T, Lecoq M, Spaans B, Ricklefs RE (2005) Disease-limited distributions? Contrasts in the prevalence of avian malaria in shorebird species using marine and freshwater habitats. Oikos 109(2):396–404
Merila J, Bjorklund M, Bennett GF (1995) Geographic and individual variation in haematozoan infections in the greenfinch, Carduelis chloris. Can J Zool 73(10):1798–1804
Merino S, Potti J, Fargallo JA (1997) Blood parasites of some passerine birds from central Spain. J Wildl Dis 33:638–641
Merino S, Moreno J, Sanz JJ, Arriero E (2000) Are avian blood parasites pathogenic in the wild? A medication experiment in blue tits (Parus caeruleus). Proc R Soc Lond B 267:2507–2510
Palinauskas V, Kosarev V, Shapoval A, Bensch S, Valkiunas G (2007) Comparison of mitochondrial cytochrome b lineages and morphospecies of two avian malaria parasites of the subgenera Haemamoeba and Giovannolaia (Haemosporida: Plasmodiidae). Zootaxa 1626:39–50
Palinauskas V, Valkiunas GN, Bolshakov CV, Bensch S (2008) Plasmodium relictum (lineage P-SGS1): effects on experimentally infected passerine birds. Exp Parasitol 120(4):372–380. doi:10.1016/j.exppara.2008.09.001
Pérez-Tris J, Bensch S (2005a) Diagnosing genetically diverse avian malarial infections using mixed-sequence analysis and TA-cloning. Parasitology 131:15–23. doi:10.1017/s003118200500733x
Pérez-Tris J, Bensch S (2005b) Dispersal increases local transmission of avian malarial parasites. Ecol Lett 8(8):838–845. doi:10.1111/j.1461-0248.2005.00788.x
Pérez-Tris J, Hellgren O, Krizanauskiene A, Waldenstrom J, Secondi J, Bonneaud C, Fjeldsa J, Hasselquist D, Bensch S (2007) Within-host speciation of malaria parasites. PloS One 2(2). doi:10.1371/journal.pone.0000235
Schultz A, Underhill LG, Earle RA, Underhill G (2010) Infection prevalence and absence of positive correlation between avian haemosporidian parasites, mass and body condition in the cape weaver Ploceus capensis. Ostrich 81(1):69–76. doi:10.2989/00306521003690630
Shurulinkov P, Ilieva M (2009) Spatial and temporal differences in the blood parasite fauna of passerine birds during the spring migration in Bulgaria. Parasitol Res 104(6):1453–1458. doi:10.1007/s00436-009-1349-5
Sol D, Jovani R, Torres J (2003) Parasite mediated mortality and host immune response explain age-related differences in blood parasitism in birds. Oecologia 135(4):542–547. doi:10.1007/s00442-003-1223-6
Statsoft (2002) STATISTICA user manual. Statsoft, Tulsa
Svensson L (1992) Identification guide to European passerines, 4th edn. Privately published, Stockholm
Valkiunas G (2005) Avian malaria parasites and other haemosporidia, 1st edn. CRC, Boca Raton
Valkiunas G, Bensch S, Iezhova TA, Krizanauskiene A, Hellgren O, Bolshakov CV (2006a) Nested cytochrome B polymerase chain reaction diagnostics underestimate mixed infections of avian blood haemosporidian parasites: microscopy is still essential. J Parasitol 92(2):418–422
Valkiunas G, Zickus T, Shapoval AP, Iezhova TA (2006b) Effect of Haemoproteus belopolskyi (Haemosporida: Haemoproteidae) on body mass of the blackcap Sylvia atricapilla. J Parasitol 92(5):1123–1125
Valkiunas G, Iezhova TA, Krizanauskiene A, Palinauskas V, Sehgal RNM, Bensch S (2008) A comparative analysis of microscopy and PCR-based detection methods for blood parasites. J Parasitol 94(6):1395–1401
Waldenström J, Bensch S, Kiboi S, Hasselquist D, Ottosson U (2002) Cross-species infection of blood parasites between resident and migratory songbirds in Africa. Mol Ecol 11(8):1545–1554
Waldenström J, Bensch S, Hasselquist D, Ostman O (2004) A new nested polymerase chain reaction method very efficient in detecting Plasmodium and Haemoproteus infections from avian blood. J Parasitol 90(1):191–194
Zehtindjiev P, Ilieva M, Westerdahl H, Hansson B, Valkiunas G, Bensch S (2008) Dynamics of parasitemia of malaria parasites in a naturally and experimentally infected migratory songbird, the great reed warbler Acrocephalus arundinaceus. Exp Parasitol 119(1):99–110. doi:10.1016/j.exppara.2007.12.018
Acknowledgments
This project was supported by the Fundação para a Ciência e Tecnologia (R.V., grant number SFRH/BD/28930/2006) and the Spanish Ministry of Science and Innovation (J.P.-T., project number CGL2007-62937/BOS). The Portuguese Instituto para a Conservação da Natureza e Biodiversidade provided official permits for bird capturing and sampling, as well as logistic support for field work. The authors thank Sara Pardal for field assistance and Joana Morais for lab work.
Author information
Authors and Affiliations
Corresponding author
Additional information
Communicated by F. Bairlein.
Electronic supplementary material
Below is the link to the electronic supplementary material.
Rights and permissions
About this article
Cite this article
Ventim, R., Tenreiro, P., Grade, N. et al. Characterization of haemosporidian infections in warblers and sparrows at south-western European reed beds. J Ornithol 153, 505–512 (2012). https://doi.org/10.1007/s10336-011-0767-1
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10336-011-0767-1