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Extremely low malaria prevalence in a wetland specialist passerine

Published online by Cambridge University Press:  12 September 2019

Eszter Szöllősi Open the ORCID record for Eszter Szöllősi [Opens in a new window] ,
Zsófia Tóth ,
Katharina Mahr ,
Herbert Hoi  and
Ádám Z. Lendvai
Eszter Szöllősi*
Affiliation:
Department of Systematic Zoology and Ecology, Behavioural Ecology Group, Eötvös Loránd University, Pázmány Péter sétány 1/c, 1117Budapest, Hungary
Zsófia Tóth
Affiliation:
Department of Evolutionary Zoology and Human Biology, University of Debrecen, Egyetem tér 1, 4032Debrecen, Hungary
Katharina Mahr
Affiliation:
Department of Evolutionary Zoology and Human Biology, University of Debrecen, Egyetem tér 1, 4032Debrecen, Hungary Department of Integrative Biology and Evolution, Konrad Lorenz Institute of Ethology (KLIVV), University of Veterinary Medicine, Vienna, Savoyenstraße 1a, A-1160Vienna, Austria
Herbert Hoi
Affiliation:
Department of Integrative Biology and Evolution, Konrad Lorenz Institute of Ethology (KLIVV), University of Veterinary Medicine, Vienna, Savoyenstraße 1a, A-1160Vienna, Austria
Ádám Z. Lendvai
Affiliation:
Department of Evolutionary Zoology and Human Biology, University of Debrecen, Egyetem tér 1, 4032Debrecen, Hungary Department of Geology, Babeş-Bolyai University, Str. Mihail Kogalniceanu nr. 1, 400084Cluj-Napoca, Romania
*
Author for correspondence: Eszter Szöllősi, E-mail: [email protected]
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Abstract

Avian malaria (caused by Plasmodium spp.) and avian malaria-like infections (caused by Haemoproteus spp.) are widespread and can seriously affect the health of their bird hosts, especially of immunologically naïve individuals. Therefore, these parasites have long been in the focus of bird-parasite studies. However, the species richness and diversity of these protozoan species have only been revealed since the use of molecular techniques. Diversity and prevalence of these parasites among different bird species and even between populations of a species show a large variation. Here, we investigated prevalence of avian malaria and avian malaria-like parasites in two distant populations of a non-migratory wetland specialist passerine, the bearded reedling (Panurus biarmicus). While previous studies have shown that reed-dwelling bird species often carry various blood parasite lineages and the presence of the vectors transmitting Plasmodium and Haemoproteus species has been confirmed from our study sites, prevalence of these parasites was extremely low in our populations. This may either suggest that bearded reedlings may avoid or quickly clear these infections, or these parasites cause high mortality in this species. The remarkably low prevalence of infection in this species is consistent with earlier studies and makes bearded reedlings a possible model organism for investigating the genetic or behavioural adaptations of parasite resistance.

Keywords

Bearded tithaemosporidiaimmune statusmosquitoreed bedtolerance
Type
Research Article
Information
Parasitology , Volume 147 , Issue 1 , January 2020 , pp. 87 - 95
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Copyright
Copyright © Cambridge University Press 2019

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References

Antonides, J, Mathur, S, Sundaram, M, Ricklefs, R and DeWoody, JA (2019) Immunogenetic response of the bananaquit in the face of malarial parasites. BMC Evolutionary Biology 19, 107.CrossRefGoogle ScholarPubMed
Asghar, M, Hasselquist, D, Hansson, B, Zehtindjiev, P, Westerdahl, H and Bensch, S (2015) Hidden costs of infection: chronic malaria accelerates telomere degradation and senescence in wild birds. Science 347, 436–438.10.1126/science.1261121CrossRefGoogle ScholarPubMed
Atkinson, CT and van Riper, CIII (1991) Pathogenicity and epizootiology of avian haematozoa: Plasmodium, Leucocytozoon, and Haemoproteus. In Loye, JE and Zuk, M (eds), Bird-Parasite Interactions. Oxford: Oxford University Press, pp. 19–48.Google Scholar
Bensch, S, Pérez-Tris, J, Waldentsröm, J and Hellgren, O (2004) Linkage between nuclear and mitochondrial DNA sequences in avian malaria parasites: multiple cases for cryptic speciation? Evolution 58, 1617–1621.CrossRefGoogle ScholarPubMed
Bensch, S, Jönsson, J and Copete, JL (2012) Low prevalence of Haemoproteus infections in Chiffchaffs. Parasitology 139, 302–309.CrossRefGoogle ScholarPubMed
Bensch, S, Waldentsröm, 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.CrossRefGoogle Scholar
Burkett-Cadena, ND, McClure, CJW, Estep, LK and Eubanks, MD (2013) Hosts or habitats: what drives the spatial distribution of mosquitoes? Ecosphere (Washington, D.C) 4, 30.Google Scholar
Campioni, L, Martínez-de la Puente, J, Figuerola, J, Granadeiro, JP, Silva, MC and Catry, P (2018) Absence of haemosporidian parasite infections in the long-lived Cory's shearwater: evidence from molecular analyses and review of the literature. Parasitology Research 117, 323–329.CrossRefGoogle ScholarPubMed
Cox, FEG (1993) Modern Parasitology: A Textbook of Parasitology, 2nd edn.Blackwell Science Ltd. ISBN: 9780632025855. Online ISBN:9781444313963. DOI:10.1002/9781444313963.CrossRefGoogle Scholar
Cramp, S and Perrins, CM (eds) (1993) The Birds of the Western Palearctic, vol. 7. Oxford: Oxford University Press.Google Scholar
Dimitrov, D, Ilieva, M, Ivanova, K, Brlík, V and Zehtindjiev, P (2018) Detecting local transmission of avian malaria and related haemosporidian parasites (Apicomplexa, Haemospoida) at a Special Protection Area of Natura 2000 network. Parasitology Research 117, 2187–2199.CrossRefGoogle Scholar
Eastwood, JR, Peacock, L, Hall, ML, Roast, M, Murphy, SA, Gonçalves da Silva, A and Peters, A (2019) Persistent low avian malaria in a tropical species despite high community prevalence. International Journal for Parasitology: Parasites and Wildlife 8, 88–93.Google Scholar
Golding, N, Nunn, MA and Purse, BV (2015) Identifying biotic interactions which drive the spatial distribution of a mosquito community. Parasites & Vectors 8, 367.CrossRefGoogle ScholarPubMed
Griffiths, R, Double, MC, Orr, K and Dawson, RJG (1998) A DNA test to sex most birds. Molecular Ecology 7, 1071–1075.CrossRefGoogle ScholarPubMed
Hall, TA (1999) Bioedit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucleic Acids Symposium Series 41, 95–98.Google Scholar
Hegemann, A, Abril, PA, Muheim, R, Sjoberg, S, Alerstam, T, Nilsson, JÅ and Hasselquist, D (2018) Immune function and blood parasite infections impact stopover ecology in passerine birds. Oecologia 188, 1011–1024.CrossRefGoogle ScholarPubMed
Hellgren, O, Waldenström, J, Pérez-Tris, J, Szöllősi, E, Hasselquist, D, Krizanauskiene, A, Ottoson, U and Bensch, S (2007) Detecting shifts of transmission areas in avian blood parasites – a phylogenetic approach. Molecular Ecology 16, 1281–1290.CrossRefGoogle ScholarPubMed
Hellgren, O, Pérez-Tris, J and Bensch, S (2009) A Jack of all trades and still a master of some: prevalence and host range in avian malaria and related blood parasites. Ecology 90, 2840–2849.CrossRefGoogle Scholar
Jones, W, Kulma, K, Bensch, S, Cichoń, M, Kerimov, A, Krist, K, Laaksonen, T, Moreno, J, Munclinger, P, Slater, FM, Szöllősi, E, Visser, ME and Qvarnström, A (2018) Interspecific transfer of parasites following a range-shift in Ficedula flycatchers. Ecology and Evolution 8, 12183–12192.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, 557–569.CrossRefGoogle ScholarPubMed
Lemke, HW, Tarka, M, Klaassen, RHG, Åkesson, M, Bensch, S, Hasselquist, D and Hansson, B (2013) Annual cycle and migration strategies of a trans-Saharan migratory songbird: a geolocator study in the great reed warbler. PLoS ONE 8, e79209.CrossRefGoogle ScholarPubMed
Lima, MR, Simpson, L, Fecchio, A and Kyaw, CM (2010) Low prevalence of haemosporidian parasites in the introduced house sparrow (Passer domesticus) in Brazil. Acta Parasitologica 55, 297–303.CrossRefGoogle Scholar
Martínez-de la Puente, J, Munoz, J, Capelli, G, Montarsi, F, Soriguer, R, Arnoldi, D, Rizzoli, A and Figuerola, J (2015) Avian malaria parasites in the last supper: identifying encounters between parasites and the invasive Asian mosquito tiger and native mosquito species in Italy. Malaria Journal 14, 32.CrossRefGoogle ScholarPubMed
Marzal, A, Ricklefs, RE, Valkiūnas, G, Albayrak, T, Arriero, E, Bonneaud, C, Czirják, GA, Ewen, J, Hellgren, O, Horakova, D, Iezhova, TA, Jensen, H, Križanauskienė, A, Lima, MR, de Lope, F, Magnussen, E, Martin, LB, Møller, AP, Palinauskas, V, Pap, PL, Pérez-Tris, J, Sehgal, RNM, Soler, M, Szöllősi, E, Westerdahl, H, Zetindjiev, P and Bensch, S (2011) Diversity, loss, and gain of malaria parasites in a globally invasive bird. PLoS ONE 6, e21905.10.1371/journal.pone.0021905CrossRefGoogle Scholar
Marzal, A, Møller, AP, Espinoza, K, Morales, S, Lujan-Vega, C, Cardenas-Callirgos, JM, Mendo, L, Alvarez-Barrientos, A, Gonzalez-Blazques, M, Garcia-Longoria, L, de Lope, F, Mendoza, C, Iannacone, J and Magallanes, S (2018) Variation in malaria infection and immune defence in invasive and endemic house sparrows. Animal Conservation 21, 505–514.CrossRefGoogle 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 London B 22, 2507–2510.CrossRefGoogle Scholar
Nacher, M (2004) Interactions between worm infections and malaria. Clinical Reviews in Allergy and Immunology 26, 85–92.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle ScholarPubMed
Nicholls, JA, Double, MC, Rowell, DM and Magrath, RD (2000) The evolution of cooperative and pair breeding in thornbills Acanthiza (pardalotidae). Journal of Avian Biology 31, 165–176.CrossRefGoogle Scholar
Nilsson, E, Taubert, HE, 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, 1812–1826.CrossRefGoogle ScholarPubMed
Pulgarín-R, PC, Gómez, JP, Robinson, S, Ricklefs, RE and Cadena, CD (2018) Host species, and not environment, predicts variation in blood parasite prevalence, distribution, and diversity along a humidity gradient in Northern South America. Ecology and Evolution 8, 3800–3814.CrossRefGoogle Scholar
Richie, TL (1988) Interactions between malaria parasites infecting the same vertebrate host. Parasitology 96, 607–639.CrossRefGoogle ScholarPubMed
Rojo, MÁ, Campos, F, Santamaría, T and Hernández, MÁ (2014) Haemosporidians in Iberian Bluethroats Luscinia svecica. Ardeola 61, 135–143.CrossRefGoogle Scholar
Scheuerlein, A and Ricklefs, R (2004) Prevalence of blood parasites in European passeriform birds. Proceedings of the Royal Society London B 271, 1363–1370.CrossRefGoogle ScholarPubMed
Soltész, Z (2017) Odúlakó madarak kétszárnyú együtteseinek vizsgálata (PhD thesis). Eötvös Loránd University.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, 371–380.CrossRefGoogle Scholar
Szöllősi, E, Cichoń, M, Eens, M, Hasselquist, D, Kempenaers, B, Merino, S, Nilsson, JÅ, Rosivall, B, Rytkönen, S, Török, J, Wood, MJ and Garamszegi, 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, 2014–2024.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, 4663–4672.CrossRefGoogle ScholarPubMed
Townsend, AK, Wheeler, SS, Freund, D, Sehgal, RNM and Boyce, WM (2018) Links between blood parasites, blood chemistry, and the survival of nestling American crows. Ecology and Evolution 8, 8779–8790.CrossRefGoogle ScholarPubMed
Valkiūnas, G (2005) Avian Malaria Parasites and Other Haemosporidia. Boca Raton, Florida: CRC Press.Google Scholar
van Riper, CIII, 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.CrossRefGoogle Scholar
Ventim, R, Tenreiro, R, Grade, N, Encarnacao, P, Araújo, M, Mendes, L, Pérez-Tris, J and Ramos, JA (2012 a) Characterization of Haemosporidian infections in warblers and sparrows at south-western European reed beds. Journal of Ornithology 153, 505–512.CrossRefGoogle Scholar
Ventim, R, Morais, J, Pardal, S, Mendes, L, Ramos, JA and Pérez-Tris, J (2012 b) Host-parasite associations and host-specificity in haemoparasites of reed bed passerines. Parasitology 139, 310–316.CrossRefGoogle ScholarPubMed
Ventim, R, Mendes, L, Ramos, JA, Cardoso, H and Pérez-Tris, J (2012c) Local haemoparasites in introduced wetland passerines. Journal of Ornithology 153, 1253–1259.CrossRefGoogle 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.CrossRefGoogle ScholarPubMed
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, 194–196.CrossRefGoogle ScholarPubMed
Westerdahl, H (2007) Passerine MHC: genetic variation and disease resistance in the wild. Journal of Ornithology 148, S469–S477.CrossRefGoogle Scholar
Wilson, J and Peach, W (2006) Impact of an exceptional winter flood on the population dynamics of bearded tits (Panurus biarmicus). Animal Conservation 9, 463–473.CrossRefGoogle Scholar
Zehtindjiev, P, Ilieva, M, Westerdahl, H, Hansson, B, Valkiūnas, 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.CrossRefGoogle Scholar