Abstract
Climate change is causing phenological shifts in the environment. Among birds, increasing temperatures have been shown to advance the spring migration and breeding, which in turn affect individual reproductive success. The autumn migration phenology has, however, been largely overlooked. Here, we study long-term changes in the timing of autumn migration in 15 northern European waterfowl species during 1979–2009. We hypothesised that waterfowl should delay their migration since they winter north of the Sahara desert. Our results show that 6 (Greylag Goose Anser anser, Eurasian Wigeon Anas penelope, Eurasian Teal Anas crecca, Tufted Duck Aythya fuligula, Velvet Scoter Melanitta fusca, and Common Goldeneye Bucephala clangula) of the 15 studied species have delayed at least one of the three phases of migration examined. The most marked delay in median migration dates was by more than a month over the past 31 years. Only the Bean Goose Anser fabalis exhibited an advanced beginning of its migration. We also analyse the timing of the entire waterfowl migration and show that the median and end of the migration have been significantly delayed. The results support our predictions and highlight how rapid phenological responses to climate change may be. Such delayed departures may be the cause for recently observed northward shifts of wintering ducks. Our results suggest that waterfowl to be a good indicator group for climate change. Changing migration times can also have population-level consequences due to differential hunting and natural predation pressures over the waterfowl flyway.
Zusammenfassung
Verzögerter Herbstzug bei nordeuropäischen Wasservögeln
Klimaänderungen bewirken phänologische Verschiebungen in der Umwelt. Für Vögel konnte gezeigt werden, dass ein Anstieg der Temperatur den Frühjahrszug und Brutbeginn vorverlegt, was wiederum den individuellen Bruterfolg beeinflusst. Der zeitliche Ablauf des Herbstzuges ist jedoch bisher weitgehend unbeachtet geblieben. In dieser Arbeit untersuchen wir die Langzeitänderungen in Beginn und Ende des Herbstzuges von 15 nordeuropäischen Wasservögel-Arten in den Jahren 1979 bis 2009. Wir stellten die Hypothese auf, dass Wasservögel ihren Zug hinauszögern würden, weil sie nördlich der Sahara überwintern. Unsere Ergebnisse zeigten, dass sechs (Graugans Anser anser, Pfeifente Anas penelope, Krickente Anas crecca, Reiherente Aythya fuligula, Samtente Melanitta fusca, Schellente Bucephala clangula) der 15 untersuchten Arten wenigstens eine der drei untersuchten Zug-Phasen hinauszögerten. Die auffälligste Verzögerung der mittleren Zugtermine betrug mehr als einen Monat über die vergangenen 31 Jahre. Einzig die Saatgänse Anser fabalis zeigten einen vorgezogenen Zugbeginn. Wir untersuchten auch den Zeitablauf des gesamten Wasservögel-Zugs und können zeigen, dass das Zug-Mittel und das Zug-Ende signifikant verzögert sind. Diese Ergebnisse unterstützen unsere Vorhersage und unterstreichen, wie rasch phänologische Änderungen als Folge von Klimaänderungen auftreten können. Die verzögerten Zug-Beginne sind möglicherweise auch die Ursache der kürzlich beobachteten Nordverschiebungen überwinternder Enten. Unsere Ergebnisse legen nahe, dass Wasservögel gute Indikatoren für Klimaänderungen sind. Die Veränderungen in den Zug-Zeiten haben möglicherweise auch Auswirkungen auf Populationsebene, da es die ziehenden Wasservögel dann mit veränderten Jagdgewohnheiten und anderem Druck durch natürliche Räuber zu tun haben.
Similar content being viewed by others
References
Adamik P, Pietruszkova J (2008) Advances in spring but variable trends in timing of inland wader migration. Acta Ornithol 43:119–128. doi:10.3161/000164508X395225
Ahola M, Laaksonen T, Sippola K, Eeva T, Rainio K, Lehikoinen E (2004) Variation in climate warming along the migration route uncouples arrival and breeding dates. Glob Change Biol 10:1610–1617. doi:10.1111/j.1365-2486.2004.00823.x
Alerstam T (1990) Bird migration. Cambridge University Press, New York
Bertin RI (2008) Plant phenology and distribution to recent climate change. J Torrey Bot Soc 135:126–146. doi:10.3159/07-RP-035R.1
BirdLife International (2004) Birds in Europe: population estimates, trends and conservation status. BirdLife conservation series no 12, Cambridge
Birkhead M, Bacon P, Walter P (1983) Factors affecting the breeding success of the mute swan Cygnus olor. J Anim Ecol 52:727–741. doi:10.2307/4450
Bregnballe T, Madsen J, Rasmussen PAF (2004) Effects of temporal and spatial hunting control in waterbird reserves. Biol Conserv 119:93–104. doi:10.1016/j.biocon.2003.10.025
Choi G, Robinson D, Kang S (2010) Changing Northern Hemisphere snow seasons. J Clim 23:5305–5310. doi:10.1175/2010JCLI3644.1
Cramp S, Simmons KEL (1977) Birds of the western Palearctic, vol 1. Oxford University Press, Oxford
Cresswell W (2008) Non-lethal effects of predation in birds. Ibis 150:3–17. doi:10.1111/j.1474-919X.2007.00793.x
Dunn P (2004) Breeding dates and reproductive performance. Adv Ecol Res 35:69–87
Filippi-Codacciuoni O, Moussus JP, Urcun JP, Jiguet F (2010) Advanced departure dates in long-distance migratory raptors. J Ornithol 151:687–694. doi:10.1007/s10336-010-0500-5
Fox AD, Madsen J (1997) Behavioural and distributional effects of hunting disturbance on waterbirds in Europe: implications for refuge design. J Appl Ecol 34:1–13. doi:10.2307/2404842
Fransson T, Pettersson J (2001) Swedish bird ringing atlas, vol 1. Swedish Museum of Natural History, Stockholm
Gordo O, Sanz JJ (2006) Climate and bird phenology: a long-term study in the Iberian Peninsula. Glob Change Biol 12:1993–2004. doi:10.1111/j.1365-2486.2006.01178.x
Guillemain M, Arzel C, Lagagneaux P, Elmberg J, Fritz H, Lepley M, Pin C, Arnaud A, Massez G (2007) Predation risk constrains the plasticity of foraging behaviour in teals, Anas crecca: a flyway-level circumannual approach. Anim Behav 73:845–854. doi:10.1016/j.anbehav.2006.06.019
Guillemain M, Elmberg J, Arzel C, Johnson AR, Simon G (2008) The income-capital breeding dichotomy revisited: late winter body condition is related to breeding success in an income breeder. Ibis 150:172–176. doi:10.1111/j.1474-919X.2007.00700.x
Halupka L, Dyrcz A, Borowiec M (2008) Climate change affects breeding of reed warblers Acrocephalus scirpaceus. J Avian Biol 39:95–100. doi:10.1111/j.0908-8857.2008.04047.x
Hüppop O, Hüppop K (2003) North Atlantic oscillation and timing of spring migration in birds. Proc R Soc B 270:233–240. doi:10.1098/rspb.2002.2236
Intergovernmental Panel on Climate Change (IPCC) (2007) Climate change 2007: synthesis report. Fourth assessment report. Available at: http://www.ipcc.ch/
Jenni L, Kery M (2003) Timing of autumn bird migration under climate change: advances in long-distance migrants, delays in short-distance migrants. Proc R Soc Lond B 270:1467–1471
Jónsson JE, Gardarsson A, Gill JA, Petersen A, Gunnarsson TG (2009) Seasonal weather effects on the common eider, a subarctic capital breeder, in Iceland over 55 years. Clim Res 38:237–248
Jonzén N, Lindén A, Ergon T, Knudsen E, Vik JO, Rubolini D, Piacentini D, Brinch C, Spina F, Karlsson L, Stervander M, Andersson A, Waldenström J, Lehikoinen A, Edvardsen E, Solvang R, Stenseth NC (2006) Rapid advance of spring arrival dates in long-distance migratory birds. Science 312:1959–1961. doi:10.1126/science.1126119
Lehikoinen A, Vähätalo A (2000) Phenology of bird migration at the Hanko Bird Observatory, Finland, in 1979–1999. Tringa 27:150–224 (In Finnish)
Lehikoinen E, Sparks TH, Zalakevicius M (2004) Arrival and departure dates. Adv Ecol Res 35:1–31
Lehikoinen A, Kilpi M, Öst M (2006) Winter climate affects subsequent breeding success of common eiders. Glob Change Biol 12:1355–1365. doi:10.1111/j.1365-2486.2006.01162.x
Lehikoinen A, Ekroos J, Jaatinen K, Lehikoinen P, Lindén A, Piha M, Vähätalo A (2008) Bird population trends based on the data of Hanko Bird Observatory (Finland) during 1979–2007. Tringa 35:146–209 (In Finnish)
Lehikoinen A, Saurola P, Valkama J, Lindén A, Byholm P (2010) Life history events of the Eurasian sparrowhawk in changing climate. J Avian Biol 41:627–636. doi:10.1111/j.1600-048X.2010.05080.x
Madsen J (1995) Impacts of disturbance on migratory waterfowl. Ibis 137:S67–S74. doi:10.1111/j.1474-919X.1995.tb08459.x
Madsen J (1998a) Experimental refuges for migratory waterfowl in Danish wetlands. I. Baseline assessment of disturbance effects of recreational activities. J Appl Ecol 35:386–397. doi:10.1046/j.1365-2664.1998.00314.x
Madsen J (1998b) Experimental refuges for migratory waterfowl in Danish wetlands. II. Tests of hunting disturbance effects. J Appl Ecol 35:398–417. doi:10.1046/j.1365-2664.1998.00315.x
Madsen J, Pihl S, Clausen P (1998) Establishing a reserve network for waterfowl in Denmark: a biological evaluation of needs and consequences. Biol Conserv 85:241–255. doi:10.1016/S0006-3207(97)00172-9
Mezquida ET, Villarán A, Pascual-Parra J (2007) Timing of autumn bird migration in central Spain in light of recent climate change. Ardeola 54:251–259
Miller-Rushing AJ, Lloyd-Evans TL, Primack RB, Satzinger P (2008) Bird migration times, climate change, and changing population sizes. Glob Change Biol 14:1959–1972. doi:10.1111/j.1365-2486.2008.01619.x
Mills AM (2005) Changes in the timing of spring and autumn migration in North American migrant passerines during a period of global warming. Ibis 147:259–269. doi:10.1111/j.1474-919X.2005.00380.x
Møller AP, Rubolini D, Lehikoinen E (2008) Populations of migratory bird species that did not show a phenological response to climate change are declining. Proc Natl Acad Sci USA 105:16195–16200. doi:10.1073/pnas.0803825105
Møller AP, Fiedler W, Berthold P (eds) (2010) Effects of climate change on birds. Oxford University Press, Oxford
Murphy-Klassen HM, Underwood TJ, Sealy SG, Czyrnyj AA (2005) Long- term trends in spring arrival dates of migrant birds at Delta Marsh, Manitoba, in relation to climate change. Auk 122:1130–1148. doi:10.1642/0004-8038(2005)122[1130:LTISAD]2.0.CO;2
Newton I (1998) Population limitation in birds. Academic, London
Newton I (2008) The migration ecology of birds. Academic, London
Nilsson L (1979) Variation in the production of young of swans wintering in Sweden. Wildfowl 30:129–134
Nilsson L (2005) Long-term trends and changes in numbers and distribution of some wintering waterfowl species along the Swedish Baltic coast. Acta Zool Lituan 15:151–157
Nilsson L (2008) Changes in numbers and distribution of wintering waterfowl in Sweden during forty years, 1967–2006. Ornis Svec 18:135–226
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. doi:10.1098/rspb.2003.2569
Parmesan C (2006) Ecological and evolutionary responses to recent climate change. Annu Rev Ecol Evol Sys 37:637–669. doi:10.1146/annurev.ecolsys.37.091305.110100
Polyak L, Alley RB, Andrews JT, Brigham-Grette J, Cronin TM, Darby DA, Dyke AS, Fitzpartick JJ, Funder S, Jennings AE, Miller GH, O’Regan M, Savelle J, Serreze M, St John K, White JWC, Wolff E (2010) History of sea ice in the Arctic. Q Sci Rev 29:1757–1778. doi:10.1016/j.quascirev.2010.02.010
Pöyhönen M (1995) Muuttolintujen matkassa. Otava, Keuruu
Rainio R, Laaksonen T, Ahola M, Vähätalo AV, Lehikoinen E (2006) Climatic responses in spring migration of boreal and arctic birds in relation to wintering area and taxonomy. J Avian Biol 37:507–515. doi:10.1111/j.0908-8857.2006.03740.x
Rassi P, Hyvärinen E, Juslén A, Mannerkoski I (eds) (2010) The red list of Finnish species. Ympäristöministeriö and Suomen ympäristökeskus, Helsinki
Rebetez M, Reinhard M (2007) Montly air temperature trends in Switzerland 1901–2000 and 1975–2004. Theor Appl Climat 91:27–34. doi:10.1007/s00704-007-0296-2
Saino N, Ambrosini R, Hüppop K, Hüppop O, Lehikoinen E, Lehikoinen A, Provenzale A, Rainio K, Romano M, Rubolini D, von Hardenberg J, Sokolov L (2011) Climate warming, ecological mismatch at arrival and population decline in migratory birds. Proc R Soc Lond B 278:835–842. doi:10.1098/rspb.2010.1778
Sauter A, Korner-Nievergelt F, Jenni L (2010) Evidence of climate change effects on within-winter movements of European Mallard Anas platyrhynchos. Ibis 152:600–609. doi:10.1111/j.1474-919X.2010.01028.x
Schneider P, Hook SJ (2010) Space observations of inland water bodies show rapid surface warming since 1985. Geophys Res Lett 37:L22405. doi:10.1029/2010GL045059
Sokolov LV, Payevsky VA (1998) Spring temperatures influence year-to-year variations in the breeding phenology of passerines on the Courish Spit, eastern Baltic. Avian Ecol Behav 1:22–36
Studds CE, Marra PP (2007) Linking fluctuations in rainfall to nonbreeding season performance in a long-distant migratory bird (Setophaga ruticilla). Climate Res 35:115–122. doi:10.3354/cr00718
Tellaria JL, Perez-Tris J (2004) Consequences of the settlement of migrant European Robins Erithacus rubecula in wintering habitats occupied by conspecific residents. Ibis 146:258–268. doi:10.1111/j.1474-919x.2003.00249.x
Telleria JL, Perz-Tris J, Ramirez A, Fernandez-Juricic E, Carbonell R (2001) Distribution of robins Erithacus rubecula in wintering grounds: effects of conspecific density, migratory status and age. Ardea 89:363–373
Thorup K, Tøttrup AP, Rahbek C (2007) Patterns of phenological changes in migratory birds. Oecologia 151:697–703. doi:10.1007/s00442-006-0608-8
Väänänen VM (2001) Hunting disturbance and the timing of autumn migration in Anas species. Wildl Biol 7:3–9
Väänänen VM (2007) Hanhijahdissa uudet tuulet. Metsästäjä 2007(4):22–25 (In Finnish)
Väänänen VM, Laine J, Lammi E, Lehtiniemi T, Luostarinen VM, Mikkola-Roos M (2010) The establishment of Barnacle Goose of Finland–rapid growth rate and expansion of the breeding grounds. Linnut-vuosikirja 2009:72–77 (In Finnish)
Vähätalo AV, Rainio K, Lehikoinen A, Lehikoinen E (2004) Spring arrival of birds depends on the North Atlantic Oscillation. J Avian Biol 35:210–216
Valkama J, Saurola P, Velmala W (2011) Finnish bird ringing atlas, vol 1 (in press)
Van Buskirk J, Mulvihill RS, Leberman RC (2009) Variable shifts in spring and autumn migration phenology in North American songbirds associated with climate change. Glob Change Biol 15:760–771. doi:10.1111/j.1365-2486.2008.01751.x
Wernham C, Siriwarden GM, Toms M, Marchant J, Clark JA, Baillie S (2002) The migration atlas: movements of the birds of Britain and Ireland. Poyser, London
Wetlands International (2006) Waterbird population estimates, 4th edn. Wetlands International, Wageningen
Acknowledgments
We thank the numerous volunteers who helped collecting migration data at the Hanko Bird Observatory and Finnish Cultural Foundation from the annual funding for the observatory. This publication is the contribution no. 104 from the Hanko Bird Observatory. During this study, K.J. was funded by The Academy of Finland (grant number 128039) and The Swedish Cultural Foundation in Finland. Comments by Ryan Norris and anonymous referees improved the earlier version of the manuscript.
Author information
Authors and Affiliations
Corresponding author
Additional information
Communicated by F. Bairlein.
Rights and permissions
About this article
Cite this article
Lehikoinen, A., Jaatinen, K. Delayed autumn migration in northern European waterfowl. J Ornithol 153, 563–570 (2012). https://doi.org/10.1007/s10336-011-0777-z
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10336-011-0777-z