Abstract
The survival of migratory passerines depends considerably on conditions experienced on their non-breeding grounds. However, these critical non-breeding sites are generally poorly known, especially for species and populations using the eastern Afro-Palearctic flyway. To fill this gap, we measured hydrogen stable isotopes in winter-grown feathers (δ2Hf) of five long-distance migratory passerines (Eurasian Blackcap, Eastern Olivaceous Warbler, Eurasian Reed Warbler, Olive-tree Warbler, and Barred Warbler) collected during spring migration at a stopover site in Israel, a major migratory bottleneck in the Afro-Palearctic Flyway. We determined non-breeding origins of these species, for the entire migrating population and for early- and late-arriving individuals separately. We used a probabilistic model based on feather isotopes and isotopic distribution of precipitation δ2H (δ2Hp) in Africa, as well as range maps derived from species distribution models and expert opinion. While our results suggested that Reed Warbler and Olive-tree Warbler occupy most of their known range during the non-breeding season, Blackcaps migrating through Jerusalem, Israel, likely spent the non-breeding season specifically in Ethiopia and near areas, and Eastern Olivaceous Warbler concentrated in two regions in eastern tropical and central Africa. Barred Warblers’ non-breeding grounds were estimated in Kenya, but the species distribution model approach suggested additional regions. Our results further suggested that early- and late-arriving Reed Warblers spent the non-breeding season in separate areas, whereas early- and late-arriving Blackcaps migrated to the same area. Given the rapid decline in many migratory species, our results are important for a more accurate evaluation of the conditions experienced during the non-breeding season and our study is a template for refining migratory connectivity estimates for species using this important flyway.
Zusammenfassung
Isotope in Federn von Rastplätzen machen afrikanische Nichtbrutplätze von Zugvögeln erkennbar.
Das Überleben von Zugvögeln hängt zu einem großen Maß von den Bedingungen ab, die sie außerhalb ihrer Brutgebiete vorfinden. Von diesen wichtigen Nichtbrutplätzen ist jedoch generell nur wenig bekannt, insbesondere für diejenigen Arten und Populationen, die die östliche afro-paläarktische Flugroute nutzen. Um diese Wissenslücke zu schließen, bestimmten wir die stabilen Wasserstoffisotope in den Winter-Federn (δ2Hf) von fünf Langstreckenziehern (Mönchsgrasmücken, Blassspötter, Teichrohrsänger, Olivenspötter und Sperbergrasmücken), die während des Frühjahrszuges an einem Rastplatz in Israel, einem wichtigen Nadelöhr auf der afro-paläarktischen Zugroute, gesammelt wurden. Wir bestimmten für die gesamte ziehende Population sowie getrennt für die früh und spät eintreffenden Tiere den Abflugort in den Nichtbrutplätzen. Dafür verwendeten wir ein Wahrscheinlichkeitsmodell, das auf den Isotopen in den Federn und der Isotopenverteilung im Niederschlag δ2H (δ2Hp) in Afrika basierte sowie auf Entfernungskarten, die anhand von Verbreitungsmodellen und Auskünften von Fachleuten erstellt wurden. Während unsere Ergebnisse darauf hindeuten, dass die Teichrohrsänger und Olivenspötter außerhalb der Brutzeit den größten Teil ihres bekannten Verbreitungsgebiets bewohnen, verbrachten die Mönchsgrasmücken, die durch Jerusalem, Israel, zogen, die Zeit außerhalb der Brutzeit wohl hauptsächlich in Äthiopien und näheren Regionen; der Blassspötter konzentrierte sich auf zwei Gebiete im östlichen tropischen und zentralen Afrika. Die Nichtbrutgebiete der Sperbergrasmücke wurden in Kenia vermutet, wobei das Modell für die Artenverteilung auf weitere Regionen hinwies. Unsere Ergebnisse deuten außerdem darauf hin, dass früh und spät eintreffende Teichrohrsänger die Nichtbrutzeit in getrennten Gebieten verbrachten, während früh und spät eintreffende Mönchsgrasmücken in dasselbe Gebiet zogen. Angesichts des raschen Rückgangs vieler Zugvogelarten sind unsere Ergebnisse für eine genauere Bewertung der Lebensumstände während der Nichtbrutzeit wichtig. Unsere Studie ist eine Grundlage für eine exaktere Bewertung der Zugwege-Vernetzung derjenigen Arten, die diese wichtige Zugroute nutzen.
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The data that support the findings of this study are available from the corresponding author upon reasonable request.
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References
Aharon-Rotman Y, Bauer S, Klaassen M (2016) A chain is as strong as its weakest link: assessing the consequences of habitat loss and degradation in a long-distance migratory shorebird. Emu 116:199–207. https://doi.org/10.1071/MU15029
Aharon-Rotman Y, Perlman G, Kiat Y, Raz T, Balaban A, Iwamura T (2021) Limited flexibility in departure timing of migratory passerines at the East-Mediterranean flyway. Sci Rep 11:5184. https://doi.org/10.1038/s41598-021-83793-x
Aharon-Rotman Y, McEvoy JF, Kiat Y, Raz T, Perlman GY (2022) Time to move on: the role of greenness in Africa and temperatures at a Mediterranean stopover site in migration decision of long-distance migratory passerines. Front Ecol Evol 10:834074. https://doi.org/10.3389/fevo.2022.834074
Aidley D, Wilkinson R (1987) Moult of some Palaearctic warblers in northern Nigeria. Bird Study 34:219–225
Aiello-Lammens ME, Boria RA, Radosavljevic A, Vilela B, Anderson RP (2015) spThin: an R package for spatial thinning of species occurrence records for use in ecological niche models. Ecography 38:541–545. https://doi.org/10.1111/ecog.01132
Atkinson PW, Adams WM, Brouwer J, Buchanan G, Cheke RA, Cresswell W, Hewson CM, Hulme MF, Manvell A, Sheehan DK, Small RDS, Sutherland WJ, Vickery JA (2014) Defining the key wintering habitats in the Sahel for declining African-Eurasian migrants using expert assessment. Bird Conserv Int 24:477–491. https://doi.org/10.1017/S0959270913000531
Baillie SR, Peach WJ (1992) Population limitation in Palaearctic-African migrant passerines. Ibis 134:120–132. https://doi.org/10.1111/j.1474-919X.1992.tb04742.x
Bairlein F (2003) The study of bird migrations—some future perspectives. Bird Study 50:243–253. https://doi.org/10.1080/00063650309461317
Bairlein F (2016) Migratory birds under threat. Science 354:547–548. https://doi.org/10.1126/science.aah6647
Billerman S, Keeney B, Rodewald P, Schulenberg T (2020) Birds of the world. Cornell Laboratory of Ornithology, Ithaca. https://birdsoftheworld.org/bow/home. Accessed 5 Apr 2020
Bird species distribution maps of the world, version 5.0. (2018) BirdLife International, Cambridge, UK and NatureServe, Arlington, USA
Boria RA, Olson LE, Goodman SM, Anderson RP (2014) Spatial filtering to reduce sampling bias can improve the performance of ecological niche models. Ecol Model 275:73–77. https://doi.org/10.1016/j.ecolmodel.2013.12.012
Bowen GJ, Wassenaar LI, Hobson KA (2005) Global application of stable hydrogen and oxygen isotopes to wildlife forensics. Oecologia 143:337–348. https://doi.org/10.1007/s00442-004-1813-y
Brink AB, Eva HD (2009) Monitoring 25 years of land cover change dynamics in Africa: a sample based remote sensing approach. Appl Geogr 29:501–512. https://doi.org/10.1016/j.apgeog.2008.10.004
Brlík V, Procházka P, Hansson B, Stricker CA, Yohannes E, Powell RL, Wunder MB (2022) Animal tracing with sulfur isotopes: Spatial segregation and climate variability in Africa likely contribute to population trends of a migratory songbird. J Anim Ecol 00:1–12. https://doi.org/10.1111/1365-2656.13848
Burnham KP, Anderson DR (2004) Multimodel inference: understanding AIC and BIC in model selection. Sociol Methods Res 33:261–304
Busse P (2001) European passerine migration system—what is known and what is lacking. Ring 23:3–36
Cárdenas-Ortiz L, Bayly NJ, Hobson KA (2021) Fuel loads of Neotropical migrant songbirds on autumn passage through the Darién region of Colombia: Influence of migratory distance, route, ENSO, age and body size. Anim Migr 8:29–39. https://doi.org/10.1515/ami-2020-0105
Delmore KE, Van Doren BM, Conway GJ, Curk T, Garrido-Garduño T, Germain RR, Hasselmann T, Hiemer D, van der Jeugd HP, Justen H, Lugo Ramos JS, Maggini I, Meyer BS, Phillips RJ, Remisiewicz M, Roberts GCM, Sheldon BC, Vogl W, Liedvogel M (2020) Individual variability and versatility in an eco-evolutionary model of avian migration. Proc R Soc B Biol Sci 287:20201339. https://doi.org/10.1098/rspb.2020.1339
Dinerstein E, Olson D, Joshi A, Vynne C, Burgess ND, Wikramanayake E, Hahn N, Palminteri S, Hedao P, Noss R et al (2017) An ecoregion-based approach to protecting half the terrestrial realm. Bioscience 67:534–545
Dormann CF, Elith J, Bacher S, Buchmann C, Carl G, Carré G, Marquéz JRG, Gruber B, Lafourcade B, Leitão PJ, Münkemüller T, Mcclean C, Osborne PE, Reineking B, Schröder B, Skidmore AK, Zurell D, Lautenbach S (2013) Collinearity: a review of methods to deal with it and a simulation study evaluating their performance. Ecography 36:027–046. https://doi.org/10.1111/j.1600-0587.2012.07348.x
Dowsett-Lemair F, Dowsett RJ (1987) European Reed and Marsh Warblers in Africa: migration patterns, moult and habitat. Ostrich 58:65–85. https://doi.org/10.1080/00306525.1987.9634145
Elith J, Leathwick JR (2009) Species distribution models: ecological explanation and prediction across space and time. Annu Rev Ecol Evol Syst 40:677–697. https://doi.org/10.1146/annurev.ecolsys.110308.120159
Fenta AA, Tsunekawa A, Haregeweyn N, Tsubo M, Yasuda H, Shimizu K, Kawai T, Ebabu K, Berihun ML, Sultan D, Belay AS, Sun J (2020) Cropland expansion outweighs the monetary effect of declining natural vegetation on ecosystem services in sub-Saharan Africa. Ecosyst Serv 45:101154. https://doi.org/10.1016/j.ecoser.2020.101154
Du Feu C, Joys A, Clark J, Fiedler W, Downie I, Van Noordwijk A, Spina F, Wassenaar R, Baillie S (2009) EURING Data Bank geographical index 2009. http://www.euring.org/edb. Accessed 23 Jul 2018
Fick SE, Hijmans RJ (2017) WorldClim 2: New 1-km spatial resolution climate surfaces for global land areas. Int J Climatol 37:4302–4315. https://doi.org/10.1002/joc.5086
Fournier AMV, Sullivan AR, Bump JK, Perkins M, Shieldcastle MC, King SL (2017) Combining citizen science species distribution models and stable isotopes reveals migratory connectivity in the secretive Virginia rail. J Appl Ecol 54:618–627. https://doi.org/10.1111/1365-2664.12723
Frumkin R, Pinshow B, Kleinhaus S (1995) A review of bird migration over Israel. J Ornithol 136:127–147. https://doi.org/10.1007/BF01651235
Gill JA, Norris K, Potts PM, Gunnarsson TG, Atkinson PW, Sutherland WJ (2001) The buffer effect and large-scale population regulation in migratory birds. Nature 412:436–438. https://doi.org/10.1038/35086568
Guisan A, Thuiller W (2005) Predicting species distribution: offering more than simple habitat models. Ecol Lett 8:993–1009. https://doi.org/10.1111/j.1461-0248.2005.00792.x
Gutiérrez-Expósito C, Ramírez F, Afán I, Forero MG, Hobson KA (2015) Toward a deuterium feather isoscape for sub-Saharan Africa: Progress, challenges and the path ahead. PLoS ONE 10:e0135938. https://doi.org/10.1371/journal.pone.0135938
Hahn S, Bauer S, Liechti F (2009) The natural link between Europe and Africa on migration. Oikos 118:624–626. https://doi.org/10.1111/j.1600-0706.2008.17309.x
Hanley JA, McNeil BJ (1982) The meaning and use of the area under a receiver operating characteristic (ROC) curve. Radiology 143:29–36. https://doi.org/10.1080/02634938208400381
Hedh L, Dänhardt J, Hedenström A (2022) Population specific annual cycles and migration strategies in a leap-frog migrant. Behav Ecol Sociobiol 76:2. https://doi.org/10.1007/s00265-021-03116-y
Helbig AJ (1996) Genetic basis, mode of inheritance and evolutionary changes of migratory directions in palearctic warblers (Aves: Sylviidae). J Exp Biol 199:49–55. http://jeb.biologists.org/content/jexbio/199/1/49.full.pdf
Hengl T, De Jesus JM, MacMillan RA, Batjes NH, Heuvelink GBM, Ribeiro E, Samuel-Rosa A, Kempen B, Leenaars JGB, Walsh MG, Gonzalez MR (2014) SoilGrids1km—global soil information based on automated mapping. PLoS ONE 9:e105992. https://doi.org/10.1371/journal.pone.0105992
Hewson CM, Noble DG (2009) Population trends of breeding birds in British woodlands over a 32-year period: relationships with food, habitat use and migratory behaviour. Ibis 151:464–486. https://doi.org/10.1111/j.1474-919X.2009.00937.x
Hijmans RJ, Phillips S, Leathwick JR, Elith J (2017) Package ‘dismo.’ Circles 9:1–68. https://doi.org/10.1016/j.jhydrol.2011.07.022
Hobson KA (2019) Application of isotopic methods to tracking animal movements. Tracking animal migration with stable isotopes, 2nd edn. Academic Press, London, pp 85–116
Hobson KA, Wassenaar LI (1997) Linking breeding and wintering grounds of neotropical migrant songbirds using stable hydrogen isotopic analysis of feathers. Oecologia 109:142–148. https://doi.org/10.1007/s004420050068
Hobson KA, Wassenaar LI (2019) Tracking animal migration with stable isotopes, 2nd edn. Academic Press, London. https://doi.org/10.1016/C2017-0-01125-4
Hobson KA, Van Wilgenburg SL, Wassenaar LI, Larson K (2012) Linking hydrogen (δ2H) isotopes in feathers and precipitation: sources of variance and consequences for assignment to isoscapes. PLoS ONE 7:e35137. https://doi.org/10.1371/journal.pone.0035137
Hobson KA, Van Wilgenburg SL, Faaborg J, Toms JD, Rengifo C, Sosa AL, Aubry Y, Brito Aguilar R (2014) Connecting breeding and wintering grounds of Neotropical migrant songbirds using stable hydrogen isotopes: a call for an isotopic atlas of migratory connectivity. J Field Ornithol 85:237–257. https://doi.org/10.1111/jofo.12065
Hobson KA, Doward K, Kardynal KJ, Mcneil JN (2018) Inferring origins of migrating insects using isoscapes: a case study using the true armyworm, Mythimna unipuncta, in North America. Ecol Entomol 43:332–341. https://doi.org/10.1111/een.12505
Jenni L, Winkler R (2020) Moult and ageing of European passerines, 2nd edn. Bloomsbury Publishing, London
Jiguet F, Kardynal KJ, Piha M, Seimola T, Copete JL, Czajkowski MA, Dombrovski V, Efrat R, Minkevicius S, Raković M, Skierczyǹski M, Hobson KA (2019) Stable isotopes reveal the common winter moult of central rectrices in a long-distance migrant songbird. J Ornithol 1:3. https://doi.org/10.1007/s10336-019-01671-w
Jiguet F, Dufour P, Kardynal KJ, Hobson KA, Copete JL, Arroyo JL, Lee RW, Rguibi-Idrissi H, Procházka P (2022) Identifying the winter grounds of the recently described Barbary Reed Warbler (Acrocephalus baeticatus ambiguus). Ibis 165:204–213. https://doi.org/10.1111/ibi.13113
Jones PJ (1995) Migration strategies of Palearctic passerines in Africa. Isr J Zool 41:393–406. https://doi.org/10.1080/00212210.1995.10688809
Kardynal KJ, Collister DM, Hobson KA (2018) Origins of Wilson’s warblers migrating through southwest Canada: adding value to banding data by using stable isotopes and genetic markers. Anim Migr 5:17–28. https://doi.org/10.1515/ami-2018-0002
Kennerley P, Pearson D (2010) Reed and bush warblers. Bloomsbury Publishing, London
Kiat Y, Izhaki I, Sapir N (2019) The effects of long-distance migration on the evolution of moult strategies in Western-Palearctic passerines. Biol Rev 94:700–720. https://doi.org/10.1111/brv.12474
La Sorte FA, Somveille M (2020) Survey completeness of a global citizen-science database of bird occurrence. Ecography 43:34–43. https://doi.org/10.1111/ecog.04632
Lawrence KB, Barlow CR, Bensusan K, Perez C, Willis SG (2022) Phenological trends in the pre- and post-breeding migration of long-distance migratory birds. Glob Change Biol 28:375–389. https://doi.org/10.1111/gcb.15916
Lindström Å, Pearson DJ, Hasselquist D, Hedenström A, Bensch S, Åkesson S (1993) The moult of Barred Warblers Sylvia nisoria in Kenya—evidence for a split wing-moult pattern initiated during the birds’ first winter. Ibis 135:403–409. https://doi.org/10.1111/j.1474-919X.1993.tb02112.x
Liu C, Berry PM, Dawson TP, Pearson RG (2005) Selecting thresholds of occurrence in the prediction of species distributions. Ecography 28:385–393. https://doi.org/10.1111/j.0906-7590.2005.03957.x
López-López P (2016) Individual-based tracking systems in ornithology: welcome to the era of big data. Ardeola 63:103–136. https://doi.org/10.13157/arla.63.1.2016.rp5
Maggini I, Spina F, Voigt CC, Ferri A, Bairlein F (2013) Differential migration and body condition in Northern Wheatears (Oenanthe oenanthe) at a Mediterranean spring stopover site. J Ornithol 154:321–328. https://doi.org/10.1007/s10336-012-0896-1
Marra PP, Hobson KA, Holmes RT (1998) Linking winter and summer events in a migratory bird by using stable- carbon isotopes. Science 282:1884–1886. https://doi.org/10.1126/science.282.5395.1884
Marx M, Rocha G, Zehtindjiev P, Peev S, Bakaloudis D, Metzger B, Cecere JG, Spina F, Cianchetti-Benedetti M, Frahnert S, Gamauf A, Voigt CC, Quillfeldt P (2020) Using stable isotopes to assess population connectivity in the declining European Turtle Dove (Streptopelia turtur). Conserv Sci Pract 2:1–13. https://doi.org/10.1111/csp2.152
Milano S, Frahnert S, Hallau A, Töpfer T, Woog F, Voigt CC (2021) Isotope record tracks changes in historical wintering ranges of a passerine in sub-Saharan Africa. Glob Change Biol 27:5460–5468. https://doi.org/10.1111/gcb.15794
Muscarella R, Galante PJ, Soley-Guardia M, Boria RA, Kass JM, Uriarte M, Anderson RP (2014) ENMeval: an R package for conducting spatially independent evaluations and estimating optimal model complexity for Maxent ecological niche models. Methods Ecol Evol 5:1198–1205. https://doi.org/10.1111/2041-210x.12261
Newton I (2004) Population limitation in migrants. Ibis 146:197–226. https://doi.org/10.1111/j.1474-919X.2004.00293.x
Newton I (2011) Migration within the annual cycle: species, sex and age differences. J Ornithol 152:169–185. https://doi.org/10.1007/s10336-011-0689-y
Niamir A, Skidmore AK, Toxopeus AG, Real R (2016) Use of taxonomy to delineate spatial extent of atlas data for species distribution models. Glob Ecol Biogeogr 25:227–237. https://doi.org/10.1111/geb.12405
Norman D, Peach WJ (2013) Density-dependent survival and recruitment in a long-distance Palaearctic migrant, the Sand martin Riparia riparia. Ibis 155:284–296. https://doi.org/10.1111/ibi.12036
Ockendon N, Johnston A, Baillie SR (2014) Rainfall on wintering grounds affects population change in many species of Afro-Palaearctic migrants. J Ornithol 155:905–917. https://doi.org/10.1007/s10336-014-1073-5
Pearce JL, Boyce MS (2006) Modelling distribution and abundance with presence-only data. J Appl Ecol 43:405–412. https://doi.org/10.1111/j.1365-2664.2005.01112.x
Pearson DJ (1973) Molt of some Palaearctic warblers wintering in Uganda. Bird Study 20:24–36. https://doi.org/10.1080/00063657309476355
Phillips SJ, Dudík M, Dudík D, Elith J, Graham CH, Lehmann A, Leathwick J, Ferrier S (2009) Sample selection bias and presence-only distribution models: implications for background and pseudo-absence data. Ecol Appl 19:181–197. https://doi.org/10.1890/07-2153.1
Phillips SJ, Dudík M, Schapire RE (2017) Maxent software for modeling species niches and distributions (Version 3.4. 1). http://biodiversityinformatics.amnh.org/open_source/maxent. Accessed 22 May 2018
Pineda E, Lobo JM (2012) The performance of range maps and species distribution models representing the geographic variation of species richness at different resolutions. Glob Ecol Biogeogr 21:935–944. https://doi.org/10.1111/j.1466-8238.2011.00741.x
Procházka P, Hobson KA, Karcza Z, Kralj J (2008) Birds of a feather winter together: migratory connectivity in the Reed Warbler Acrocephalus scirpaceus. J Ornithol 149:141–150. https://doi.org/10.1007/s10336-007-0250-1
Procházka P, Van Wilgenburg SL, Neto JM, Yosef R, Hobson KA (2013) Using stable hydrogen isotopes (δ2H) and ring recoveries to trace natal origins in a Eurasian passerine with a migratory divide. J Avian Biol 44:541–550. https://doi.org/10.1111/j.1600-048X.2013.00185.x
Procházka P, Brlík V, Yohannes E, Meister B, Auerswald J, Ilieva M, Hahn S (2018) Across a migratory divide: divergent migration directions and non-breeding grounds of Eurasian Reed Warblers revealed by geolocators and stable isotopes. J Avian Biol 49:jav-012516. https://doi.org/10.1111/jav.01769
QGIS (2018) QGIS Geographic Information System. Open source geospatial foundation project. http://www.qgis.org/. Accessed 2 Jan 2018
R Development Core Team (2019) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna
Royle JA, Rubenstein DR (2004) The role of species abundance in determining breeding origins of migratory birds with stable isotopes. Ecol Appl 14:1780–1788. http://www.jstor.org/stable/4493691
Rubenstein DR, Hobson KA (2004) From birds to butterflies: animal movement patterns and stable isotopes. Trends Ecol Evol 19:256–263. https://doi.org/10.1016/j.tree.2004.03.017
Ruegg KC, Anderson EC, Harrigan RJ, Paxton KL, Kelly JF, Moore F, Smith TB (2017) Genetic assignment with isotopes and habitat suitability (GAIAH), a migratory bird case study. Methods Ecol Evol 8:1241–1252. https://doi.org/10.1111/2041-210X.12800
Saino N, Szep T, Ambrosini R, Romano M, Moller AP (2004) Ecological conditions during winter affect sexual selection and breeding in a migratory bird. Proc R Soc b Biol Sci 271:681–686. https://doi.org/10.1098/rspb.2003.2656
Salewski V, Flade M, Lisovski S, Poluda A, Iliukha O, Kiljan G, Malashevich U, Hahn S (2019) Identifying migration routes and non-breeding staging sites of adult males of the globally threatened Aquatic Warbler Acrocephalus paludicola. Bird Conserv Int 29:503–514. https://doi.org/10.1017/S0959270918000357
Sanderson FJ, Donald PF, Pain DJ, Burfield IJ, Van Bommel FPJ (2006) Long-term population declines in Afro-Palearctic migrant birds. Biol Cons 131:93–105. https://doi.org/10.1016/j.biocon.2006.02.008
Shirihai H (1996) The birds of Israel. Academic Press, London
Shirihai H, Gargallo G, Helbig AJ, Kirwan GM, Svensson L (2001) Sylvia Warblers: identification, taxonomy and phylogeny of the genus Sylvia, 1st edn. Bloomsbury Publishing, London
Smith RJ, Moore FR (2005) Arrival timing and seasonal reproductive performance in a long-distance migratory landbird. Behav Ecol Sociobiol 57:231–239. https://doi.org/10.1007/s00265-004-0855-9
Svensson L (1992) Identification guide to European passerines. 4th edn. British Trust for Ornithology, Norfolk
Tøttrup AP, Pedersen L, Thorup K (2018) Autumn migration and wintering site of a Wood Warbler Phylloscopus sibilatrix breeding in Denmark identified using geolocation. Anim Biotelemetry 6:1–6. https://doi.org/10.1186/s40317-018-0159-x
Urban EK, Fry CH, Keith S (1997) The birds of Africa, vol V. Academic Press, London
Van Wilgenburg SL, Hobson KA (2011) Combining stable-isotope (δD) and band recovery data to improve probabilistic assignment of migratory birds to origin. Ecol Appl 21:1340–1351. https://doi.org/10.1890/09-2047.1
Van Dijk JGB, Meissner W, Klaassen M (2014) Improving provenance studies in migratory birds when using feather hydrogen stable isotopes. J Avian Biol 45:103–108. https://doi.org/10.1111/j.1600-048X.2013.00232.x
Vander Zanden HB, Wunder MB, Hobson KA, Van Wilgenburg SL, Wassenaar LI, Welker JM, Bowen GJ (2014) Contrasting assignment of migratory organisms to geographic origins using long-term versus year-specific precipitation isotope maps. Methods Ecol Evol 5:891–900. https://doi.org/10.1111/2041-210x.12229
Vickery JA, Adams WM (2020) Action before certainty for Africa’s European migrant birds. Oryx 54:1–2. https://doi.org/10.1017/S0030605319001273
Vickery JA, Ewing S, Smith KW, Pain DJ, Bairlein F, Škorpilová J, Gregory RD (2014) The decline of Afro-Paleartic migrants and an assessment of potential causes. Ibis 156:1–22. https://doi.org/10.1111/ibi.12118
Walther BA, Rahbek C (2002) Where do Palearctic migratory birds overwinter in Africa? Dansk Ornitologisk Forenings Tidsskrift 96:4–8. http://macroecointern.dk/pdf-reprints/WaltherRahbek2002.pdf
Walther BA, Wisz MS, Rahbek C (2004) Known and predicted African winter distributions and habitat use of the endangered Basra Beed Warbler (Acrocephalus griseldis) and the near-threatened Cinereous Bunting (Emberiza cineracea). J Ornithol 145:287–299. https://doi.org/10.1007/s10336-004-0036-7
Walther BA, Van Niekerk A, Thuiller W, Baumann S, Dean WRJ, De Bruijn B, Gutteridge K, Jones P, Nikolaus G, Pearson DJ, Robinson SP, Salewski V, Schäffer N, Taylor PB, Tushabe H, Williams PH, Rahbek C (2010) A database of Western Palearctic birds migrating within Africa to guide conservation decisions. In: Proceedings of the 12th Pan-African ornithological congress, 2008, pp 50–104
Warren DL, Glor RE, Turelli M (2008) Environmental niche equivalency versus conservatism: quantitative approaches to niche evolution. Evolution 62:2868–2883. https://doi.org/10.1111/j.1558-5646.2008.00482.x
Wassenaar LI, Hobson KA (2003) Comparative equilibration and online technique for determination of non-exchangeable hydrogen of keratins for use in animal migration studies. Isot Environ Health Stud 39:211–217. https://doi.org/10.1080/1025601031000096781
West JB, Bowen GJ, Dawson TE, Tu KP (2010) Isoscapes: understanding movement, pattern, and process on Earth through isotope mapping. Springer Science, Berlin
Wolff C, Haug GH, Timmermann A, Damsté JSS, Brauer A, Sigman DM, Cane MA, Verschuren D (2011) Reduced interannual rainfall variability in East Africa during the last ice age. Science 333:743–747. https://doi.org/10.1126/science.1203724
Xenophontos M, Blackburn E, Cresswell W (2017) Cyprus Wheatears Oenanthe cypriaca likely reach sub-Saharan African wintering grounds in a single migratory flight. J Avian Biol 48:529–535. https://doi.org/10.1111/jav.01119
Yosef R (1997) Clues to the migratory routes of the eastern flyway of the western Palearctics—ringing recoveries at Eilat, Israel [I—Ciconiiformes, Charadriiformes, Coraciiformes, and Passeriformes.]. Vogelwarte 39:131–140. https://www.zobodat.at/pdf/Vogelwarte_39_1997_0131-0140.pdf
Acknowledgements
We heartily thank the ringers and staff of the JBO, in particular Yotam Lenard and Yishai Landoi for managing the feather collection. We thank Blanca X. Mora-Alvarez for assistance in the preparation of samples for stable-isotope analyses which were performed by KAH. We also thank Dr. Yoav Perlman of Society for the Protection of Nature in Israel for providing us friendly review on this paper. We also extend our sincere gratitude to the reviewers for their time and effort in reading the manuscript and for their insightful remarks and recommendations.
Funding
KAH was funded by a Discovery Grant from the National Science and Engineering and Research Council (NSERC) of Canada (2017-04430). TI was funded by Tel Aviv University for the new faculty start-up fund.
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TI, YK, GP, and YA-R originally conceived the idea. GP was responsible for the entire fieldwork operation at the JBO and performed the fieldwork with TR and YK. YK was responsible to identify moult feathers for each bird. KH performed the laboratory isotope work. TR, KK, TI, and KH analyzed the data. TR led the writing of the manuscript; All authors contributed critically to the drafts and gave final approval for publication.
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Feather collection was approved by the Israel Nature and Parks Authority (NPA; permit number 41567).
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Communicated by N. Chernetsov.
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Raz, T., Kiat, Y., Kardynal, K.J. et al. Stopover-site feather isotopes uncover African non-breeding grounds of migratory passerines. J Ornithol 164, 859–873 (2023). https://doi.org/10.1007/s10336-023-02078-4
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DOI: https://doi.org/10.1007/s10336-023-02078-4