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Full-year tracking suggests endogenous control of migration timing in a long-distance migratory songbird

  • Lykke Pedersen
  • Kayla Jackson
  • Kasper Thorup
  • Anders P. Tøttrup
Original Article

Abstract

Following ongoing technological advances, an increasing amount of full-year tracking data on individual migratory movements is becoming available. This opens up the opportunity to study how migration develops within individuals in consecutive years and the extent to which the migratory program is constrained. Such knowledge is essential for understanding the degree of individual flexibility during the annual cycle, which may help identifying potential bottlenecks, where the range of individual decisions is restricted. In this study, we investigate repeatability in time of a long-distance migratory songbird, the red-backed shrike Lanius collurio, tracked across consecutive years (n = 7). Furthermore, we explore the population variability and dependencies between consecutive events of departure and arrival throughout the annual cycle in this species (n = 15). We find that individuals show high repeatability in timing of departure from their two main non-breeding areas in sub-Saharan Africa. In contrast, low repeatability is found in timing of arrivals to stationary sites throughout the annual cycle. Population variation in timing of departure and arrival was similar across all events, ranging from 30 to 41 days, and was highly dependent on timing of preceding events. We conclude that timing of departures is the key event potentially controlled by the individual innate migration program, while arrivals are more flexible, likely dependent on the environmental conditions experienced en route in red-backed shrikes. Still, apparent flexibility in the individual schedule may be hampered by overall constraints of the annual cycle.

Significance statement

The annual migration schedule of migratory animals is controlled by a combination of endogenous and exogenous factors. Understanding the temporal dynamics within and between individuals across the annual cycle is important to assess to which extent the migratory schedule is constrained in time. By using full-annual cycle tracking data of individual red-backed shrikes tracked across consecutive years, we find that individuals are highly consistent in their decision to depart from their main non-breeding areas in sub-Saharan Africa, whereas arrivals are less consistent throughout the annual cycle. Overall, the migration schedule is highly constrained across the annual cycle, with each arrival and departure event being dependent on the previous event. Our results suggest that departure decision is underlying endogenous control and that little flexibility is available throughout this complex migration system.

Keywords

Repeatability Migration Endogenous control Timing Geolocator Lanius collurio 

Notes

Acknowledgments

We thank P. Ekberg, T.E. Ortvad, T.L. Petersen, P.S. Jørgensen, D. Papageorgiou, D.P. Eskildsen, R. Strandberg, R. Klaassen, Y. Vardanis, and M. Ström-Eriksson for field assistance. We thank two anonymous reviewers for valuable suggestions that helped improve this paper and S. Davidson for setting up the data in the Movebank Data Repository. We acknowledge the Aage V Jensen Foundation as well as the Danish National Research Foundation for supporting the Center for Macroecology, Evolution and Climate (Grant No. DNRF96).

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflict of interest.

Ethical approval

All procedures in this study complied with the ethical standards of Danish and Swedish authorities. Capture and sampling methods, including spring-traps, were approved by the Copenhagen Bird Ringing Center with permission from the Danish Nature Agency (J.nr. SN 302-009). In Sweden, capture methods were approved by the Swedish Ringing Center with permission from the ethical committees in Malmö/Lund (M112-09).

Supplementary material

265_2018_2553_MOESM1_ESM.docx (28.2 mb)
ESM 1 (DOCX 28904 kb)

References

  1. Alerstam T, Hake M, Kjellén N (2006) Temporal and spatial patterns of repeated migratory journeys by ospreys. Anim Behav 71:555–566.  https://doi.org/10.1016/j.anbehav.2005.05.016 CrossRefGoogle Scholar
  2. Alerstam T, Lindström Å (1990) Optimal bird migration: the relative importance of time, energy, and safety. In: Gwinner E (ed) Bird migration. Springer, Berlin, pp 331–351CrossRefGoogle Scholar
  3. Bäckman J, Andersson A, Alerstam T, Pedersen L, Sjöberg S, Thorup K, Tøttrup AP (2017a) Activity and migratory flights of individual free-flying songbirds throughout the annual cycle: method and first case study. J Avian Biol 48:309–319.  https://doi.org/10.1111/jav.01068 CrossRefGoogle Scholar
  4. Bäckman J, Andersson A, Pedersen L, Sjöberg S, Tøttrup AP, Alerstam T (2017b) Actogram analysis of free-flying migratory birds: new perspectives based on acceleration logging. J Comp Physiol A 203:543–564.  https://doi.org/10.1007/s00359-017-1165-9 CrossRefGoogle Scholar
  5. Becker PH, Zhang H (2010) Renesting of common terns Sterna hirundo in the life history perspective. J Ornithol 152:1–13.  https://doi.org/10.1007/s10336-010-0639-0 CrossRefGoogle Scholar
  6. Bell AM, Hankison SJ, Laskowski KL (2009) The repeatability of behavior: a meta-analysis. Anim Behav 77:771–783.  https://doi.org/10.1016/j.anbehav.2008.12.022 CrossRefPubMedPubMedCentralGoogle Scholar
  7. Berthold P (1996) Control of bird migration. Chapman and Hall, LondonGoogle Scholar
  8. Blackburn E, Cresswell W (2016) High winter site fidelity in a long-distance migrant: implications for wintering ecology and survival estimates. J Ornithol 157:93–108.  https://doi.org/10.1007/s10336-015-1252-z CrossRefGoogle Scholar
  9. Both C (2010) Flexibility of timing of avian migration to climate change masked by environmental constraints en route. Curr Biol 20:243–248.  https://doi.org/10.1016/j.cub.2009.11.074 CrossRefPubMedGoogle Scholar
  10. Both C, Bijlsma RG, Ouwehand J (2016) Repeatability in spring arrival dates in pied flycatchers varies among years and sexes. Ardea 104:3–21.  https://doi.org/10.5253/arde.v104i1.a1 CrossRefGoogle Scholar
  11. 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 47:743–748.  https://doi.org/10.1111/jav.01002 CrossRefGoogle Scholar
  12. Bruderer B (2007) Notes on the moult of red-backed shrikes (Lanius collurio) in their non-breeding range. J Ornithol 148:557–561.  https://doi.org/10.1007/s10336-007-0190-9 CrossRefGoogle Scholar
  13. Buehler DM, Piersma T (2008) Travelling on a budget: predictions and ecological evidence for bottlenecks in the annual cycle of long-distance migrants. Phil Trans R Soc B 363:247–266.  https://doi.org/10.1098/rstb.2007.2138 CrossRefPubMedGoogle Scholar
  14. Catry P, Encarnação V, Araújo A, Fearon P, Fearon A, Armelin M, Delaloye P (2004) Are long-distance migrant passerines faithful to their stopover sites? J Avian Biol 35:170–181.  https://doi.org/10.1111/j.0908-8857.2004.03112.x CrossRefGoogle Scholar
  15. Conklin JR, Battley PF (2012) Carry-over effects and compensation: late arrival on non-breeding grounds affects wing moult but not plumage or schedules of departing bar-tailed godwits Limosa lapponica baueri. J Avian Biol 43:252–263.  https://doi.org/10.1111/j.1600-048X.2012.05606.x CrossRefGoogle Scholar
  16. Conklin JR, Battley PF, Potter MA (2013) Absolute consistency: individual versus population variation in annual-cycle schedules of a long-distance migrant bird. PLoS One 8:e54535.  https://doi.org/10.1371/journal.pone.0054535 CrossRefPubMedPubMedCentralGoogle Scholar
  17. Core Team R (2017) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria http://www.R-project.org Google Scholar
  18. Cresswell W (2014) Migratory connectivity of Palaearctic-African migratory birds and their responses to environmental change: the serial residency hypothesis. Ibis 156:493–510.  https://doi.org/10.1111/ibi.12168 CrossRefGoogle Scholar
  19. Fudickar AM, Wikelski M, Partecke J (2012) Tracking migratory songbirds: accuracy of light-level loggers (geolocators) in forest habitats. Methods Ecol Evol 3:47–52.  https://doi.org/10.1111/j.2041-210X.2011.00136.x CrossRefGoogle Scholar
  20. Greenwood PJ (1980) Mating systems, philopatry and dispersal in birds and mammals. Anim Behav 28:1140–1162.  https://doi.org/10.1016/S0003-3472(80)80103-5 CrossRefGoogle Scholar
  21. Greenwood PJ, Harvey PH (1982) The natal and breeding dispersal of birds. Annu Rev Ecol Syst 13:1–21.  https://doi.org/10.1146/annurev.es.13.110182.000245 CrossRefGoogle Scholar
  22. Guilford T, Freeman R, Boyle D, Dean B, Kirk H, Phillips R, Perrins C (2011) A dispersive migration in the Atlantic puffin and its implications for migratory navigation. PLoS One 6:e21336.  https://doi.org/10.1371/journal.pone.0021336 CrossRefPubMedPubMedCentralGoogle Scholar
  23. Gwinner E, Biebach H (1977) Endogene Kontrolle der Mauser und der Zugdisposition bei südfinnischen und südfranzösischen Neuntötern (Lanius collurio). Vogelwarte 29:56–63Google Scholar
  24. Hake M, Kjellén N, Alerstam T (2003) Age-dependent migration strategy in honey buzzards Pernis apivorus tracked by satellite. Oikos 103:385–396.  https://doi.org/10.1034/j.1600-0706.2003.12145.x CrossRefGoogle Scholar
  25. Hasselquist D, Montràs-Janer T, Tarka M, Hansson B (2017) 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 48:91–102.  https://doi.org/10.1111/jav.01292 CrossRefGoogle Scholar
  26. Hijmans RJ (2016) Geosphere: spherical trigonometry, http://cran.r-project.org/package=geosphere
  27. Knudsen E, Lindén A, Both C, Jonzén N, Pulido F, Saino N, Sutherland WJ, Bach LA, Coppack T, Ergon T, Gienapp P, Gill JA, Gordo O, Hedenström A, Lehikoinen E, Marra PP, Møller AP, Nilsson ALK, Péron G, Ranta E, Rubolini D, Sparks TH, Spina F, Studds CE, Saether SA, Tryjanowski P, Stenseth NC (2011) Challenging claims in the study of migratory birds and climate change. Biol Rev 86:928–946.  https://doi.org/10.1111/j.1469-185X.2011.00179.x CrossRefPubMedGoogle Scholar
  28. Kokko H (1999) Competition for early arrival birds in migratory birds. J Anim Ecol 68:940–950.  https://doi.org/10.1046/j.1365-2656.1999.00343.x CrossRefGoogle Scholar
  29. Lemon J (2006) Plotrix: a package in the red light district of R. R-News 6:8–12Google Scholar
  30. Lessells C, Boag PT (1987) Unrepeatable repeatabilities: a common mistake. Auk 104:116–121CrossRefGoogle Scholar
  31. Lindström Å, Alerstam T, Bahlenberg P, Ekblom R, Fox JW, Råghall J, Klaassen RHG (2016) The migration of the great snipe Gallinago media: intriguing variations on a grand theme. J Avian Biol 47:321–334.  https://doi.org/10.1111/jav.00829 CrossRefGoogle Scholar
  32. Lisovski S, Hahn S (2012) GeoLight—processing and analysing light-based geolocator data in R. Methods Ecol Evol 3:1055–1059.  https://doi.org/10.1111/j.2041-210X.2012.00248.x CrossRefGoogle Scholar
  33. Lisovski S, Hewson CM, Klaassen RHG, Korner-Nievergelt F, Kristensen MW, Hahn S (2012) Geolocation by light: accuracy and precision affected by environmental factors. Methods Ecol Evol 3:603–612.  https://doi.org/10.1111/j.2041-210X.2012.00185.x CrossRefGoogle Scholar
  34. Mckinnon EA, Fraser KC, Stutchbury BJ (2013) New discoveries in landbird migration using geolocators, and a flight plan for the future. Auk 130:211–222.  https://doi.org/10.1525/auk.2013.130.2.12226 CrossRefGoogle Scholar
  35. McNamara JM, Welham RK, Houston AI (1998) The timing of migration within the context of an annual routine. J Avian Biol 29:416–423.  https://doi.org/10.2307/3677160 CrossRefGoogle Scholar
  36. Naef-Daenzer B (2007) An allometric function to fit leg-loop harnesses to terrestrial birds. J Avian Biol 38:404–407.  https://doi.org/10.1111/j.2007.0908-8857.03863.x CrossRefGoogle Scholar
  37. Nakagawa S, Schielzeth H (2010) Repeatability for Gaussian and non-Gaussian data: a practical guide for biologists. Biol Rev 85:935–956.  https://doi.org/10.1111/j.1469-185X.2010.00141.x PubMedCrossRefGoogle Scholar
  38. Newton I (2008) The migration ecology of birds. Elsevier-Academic Press, AmsterdamGoogle Scholar
  39. Nichols JD, Reinecke KJ, Hines JE (1983) Factors affecting the distribution of mallards wintering in the Mississippi. Auk 100:932–946Google Scholar
  40. Norevik G, Åkesson S, Hedenström A (2017) Migration strategies and annual space-use in an Afro-Palaearctic aerial insectivore—the European nightjar Caprimulgus europaeus. J Avian Biol 48:738–747.  https://doi.org/10.1111/jav.01071 CrossRefGoogle Scholar
  41. Pedersen L, Jackson K, Thorup K, Tøttrup AP (2018) Data from: Full-year tracking suggests endogenous control of migration timing in a long-distance migratory songbird. Movebank Data Repository.  https://doi.org/10.5441/001/1.7mf48770
  42. Pennisi E (2011) Global tracking of small animals gains momentum. Science 334:1042–1042.  https://doi.org/10.1126/science.334.6059.1042 CrossRefPubMedGoogle Scholar
  43. Phillips RA, Silk JR, Croxall JP, Afanasyev V, Bennett VJ (2005) Summer distribution and migration of nonbreeding albatrosses: individual consistencies and implications for conservation. Ecology 86:2386–2396.  https://doi.org/10.1890/04-1885 CrossRefGoogle Scholar
  44. Richardson JW (1978) Timing and amount of bird migration in relation to weather: a review. Oikos 30:224–272.  https://doi.org/10.2307/3543482 CrossRefGoogle Scholar
  45. Richardson JW (1990) Timing of bird migration in relation to weather: updated review. In: Gwinner E (ed) Bird migration: physiology and ecophysiology. Springer Verlag, Berlin, pp 78–101CrossRefGoogle Scholar
  46. Robinson WD, Bowlin MS, Bisson I, Shamoun-Baranes J, Thorup K, Diehl RH, Kunz TH, Mabey S, Winkler DW (2010) Integrating concepts and technologies to advance the study of bird migration. Front Ecol Environ 8:354–361.  https://doi.org/10.1890/080179 CrossRefGoogle Scholar
  47. Sæther B-E (1989) Survival rates in relation to body weight in European birds. Ornis Scand 20:13–21.  https://doi.org/10.2307/3676702 CrossRefGoogle Scholar
  48. 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.  https://doi.org/10.1371/journal.pone.0086588 CrossRefPubMedPubMedCentralGoogle Scholar
  49. Snow D, Perrins C (1998) The birds of the Western Palearctic, 2nd edn. Oxford University Press, New YorkGoogle Scholar
  50. Sokolov LV, Markovets MY, Morozov YG (1999) Long-term dynamics of the mean date of autumn migration in passerines on the Courish Spit of the Baltic Sea. Proc biol Stn “Rybachy” 2:1–18Google Scholar
  51. Stanley CQ, MacPherson M, Fraser KC, McKinnon EA, Stutchbury BJM (2012) Repeat tracking of individual songbirds reveals consistent migration timing but flexibility in route. PLoS One 7:e40688.  https://doi.org/10.1371/journal.pone.0040688 CrossRefPubMedPubMedCentralGoogle Scholar
  52. Stoffel MA, Nakagawa S, Schielzeth H (2017) rptR: repeatability estimation and variance decomposition by generalized linear mixed-effects models. Methods Ecol Evol 8:1639–1644.  https://doi.org/10.1111/2041-210X.12797 CrossRefGoogle Scholar
  53. Stutchbury BJM, Tarof SA, Done T, Gow E, Kramer PM, Tautin J, Fox JW, Afanasyev V (2009) Tracking long-distance songbird migration by using geolocators. Science 323:896.  https://doi.org/10.1126/science.1166664 CrossRefPubMedGoogle Scholar
  54. Tarka M, Hansson B, Hasselquist D (2015) Selection and evolutionary potential of spring arrival phenology in males and females of a migratory songbird. J Evol Biol 28:1024–1038.  https://doi.org/10.1111/jeb.12638 CrossRefPubMedGoogle Scholar
  55. Thorup K, Bisson I-A, Bowlin MS, Holland RA, Wingfield JC, Ramenofsky M, Wikelski M (2007) Evidence for a navigational map stretching across the continental U.S. in a migratory songbird. P Natl Acad Sci USA 104:18115–18119.  https://doi.org/10.1073/pnas.0704734104 CrossRefGoogle Scholar
  56. Thorup K, Tøttrup AP, Willemoes M, Klaassen RHG, Strandberg R, Vega ML, Dasari HP, Araújo MB, Wikelski M, Rahbek C (2017) Resource tracking within and across continents in long-distance bird migrants. Sci Adv 3:e1601360.  https://doi.org/10.1126/sciadv.1601360 CrossRefPubMedPubMedCentralGoogle Scholar
  57. Thorup K, Vardanis Y, Tøttrup AP, Kristensen MW, Alerstam T (2013) Timing of songbird migration: individual consistency within and between seasons. J Avian Biol 44:486–494.  https://doi.org/10.1111/j.1600-048X.2013.05871.x CrossRefGoogle Scholar
  58. Tøttrup AP, Klaassen R, Strandberg R, Thorup K, Kristensen MW, Jørgensen PS, Fox J, Afanasyev V, Rahbek C, Alerstam T (2012) The annual cycle of a trans-equatorial Eurasian–African passerine migrant: different spatio-temporal strategies for autumn and spring migration. Proc R Soc Lond B 279:1008–1016.  https://doi.org/10.1098/rspb.2011.1323 CrossRefGoogle Scholar
  59. Tøttrup AP, Pedersen L, Onrubia A, Klaassen RHG, Thorup K (2017) Migration of red-backed shrikes from the Iberian Peninsula: optimal or sub-optimal detour? J Avian Biol 48:149–154.  https://doi.org/10.1111/jav.01352 CrossRefGoogle Scholar
  60. van Noordwijk AJ, Pulido F, Helm B, Coppack T, Delingat J, Dingle H, Hedenström A, van der Jeugd H, Marchetti C, Nilsson A, Pérez-Tris J (2006) A framework for the study of genetic variation in migratory behaviour. J Ornithol 147:221–233.  https://doi.org/10.1007/s10336-005-0047-z CrossRefGoogle Scholar
  61. van Wijk RE, Schaub M, Bauer S (2016) Dependencies in the timing of activities weaken over the annual cycle in a long-distance migratory bird. Behav Ecol Sociobiol 71:73.  https://doi.org/10.1007/s00265-017-2305-5 CrossRefGoogle Scholar
  62. Vardanis Y, Klaassen RHG, Strandberg R, Alerstam T (2011) Individuality in bird migration: routes and timing. Biol Lett 7:502–505.  https://doi.org/10.1098/rsbl.2010.1180 CrossRefPubMedPubMedCentralGoogle Scholar
  63. Vardanis Y, Nilsson JÅ, Klaassen RHG, Strandberg R, Alerstam T (2016) Consistency in long-distance bird migration: contrasting patterns in time and space for two raptors. Anim Behav 113:177–187.  https://doi.org/10.1016/j.anbehav.2015.12.014 CrossRefGoogle Scholar
  64. Vavrek MJ (2011) Fossil: palaeoecological and paelaeogeogrpahical analysis tools. Palaeontol Electron 14:1–16Google Scholar
  65. Warkentin IG, Hernández D (1996) The conservation implications of site fidelity: a case study involving nearctic-neotropical migrant songbirds wintering in a Costa Rican mangrove. Biol Conserv 77:143–150.  https://doi.org/10.1016/0006-3207(95)00146-8 CrossRefGoogle Scholar
  66. Wikelski M, Kays RW, Kasdin NJ, Thorup K, Smith JA, Swenson GW (2007) Going wild: what a global small-animal tracking system could do for experimental biologists. J Exp Biol 210:181–186.  https://doi.org/10.1242/jeb.02629 CrossRefPubMedGoogle Scholar
  67. Wolak ME, Fairbairn DJ, Paulsen YR (2012) Guidelines for estimating repeatability. Methods Ecol Evol 3:129–137.  https://doi.org/10.1111/j.2041-210X.2011.00125.x CrossRefGoogle Scholar
  68. Wotherspoon S, Sumner M, Lisovski S (2016) BAStag: basic data processing for British Antarctic Survey archival tags, https://github.com/SWotherspoon/BAStag
  69. Yamamoto T, Takahashi A, Sato K, Oka N, Yamamoto M, Trathan PN (2014) Individual consistency in migratory behaviour of a pelagic seabird. Behaviour 151:683–701.  https://doi.org/10.1163/1568539X-00003163 CrossRefGoogle Scholar

Copyright information

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

Authors and Affiliations

  1. 1.Center for Macroecology, Evolution and Climate, Natural History Museum of DenmarkUniversity of CopenhagenCopenhagenDenmark
  2. 2.Department of Fisheries and WildlifeOregon State UniversityCorvallisUSA

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