Stable isotope analysis provides valuable insights into the ecology of long-distance migratory birds during periods spent away from a specific study site. In a previous study, Swedish great reed warblers (Acrocephalus arundinaceus) infected with haemosporidian parasites differed in feather isotope ratios compared to non-infected birds, suggesting that infected and non-infected birds spent the non-breeding season in different locations or habitats. Here, we use a novel dataset comprising geolocator data, isotopes, and haemosporidian infection status of 92 individuals from four Eurasian populations to investigate whether parasite transmission varies with geography or habitats. We found that the probability of harbouring Plasmodium and Leucocytozoon parasites was higher in birds moulting in the eastern region of the non-breeding grounds. However, no geographic pattern occurred for Haemoproteus infections or overall infection status. In contrast to the previous study, we did not find any relationship between feather isotope ratios and overall haemosporidian infection for the entire current dataset. Plasmodium-infected birds had lower feather δ15N values indicating that they occupied more mesic habitats. Leucocytozoon-infected birds had higher feather δ34S values suggesting more coastal sites or wetlands with anoxic sulphate reduction. As the composition and prevalence of haemosporidian parasites differed between the old and the current dataset, we suggest that the differences might be a consequence of temporal dynamics of haemosporidian parasites. Our results emphasize the importance of replicating studies conducted on a single population over a restricted time period, as the patterns can become more complex for data from wider geographical areas and different time periods.

Department Bird Migration Swiss Ornithological Institute Seerose 1 6204 Sempach Switzerland

Department of Parasitology Faculty of Veterinary Medicine Erciyes University 38280 Kayseri Turkey

Institute of Biodiversity and Ecosystem Research Bulgarian Academy of Sciences 2 Gagarin Street 1113 Sofia Bulgaria

Institute of Vertebrate Biology Czech Academy of Sciences Květná 8 603 65 Brno Czech Republic

Molecular Ecology and Evolution Lab Department of Biology Lund University Sölvegatan 37 223 62 Lund Sweden

Vectors and Vector Borne Diseases Implementation and Research Center Erciyes University 38280 Kayseri Turkey

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Ambrose SH. Effects of diet, climate and physiology on nitrogen isotope abundance in terrestrial food webs. J Arch Sci. 1991;18:293–317. doi: 10.1016/0305-4403(91)90067-Y. DOI

Asghar M, Hasselquist D, Bensch S. Are chronic avian haemosporidian infections costly in wild birds? J Avian Biol. 2011;42:530–537. doi: 10.1111/j.1600-048X.2011.05281.x. DOI

Asghar M, Westerdahl H, Zehtindjiev P, Ilieva M, Hasselquist D, Bensch S. Primary peak and chronic malaria infection levels are correlated in experimentally infected great reed warblers. Parasitology. 2012;139:1246–1252. doi: 10.1017/S0031182012000510. PubMed DOI

Asghar M, Hasselquist D, Hansson B, Zehtindjiev P, Westerdahl H, Bensch S. Hidden costs of infection: chronic malaria accelerates telomere degradation and senescence in wild birds. Science. 2015;347:436–438. doi: 10.1126/science.1261121. PubMed DOI

Bearhop S, Fiedler W, Furness RW, Votier SC, Waldron S, Newton J, Bowen GJ, Berthold P, Farnsworth K. Assortative mating as a mechanism for rapid evolution of a migratory divide. Science. 2005;310:502–504. doi: 10.1126/science.1115661. PubMed DOI

Bensch S, Hasselquist D, Hedenström A, Ottosson U. Rapid moult among Palearctic passerines in West Africa—an adaptation to the oncoming dry season. Ibis. 1991;133:47–52. doi: 10.1111/j.1474-919X.1991.tb04809.x. DOI

Bensch S, Waldenström J, Jonzén N, Westerdahl H, Hansson B, Sejberg D, Hasselquist D. Temporal dynamics and diversity of avian malaria parasites in a single host species. J Anim Ecol. 2007;76:112–122. doi: 10.1111/j.1365-2656.2006.01176.x. PubMed DOI

Bensch S, Hellgren O, Pérez-Tris J. MalAvi: a public database of malaria parasites and related haemosporidians in avian hosts based on mitochondrial cytochrome b lineages. Mol Ecol Res. 2009;9:1353–1358. doi: 10.1111/j.1755-0998.2009.02692.x. PubMed DOI

Berntell E, Zhang Q, Chafik L, Körnich H. Representation of multidecadal Sahel rainfall variability in 20th century reanalyses. Sci Rep. 2018;8:10937. doi: 10.1038/s41598-018-29217-9. PubMed DOI PMC

Brlík V, Malmiga G, Dimitrov D, Emmenegger T, Gavrilov A, Hasselquist D, Peev S, Willemoes M, Yohannes E, Hahn S, Hansson B, Procházka P. Population-specific assessment of carry-over effects across the range of a migratory songbird. Behav Ecol Sociobiol. 2020;74:143. doi: 10.1007/s00265-020-02929-7. DOI

Brlík V, Procházka P, Hansson B, Stricker CA, Yohannes E, Powell RL, Wunder MB. Animal tracing with sulfur isotopes: Spatial segregation and climate variability in Africa likely contribute to population trends of a migratory songbird. J Anim Ecol. 2022 doi: 10.1111/1365-2656.13848. PubMed DOI

Bürkner P-C. Bayesian item response modeling in R with brms and Stan. J Stat Softw. 2021;100(5):1–54. doi: 10.18637/jss.v100.i05. DOI

Chamberlain CP, Blum JD, Holmes RT, Feng X, Sherry TW, Graves GR. The use of isotope tracers for identifying populations of migratory birds. Oecologia. 1996;109:132–141. doi: 10.1007/s004420050067. PubMed DOI

Chamberlain CP, Bensch S, Feng X, Åkesson S, Andersson T. Stable isotopes examined across a migratory divide in Scandinavian willow warblers (Phylloscopus trochilus trochilus and Phylloscopus trochilus acredula) reflect their African winter quarters. Proc R Soc B. 2000;267:43–48. doi: 10.1098/rspb.2000.0964. PubMed DOI PMC

Cherel Y, Quillfeldt P, Delord K, Weimerskirch H. Combination of at-sea activity, geolocation and feather stable isotopes documents where and when seabirds molt. Front Ecol Evol. 2016;4:3. doi: 10.3389/fevo.2016.00003. DOI

Ciloglu A, Ellis VA, Bernotienė R, Valkiūnas G, Bensch S. A new one-step multiplex PCR assay for simultaneous detection and identification of avian haemosporidian parasites. Parasitol Res. 2019;118:191–201. doi: 10.1007/s00436-018-6153-7. PubMed DOI

De Roo A, Deheegher J. Ecology of the great reed warbler Acrocephalus arundinaceus (L.) wintering in the southern Congo savanna. Gerfaut. 1969;59:260–275.

Dyrcz A (2020) Great reed warbler (Acrocephalus arundinaceus), version 1.0. In: del Hoyo J, Elliott A, Sargatal J, Christie DA, de Juana E (eds): Birds of the world. Cornell Lab of Ornithology, Ithaca, NY, USA. 10.2173/bow.grrwar1.01

Ekolu J, Dieppois B, Sidibe M, Eden JM, Tramblay Y, Villarini G, Peña-Anguloc D, Mahé G, Paturel J-E, Onyutha C, Van De Wiel M. Long-term variability in hydrological droughts and floods in sub-Saharan Africa: new perspectives from a 65-year daily streamflow dataset. J Hydrol. 2022;613:128359. doi: 10.1016/j.jhydrol.2022.128359. DOI

Emmenegger T, Hahn S, Bauer S. Individual migration timing of common nightingales is tuned with vegetation and prey phenology at breeding sites. BMC Ecol. 2014;14:9. doi: 10.1186/1472-6785-14-9. PubMed DOI PMC

Emmenegger T, Bensch S, Hahn S, Kishkinev D, Procházka P, Zehtindjiev P, Bauer S. Effects of blood parasite infections on spatiotemporal migration patterns and activity budgets in a long-distance migratory passerine. Ecol Evol. 2021;11:753–762. doi: 10.1002/ece3.7030. PubMed DOI PMC

Fecchio A, Clark NJ, Bell JA, Skeen HR, Lutz HL, De La Torre GM, Vaughan JA, Tkach VV, Schunck F, Ferreira FC, Braga EM, Lugarini C, Wamiti W, Dispoto JH, Galen SC, Kirchgatter K, Sagario MC, Cueto VR, Gonzalez-Acuna D, Inumaru M, Sato Y, Schumm YR, Quillfeldt P, Pellegrino I, Dharmarajan G, Gupta P, Robin VV, Ciloglu A, Yildirim A, Huang X, Chapa-Vargas L, Alvarez-Mendizabal P, Santiago-Alarcon D, Drovetski SV, Hellgren O, Voelker G, Ricklefs RE, Hackett SJ, Collins MD, Weckstein JD, Wells K. Global drivers of avian haemosporidian infections vary across zoogeographical regions. Glob Ecol Biogeogr. 2021;30:2393–2406. doi: 10.1111/geb.13390. DOI

Finch T, Butler SJ, Franco AM, Cresswell W. Low migratory connectivity is common in long-distance migrant birds. J Anim Ecol. 2017;86:662–673. doi: 10.1111/1365-2656.12635. PubMed DOI

Galen SC, Borner J, Martinsen ES, Schaer J, Austin CC, West CJ, Perkins SL. The polyphyly of Plasmodium: comprehensive phylogenetic analyses of the malaria parasites (order Haemosporida) reveal widespread taxonomic conflict. R Soc Open Sci. 2018;5:171780. doi: 10.1098/rsos.171780. PubMed DOI PMC

García-Pérez B, Hobson KA. A multi-isotope (δ2H, δ13C, δ15N) approach to establishing migratory connectivity of Barn Swallow (Hirundo rustica) Ecosphere. 2014;5:21. doi: 10.1890/ES13-00116.1. DOI

Glew KSJ, Wanless S, Harris MP, Daunt F, Erikstad KE, Strøm H, Trueman CN. Moult location and diet of auks in the North Sea inferred from coupled light-based and isotope-based geolocation. Mar Ecol Prog Ser. 2018;599:239–251. doi: 10.3354/meps12624. DOI

Gu W, Regens JL, Beier JC, Novak RJ. Source reduction of mosquito larval habitats has unexpected consequences on malaria transmission. Proc Natl Acad Sci. 2006;103:17560–17563. doi: 10.1073/pnas.0608452103. PubMed DOI PMC

Hallworth MT, Marra PP. Miniaturized GPS tags identify non-breeding territories of a small breeding migratory songbird. Sci Rep. 2015;5:11069. doi: 10.1038/srep11069. PubMed DOI PMC

Hallworth MT, Studds CE, Sillett TS, Marra PP. Do archival light-level geolocators and stable hydrogen isotopes provide comparable estimates of breeding-ground origin? Auk. 2013;130:273–282. doi: 10.1525/auk.2013.13037. DOI

Hanmer DB. A trapping study of Palaearctic passerines at Nchalo, southern Malawi. Scopus. 1979;3:81–92.

Hasselquist D, Montràs-Janer T, Tarka M, Hansson B. Individual consistency of long-distance migration in a songbird: significant repeatability of autumn route, stopovers and wintering sites but not in timing of migration. J Avian Biol. 2017;48:91–102. doi: 10.1111/jav.01292. DOI

Heaton THE, Vogel JC, von la Chevallerie G, Gollet G. Climatic influence on the isotopic composition of bone nitrogen. Nature. 1986;322:822–823. doi: 10.1038/322822a0. DOI

Hedenström A, Bensch S, Hasselquist D, Lockwood M, Ottosson U. Migration, stopover and moult of the great reed warbler Acrocephalus arundinaceus in Ghana, West Africa. Ibis. 1993;135:177–180. doi: 10.1111/j.1474-919X.1993.tb02829.x. DOI

Hellgren O, Waldenström J, Bensch S. A new PCR assay for simultaneous studies of Leucocytozoon, Plasmodium and Haemoproteus from avian blood. J Parasitol. 2004;90:797–802. doi: 10.1645/GE-184R1. PubMed DOI

Hill RD. Theory of geolocation by light levels. Elephant seals: population ecology, behavior, and physiology. Berkeley: University of California Press; 1994.

Hobson KA, Wassenaar LI. Linking breeding and wintering grounds of Neotropical migrant songbirds using stable hydrogen isotopic analysis of feathers. Oecologia. 1996;109:142–148. doi: 10.1007/s004420050068. PubMed DOI

Hobson KA, Van Wilgenburg SL, Wassenaar LI, Powell RL, Still CJ, Craine JM. A multi-isotope (δ13C, δ15N, δ2H) feather isoscape to assign Afrotropical migrant birds to origins. Ecosphere. 2012;3:44. doi: 10.1890/ES12-00018.1. DOI

Hoffman MD, Gelman A. The no-U-turn sampler: adaptively setting path lengths in hamiltonian Monte Carlo. J Mach Learn Res. 2014;15:1593–1623. doi: 10.48550/arXiv.1111.4246. DOI

Jenni L, Winkler R. Moult and ageing of European passerines. London: Bloomsbury; 2020.

Koleček J, Procházka P, El-Arabany N, Tarka M, Ilieva M, Hahn S, Honza M, de la Puente J, Bermejo A, Gürsoy A, Bensch S, Zehtindjiev P, Hasselquist D, Hansson B. Cross-continental migratory connectivity and spatiotemporal migratory patterns in the great reed warbler. J Avian Biol. 2016;47:756–767. doi: 10.1111/jav.00929. DOI

Koleček J, Hahn S, Emmenegger T, Procházka P. Intra-tropical movements as a beneficial strategy for Palearctic migratory birds. Royal Soc Open Sci. 2018;5:171675. doi: 10.1098/rsos.171675. PubMed DOI PMC

Laird M. The natural history of larval mosquito habitats. London: Academic Press; 1988.

Lemke HW, Tarka M, Klaassen RH, Åkesson M, Bensch S, Hasselquist D, Hansson B. Annual cycle and migration strategies of a trans-Saharan migratory songbird: a geolocator study in the great reed warbler. PLoS ONE. 2013;8:e79209. doi: 10.1371/journal.pone.0079209. PubMed DOI PMC

Lisovski S, Hahn S. GeoLight—processing and analysing light-based geolocator data in R. Methods Ecol Evol. 2012;3:1055–1059. doi: 10.1111/j.2041-210X.2012.00248.x. DOI

Lisovski S, Hewson CM, Klaassen RH, Korner-Nievergelt F, Kristensen MW, Hahn S. Geolocation by light: accuracy and precision affected by environmental factors. Methods Ecol Evol. 2012;3:603–612. doi: 10.1111/j.2041-210X.2012.00185.x. DOI

Lott CA, Meehan TD, Heath JA. Estimating the latitudinal origins of migratory birds using hydrogen and sulfur stable isotopes in feathers: influence of marine prey base. Oecologia. 2003;134:505–510. doi: 10.1007/s00442-002-1153-8. PubMed DOI

Marra PP, Hobson KA, Holmes RT. Linking winter and summer events in a migratory bird by using stable-carbon isotopes. Science. 1998;282:1884–1886. doi: 10.1126/science.282.5395.1884. PubMed DOI

Palmer RW, de Moor F. Annotated records of blackfly (Diptera: Simuliidae) distribution in southern Africa. Afr Entomol. 1998;6:223–251.

Pearson DJ. The timing of complete moult in the Great Reed Warbler Acrocephalus arundinaceus. Ibis. 1975;117:506–509. doi: 10.1111/j.1474-919X.1975.tb04244.x. DOI

Quinby BM, Creighton JC, Flaherty EA. Stable isotope ecology in insects: a review. Ecol Entomol. 2020;45:1231–1246. doi: 10.1111/een.12934. DOI

R Core Team (2020) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna. https://www.R-project.org/

Sealy JC, van der Merwe NJ, Lee-Thorp JA, Lanhamm JL. Nitrogen isotopic ecology in southern Africa: implications for environmental and dietary tracing. Geochim Cosmochim Acta. 1987;51:2707–2717. doi: 10.1016/0016-7037(87)90151-7. DOI

Seifert N, Ambrosini R, Bontempo L, Camin F, Liechti F, Rubolini D, Scandolara C, Saino N, Hahn S. Matching geographical assignment by stable isotopes with African non-breeding sites of barn swallows Hirundo rustica tracked by geolocation. PLoS ONE. 2018;13:e0202025. doi: 10.1371/journal.pone.0202025. PubMed DOI PMC

Stan Development Team (2021) Stan user’s guide version 2.28. https://mc-stan.org/docs/2_28/stan-users-guide/

Svensson L (1992) Identification guide to European passerines, 4th edn. Lars Svensson, Stockholm

Thode HG. Sulphur isotopes in nature and the environment: an overview. In: Krouse HR, Grinenko VA, editors. Stable isotopes in the assessment of natural and anthropogenic sulphur in the environment. New York: Wiley; 1991. pp. 1–26.

van der Merwe NJ, Lee-Thorp JA, Thackeray JF, Hall-Martin A, Kruger FJ, Coetzee H, Bell RH, Lindeque M. Source-area determination of elephant ivory by isotopic analysis. Nature. 1990;346:744–746. doi: 10.1038/346744a0. DOI

Veen T, Hjernquist MB, Van Wilgenburg SL, Hobson KA, Folmer E, Font L, Klaassen M. Identifying the African wintering grounds of hybrid flycatchers using a multi-isotope (δ2H, δ13C, δ15N) assignment approach. PLoS ONE. 2014;9:e98075. doi: 10.1371/journal.pone.0098075. PubMed DOI PMC

Waldenström J, Bensch S, Kiboi S, Hasselquist D, Ottosson U. Cross-species infection of blood parasites between resident and migratory songbirds in Africa. Mol Ecol. 2002;11:1545–1554. doi: 10.1046/j.1365-294x.2002.01523.x. PubMed DOI

Webster MS, Marra PP, Haig SM, Bensch S, Holmes RT. Links between worlds: unraveling migratory connectivity. Trends Ecol Evol. 2002;17:76–83. doi: 10.1016/S0169-5347(01)02380-1. DOI

Westerdahl H, Waldenström J, Hansson B, Hasselquist D, von Schantz T, Bensch S. Associations between malaria and MHC genes in a migratory songbird. Proc R Soc B. 2005;272:1511–1518. doi: 10.1098/rspb.2005.3113. PubMed DOI PMC

Yanco SW, Linkhart BD, Marra PP, Mika M, Ciaglo M, Carver A, Wunder MB. Niche dynamics suggest ecological factors influencing migration in an insectivorous owl. Ecology. 2022;103:e3617. doi: 10.1002/ecy.3617. PubMed DOI

Yohannes E, Bensch S, Lee R. Philopatry of winter moult area in migratory Great Reed Warblers Acrocephalus arundinaceus demonstrated by stable isotope profiles. J Ornithol. 2008;149:261–265. doi: 10.1007/s10336-007-0271-9. DOI

Yohannes E, Hansson B, Lee RW, Waldenström J, Westerdahl H, Åkesson M, Hasselquist D, Bensch S. Isotope signatures in winter moulted feathers predict malaria prevalence in a breeding avian host. Oecologia. 2008;158:299–306. doi: 10.1007/s00442-008-1138-3. PubMed DOI

Yohannes E, Palinauskas V, Valkiūnas G, Lee RW, Bolshakov CV, Bensch S. Does avian malaria infection affect feather stable isotope signatures? Oecologia. 2011;167:937–942. doi: 10.1007/s00442-011-2041-x. PubMed DOI

Zazzo A, Monahan FJ, Moloney AP, Green S, Schmidt O. Sulphur isotopes in animal hair track distance to sea. Rapid Commun Mass Spectrom. 2011;25:2371–2378. doi: 10.1002/rcm.5131. PubMed DOI