Linking events throughout the annual cycle in a migratory bird—non-breeding period buffers accumulation of carry-over effects

  • Martins BriedisEmail author
  • Miloš Krist
  • Miroslav Král
  • Christian C. Voigt
  • Peter Adamík
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Annual cycles of animals consist of distinct life history phases linked in a unified sequence, and processes taking place in one season can influence an individual’s performance in subsequent seasons via carry-over effects. Here, using a long-distance migratory bird, the collared flycatcher Ficedula albicollis, we link events throughout the annual cycle by integrating breeding data, individual-based tracking, and stable-carbon isotopes to unravel the connections between different annual phases. To disentangle true carry-over effects from an individuals’ intrinsic quality, we experimentally manipulated the brood size of geolocator-tracked males prior to tracking. We did not find unambiguous differences in annual schedules between individuals of reduced and increased broods; however, in the following spring, the latter crossed the Sahara and arrived at the breeding grounds earlier. Individuals with higher absolute parental investment delayed their autumn migration, had shorter non-breeding residency period but advanced spring migration compared to individuals with lower breeding effort. Neither the local non-breeding conditions (as inferred from δ13C values) nor the previous breeding effort was linked to the timing of the following breeding period. Furthermore, while on migration, collared flycatchers showed a pronounced “domino effect” but it did not carry over across different migration seasons. Thus, the non-breeding period buffered further accumulation of carry-over effects from the previous breeding season and autumn migration. Our results demonstrate tight links between spatially and temporally distinct phases of the annual cycles of migrants which can have significant implications for population dynamics.

Significance statement

Timing is everything! This holds true also for migratory animals which must time their annual movements, breeding and non-breeding seasons according to the environment they live in. However, perfect timing of a particular event can be hampered by past events. We studied connections between spatially and temporarily distinct annual phases in collared flycatchers, a small bodied bird which twice a year migrates between Europe and sub-Saharan Africa. We found tight links between individual’s parental investment and timing of autumn migration, but not spring migration. Similarly, the timing of autumn migration did not translate to influence the timing of spring migration. Thus, our results demonstrate that the non-breeding period may serve as a buffer to overcome high energy expenditure during the previous breeding season and prevent further accumulation of carry-over effects in migratory birds.


Autumn migration Geolocator Phenology Spring migration Seasonal interactions Stable isotope 



We thank R. Dzuro, A. Edme, A. Höchsmannová, T. Koutný, L. Pietrement, H. Ringlová, J. Spurná, J. Stříteský, S. Vikmane, B. Vyroubalová, M. Zemánek and P. Zobač for their help in the field. S. Hahn assisted with geolocator data analyses. D. Hanley and J. Cuthbert helped with language editing and two anonymous reviewers provided helpful comments on an earlier version of the manuscript.

Funding information

This study was funded by the Czech Science Foundation (grant number: 13-06451S to PA).

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflict of interest.

Ethical approval

This study was carried out in accordance with the Ethical Committee of Palacký University and approved by the Ministry of Education, Youth and Sports of the Czech Republic (Licence number: MSMT-56147/2012-310). All applicable institutional and national guidelines for the care and use of animals were followed.

Supplementary material

265_2018_2509_MOESM1_ESM.pdf (737 kb)
ESM 1 (PDF 737 kb)


  1. Adamík P, Emmenegger T, Briedis M, Gustafsson L, Henshaw I, Krist M, Laaksonen T, Liechti F, Procházka P, Salewski V, Hahn S (2016) Barrier crossing in small avian migrants: individual tracking reveals prolonged nocturnal flights into the day as a common migratory strategy. Sci Rep 6:21560. CrossRefPubMedPubMedCentralGoogle Scholar
  2. Balbontín J, Møller AP, Hermosell IG, Marzal A, Reviriego M, de Lope F (2009) Individual responses in spring arrival date to ecological conditions during winter and migration in a migratory bird. J Anim Ecol 78:981–989. CrossRefPubMedGoogle Scholar
  3. Bauer S, Lisovski S, Hahn S (2015) Timing is crucial for consequences of migratory connectivity. Oikos 125:605–612. CrossRefGoogle Scholar
  4. Bearhop S, Hilton GM, Votier SC, Waldron S (2004) Stable isotope ratios indicate that body condition in migrating passerines is influenced by winter habitat. Proc R Soc Lond B 271:215–218. CrossRefGoogle Scholar
  5. Bogdanova MI, Daunt F, Newell M, Phillips RA, Harris MP, Wanless S (2011) Seasonal interactions in the black-legged kittiwake, Rissa tridactyla: links between breeding performance and winter distribution. Proc R Soc Lond B 278:2412–2418. CrossRefGoogle Scholar
  6. Boone AT, Rodewald PG, DeGroote LW (2010) Neotropical winter habitat of the magnolia warbler: effects on molt, energetic condition, migration timing, and hematozoan infection during spring migration. Condor 112:115–122. CrossRefGoogle Scholar
  7. Briedis M, Hahn S, Gustafsson L, Henshaw I, Träff J, Král M, Adamík P (2016) Breeding latitude leads to different temporal but not spatial organization of the annual cycle in a long-distance migrant. J Avian Biol 47:743–478. CrossRefGoogle Scholar
  8. Catry P, Dias M, Phillips R, Granadeiro J (2013) Carry-over effects from breeding modulate the annual cycle of a long-distnace migrant: an experimental demonstration. Ecology 94:1230–1235. CrossRefPubMedGoogle Scholar
  9. Cramp S, Perrins CM (1993) Handbook of the birds of Europe, the Middle East and Africa. The birds of the western Palearctic, vol. VII. Flycatchers to shrikes. Oxford University Press, Oxford, UKGoogle Scholar
  10. Drake A, Martin M, Green DJ (2014) Winter habitat use does not influence spring arrival dates or the reproductive success of yellow warblers breeding in the arctic. Polar Biol 37:181–191. CrossRefGoogle Scholar
  11. Drake A, Rock C, Quinlan SP, Green DJ (2013) Carry-over effects of winter habitat vary with age and sex in yellow warblers Setophaga petechia. J Avian Biol 44:321–330. CrossRefGoogle Scholar
  12. Fayet AL, Freeman R, Shoji A, Kirk HL, Padget O, Perrins CM, Guilford T (2016) Carry-over effects on the annual cycle of a migratory seabird: an experimental study. J Anim Ecol 85:1516–1527. CrossRefPubMedPubMedCentralGoogle Scholar
  13. Gunnarsson TG, Gill JA, Newton J, Potts PM, Sutherland WJ (2005) Seasonal matching of habitat quality and fitness in a migratory bird. Proc R Soc Lond B 272:2319–2323. CrossRefGoogle Scholar
  14. Gustafsson L, Qvarnström A, Sheldon BC (1995) Trade-offs between life-history traits and a secondary sexual character in male collared flycatchers. Nature 375:311–313. CrossRefGoogle Scholar
  15. Gustafsson L, Sutherland WJ (1988) The costs of reproduction in the collared flycatcher Ficedula albicollis. Nature 335:813–815. CrossRefGoogle Scholar
  16. Harrison XA, Blount JD, Inger R, Norris DR, Bearhop S (2011) Carry-over effects as drivers of fitness differences in animals. J Anim Ecol 80:4–18. CrossRefPubMedGoogle Scholar
  17. Hedenström A (2008) Adaptations to migration in birds: behavioural strategies, morphology and scaling effects. Phil Trans R Soc B 363:287–299. CrossRefPubMedGoogle Scholar
  18. Inger R, Harrison XA, Ruxton GD, Newton J, Colhoun K, Gudmundsson GA, McElwaine G, Pickford M, Hodgson D, Bearhop S (2010) Carry-over effects reveal reproductive costs in a long-distance migrant. J Anim Ecol 79:974–982. CrossRefPubMedGoogle Scholar
  19. Kokko H (1999) Competition for early arrival in migratory birds. J Anim Ecol 68:940–950. CrossRefGoogle Scholar
  20. Lisovski S, Hahn S (2012) GeoLight—processing and analysing light-based geolocator data in R. Methods Ecol Evol 3:1055–1059. CrossRefGoogle Scholar
  21. López-Calderón C, Hobson KA, Marzal A, Balbontín J, Reviriego M, Magallanes S, García-Longoria L, de Lope F, Møller AP (2017) Environmental conditions during winter predict age- and sex-specific differences in reproductive success of a trans-Saharan migratory bird. Sci Rep 7:18082. CrossRefPubMedPubMedCentralGoogle Scholar
  22. Low M, Arlt D, Pärt T, Öberg M (2015) Delayed timing of breeding as a cost of reproduction. J Avian Biol 46:325–331. CrossRefGoogle Scholar
  23. Marra PP, Cohen EB, Loss SR, Rutter JE, Tonra CM (2015) A call for full annual cycle research in animal ecology. Biol Lett 11:20150552. CrossRefPubMedPubMedCentralGoogle Scholar
  24. 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. CrossRefPubMedGoogle Scholar
  25. Marshall JD, Brooks JR, Lajtha K (2007) Sources of variation in the stable isotopic composition of plants. In: Michener R, Lajtha K (eds) Stable isotopes in ecology and environmental science, 2nd edn. Blackwell Publishing Ltd, Oxford, UK, pp 22–60CrossRefGoogle Scholar
  26. McNamara JM, Welham RK, Houston AI (1998) The timing of migration within the context of an annual routine. J Avian Biol 29:416–423. CrossRefGoogle Scholar
  27. Mitchell GW, Newman AEM, Wikelski M, Ryan Norris D (2012) Timing of breeding carries over to influence migratory departure in a songbird: an automated radiotracking study. J Anim Ecol 81:1024–1033. CrossRefPubMedGoogle Scholar
  28. Nakagawa S, Cuthill IC (2007) Effect size, confidence interval and statistical significance: a practical guide for biologists. Biol Rev 82:591–605. CrossRefPubMedGoogle Scholar
  29. Norris DR, Marra PP (2007) Seasonal interactions, habitat quality, and population dynamics in migratory birds. Condor 109:535–547. CrossRefGoogle Scholar
  30. Norris DR, Marra PP, Kyser TK, Sherry TW, Ratcliffe LM (2004) Tropical winter habitat limits reproductive success on the temperate breeding grounds in a migratory bird. Proc R Soc Lond B 271:59–64. CrossRefGoogle Scholar
  31. Ouwehand J, Both C (2016) Alternate non-stop migration strategies of pied flycatchers to cross the Sahara desert. Biol Lett 12:20151060. CrossRefPubMedPubMedCentralGoogle Scholar
  32. Ouwehand J, Both C (2017) African departure rather than migration speed determines variation in spring arrival in pied flycatchers. J Anim Ecol 86:88–97. CrossRefPubMedGoogle Scholar
  33. Paxton KL, Moore FR (2015) Carry-over effects of winter habitat quality on en route timing and condition of a migratory passerine during spring migration. J Avian Biol 46:495–506. CrossRefGoogle Scholar
  34. Pedersen L, Fraser KC, Kyser TK, Tøttrup AP (2016) Combining direct and indirect tracking techniques to assess the impact of sub-Saharan conditions on cross-continental songbird migration. J Ornithol 157:1037–1047. CrossRefGoogle Scholar
  35. Piersma T (1987) Hop, skip, or jump? Constraints on migration of Arctic waders by feeding, fattening, and flight speed. Limosa 60:185–194Google Scholar
  36. 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. CrossRefGoogle Scholar
  37. R Core Team (2016) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria Google Scholar
  38. Rockwell SM, Bocetti CI, Marra PP, Amenazada M (2012) Carry-over effects of winter climate on spring arrival date and reproductive success in an endangered migratory bird, Kirtland’s warbler (Setophaga kirtlandii). Auk 129:744–752. CrossRefGoogle Scholar
  39. Rosseel Y (2012) Lavaan: an R package for structural equation modelling. J Stat Softw 48:1–36CrossRefGoogle Scholar
  40. Saino N, Ambrosini R, Caprioli M, Romano A, Romano M, Rubolini D, Scandolara C, Liechti F (2017) Sex-dependent carry-over effects on timing of reproduction and fecundity of a migratory bird. J Anim Ecol 86:239–249. CrossRefPubMedGoogle Scholar
  41. Saino N, Szép T, Romano M, Rubolini D, Spina F, Møller AP (2004) Ecological conditions during winter predict arrival date at the breeding quarters in a trans-Saharan migratory bird. Ecol Lett 7:21–25. CrossRefGoogle Scholar
  42. Senner NR, Hochachka WM, Fox JW, Afanasyev V (2014) An exception to the rule: carry-over effects do not accumulate in a long-distance migratory bird. PLoS One 9:e86588. CrossRefPubMedPubMedCentralGoogle Scholar
  43. Souchay G, van Wijk RE, Schaub M, Bauer S (2018) Identifying drivers of breeding success in a long-distance migrant using structural equation modelling. Oikos 127:125–133. CrossRefGoogle Scholar
  44. Stresemann E, Stresemann V (1966) Die Mauser der Vögel. J Ornithol 107:1–448Google Scholar
  45. Studds CE, Marra PP (2005) Nonbreeding habitat occupancy and population processes: an upgrade experiment with a migratory bird. Ecology 86:2380–2385. CrossRefGoogle Scholar
  46. Studds CE, Marra PP (2007) Linking fluctuations in rainfall to nonbreeding season performance in a long-distance migratory bird, Setophaga ruticilla. Clim Res 35:115–122. CrossRefGoogle Scholar
  47. Stutchbury BJM, Gow EA, Done T, MacPherson M, Fox JW, Avanasjev V (2011) Effects of post-breeding moult and energetic condition on timing of songbird migration into the tropics. Proc R Soc Lond B 278:131–137. CrossRefGoogle Scholar
  48. Svensson L (1992) Identification guide to European passerines, 4th, revised and enlarged edn. StockholmGoogle Scholar
  49. Tonra CM, Marra PP, Holberton RL (2011) Migration phenology and winter habitat quality are related to circulating androgen in a long-distance migratory bird. J Avian Biol 42:397–404. CrossRefGoogle Scholar
  50. Vágási CI, Pap PL, Vincze O, Benkö Z, Marton A, Barta Z (2012) Haste makes waste but condition matters: molt rate-feather quality trade-off in a sedentary songbird. PLoS One 7:e40651. CrossRefPubMedPubMedCentralGoogle Scholar
  51. van Wijk RE, Schaub M, Bauer S (2017) Dependencies in the timing of activities weaken over the annual cycle in a long-distance migratory bird. Behav Ecol Sociobiol 71:73. CrossRefGoogle Scholar
  52. Vickery JA, Ewing SR, Smith KW, Pain DJ, Bairlein F, Škorpilová J, Gregory RD (2014) The decline of Afro-Palaearctic migrants and an assessment of potential causes. Ibis 156:1–22. CrossRefGoogle Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2018

Authors and Affiliations

  1. 1.Department of ZoologyPalacký UniversityOlomoucCzech Republic
  2. 2.Department of Bird Migration, Swiss Ornithological InstituteSempachSwitzerland
  3. 3.Museum of Natural HistoryOlomoucCzech Republic
  4. 4.Leibniz Institute for Zoo and Wildlife Research, Evolutionary EcologyBerlinGermany

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