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Compensation for wind drift during raptor migration improves with age through mortality selection

Abstract

Each year, billions of flying and swimming migrants negotiate the challenging displacement imposed by travelling through a flowing medium. However, little is known about how the ability to cope with drift improves through life and what mechanisms drive its development. We examined 3,140 days of migration by 90 GPS-tagged raptorial black kites (Milvus migrans) aged 1–27 years to show that the ability to compensate for lateral drift develops gradually through many more years than previously appreciated. Drift negotiation was under strong selective pressure, with inferior navigators subject to increased mortality. This progressively selected for adults able to compensate for current cross flows and for previously accumulated drift in a flexible, context-dependent and risk-dependent manner. Displacements accumulated en route carried over to shape the wintering distribution of the population. For many migrants, migratory journeys by younger individuals represent concentrated episodes of trait selection that shape adult populations and mediate their adaptation to climate change.

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Fig. 1: Strategies of drift negotiation by migrating black kites.
Fig. 2: Age-dependent drift changed by geographic area and with wind direction in the pre-breeding migration.
Fig. 3: Migrating black kites strategically interrupted and restarted their journeys on the basis of wind conditions and local food availability, as estimated by ecosystem productivity (NDVI).
Fig. 4: Individual improvements in wind-negotiation capabilities by migrating black kites and their mortality consequences.

Data availability

Data are available from DIGITAL.CSIC at https://doi.org/10.20350/digitalCSIC/14652.

References

  1. Newton, I. The Migration Ecology of Birds (Academic Press, 2008).

  2. Dingle, H. Migration: The Biology of Life on the Move (Oxford Univ. Press, 1996).

  3. Chapman, J. W. et al. Animal orientation strategies for movement in flows. Curr. Biol. 21, R861–R870 (2011).

    CAS  PubMed  Google Scholar 

  4. Alerstam, T. Wind as a selective agent in bird migration. Ornis Scand. 10, 76–93 (1979).

    Google Scholar 

  5. Berthold, P. Bird Migration: A General Survey (Oxford Univ. Press, 2001).

  6. Alerstam, T. & Lindstrom, A. in Bird Migration: Physiology and Ecophysiology (ed. Gwinner, E.) 331–351 (Springer, 1990).

  7. Chapman, J. W. et al. Wind selection and drift compensation optimize migratory pathways in a high-flying moth. Curr. Biol. 18, 514–518 (2008).

    CAS  PubMed  Google Scholar 

  8. Hays, G. C. et al. Route optimisation and solving Zermelo’s navigation problem during long distance migration in cross flows. Ecol. Lett. 17, 137–143 (2014).

    PubMed  Google Scholar 

  9. Chapman, J. W. et al. Adaptive strategies in nocturnally migrating insects and songbirds: contrasting responses to wind. J. Anim. Ecol. 85, 115–124 (2016).

    PubMed  Google Scholar 

  10. Alerstam, T. Optimal bird migration revisited. J. Ornithol. 152, 5–23 (2011).

    Google Scholar 

  11. Alerstam, T. & Hedenström, A. The development of bird migration theory. J. Avian Biol. 29, 343–369 (1998).

    Google Scholar 

  12. Shamoun, J., Felix, B. & Wouter, L. Atmospheric conditions create freeways, detours and tailbacks for migrating birds. J. Comp. Physiol. A 203, 509–529 (2017).

    Google Scholar 

  13. Liechti, F. Birds: Blowin’ by the wind? J. Ornithol. 147, 202–211 (2006).

    Google Scholar 

  14. Thorup, K., Alerstam, T., Hake, M. & Kjellén, N. Bird orientation: compensation for wind drift in migrating raptors is age dependent. Proc. R. Soc. B 270, 8–11 (2003).

    Google Scholar 

  15. Sergio, F. et al. Migration by breeders and floaters of a long-lived raptor: implications for recruitment and territory quality. Anim. Behav. 131, 59–72 (2017).

    Google Scholar 

  16. Sergio, F. et al. Individual improvements and selective mortality shape lifelong migratory performance. Nature 515, 410–413 (2014).

    CAS  PubMed  Google Scholar 

  17. Sergio, F., Blas, J. & Hiraldo, F. Predictors of floater status in a long-lived bird: a cross-sectional and longitudinal test of hypotheses. J. Anim. Ecol. 78, 109–118 (2009).

    PubMed  Google Scholar 

  18. Bildstein, K. L. Migrating Raptors of the World: Their Ecology and Conservation (Cornell Univ. Press, 2006).

  19. Zalles, J. I. & Bildstein, K. L. Raptor Watch: A Global Directory of Raptor Migration Sites (Birdlife International, 2000).

  20. Kerlinger, P. Flight Strategies of Migrating Hawks (University of Chicago Press, 1989).

  21. Sergio, F. et al. When and where mortality occurs throughout the annual cycle changes with age in a migratory bird: individual vs population implications. Sci. Rep. 9, 17352 (2019).

    PubMed  PubMed Central  Google Scholar 

  22. Sergio, F. et al. Raptor nest decorations are a reliable threat against conspecifics. Science 331, 327–330 (2011).

    CAS  PubMed  Google Scholar 

  23. Parker, D. & Diop-Kane, M. Meteorology of Tropical West Africa: The Forecaster’s Handbook (2017).

  24. Liechti, F., Hedenström, A. & Alerstam, T. Effects of sidewinds on optimal flight speed of birds. J. Theor. Biol. 170, 219–225 (1994).

    Google Scholar 

  25. Liechti, F. & Bruderer, B. The relevance of wind for optimal migration theory. J. Avian Biol. 29, 561–568 (1998).

    Google Scholar 

  26. Cresswell, W. Migratory connectivity of Palaearctic–African migratory birds and their responses to environmental change: the serial residency hypothesis. Ibis 156, 493–510 (2014).

    Google Scholar 

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

    Google Scholar 

  28. Bowlin, M. S. et al. Grand challenges in migration biology. Integr. Comp. Biol. 50, 261–279 (2010).

    PubMed  Google Scholar 

  29. Mitchell, G. W., Woodworth, B. K., Taylor, P. D. & Norris, D. R. Automated telemetry reveals age specific differences in flight duration and speed are driven by wind conditions in a migratory songbird. Mov. Ecol. https://doi.org/10.1186/s40462-015-0046-5 (2015).

  30. Rotics, S. et al. The challenges of the first migration: movement and behaviour of juvenile vs. adult white storks with insights regarding juvenile mortality. J. Anim. Ecol. 85, 938–947 (2016).

  31. Horvitz, N. et al. The gliding speed of migrating birds: slow and safe or fast and risky? Ecol. Lett. 17, 670–679 (2014).

    PubMed  Google Scholar 

  32. Reichler, T. Changes in the Atmospheric Circulation as Indicator of Climate Change (Elsevier, 2009).

  33. Kling, M. M. & Ackerly, D. D. Global wind patterns and the vulnerability of wind-dispersed species to climate change. Nat. Clim. Change 10, 868–875 (2020).

    Google Scholar 

  34. Drake, A., Rock, C. A., Quinlan, S. P., Martin, M. & Green, D. J. Wind speed during migration influences the survival, timing of breeding, and productivity of a neotropical migrant, Setophaga petechia. PLoS ONE 9, e97152 (2014).

    PubMed  PubMed Central  Google Scholar 

  35. Newton, I. Can conditions experienced during migration limit the population levels of birds? J. Ornithol. 147, 146–166 (2006).

    Google Scholar 

  36. Loonstra, A. H. J., Verhoeven, M. A., Senner, N. R., Both, C. & Piersma, T. Adverse wind conditions during northward Sahara crossings increase the in-flight mortality of black-tailed godwits. Ecol. Lett. 22, 2060–2066 (2019).

    PubMed  PubMed Central  Google Scholar 

  37. Blas, J., Sergio, F. & Hiraldo, F. Age-related improvement in reproductive performance in a long-lived raptor: a cross-sectional and longitudinal study. Ecography 32, 647–657 (2009).

    Google Scholar 

  38. Sergio, F. et al. No effect of satellite tagging on survival, recruitment, longevity, productivity and social dominance of a raptor, and the provisioning and condition of its offspring. J. Appl. Ecol. 52, 1665–1675 (2015).

    Google Scholar 

  39. Kenward, R. A Manual for Wildlife Radio Tagging (Academic Press, 2001).

  40. Hersbach, H., et al. ERA5 hourly data on pressure levels from 1979 to present. Copernicus Climate Change Service Climate Data Store https://doi.org/10.24381/cds.bd0915c6 (2018).

  41. Klaassen, R. H. G., Hake, M., Strandberg, R. & Alerstam, T. Geographical and temporal flexibility in the response to crosswinds by migrating raptors. Proc. R. Soc. B 278, 1339–1346 (2011).

    PubMed  Google Scholar 

  42. Bohrer, G. et al. Estimating updraft velocity components over large spatial scales: contrasting migration strategies of golden eagles and turkey vultures. Ecol. Lett. 15, 96–103 (2012).

    PubMed  Google Scholar 

  43. Shannon, H. D., Young, G. S., Yates, M. A., Fuller, M. R. & Seegar, W. S. Measurements of thermal updraft intensity over complex terrain using American white pelicans and a simple boundary-layer forecast model. Bound. Layer Meteorol. 104, 167–199 (2002).

    Google Scholar 

  44. Stull, R. B. An Introduction to Boundary Layer Meteorology (Springer, 1988).

  45. Safi, K. et al. Flying with the wind: scale dependency of speed and direction measurements in modelling wind support in avian flight. Mov. Ecol. 1, 1–13 (2013).

    Google Scholar 

  46. Batschelet, E. Circular Statistics in Biology (Academic Press, 1981).

  47. R Core Team. R: A Language and Environment for Statistical Computing (R Foundation for Statistical Computing, 2019).

  48. O’Neill, P. Magnetoreception and baroreception in birds. Dev. Growth Differ. 55, 188–197 (2013).

    PubMed  Google Scholar 

  49. Bingman, V.P. and Moore, P. in Aeroecology (eds. Chilson, P. B. et al.) 119–143 (Springer International Publishing, 2017).

  50. Liechti, F. and McGuire, L. P. in Aeroecology (eds. Chilson, P. B. et al.) 179–198 (Springer International Publishing, 2017).

  51. Richardson, W. J. Wind and orientation of migrating birds: a review. EXS 60, 226–249 (1991).

    CAS  PubMed  Google Scholar 

  52. Pettorelli, N. et al. Using the satellite-derived NDVI to assess ecological responses to environmental change. Trends Ecol. Evol. 20, 503–510 (2005).

    PubMed  Google Scholar 

  53. Dodge, S. et al. Environmental drivers of variability in the movement ecology of turkey vultures (Cathartes aura) in North and South America. Philos. Trans. R. Soc. B 369, 20130195 (2014).

    Google Scholar 

  54. Schaub, M., Kania, W. & Köppen, U. Variation of primary production during winter induces synchrony in survival rates in migratory white storks Ciconia ciconia. J. Anim. Ecol. 74, 656–666 (2005).

    Google Scholar 

  55. Despland, E., Rosenberg, J. & Simpson, S. J. Landscape structure and locust swarming: a satellite’s eye view. Ecography 27, 381–391 (2004).

    Google Scholar 

  56. Trierweiler, C. et al. A Palaearctic migratory raptor species tracks shifting prey availability within its wintering range in the Sahel. J. Anim. Ecol. 82, 107–120 (2013).

    PubMed  Google Scholar 

  57. Zuur, A. F., Ieno, E. N., Walker, N. J., Saveliev, A. A. & Smith, G. M. Mixed Effects Models and Extensions in Ecology with R (Springer, 2009).

  58. Sapir, N., Horvitz, N., Dechmann, D. K. N., Fahr, J. & Wikelski, M. Commuting fruit bats beneficially modulate their flight in relation to wind. Proc. R. Soc. B 281, 20140018 (2014).

    PubMed  PubMed Central  Google Scholar 

  59. Becciu, P., Panuccio, M., Catoni, C., Dell'omo, G. & Sapir, N. Contrasting aspects of tailwinds and asymmetrical response to crosswinds in soaring migrants. Behav. Ecol. Sociobiol. 72, 28 (2018).

    Google Scholar 

  60. Klaassen, R. H. G. et al. Loop migration in adult marsh harriers Circus aeruginosus, as revealed by satellite telemetry. J. Avian Biol. 41, 200–207 (2010).

    Google Scholar 

  61. Strandberg, R., Klaassen, R. H. G., Hake, M. & Alerstam, T. How hazardous is the Sahara Desert crossing for migratory birds? Indications from satellite tracking of raptors. Biol. Lett. 6, 297–300 (2010).

    PubMed  Google Scholar 

  62. Pennycuick, D. J. Modelling the Flying Bird (Academic Press, 2008).

  63. Shepard, E. L. C., Ross, A. N. & Portugal, S. J. Moving in a moving medium: new perspectives on flight. Phil. Trans. R. Soc. B 371, 20150382 (2016).

    PubMed  PubMed Central  Google Scholar 

  64. Van Doren, B. M., Horton, K. G., Stepanian, P. M., Mizrahi, D. S. & Farnsworth, A. Wind drift explains the reoriented morning flights of songbirds. Behav. Ecol. 27, 1122–1131 (2016).

    Google Scholar 

  65. Sergio, F., Tanferna, A., Blas, J., Blanco, G. & Hiraldo, F. Reliable methods for identifying animal deaths in GPS- and satellite-tracking data: review, testing, and calibration. J. Appl. Ecol. 56, 562–572 (2019).

    Google Scholar 

  66. Crawley, M. J. The R Book (Wiley, 2013).

  67. Nakagawa, S. & Schielzeth, H. A general and simple method for obtaining R2 from generalized linear mixed-effects models. Methods Ecol. Evol. 4, 133–142 (2013).

    Google Scholar 

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Acknowledgements

We thank F.J. Chicano, F.G. Vilches, J.M. Giralt and M. Anjos for help in the field, I. Afán and D. Aragonés of LAST–EBD for support with GIS analyses, the personnel of the Reserva Biológica de Doñana–ICTS for logistical help and accommodation, E. Palazuelos for preparing Supplementary Video 1 and F.J. Hernández for the kite drawing in Fig. 1. Part of the study was funded by Natural Research Ltd. and research projects CGL2008-01781 (F.S.), CGL2011-28103 (F.S.), CGL2012-32544 (J.B.) and PGC2018-095860-B-I00 (F.S.) of the Spanish Ministry of Science and Innovation/Economy and Competitiveness and FEDER funds; 511/2012 (J.B.) of the Spanish Ministry of Agriculture, Food and the Environment (Autonomous Organism of National Parks); JA-58 (F.S.) of the Consejería de Medio Ambiente de la Junta de Andalucía and by the Excellence Projects RNM 1790 (F.S.), RNM 3822 (F.S.), RNM 7307 (F.S.) and P18-FR-4239 (F.S.) of the Junta de Andalucía. J.M.B was supported by Generalitat Valenciana (CIDEGENT/2020/030).

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F.S., A.T., J.B. and F.H. conducted fieldwork. F.S., A.T. and J.M.B. prepared the database, extracted and processed the environmental data from internet sources and analysed the data. F.S., J.B. and F.H. obtained funding. F.S., J.M.B, A.T., R.S., J.B. and F.H. took part in the conceptual planning of the study and in the preparation of the manuscript.

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Correspondence to Fabrizio Sergio.

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Nature Ecology & Evolution thanks Jason Chapman, Will Cresswell and two other, anonymous, reviewers for their contribution to the peer review of this work.

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Supplementary Figs. 1–7 and Tables 1–6.

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Supplementary Video 1.

Flow negotiation strategies by migrants. Conceptual representation of crosswind negotiation strategies by migrating raptors; by orienting their heading progressively more towards a lateral crosswind, migrants can compensate progressively more for the drift imposed by the side flow. The outcome of such orientation strategies can range from full drift to partial compensation or full compensation.

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Sergio, F., Barbosa, J.M., Tanferna, A. et al. Compensation for wind drift during raptor migration improves with age through mortality selection. Nat Ecol Evol 6, 989–997 (2022). https://doi.org/10.1038/s41559-022-01776-1

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