Abstract
The annual cycle of migrating birds is shaped by their seasonal movements between breeding and non-breeding sites. Studying how migratory populations are linked throughout the annual cycle—migratory connectivity, is crucial to understanding the population dynamics of migrating bird species. This requires the consideration not only of spatial scales as has been the main focus to date but also of temporal scales: only when both aspects are taken into account, the degree of migratory connectivity can be properly defined. We investigated the migration behaviour of hoopoes (Upupa epops) from four breeding populations across Europe and characterised migration routes to and from the breeding grounds, location of non-breeding sites and the timing of key migration events. Migration behaviour was found to vary both within and amongst populations, and even though the spatial migratory connectivity amongst the populations was weak, temporal connectivity was strong with differences in timing amongst populations, but consistent timing within populations. The combination of diverse migration routes within populations and co-occurrence on the non-breeding grounds between populations might promote exchange between breeding populations. As a result, it might make hoopoes and other migrating bird species with similar strategies more resilient to future habitat or climatic changes and stabilise population trends.
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References
Alvarado AH, Fuller TL, Smith TB (2014) Integrative tracking methods elucidate the evolutionary dynamics of a migratory divide. Ecol Evol 4:3456–3469. https://doi.org/10.1002/ece3.1205
Ambrosini R, Møller AP, Saino N (2009) A quantitative measure of migratory connectivity. J Theor Biol 257:203–211. https://doi.org/10.1016/j.jtbi.2008.11.019
Bächler E, Hahn S, Schaub M, Arlettaz R, Jenni L, Fox JW, Afanasyev V, Liechti F (2010) Year-round tracking of small trans-Saharan migrants using light-level geolocators. PLoS One 5:e9566. https://doi.org/10.1371/journal.pone.0009566
Bauer S, Lisovski S, Hahn S (2016) Timing is crucial for consequences of migratory connectivity. Oikos 125:605–612. https://doi.org/10.1111/oik.02706
Bearhop S, Fiedler W, Furness RW, Votier SC, Waldron S, Newton J, Bowen GJ, Berthold P, Farnsworth K (2005) Assortative mating as a mechanism for rapid evolution of a migratory divide. Science 310:502–504. https://doi.org/10.1126/science.1115661
Bernis F (1970) Aves migradoras ibéricas. Fascículo 6. Sociedad Española de Ornitología, Madrid
BirdLife International (2017) European birds of conservation concern: populations, trends and national responsibilities. BirdLife International, Cambridge
Blackburn E, Burgess M, Freeman B, Risely A, Izang A, Ivande S, Hewson C, Cresswell W (2017) Low and annually variable migratory connectivity in a long-distance migrant: whinchats Saxicola rubetra may show a bet-hedging strategy. Ibis (Lond 1859) 159:902–918. https://doi.org/10.1111/ibi.12509
Bötsch Y, Arlettaz R, Schaub M (2012) Breeding dispersal of Eurasian hoopoes within and between years in relation to reproductive success, sex and age. Auk 129:283–295. https://doi.org/10.1525/auk.2012.11079
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
Cohen EB, Hostetler JA, Hallworth MT, Rushing CS, Sillett TS, Marra PP (2018) Quantifying the strength of migratory connectivity. Methods Ecol Evol 9:513–524. https://doi.org/10.1111/2041-210X.12916
Cramp S, Brooks DJ, Dunn E, Gillmor R (1985) Handbook of the birds of Europe, the Middle East and North Africa. The Birds of the Western Palearctic, Vol. IV: Terns to woodpeckers. Oxford University Press, Oxford
Delmore KE, Fox JW, Irwin DE (2012) Dramatic intraspecific differences in migratory routes, stopover sites and wintering areas, revealed using light-level geolocators. Proc R Soc B Biol Sci 279:1–8. https://doi.org/10.1098/rspb.2012.1229
Dray S, Dufour AB (2007) The ade4 package: implementing the duality diagram for ecologists. J Stat Softw 22:1–20
Durrant KL, Marra PP, Fallon SM, Colbeck GJ, Gibbs HL, Hobson KA, Norris DR, Bernik B, Lloyd VL, Fleischer RC (2008) Parasite assemblages distinguish populations of a migratory passerine on its breeding grounds. J Zool 274:318–326. https://doi.org/10.1111/j.1469-7998.2007.00387.x
Finch T, Butler SJ, Franco AMA, Cresswell W (2017) Low migratory connectivity is common in long-distance migrant birds. J Anim Ecol 86:662–673. https://doi.org/10.1111/1365-2656.12635
Fraser KC, Stutchbury BJM, Silverio C, Kramer PM, Barrow J, Newstead D, Mickle N, Cousens BF, Lee JC, Morrison DM, Shaheen T, Mammenga P, Applegate K, Tautin J (2012) Continent-wide tracking to determine migratory connectivity and tropical habitat associations of a declining aerial insectivore. Proc R Soc B Biol Sci 279:4901–4906. https://doi.org/10.1098/rspb.2012.2207
Gilroy JJ, Gill JA, Butchart SHM, Jones VR, Franco AMA (2016) Migratory diversity predicts population declines in birds. Ecol Lett 19:308–317. https://doi.org/10.1111/ele.12569
Gudmundsson GA (1994) Spring migration of the knot Calidris c . canutus over southern Scandinavia, as recorded by radar. J Avian Biol 25:15–26. https://doi.org/10.2307/3677290
Hahn S, Amrhein V, Zehtindijev P, Liechti F (2013) Strong migratory connectivity and seasonally shifting isotopic niches in geographically separated populations of a long-distance migrating songbird. Oecologia 173:1217–1225. https://doi.org/10.1007/s00442-013-2726-4
Hallworth MT, Sillett TS, Van Wilgenburg SL et al (2015) Migratory connectivity of a neotropical migratory songbird revealed by archival light-level geolocators. Ecol Appl 25:336–347. https://doi.org/10.1890/14-0195.1
Harrison XA, Tregenza T, Inger R et al (2010) Cultural inheritance drives site fidelity and migratory connectivity in a long-distance migrant. Mol Ecol 19:5484–5496. https://doi.org/10.1111/j.1365-294X.2010.04852.x
Helbig AJ (1991) Inheritance of migratory direction in a bird species: a cross-breeding experiment with SE- and SW-migrating blackcaps (Sylvia atricapilla). Behav Ecol Sociobiol 28:9–12. https://doi.org/10.1007/BF00172133
Iwamura T, Possingham HP, Chadès I et al (2013) Migratory connectivity magnifies the consequences of habitat loss from sea-level rise for shorebird populations. Proc R Soc B Biol Sci 280:20130325. https://doi.org/10.1098/rspb.2013.0325
Korner-Nievergelt F, Liechti F, Hahn S (2012) Migratory connectivity derived from sparse ring reencounter data with unknown numbers of ringed birds. J Ornithol 153:771–782. https://doi.org/10.1007/s10336-011-0793-z
Kuyt E (1992) Aerial radio-tracking of whooping cranes migrating between Wood Buffalo National Park and Aransas National Wildlife Refuge, 1981–84. Can Wildl Serv 74. http://parkscanadahistory.com/wildlife/paper-74.pdf
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
Martell MS, Henny CJ, Nye PE, Solensky MJ (2001) Fall migration routes, timing and wintering sites of north American ospreys as determined by satellite telemetry. Condor 103:715–724. https://doi.org/10.1650/0010-5422(2001)103
Mellone U, Limiñana R, Mallia E, Urios V (2011) Extremely detoured migration in an inexperienced bird: interplay of transport costs and social interactions. J Avian Biol 42:468–472
Morganti M, Mellone U, Bogliani G, Saino N, Ferri A, Spina F, Rubolini D (2011) Flexible tuning of departure decisions in response to weather in black redstarts Phoenicurus ochruros migrating across the Mediterranean Sea. J Avian Biol 42:323–334. https://doi.org/10.1111/j.1600-048X.2011.05331.x
Ouwehand J, Ahola MP, Ausems ANMA, Bridge ES, Burgess M, Hahn S, Hewson CM, Klaassen RHG, Laaksonen T, Lampe HM, Velmala W, Both C (2016) Light-level geolocators reveal migratory connectivity in European populations of pied flycatchers Ficedula hypoleuca. J Avian Biol 47:69–83. https://doi.org/10.1111/jav.00721
Pagenkopp KM, Klicka J, Durrant KL, Garvin JC, Fleischer RC (2008) Geographic variation in malarial parasite lineages in the common yellowthroat (Geothlypis trichas). Conserv Genet 9:1577–1588. https://doi.org/10.1007/s10592-007-9497-6
Procházka P, Hahn S, Rolland S, van der Jeugd H, Csörgő T, Jiguet F, Mokwa T, Liechti F, Vangeluwe D, Korner-Nievergelt F (2017) Delineating large-scale migratory connectivity of reed warblers using integrated multistate models. Divers Distrib 23:27–40. https://doi.org/10.1111/ddi.12502
R Core Team (2014) R: a language and environment for statistical computing, version 3.1. R Foundation for Statistical Computing, Vienna, Austria, www.R-project.org
Reichlin TS, Schaub M, Menz MHM, Mermod M, Portner P, Arlettaz R, Jenni L (2009) Migration patterns of hoopoe Upupa epops and wryneck Jynx torquilla: an analysis of European ring recoveries. J Ornithol 150:393–400. https://doi.org/10.1007/s10336-008-0361-3
Reichlin TS, Hobson KA, Van Wilgenburg SL, Hobson KA, van Wilgenburg SL, Schaub M, Wassenaar LI, Martín-Vivaldi M, Arlettaz R, Jenni L (2013) Conservation through connectivity: can isotopic gradients in Africa reveal winter quarters of a migratory bird? Oecologia 171:591–600. https://doi.org/10.1007/s00442-012-2418-5
Rodríguez A, Alcaide M, Negro JJ, Pilard P (2011) Using major histocompatibility complex markers to assign the geographic origin of migratory birds: examples from the threatened lesser kestrel. Anim Conserv 14:306–313. https://doi.org/10.1111/j.1469-1795.2010.00431.x
von Rönn JAC, Harrod C, Bensch S, Wolf JBW (2015) Transcontinental migratory connectivity predicts parasite prevalence in breeding populations of the European barn swallow. J Evol Biol 28:535–546. https://doi.org/10.1111/jeb.12585
Ruegg KC, Smith TB (2002) Not as the crow flies: a historical explanation for circuitous migration in Swainson’s thrush (Catharus ustulatus). Proc Biol Sci 269:1375–1381. https://doi.org/10.1098/rspb.2002.2032
Rushing CS, Ryder TB, Marra PP (2016) Quantifying drivers of population dynamics for a migratory bird throughout the annual cycle. Proc Biol Sci 283:20152846. https://doi.org/10.1098/rspb.2015.2846
Schaub M, Reichlin TS, Abadi F, Kéry M, Jenni L, Arlettaz R (2012) The demographic drivers of local population dynamics in two rare migratory birds. Oecologia 168:97–108. https://doi.org/10.1007/s00442-011-2070-5
Sjöberg S, Alerstam T, Åkesson S, Schulz A, Weidauer A, Coppack T, Muheim R (2015) Weather and fuel reserves determine departure and flight decisions in passerines migrating across the Baltic Sea. Anim Behav 104:59–68. https://doi.org/10.1016/j.anbehav.2015.02.015
Trierweiler C, Klaassen RHG, Drent RH, Exo KM, Komdeur J, Bairlein F, Koks BJ (2014) Migratory connectivity and population-specific migration routes in a long-distance migratory bird. Proc Biol Sci 281:20132897. https://doi.org/10.1098/rspb.2013.2897
Wang E, Van Wijk RE, Braun MS, Wink M (2017) Gene flow and genetic drift contribute to high genetic diversity with low phylogeographical structure in European hoopoes (Upupa epops). Mol Phylogenet Evol 113:113–125. https://doi.org/10.1016/j.ympev.2017.05.018
Webster M, Marra PP (2005) The importance of understanding migratory connectivity and seasonal interactions. In: Greenberg R, Marra PP (eds) Birds of Two worlds: The Ecology and Evolution of Migration. Johns Hopkins University, Baltimore, pp 199–209
Webster MS, Marra PP, Haig SM et al (2002) Links between worlds: unraveling migratory connectivity. Trends Ecol Evol 17:76–83
van Wijk RE, Bauer S, Schaub M (2016a) Repeatability of individual migration routes, wintering sites, and timing in a long-distance migrant bird. Ecol Evol 6:8679–8685. https://doi.org/10.1002/ece3.2578
van Wijk RE, Souchay G, Jenni-Eiermann S, Bauer S, Schaub M (2016b) No detectable effects of lightweight geolocators on a Palaearctic-African long-distance migrant. J Ornithol 157:255–264. https://doi.org/10.1007/s10336-015-1274-6
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
Acknowledgments
We would like to thank the numerous people that have helped conduct the fieldwork, in particular Juan José Soler and Laura Arco in Spain, Frank Raden in Germany and Jael Hoffmann, Muriel Perron, Nico Guillod, Valentijn van Bergen, Carolyn Nabholz, Başak Şentürk, Anna Sandor, Valentina Falchi, Barbara Hildebrandt, Ángela Martínez García, Roman Bühler and Lara Moreno Zárate in Switzerland. RVW was supported by the Swiss National Science Foundation (grant number 31003A_138354). The fieldwork in Spain was supported by the European funds of the Spanish Ministry of Science and Innovation (FEDER, CGL2010-19233-C03-01, CGL2010-19233-C03-03). The Swiss Federal Office for Environment contributed financial support for the development of the geolocators (UTF-Nr. 254, 332, 363, 400), and geolocators were acquired with the financial support of “Stiftung Accentus”.
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van Wijk, R.E., Schaub, M., Hahn, S. et al. Diverse migration strategies in hoopoes (Upupa epops) lead to weak spatial but strong temporal connectivity. Sci Nat 105, 42 (2018). https://doi.org/10.1007/s00114-018-1566-9
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DOI: https://doi.org/10.1007/s00114-018-1566-9