Hostname: page-component-cd9895bd7-jkksz Total loading time: 0 Render date: 2024-12-27T09:34:04.007Z Has data issue: false hasContentIssue false
  • English
  • Français

Malaria infection status of European Robins seems to associate with timing of autumn migration but not with actual condition

Published online by Cambridge University Press:  14 January 2019

Nóra Ágh Open the ORCID record for Nóra Ágh [Opens in a new window] ,
Imre Sándor Piross ,
Gábor Majoros ,
Tibor Csörgő  and
Eszter Szöllősi
Nóra Ágh*
Affiliation:
MTA-PE Evolutionary Ecology Research Group, University of Pannonia, H-8200 Veszprém, Hungary Conservation Genetic Research Group, Institute of Biology, University of Veterinary Medicine Budapest, H-1078 Budapest, Hungary Department of Biomathematics and Informatics, University of Veterinary Medicine Budapest, H-1078 Budapest, Hungary
Imre Sándor Piross
Affiliation:
Department of Biomathematics and Informatics, University of Veterinary Medicine Budapest, H-1078 Budapest, Hungary
Gábor Majoros
Affiliation:
Department of Parasitology, University of Veterinary Medicine Budapest, H-1078 Budapest, Hungary
Tibor Csörgő
Affiliation:
Department of Anatomy Cell- and Developmental Biology, Eötvös Loránd University, H-1117, Budapest, Hungary
Eszter Szöllősi
Affiliation:
Behavioural Ecology Group, Department of Systematic Zoology and Ecology, Eötvös Loránd University, H-1117 Budapest, Hungary
*
Author for correspondence: Nóra Ágh, E-mail: [email protected]
Get access Rights & Permissions [Opens in a new window]

Abstract

Avian malaria parasites can negatively affect many aspects of the life of the passerines. Though these parasites may strongly affect the health and thus migration patterns of the birds also during autumn, previous studies on avian malaria focused mainly on the spring migration and the breeding periods of the birds. We investigated whether the prevalence of blood parasites varies in relation to biometrical traits, body condition and arrival time in the European Robin (Erithacus rubecula) during autumn migration. We found no sex or age related differences in avian malaria prevalence and no relationship between infection status and body size or actual condition of the birds was found either. However, the timing of autumn migration differed marginally between infected and non-infected juveniles, so that parasitized individuals arrived later at the Hungarian stopover site. This is either because avian malaria infections adversely affect the migration timing or migration speed of the birds, or because later arriving individuals come from more distant populations with possibly higher blood parasite prevalence. The possible delay that parasites cause in the arrival time of the birds during autumn migration could affect the whole migratory strategy and the breeding success of the birds in the next season.

Keywords

Arrival timeavian haematozoanbody massCentral EuropeErithacus rubeculahaemoproteusplasmodiumwing length
Type
Research Article
Information
Parasitology , Volume 146 , Issue 6 , May 2019 , pp. 814 - 820
Check for updates
Copyright
Copyright © Cambridge University Press 2019 

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Adamska, K and Filar, M (2005) Directional preferences of the Chiffchaff (Phylloscopus collybita) and the Robin (Erithacus rubecula) on autumn migration in the Beskid Niski Mountains (S Poland). Ring 27, 159–176.Google Scholar
Alerstam, T, Hedenström, A and Åkesson, S (2003) Long-distance migration: evolution and determinants. Oikos 103, 247–260.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
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.Google Scholar
Atkinson, CT and van Riper, I (1991) Pathogenicity and epizootiology of avian haematozoa: plasmodium, leucocytozoon, and haemoproteus. In Loye, JE and Zuk, M (eds), Bird–Parasite Interactions: Ecology, Evolution and Behaviour. Oxford, UK: Oxford University Press, pp. 19–48.Google Scholar
Atkinson, CT, Dusek, RJ, Woods, KL and Iko, WM (2000) Pathogenicity of avian malaria in experimentally-infected Hawaii Amakihi. Journal of Wildlife Diseases 36, 197–201.Google Scholar
Bairlein, F, Dierschke, V, Salewski, V, Geiter, O, Hüppop, K, Köppen, U and Fiedler, W (2014) Robin (Erihacus rubecula). In Bairlein, F, Dierschke, V, Salewski, V, Geiter, O, Hüppop, K, Köppen, U and Fiedler, W (eds), Atlas des Vogelzugs: Ringfunde deutscher Brut- und Gastvögel [Bird Migration Atlas: Ring recoveries of German breeding and visiting birds]. Frankfurt: AULA-Verlag, pp. 467–470 (in German with English summary).Google Scholar
Bensch, S and Åkesson, S (2003) Temporal and spatial variation of hematozoans in Scandinavian Willow Warblers. Journal of Parasitology 89, 388–391.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
Clark, NJ, Clegg, SM and Klaassen, M (2015) Migration strategy and pathogen risk: non-breeding distribution drives malaria prevalence in migratory waders. Oikos 125, 1358–1368.Google Scholar
Coppack, T and Pulido, F (2009) Proximate control and adaptive potential of protandrous migration in birds. Integrative and Comparative Biology 49, 493–506.Google Scholar
Cornet, S, Nicot, A, Rivero, A and Gandon, S (2014) Evolution of plastic transmission strategies in avian malaria. PLoS Pathogens 10, e1004308.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, 540–548.Google Scholar
Csörgő, T, Harnos, A, Rózsa, L, Karcza, ZS and Fehérvári, P (2016) Detailed description of the Ócsa Bird Ringing Station, Hungary. Ornis Hungarica 24, 91–108.Google Scholar
DeGroote, LW and Rodewald, PG (2010) Blood parasites in migrating wood-warblers (Parulidae): effects on refueling, energetic condition, and migration timing. Journal of Avian Biology 41, 147–153.Google Scholar
Demongin, L (2016) Identification Guide to Birds in the Hand. Cambridge: Cambridge University Press, pp. 245–246.Google Scholar
Deviche, P, Greiner, AC 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, 456–466.Google Scholar
Dubiec, A, Podmokła, E, Zagalska-Neubauer, M, Drobniak, SM, Arct, A, Gustafsson, L and Cichoń, M (2016) Differential prevalence and diversity of haemosporidian parasites in two sympatric closely related non-migratory passerines. Parasitology 143, 1320–1329.Google Scholar
Emmenegger, T, Bauer, S, Hahn, S, Müller, SB, Spina, F and Jenni, L (2018) Blood parasites prevalence of migrating passerines increases over the spring passage period. Journal of Zoology 306, 23–27.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
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, 2137–2142.Google Scholar
Garvin, MC and Remsen, JV Jr (1997) An alternative hypothesis for heavier parasite loads of brightly colored birds: exposure at the nest. The Auk 114, 179–191.Google Scholar
Garvin, MC, Szell, CC and Moore, FR (2006) Blood parasites of Nearctic–Neotropical migrant Passerine birds during spring Trans-Gulf migration: impact on host body condition. Journal of Parasitology 92, 990–996.Google Scholar
Gyimóthy, ZS, Gyurácz, J, Bank, L, Bánhidi, P, Farkas, R, Németh, Á and Csörgő, T (2011) Autumn migration of Robins (Erithacus rubecula) in Hungary. Biologia (Bratislava) 66, 548–555.Google Scholar
Gyurácz, J and Csörgő, T (2009) European robin. In Csörgő, T, Karcza, ZS, Halmos, G, Magyar, G, Gyurácz, J, Szép, T, Bankovics, A, Schmidt, A and Schmidt, E (eds), Hungarian Bird Migration Atlas. Budapest: Kossuth Kiadó, pp. 440–442 (in Hungarian with English summary)Google Scholar
Hahn, S, Bauer, S, Dimitrov, D, Emmenegger, T, Ivanova, K, Zehtindjiev, P and Buttemer, WA (2018) Low intensity blood parasite infections do not reduce the aerobic performance of migratory birds. Proceedings of the Royal Society B: Biological Sciences 285, 20172307.Google Scholar
Harnos, A, Fehérvári, P and Csörgő, T (2015) Hitchhikers’ guide to analysing bird ringing data. Ornis Hungarica 23, 163–188.Google Scholar
Harnos, A, Ágh, N, Fehérvári, P, Karcza, ZS, Ócsai, P and Csörgő, T (2018) Exploratory analyses ofmigration timing and morphometrics of the European Robin (Erithacus rubecula). Ornis Hungarica 26, 124–148.Google Scholar
Hasselquist, D (2007) Comparative immunoecology in birds: hypotheses and tests. Journal of Ornithology 148, 572–582.Google Scholar
Hatchwell, BJ, Wood, MJ, Anwar, M and Perrins, CM (2000) The prevalence and ecology of the haematozoan parasites of European Blackbirds, (Turdus merula). Canadian Journal of Zoology 78, 684–687.Google Scholar
Hegemann, A, Abril, PA, Sjöberg, S, Muheim, R, Alerstam, T, Nilsson, JÅ and Hasselquist, D (2018a) A mimicked bacterial infection prolongs stopover duration in songbirds – but more pronounced in short- than long-distance migrants. Journal of Animal Ecology 87, 1698–1708.Google Scholar
Hegemann, A, Abril, PA, Muheim, R, Sjöberg, S, Alerstam, T, Nilsson, JÅ and Hasselquist, D (2018b) Immune function and blood parasite infections impact stopover ecology in passerine birds. Oecologia 188, 1011–1024.Google Scholar
Heise, CD and Moore, FR (2003) Age-related differences in foraging efficiency, molt, and fat deposition of Gray Catbirds prior to autumn migration. The Condor 105, 496–504.Google Scholar
Hothorn, T, Bretz, F and Westfall, P (2008) Simultaneous inference in general parametric models. Biometrical Journal 50, 346–363.Google Scholar
Hromádko, M (2008) Robin (Erithacus rubecula). In Cepak, J, Klvăna, P, Škopek, J, Schröpfer, L, Jelínek, M, Hořák, D, Formánek, J and Zárybnický, J (eds), Atlas migrace ptáku° Cˇeské a Slovenské republiky [Czech and Slovak Bird Migration Atlas]. Praha: Aventinum, pp. 368–371 (in Slovakian with English summary).Google Scholar
Jarvi, SI, Atkinson, CT and Fleischer, RC (2001) Immunogenetics and resistance to avian malaria in Hawaiian honeycreepers (Drepanidinae). Studies in Avian Biology 22, 254–263.Google Scholar
Kaiser, A (1993) A new multi-category classification of subcutaneous fat deposits of songbird. Journal of Field Ornithology 64, 246–255.Google Scholar
Knowles, S, Wood, M, Alves, R, 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
Krams, IA, Suraka, V, Rantala, MJ, 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, 34–41.Google Scholar
Lapointe, DA, Atkinson, CT and Samuel, MD (2012) Ecology and conservation biology of avian malaria. Annals of the New York Academy of Sciences 1249, 211–226.Google Scholar
Marinov, MP, Zehtindijev, P, Dimitrov, D, Ilieva, M, Bobeva, A and Marchetti, C (2017) Haemosporidian infections and host behavioural variation: a case study on wild-caught nightingales (Luscinia megarhynchos). Ethology Ecology and Evolution 29, 126–137.Google Scholar
Marzal, A, Ricklefs, RE, Valkiūnas, G, Albayrak, T, Arriero, E, Bonneaud, C, Czirják, GA, Ewen, J, Hellgren, O, Hořáková, 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.Google Scholar
McCurdy, D, Shutler, D, Mulie, 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
Merilä, J, Björklund, M and Bennett, GF (1995) Geographic and individual variation in haematozoan infections in the greenfinch (Carduelis chloris). Canadian Journal of Zoology 73, 1798–1804.Google Scholar
Merino, S, Moreno, J, Vásquez, RA, Martínez, J, Sánchez- Monsálvez, I, Estades, CF, Ippi, S, Sabat, P, Rozzi, R and MCGehee, S (2008) Haematozoa in forest birds from southern Chile: latitudinal gradients in prevalence and parasite lineage richness. Austral Ecology 33, 329–340.Google Scholar
Møller, AP, de Lope, F and Saino, N (2004) Parasitism, immunity, and arrival date in a migratory bird, the Barn Swallow. Ecology 85, 206–219.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
Newton, I (2008) The Migration Ecology of Birds. London, Elsevier Press.Google Scholar
Nunn, CL, Altizer, SM, Sechrest, W and Cunningham, AA (2005) Latitudinal gradients of parasite species richness in primates. Diversity and Distributions 11, 249–256.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, 1577–1588.Google Scholar
Palinauskas, V, Valkiūnas, G, Bolshakov, CV and Bensch, S (2008) Plasmodium relictum (lineage P-SGS1): effects on experimentally infected passerine birds. Experimental Parasitology 120, 372–380.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, 613–617.Google Scholar
Pérez–Tris, J and Bensch, S (2005) Dispersal increases local transmission of avian malarial parasites. Ecology Letters 8, 838–845.Google Scholar
R Development Core Team, R (2017) A Language and Environment for Statistical Computing. Vienna, Austria: R Foundation for Statistical Computing.Google Scholar
Reiczigel, J and Rózsa, L (2005) Quantitative Parasitology 3.0. Budapest, Hungary: Distributed by the Authors.Google Scholar
Rintamäki, PT, Halonen, M, Kilpimaa, J and Lundberg, A (1997) Blood parasites found in three passerine species during spring migration. Ornis Fennica 74, 195–200.Google Scholar
Ripley, B, Hornik, K, Gebhardt, A and Firth, D (2012) Support functions and datasets for Venables and Ripley's MASS. Available at http://cran.r-project.org/web/packages/MASS/MASS.pdf.Google Scholar
Rivera, J, Barba, E, Mestre, A, Schaefer, HM and Segelbacher, G (2013) Effects of migratory status and habitat on the prevalence and intensity of infection by haemoparasites in passerines in eastern Spain. Animal Biodiversity and Conservation 36, 113–122.Google Scholar
Santiago-Alarcon, D, Bloch, R, Rolshausen, G, Schaefer, HM and Segelbacher, G (2011) Prevalence, diversity, and interaction patterns of avian haemosporidians in a four-year study of Blackcaps in a migratory divide. Parasitology 138, 824–835.Google Scholar
Santiago-Alarcon, D, MacGregor-Fors, I, Kühnert, K, Segelbacher, G and Schaefer, HM (2016) Avian haemosporidian parasites in an urban forest and their relationship to bird size and abundance. Urban Ecosystems 19, 331–346.Google Scholar
Schrader, MS, Walters, EL, James, FC and Greiner, EC (2003) Seasonal Prevalence of a Haematozoan parasite of Red-Bellied Woodpeckers (Melanerpes carolinus) and its association with host condition and overwinter survival. Auk 120, 130–137.Google Scholar
Ściborska, M and Busse, P (2004) Intra-seasonal changes in directional preferences of Robins (Erithacus rubecula) caught on autumn migration at Bukowo-Kopań ringing Station (N Poland) in 1996. Ring 26, 41–58.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
Sorensen, MC, Asghar, M, Bensch, S, Fairhurst, GD, Jenni-Eiermann, S and Spottiswoode, CN (2016) A rare study from the wintering grounds provides insight into the costs of malaria infection for migratory birds. Journal of Avian Biology 47, 575–582.Google Scholar
Sterne, TE (1954) Some remarks on confidence or fiducial limits. Biometrika 41, 275–278.Google Scholar
Suh, A, Kriegs, JO, Brosius, J and Schmitz, J (2011) Retroposon insertions and the chronology of avian sex chromosome evolution. Molecular Biology and Evolution 28, 2993–2997.Google Scholar
Svensson, L (1992) Identification Guide to European Passerines, 4th Edn. Stockholm: Published by the Author.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.Google 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.Google Scholar
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.Google Scholar
Valkama, J, Saurola, P, Lehikoinen, A, Piha, M, Sola, P and Velmala, W (2014) Robin (Erithacus rubecula). In Valkama, J, Saurola, P, Lehikoinen, A, Piha, M, Sola, P and Velmala, W (eds), Suomen Rengastusatlas. Osa II. [The Finnish Bird Ringing Atlas Vol. II]. Helsinki: Finnish Museum of Natural History and Ministry of Environment, pp. 396–403 (in Finnish with English summary).Google Scholar
Valkiūnas, G (2005) Avian Malaria Parasites and Other Haemosporidia. London, New York, Washington: CRC Press.Google Scholar
Valkiūnas, G, Zickus, T, Shapoval, AP and Lezhova, 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 Rooyen, J, Lalubin, F, Glaizot, O and Christe, P (2013) Altitudinal variation in haemosporidian parasite distribution in Great Tit populations. Parasites & Vectors 6, 139.Google Scholar
Venables, WN and Ripley, BD (2002) Generalized linear models. In Venables, WN and Ripley, BD (eds), Modern Applied Statistics with S. New York, NY: Springer Press, pp. 183–210.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
Waldenström, J, Bensch, S, Hasselquist, D and Ostman, O (2004) A new nested polymerase chain reaction method very efficient in detecting Plasmodium and Haemoproteus infections from avian blood. Journal of Parasitology 90, 191–194.Google Scholar
Wojczulanis-Jakubas, K, Jakubas, D, Czujkowska, A, Kulaszewicz, I and Kruszewicz, AG (2012) Blood parasite infestation and the leukocyte profiles in adult and immature Reed Warblers (Acrocephalus scirpaceus) and Sedge Warblers (Acrocephalus schoenobaenus) during autumn migration. Annales Zoologici Fennici 49, 341–349.Google Scholar
Wood, MJ, Cosgrove, CL, Wilkin, TA, Knowles, SC, 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
Yorinks, N and Atkinson, CT (2000) Effects of malaria on activity budgets of experimentally infected juvenile Apapane (Himatione sanguinea). The Auk 117, 731–738.Google Scholar