The use of molecular diagnostics to infer migration directions of Willow Warblers in the southeast Baltic

Abstract

The Willow Warbler (Phylloscopus trochilus, Linnaeus, 1758) is a long distance migrant and one of the most common breeding birds in the Western Palearctic. Its migratory directions have been studied in detail in Scandinavia where a narrow migratory divide is located around 62°30′ N that separates southern SW migrating Phylloscopus t. trochilus from SSE migrating Phylloscopus t. acredula. The shape and location of the migratory divide in the countries south and east of the Baltic Sea is less well understood. In this study we explored the geographic origin and migratory phenotype of the Willow Warbler during breeding and migration at Rybachy, Kaliningrad, Russia. The sampling was divided into three periods: breeding (1–9 July), early autumn migration (25–31 August), and late autumn migration (1–17 September). The birds were genotyped at two bi-allelic loci (AFLP-WW1 and AFLP-WW2) and the results were compared to genotypes from several reference breeding populations from around the Baltic Sea. Samples from the breeding and early migration periods were dominated by genotypes associated with SW-migrating trochilus. However, several intermediate genotypes were also present among breeding birds suggesting that this area overlaps the hybrid zone extending from territories south of the Baltic Sea. During late migration, birds carried genotypes that are common among north Scandinavian Willow Warblers that apparently pass Rybachy on their migration SSE to wintering areas in tropical East and South Africa.

Zusammenfassung

Die Anwendung molekularer Diagnoseverfahren ermöglicht Rückschlüsse auf Zugrichtungen bei Fitissen Phylloscopus trochilus im südöstlichen Baltikum

Der Fitis ist ein Langstreckenzieher und gehört zu den häufigsten Brutvögeln der Westpaläarktis. Seine Zugrichtungen sind in Skandinavien bestens untersucht, wo eine schmale Zugscheide bei etwa 62°30’ N verläuft, welche die südlich davon nach SW ziehende Unterart trochilus von den nach SSO ziehenden acredula-Individuen trennt. Form und Lage der Zugscheide in den südlich und östlich der Ostsee gelegenen Ländern sind weniger gut bekannt. In dieser Studie erforschten wir die geografische Herkunft und den Zugphänotyp von Fitissen während der Brutzeit und auf dem Zug in Rybatschi, Kaliningrad, Russland. Die Probennahme erfolgte während dreier Zeiträume: Brutzeit (1.-9. Juli), früher Herbstzug (25.-31. August) und später Herbstzug (1.-17. September). Die Vögel wurden an zwei bi-allelischen Loci (AFLP-WW1 und AFLP-WW2) genotypisch charakterisiert, und die Ergebnisse wurden mit Genotypdaten von verschiedenen Referenz-Brutpopulationen rund um die Ostsee verglichen. In den Proben aus der Brutzeit und vom Beginn des Herbstzuges überwogen Genotypen, die mit nach SW ziehenden trochilus-Individuen assoziiert sind. Allerdings waren ebenfalls mehrere intermediäre Genotypen unter den Brutvögeln vertreten, was darauf hindeutet, dass dieses Gebiet mit der Hybridzone überlappt, welche sich von den Regionen südlich der Ostsee erstreckt. Später im Zuggeschehen wiesen die Vögel Genotypen auf, wie sie bei nordskandinavischen Fitissen häufig vorkommen, welche Rybatschi offenbar auf ihrem Zug nach SSO in Wintergebiete im tropischen Süd- und Ostafrika passieren.

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References

  1. Åkesson S, Hedenström A (2007) How migrants get there: migratory performance and orientation. Bioscience 57:123–133

    Article  Google Scholar 

  2. Alerstam T (1979) Wind as selective agent in bird migration. Ornis Scand 10:76–93

    Article  Google Scholar 

  3. Alerstam T, Hedenström A, Åkesson S (2003) Long-distance migration: evolution and determinants. Oikos 103:247–260

    Article  Google Scholar 

  4. Bauer W, Helversen OV, Hodge M, Martens J (1969) Catalogus Faunae Graeciae. Pars II Aves, Thessaloniki, p 203

    Google Scholar 

  5. Belliure J, Sorci G, Møller AP, Clobert J (2000) Dispersal distances predict subspecies richness in birds. J Evol Biol 13:480–487

    Article  Google Scholar 

  6. Bensch S, Andersson T, Åkesson S (1999) Morphological and molecular variation across a migratory divide in willow warblers, Phylloscopus trochilus. Evolution 53:1925–1935

    Article  PubMed  Google Scholar 

  7. Bensch S, Åkesson S, Irwin DE (2002) The use of AFLP to find an informative SNP: genetic differences across a migratory divide in willow warblers. Mol Ecol 11:2359–2366. doi:10.1046/j.1365-294X.2002.01629.x

    CAS  Article  PubMed  Google Scholar 

  8. Bensch S, Bengtsson G, Åkesson S (2006) Patterns of stable isotope signatures in willow warbler feathers collected in Africa. J Avian Biol 37:323–330. doi:10.1111/j.2006.0908-8857.03628.x

    Article  Google Scholar 

  9. Bensch S, Grahn M, Müller N, Gay L, Åkesson S (2009) Genetic, morphological, and feather isotope variation of migratory willow warblers show gradual divergence in a ring. Mol Ecol 18:3087–3096. doi:10.1111/j.1365-294X.2009.04210.x

    Article  PubMed  Google Scholar 

  10. Bolshakov CV, Shapoval AP, Zelenova NP (2000) Results of bird trapping and ringing by the Biological Station “Rybachy” on the Courish Spit in 1999. Avian Ecol Behav 4:85–145

    Google Scholar 

  11. Bolshakov CV, Shapoval AP, Zelenova NP (2001) Results of bird ringing by the Biological Station “Rybachy” on the Courish Spit: long-distance recoveries of birds ringed in 1956-1997. Avian Ecol Behav Suppl 1:1–126

    Google Scholar 

  12. Bolshakov CV, Shapoval AP, Zelenova NP (2002) Results of bird ringing by the Biological Station “Rybachy”: controls of birds ringed outside the Courish Spit in 1956-1997. Avian Ecol Behav Suppl 5:1–106

    Google Scholar 

  13. Bolshakov CV, Shapoval AP, Zelenova NP (2004) Results of bird trapping and ringing by the Biological Station “Rybachy” on the Courish Spit in 2003. Avian Ecol Behav 12:77–132

    Google Scholar 

  14. Bolshakov CV, Shapoval AP, Zelenova NP (2009) Results of bird trapping and ringing by the Biological Station “Rybachy” on the Courish Spit in 2006. Avian Ecol Behav 15:49–85

    Google Scholar 

  15. Bolshakov CV, Shapoval AP, Zelenova NP (2013) Results of bird trapping and ringing by the Biological Station “Rybachy” on the Courish Spit in 2012. Avian Ecol Behav 24:51–91

    Google Scholar 

  16. Busse P (2001) European passerine migration system—what is known and what is lacking. Ring 23:3–36

    Google Scholar 

  17. Chamberlain CP, Bensch S, Feng X, Åkesson S, Andersson T (2000) 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 SocB 267:43–48. doi:10.1098/rspb.2000.0964

    CAS  Article  Google Scholar 

  18. Ciach M (2009) Leaf warblers (Phylloscopus spp.) as a model group in migration ecology studies. Ring 31(2):3–13. doi:10.2478/v10050-008-0050-x

    Article  Google Scholar 

  19. Cramp S, Brooks DJ (eds) (1992) Handbook of the Birds of Europe and Middle East and North Africa, vol 6. Oxford University Press, Oxford

    Google Scholar 

  20. Del Hoyo J, Elliott A, Christie D (2006) Handbook of the Birds of the World, vol Volume 11., Old World Flycatchers to Old World WarblersLynx Edicions, Barcelona

    Google Scholar 

  21. Dickinson EC (ed) (2003) The Howard and Moore Complete Checklist of the Birds of the World. Christopher Helm, London

    Google Scholar 

  22. Flint PR, Stewart RF (1983) The birds of Cyprus. British Ornithologist’ Union Check List

  23. Gaginskaja AR (1995) Willow warbler (Phylloscopus trochilus L.). In: Noskov GA, Rezvyi SP (eds) Atlas of bird migration according to ringing and recovery data for Leningrad Region, St. Petersburg, pp 132–134 (Proceedings St. Petersburg Naturalists’ Society, vol 85:4) (in Russian)

  24. Goodman SM, Meininger PL (eds) (1989) The birds of Egypt. Oxford University Press, Oxford

    Google Scholar 

  25. Hedenström A, Pettersson J (1987) Migration routes and wintering areas of Willow Warblers Phylloscopus trochilus (L.) ringed in Fennoscandia. Ornis Fennica 64:137–143

    Google Scholar 

  26. Helbig AJ (1991) SE- and SW-migrating blackcap (Sylvia atricapilla) populations in central Europe: orientation of birds in the contact zone. J Evol Biol 4:657–670. doi:10.1046/j.1420-9101.1991.4040657.x

    Article  Google Scholar 

  27. Helbig AJ (1996) Genetic basis, mode of inheritance and evolutionary changes of migratory directions in Palaearctic warblers (Aves: sylviidae). J Exp Biol 199:49–55

    CAS  PubMed  Google Scholar 

  28. Hewitt G (2000) The genetic legacy of the Quaternary ice ages. Nature 405:907–913

    CAS  Article  PubMed  Google Scholar 

  29. Ilieva M, Towes D, Bensch S, Sjöholm C, Åkesson S (2012) Autumn migratory orientation and displacement responses in two subspecies of willow warblers (Phylloscopus trochilus trochilus and P. t. acredula) in South Sweden. Behav Process 91:253–261

    Article  Google Scholar 

  30. Irwin DE, Irwin JH (2005) Siberian migratory divides: the role of seasonal migration in speciation. In: Birds of two worlds: the ecology and evolution of migration. Johns Hopkins University Press, pp 27–40

  31. 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 (2016) Cross-continental migratory connectivity and spatiotemporal migratory patterns in the great reed warbler. J Avian Biol l47:1–12. doi:10.1111/jav.00929

    Google Scholar 

  32. Liechti F (2006) Birds: blowin’ by the wind? J Ornithol 147:202211

    Article  Google Scholar 

  33. Lundberg M, Boss J, Canbäck B, Liedvogel M, Larson KW, Grahn M, Åkesson S, Bensch S, Wright A (2013) Characterisation of a transcriptome to find sequence differences between two differentially migrating subspecies of the willow warbler Phylloscopus trochilus. BMC Genom 14:330. doi:10.1186/1471-2164-14-330

    CAS  Article  Google Scholar 

  34. Møller AP, Garamszegi LZ, Peralta JM, Sanchez JM, Soler JJ (2011) Migratory divides and their consequences for dispersal, population size and parasite–host interactions. J Evolution Biol 24:1744–1755. doi:10.1111/j.1420-9101.2011.02302.x

    Article  Google Scholar 

  35. 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. doi:10.1007/s10336-007-0250-1

    Article  Google Scholar 

  36. Richardson WJ (1990) Timing of bird migration in relation to weather: updated review. In: Bird migration. Springer, Berlin, pp 78–101

  37. Ruegg KC (2007) The origin and maintenance of a migratory divide in the Swainson’s Thrush (Catharus ustulatus) and its implications for speciation. Dissertation, University of California, Berkeley

  38. Salomonsen F (1955) The evolutionary significance of bird migration. Dan Biol Medd 22:6

    Google Scholar 

  39. Sultana J, Gauci C (1982) A new guide to the birds of Malta. The Ornithological Society, Valetta

    Google Scholar 

  40. Svensson L (1992) Identification Guide to European Passerines. Marstatryck, Stockholm

    Google Scholar 

  41. Tomiałojć L, Stawarczyk T (2003) The Avifauna of Poland. Distribution, numbers and trends. PTPP “pro Natura”, Wrocław (in Polish)

  42. Webster MS, Marra PP, Haig SM, Bensch S, Holmes RT (2002) Links between worlds: unraveling migratory connectivity. Trends Ecol Evol 17:2

    Article  Google Scholar 

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Acknowledgements

We appreciate the help from Jane Jönsson, Miriam Liedvogel and Evrim Sönmez in the course of completing the study.

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Correspondence to Arzu Gürsoy Ergen.

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Post-doctoral grant was supported by The Turkish Council of Higher Education (2547/10) for AGE. The study was supported by the Swedish Research Council to SB (621-2007-5193). SÅ was supported by grants from the Swedish Research Council (621-2010-5584, 621-2013-4361), and by a Linnaeus grant to the Centre for Animal Movement Research from the Swedish Research Council (349-2007-8690) and Lund University. NC was supported by the Zoological Institute of Russian Academy of Sciences (AAAA-A16-116123010004-1) and by a grant from St. Petersburg State University (1.37.149.2014).

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Communicated by M. Wink.

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Ergen, A.G., Chernetsov, N., Lundberg, M. et al. The use of molecular diagnostics to infer migration directions of Willow Warblers in the southeast Baltic. J Ornithol 158, 737–743 (2017). https://doi.org/10.1007/s10336-017-1434-y

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Keywords

  • Phylloscopus trochilus
  • AFLP
  • Avian migration
  • Migratory divide
  • Migratory direction