Skip to main content
Log in

Earlier Arctic springs cause phenological mismatch in long-distance migrants

  • Global Change Ecology - Original Research
  • Published:
Oecologia Aims and scope Submit manuscript

Abstract

An uneven change in climate across the Northern Hemisphere might severely affect the phenology of migrating animals, and especially long-distance migrating birds relying on local climatic cues to regulate the timing of migration. We examine the forward displacement of spring in both staging areas and breeding grounds of one such population, the East Atlantic light-bellied brent goose Branta bernicla hrota, and evaluate to what extent their migration has made a proportional response. On the breeding grounds in Svalbard the onset of spring advanced 2 weeks during the 24-year period, whereas no significant trend was found in the temperate staging areas. The timing of migration was constant throughout the study period, mirroring the static climatic conditions in the spring staging areas. These findings indicate a global warming-induced phenological mismatch in light-bellied brent geese, as these might arrive on their breeding grounds well beyond optimal breeding conditions. Our data indicated that productivity was negatively influenced by phenological delay and positively influenced by prolonged snow cover. We argue that both these effects might be representative of a negative influence of the growing phenological mismatch, because years with later thaw might partly offset the effects of increasingly earlier Svalbard springs. During the study period reproduction fell below annual mortality, and the population declined in recent years. The wider implications of these findings may extend to many migrating species, and highlight the urgent need to clarify how global change may influence cues and the associated timing of important life history activities.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6

Similar content being viewed by others

References

  • 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

    Article  Google Scholar 

  • Bauer S, Gienapp P, Madsen J (2008) The relevance of environmental conditions for departure decision changes en route in migrating geese. Ecology 89:1953–1960. doi:10.1890/07-1101.1

    Article  PubMed  Google Scholar 

  • Bêty J, Gauthier G, Giroux JF, Korpimaki E (2001) Are goose nesting success and lemming cycles linked? Interplay between nest density and predators. Oikos 93:388–400. doi:10.1034/j.1600-0706.2001.930304

    Article  Google Scholar 

  • Bêty J, Giroux JF, Gauthier G (2004) Individual variation in timing of migration: causes and reproductive consequences in greater snow geese (Anser caerulescens atlanticus). Behav Ecol Sociobiol 57:1–8. doi:10.1007/s00265-004-0840-3

    Article  Google Scholar 

  • Both C, Visser ME (2005) The effect of climate change on the correlation between avian life-history traits. Glob Change Biol 11:1606–1613. doi:10.1111/j.1365-2486.2005.01038.x

    Article  Google Scholar 

  • Box GEP, Jenkins GM, Reinsel GC (1994) Time series analysis: forecasting and control, 3rd edn. Prentice Hall, Englewood Cliffs

    Google Scholar 

  • Boyd H, Bell MV, Watson D (2000) Spring weather and migration of geese from Scotland to Iceland. Ring Migr 20:153–165. doi:10.1080/03078698.2000.9674238

    Article  Google Scholar 

  • Brockwell PJ, Davis RA (2009) Time series: theory and methods, 2nd edn. Springer, New York

    Google Scholar 

  • Burnham KP, Anderson DR (2002) Model selection and multimodel inference: a practical information-theoretic approach. Springer, New York

    Google Scholar 

  • Callaghan TV, Björn LO, Chernov Y, et al. (2004) Biodiversity, distributions and adaptations of Arctic species in the context of environmental change. Ambio 33:404–417. doi:10.1639/0044-7447(2004)033[0404:BDAAOA]2.0.CO;2

    PubMed  Google Scholar 

  • Clausen P (2006) Summer 2006—worst ever breeding season for East Atlantic light-bellied brent geese. GooseNews 6:17–18

    Google Scholar 

  • Clausen P, Bustnes JO (1998) Flyways of North Atlantic light-bellied brent geese Branta bernicla hrota reassessed by satellite telemetry. Nor Polarinst Skr 200:235–249

    Google Scholar 

  • Clausen P, Percival SM (1998) Changes in distribution and habitat use of Svalbard light-bellied brent geese Branta bernicla hrota, 1980–1995: driven by Zostera availability? Nor Polarinst Skr 200:253–276

    Google Scholar 

  • Clausen P, Madsen J, Percival SM, O’Connor D, Anderson GQA (1998) Population development and changes in winter site use by the Svalbard light-bellied brent goose, Branta bernicla hrota 1980–94. Biol Conserv 84:157–165. doi:10.1016/S0006-3207(97)00097-9

    Article  Google Scholar 

  • Clausen P, Madsen J, Percival SM, Anderson GQA, Koffijberg K, Mehlum F, Vangeluwe D (1999) Light-bellied brent goose Branta bernicla hrota: Svalbard. In: Madsen J, Cracknell G, Fox T (eds) Goose populations of the western Palearctic. A review of status and distribution. National Environmental Research Institute, Rønde and Wetlands International, Wageningen. Wetlands International Publication 48, pp 312–327

  • Clausen P, Frederiksen M, Percival SM, Anderson GQA, Denny MJH (2001) Seasonal and annual survival of east-Atlantic pale-bellied brent geese Branta hrota assessed by capture–recapture analysis. Ardea 89:101–112

    Google Scholar 

  • Clausen P, Green M, Alerstam T (2003) Energy limitations for spring migration and breeding: the case of brent geese Branta bernicla tracked by satellite telemetry to Svalbard and Greenland. Oikos 103:426–445. doi:10.1034/j.1600-0706.2003.12340.x

    Article  Google Scholar 

  • Denny MJH, Clausen P, Percival S, Anderson GQA, Koffijberg K, Robinson JA (2004) Light-bellied brent goose Branta bernicla hrota [East Atlantic population] in Svalbard, Greenland, Franz Josef Land, Norway, Denmark, The Netherlands and Britain 1960/61–2000/01. The Wildfowl and Wetlands Trust/Joint Nature Conservation Committee, Slimbridge

    Google Scholar 

  • Dickey MH, Gauthier G, Cadieux MC (2008) Climatic effects on the breeding phenology and reproductive success of an Arctic-nesting goose species. Glob Change Biol 14:1973–1985. doi:10.1111/j.1365-2486.2008.01622.x

    Article  Google Scholar 

  • Ebbinge BS, Spaans B (1995) The importance of body reserves accumulated in spring staging areas in the temperate zone for breeding in dark-bellied brent geese Branta-B-Bernicla in the High Arctic. J Avian Biol 26:105–113. doi:10.2307/3677058

    Article  Google Scholar 

  • Fox AD, Ebbinge BS, Mitchell C, Heinicke T, Aarvak T, Colhoun K, Clausen P, Dereliev S, Faragó S, Koffijberg K, Kruckenberg H, Loonen MJJE, Madsen J, Mooij J, Musil P, Nilsson L, Pihl S, Van der Jeugd H (2010) Current estimates of goose population sizes in western Europe, a gap analysis and an assessment of trends. Ornis Svec 20:115–127

    Google Scholar 

  • Fuglei E, Oritsland NA, Prestrud P (2003) Local variation in Arctic fox abundance on Svalbard, Norway. Pol Biol 26:93–98. doi:10.1007/s00300-002-0458-8

    Google Scholar 

  • Green M, Alerstam T (2000) Flight speeds and climb rates of Brent Geese: mass-dependent differences between spring and autumn migration. J Avian Biol 31:215–225. doi:10.1034/j.1600-048X.2000.310213.x

    Article  Google Scholar 

  • Høye TT, Post E, Meltofte H, Schmidt NM, Forchhammer MC (2007) Rapid advancement of spring in the High Arctic. Curr Biol 17:449–451. doi:10.1016/j.cub.2007.04.047

    Article  Google Scholar 

  • IPCC (2007) Climate Change 2007: the physical science basis. Contribution of Working Group I to the Fourth Assessment Report of the Intergovernmental Panel on Climate Change. Cambridge University press, Cambridge

  • Jensen RA, Madsen J, O’Connell M, Wisz MS, Tømmervik H, Mehlum F (2008) Prediction of the distribution of Arctic-nesting pink-footed geese under a warmer climate scenario. Glob Change Biol 14:1–10. doi:10.1111/j.1365-2486.2007.01461.x

    Google Scholar 

  • Karlsen SR, Høgda KA, Solbø S, Storvold R (2010) Mapping of the growing season on Svalbard based on satellite data for the 1985 to 2009 period. Presentation at State of the Arctic Conference, Miami, FL. http://soa.arcus.org/sites/soa.arcus.org/files/sessions/2-1-observations-arctic-change/pdf/2-1-9-storvold-rune.pdf

  • Lambeck RHD (1990) The applicability of age ratio and brood size counts in population dynamic studies of the brent goose Branta b. bernicla. Ardea 78:414–425

    Google Scholar 

  • Lehikoinen E, Sparks T, Zalakevicius M (2004) Arrival and departure dates. Adv Ecol Res 35:1–31. doi:10.1016/S0065-2504(04)35001-4

    Article  Google Scholar 

  • Lepage D, Gauthier G, Reed A (1998) Seasonal variation in growth of greater snow goose goslings: the role of food supply. Oecologia 114:226–235. doi:10.1007/s004420050440

    Article  Google Scholar 

  • Madsen J, Bregnballe T, Frikke J, Kristensen JB (1998) Correlates of predator abundance with snow and ice conditions and their role in determining timing of nesting and breeding success in Svalbard light-bellied brent geese Branta bernicla hrota. Nor Polarinst Skr 200:221–234

    Google Scholar 

  • Madsen J, Cracknell G, Fox AD (eds) (1999) Goose populations of the western PaleArctic. A review of status and distribution. National Environmental Research Institute, Rønde and Wetlands International, Wageningen. Wetlands International Publication 48

  • Madsen J, Tamstorf M, Klaassen M, Eide N, Glahder C, Rigét F, Nyegaard H, Cottaar F (2007) Effects of snow cover on the timing and success of reproduction in high-Arctic pink-footed geese Anser brachyrhynchus. Polar Biol 30:1363–1372. doi:10.1007/s00300-007-0296-9

    Article  Google Scholar 

  • McNamara JM, Barta Z, Klaassen M, Bauer S (2011) Cues and the optimal timing of activities under environmental change. Ecol Lett 14:1183–1190. doi:10.1111/j.1461-0248.2011.01686.x

    Article  PubMed  Google Scholar 

  • Mehlum F (1998) Areas in Svalbard important for geese during the pre-breeding, breeding and post-breeding periods. Nor Polarinst Skr 200:41–56

    Google Scholar 

  • Miller-Rushing AJ, Høye TT, Inouye DW, Post E (2010) The effects of phenological mismatches on demography. Philos Trans R Soc (B) 365:3177–3186. doi:10.1098/rstb.2010.0148

    Article  Google Scholar 

  • Moe B, Stempniewicz L, Jakubas D, Angelier F, Chastel O, Dinesen F, Gabrielsen GW, Hanssen F, Karnovsky NJ, Rønning B, Welcker J, Wojczulanis-Jakubas K, Bech C (2009) Climate change and phenological responses of two seabird species breeding in the high-Arctic. Mar Ecol Prog Ser 393:235–246. doi:10.3354/meps08222

    Article  Google Scholar 

  • Morrissette M, Bêty J, Gauthier G, Reed A, Lefebvre J (2010) Climate, trophic interactions, density dependence and carry-over effects on the population productivity of a migratory Arctic herbivorous bird. Oikos 119:1181–1191. doi:10.1111/j.1600-0706.2009.18079.x

    Article  Google Scholar 

  • Nordli Ø (2005) Temperature variations at Svalbard during the last century. Nord Space Act 13:6–7

    Google Scholar 

  • Parmesan C, Yohe G (2003) A globally coherent fingerprint of climate change impacts across natural systems. Nature 421:37–42. doi:10.1038/nature01286

    Article  PubMed  CAS  Google Scholar 

  • Pearce-Higgins JW, Yalden DW, Whittingham MJ (2005) Warmer springs advance the breeding phenology of golden plovers Pluvialis apricaria and their prey (Tipulidae). Oecologia 143:470–476. doi:10.1007/s00442-004-1820-z

    Article  PubMed  CAS  Google Scholar 

  • Post E, Forchhammer MC, Bret-Harte MS, Callaghan TV, Christensen TR, Elberling B, Fox AD, Gilg O, Hik DS, Høye TT, Ims RA, Jeppesen E, Klein DR, Madsen J, McGuire AD, Rysgaard S, Schindler DE, Stirling I, Tamstorf MP, Tyler NJC, van der Wal R, Welker J, Wookey PA, Schmidt NM, Aastrup P (2009) Ecological dynamics across the Arctic associated with recent climate change. Science 325:1355–1358. doi:10.1126/science.1173113

    Article  PubMed  CAS  Google Scholar 

  • Saino N, Ambrosini R, Rubolini D, von Hardenberg J, Provenzale A, Huppop K, Huppop O, Lehikoinen A, Lehikoinen E, Rainio K, Romano M, Sokolov L (2011) Climate warming, ecological mismatch at arrival and population decline in migratory birds. Proc R Soc B 278:835–842

    Article  PubMed  Google Scholar 

  • Scott DA, Rose PM (1996) Atlas of Anatidae populations in Africa and Western Eurasia. Wetlands International, Wageningen

    Google Scholar 

  • Sedinger JS, Flint PL (1991) Growth rate is negatively correlated with hatch date in black brant. Ecology 72:496–502. doi:10.2307/2937190

    Article  Google Scholar 

  • Sedinger JS, Raveling DG (1986) Timing of nesting by Canada geese in relation to the phenology and availability of their food plants. J Anim Ecol 55:1083–1102

    Article  Google Scholar 

  • Smith BD, Hagmeier KR, Boyd WS, Dawe NK, Martin TD, Monty GL (2012) Trends in volume migration chronology in spring staging Pacific black brant. J Wildl Manage 76:593–599. doi:10.1002/jwmg.307

    Article  Google Scholar 

  • Sparks TH, Aasa A, Huber K, Wadsworth R (2009) Changes and patterns in biologically relevant temperatures in Europe 1941–2000. Clim Res 39:191–207. doi:10.3354/cr00814

    Article  Google Scholar 

  • Stone RS, Dutton EG, Harris JM, Longenecker D (2002) Earlier spring snowmelt in northern Alaska as an indicator of climate change. J Geophys Res (D) 107(D10):4089. doi:10.1029/2000JD000286

  • Tombre IM, Høgda KA, Madsen J, Griffin LR, Kuijken E, Shimmings P, Rees E, Verscheure C (2008) The onset of spring and timing of migration in two Arctic nesting goose populations: the pink-footed goose Anser brachyrhynchus and the barnacle goose Branta leucopsis. J Avian Biol 39:691–703. doi:10.1111/j.1600-048X.2008.04440.x

    Article  Google Scholar 

  • Tottrup AP, Rainio K, Coppack T, Lehikoinen E, Rahbek C, Thorup K (2010) Local Temperature fine-tunes the timing of spring migration in birds. Integr Comp Biol 50:293–304. doi:10.1093/Icb/Icq028

    Article  PubMed  Google Scholar 

  • van der Jeugd HP, Eichhorn G, Litvin KE, Stahl J, Larsson K, van der Graaf AJ, Drent RH (2009) Keeping up with early springs: rapid range expansion in an avian herbivore incurs a mismatch between reproductive timing and food supply. Glob Change Biol 15:1057–1071. doi:10.1111/j.1365-2486.2008.01804.x

    Article  Google Scholar 

  • Visser ME (2008) Keeping up with a warming world; assessing the rate of adaptation to climate change. Proc R Soc (B) 275:649–659. doi:10.1098/rspb.2007.0997

    Article  Google Scholar 

  • Ward DH, Dau CP, Tibbitts TL, Sedinger JS, Anderson BA, Hines JE (2009) Change in abundance of Pacific brant wintering in Alaska: evidence of a climate warming effect? Arctic 62:301–311

    Google Scholar 

  • Watkinson AR, Gill JA, Hulme M (2004) Flying in the face of climate change: a review of climate change, past, present and future. Ibis 146:4–10. doi:10.1111/j.1474-919X.2004.00321.x

    Article  Google Scholar 

Download references

Acknowledgments

Thanks are due to Jesper Madsen who initiated the long-term monitoring of the East Atlantic light-bellied brent geese. We are particularly indebted to all the committed observers that worked at Lista Bird Observatory during the study period and kindly provided the necessary data, to Guy Q. A. Anderson who contributed to the collection of data in the early 1990s, and to all professional and volunteer observers who help with age counts of brent goose flocks every year. Data from the two Norwegian citizen science portals http://www.fugler.net and http://www.artsobservasjoner.no/fugler/ were extracted and sent to us by Oskar Kenneth Bjørnstad and Tomas Aarvak, respectively, and Nick Hughes provided the data on sea ice coverage. Toke Høye, Jesper Madsen and Tony Fox are thanked for fruitful suggestions to outline the study, and Gilles Gauthier, Hannu Pöysä and two anonymous reviewers for their very constructive comments on an earlier draft.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Kevin Kuhlmann Clausen.

Additional information

Communicated by Hannu Pöysä.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Clausen, K.K., Clausen, P. Earlier Arctic springs cause phenological mismatch in long-distance migrants. Oecologia 173, 1101–1112 (2013). https://doi.org/10.1007/s00442-013-2681-0

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00442-013-2681-0

Keywords

Navigation