BACKGROUND: Migratory birds generally have tightly scheduled annual cycles, in which delays can have carry-over effects on the timing of later events, ultimately impacting reproductive output. Whether temporal carry-over effects are more pronounced among migrations over larger distances, with tighter schedules, is a largely unexplored question. METHODS: We tracked individual Arctic Skuas Stercorarius parasiticus, a long-distance migratory seabird, from eight breeding populations between Greenland and Siberia using light-level geolocators. We tested whether migration schedules among breeding populations differ as a function of their use of seven widely divergent wintering areas across the Atlantic Ocean, Mediterranean Sea and Indian Ocean. RESULTS: Breeding at higher latitudes led not only to later reproduction and migration, but also faster spring migration and shorter time between return to the breeding area and clutch initiation. Wintering area was consistent within individuals among years; and more distant areas were associated with more time spent on migration and less time in the wintering areas. Skuas adjusted the period spent in the wintering area, regardless of migration distance, which buffered the variation in timing of autumn migration. Choice of wintering area had only minor effects on timing of return at the breeding area and timing of breeding and these effects were not consistent between breeding populations. CONCLUSION: The lack of a consistent effect of wintering area on timing of return between breeding areas indicates that individuals synchronize their arrival with others in their population despite extensive individual differences in migration strategies.

Applied Zoology Animal Ecology Institute of Biology Freie Universität Berlin Berlin Germany

Arctic Research Station of Institute of Plant and Animal Ecology Ural Branch Russian Academy of Sciences Labytnangi Russia

British Antarctic Survey Cambridge UK

British Trust for Ornithology Scotland Stirling University Innovation Park Stirling FK9 4NF UK

British Trust for Ornithology The Nunnery Thetford Norfolk IP24 2PU UK

Center for Macroecology Evolution and Climate Globe Institute University of Copenhagen Copenhagen Denmark

Centre for the Advanced Study of Collective Behaviour University of Konstanz Constance Germany

Conservation Ecology Group Groningen Institute for Evolutionary Life Sciences Groningen University Groningen The Netherlands

Department of Life and Environmental Sciences University of Iceland Reykjavik Iceland

Environmental Agency Pori Finland

Faculty of Science and Technology University of the Faroe Islands Vestarabryggja 15 100 Tórshavn Faroe Islands

Faculty of Sciences University of South Bohemia České Budějovice Czech Republic

Groupe de Recherche en Ecologie Arctique 16 Rue de Vernot 21440 Francheville France

Institute of Entomology Biology Centre of the Czech Academy of Sciences České Budějovice Czech Republic

Max Planck Institute of Animal Behavior Radolfzell Germany

Northeast Iceland Nature Research Centre Husavik Iceland

Norwegian Institute for Nature Research Tromsø Norway

Norwegian Institute for Nature Research Trondheim Norway

Pori Ornithological Society Pori Finland

Section of Ecology Department of Biology University of Turku Turku Finland

SOVON Vogelonderzoek Nederland Nijmegen The Netherlands

Sudurnes Science and Learning Center Suðurnesjabær Iceland

UiT The Arctic University of Norway Tromsø Norway

UMR 6249 Chrono Environnement CNRS Université de Bourgogne Franche Comté 25000 Besançon France

University of Freiburg Freiburg Germany

University of Giessen Giessen Germany

Waardenburg Ecology Culemborg The Netherlands

Wageningen Marine Research Haringkade 1 1976 CP IJmuiden The Netherlands

See more in PubMed

Piersma T. Hink, stap of sprong? Reisbeperkingen van arctische steltlopers door voedselzoeken, vetopbouw en vliegsnelheid. Limosa. 1987;60:185–194.

Harrison XA, Blount JD, Inger R, Norris DR, Bearhop S. Carry-over effects as drivers of fitness differences in animals. J Anim Ecol. 2011;80:4–18. doi: 10.1111/j.1365-2656.2010.01740.x. PubMed DOI

Alerstam T. Bird migration. Cambridge: Cambridge University Press; 1990.

Norris DR, Taylor CM. Predicting the consequences of carry-over effects for migratory populations. Biol Lett. 2006;2:148–151. doi: 10.1098/rsbl.2005.0397. PubMed DOI PMC

Wingfield JC. Organization of vertebrate annual cycles: implications for control mechanisms. Philos Trans R Soc B: Biol Sci. 2008;363:425–441. doi: 10.1098/rstb.2007.2149. PubMed DOI PMC

Marra PP, Cohen EB, Loss SR, Rutter JE, Tonra CM. A call for full annual cycle research in animal ecology. Biol Lett. 2015;2015(11):0552. PubMed PMC

Klaassen RHG, Hake M, Strandberg R, Koks BJ, Trierweiler C, Exo K-M, et al. When and where does mortality occur in migratory birds? Direct evidence from long-term satellite tracking of raptors. J Anim Ecol. 2014;83:176–184. doi: 10.1111/1365-2656.12135. PubMed DOI

Buechley ER, Oppel S, Efrat R, Phipps WL, Carbonell Alanís I, Álvarez E, et al. Differential survival throughout the full annual cycle of a migratory bird presents a life-history trade-off. J Anim Ecol. 2021;90:1228–1238. doi: 10.1111/1365-2656.13449. PubMed DOI

Norris DR, Marra PP. Seasonal interactions, habitat quality, and population dynamics in migratory birds. The Condor. 2007;109:535–547. doi: 10.1093/condor/109.3.535. DOI

Bauer S, Lisovski S, Hahn S. Timing is crucial for consequences of migratory connectivity. Oikos. 2016;125:605–612. doi: 10.1111/oik.02706. DOI

Bogdanova MI, Butler A, Wanless S, Moe B, Anker-nilssen T, Frederiksen M, et al. Multi-colony tracking reveals spatio-temporal variation in carry-over effects between breeding success and winter movements in a pelagic seabird. Mar Ecol Prog Ser. 2017;578:167–181. doi: 10.3354/meps12096. DOI

Gow EA, Burke L, Winkler DW, Knight SM, Bradley DW, Clark RG, et al. A range-wide domino effect and resetting of the annual cycle in a migratory songbird. Proc R Soc B: Biol Sci. 2018;286:20181916. doi: 10.1098/rspb.2018.1916. PubMed DOI PMC

Reneerkens J, Versluijs TSL, Piersma T, Alves JA, Boorman M, Corse C, et al. Low fitness at low latitudes: wintering in the tropics increases migratory delays and mortality rates in an Arctic breeding shorebird. J Anim Ecol. 2019;89:671–932. PubMed PMC

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

Conklin JR, Battley PF, Potter MA, Fox JW. Breeding latitude drives individual schedules in a trans-hemispheric migrant bird. Nat Commun. 2010;1:67. doi: 10.1038/ncomms1072. PubMed DOI

Briedis M, Hahn S, Gustafsson L, Henshaw I, Träff J, Král M, et al. Breeding latitude leads to different temporal but not spatial organization of the annual cycle in a long-distance migrant. J Avian Biol. 2016;47:743–748. doi: 10.1111/jav.01002. DOI

Gow EA, Knight SM, Bradley DW, Clark RG, Winkler DW, Bélisle M, et al. Effects of spring migration distance on tree swallow reproductive success within and among flyways. Front Ecol Evol. 2019;7:380. doi: 10.3389/fevo.2019.00380. DOI

Pedersen L, Jackson K, Thorup K, Tøttrup AP. Full-year tracking suggests endogenous control of migration timing in a long-distance migratory songbird. Behav Ecol Sociobiol. 2018;72:139. doi: 10.1007/s00265-018-2553-z. DOI

Alerstam T, Lindström Å. Optimal bird migration: the relative importance of time, energy and safety. In: Gwinner E, editor. Bird migration: the physiology and ecophysiology. Berlin: Springer; 1990. pp. 331–351.

Lisovski S, Ramenofsky M, Wingfield JC. Defining the degree of seasonality and its significance for future research. Integr Comp Biol. 2017;57:934–942. doi: 10.1093/icb/icx040. PubMed DOI

Morbey YE, Hedenström A. Leave earlier or travel faster—optimal mechanisms for managing arrival time in migratory songbirds. Front Ecol Evol. 2020;7:492. doi: 10.3389/fevo.2019.00492. DOI

Sorte FAL, Fink D, Hochachka WM, DeLong JP, Kelling S. Population-level scaling of avian migration speed with body size and migration distance for powered fliers. Ecology. 2013;94:1839–1847. doi: 10.1890/12-1768.1. PubMed DOI

Marra PP, Hobson KA, Holmes RT. Linking winter and summer events in a migratory bird by using stable-carbon isotopes. Science. 1998;282:1884–1886. doi: 10.1126/science.282.5395.1884. PubMed DOI

Tøttrup AP, Klaassen RHG, Kristensen MW, Strandberg R, Vardanis Y, Lindström Å, et al. Drought in Africa caused delayed arrival of European songbirds. Science (New York, NY) 2012;338:1307. doi: 10.1126/science.1227548. PubMed DOI

Dossman BC, Rodewald AD, Studds CE, Marra PP. Migratory birds with delayed spring departure migrate faster but pay the costs. Ecology. 2023;104:e3938. doi: 10.1002/ecy.3938. PubMed DOI

Dingle H. Migration. The biology of life on the move. 2. Oxford: Oxford University Press; 2014.

Senner NR, Hochachka WM, Fox JW, Afanasyev V. An exception to the rule: carry-over effects do not accumulate in a long-distance migratory bird. PLoS ONE. 2014;9:e86588. doi: 10.1371/journal.pone.0086588. PubMed DOI PMC

Dufour P, Wojczulanis-Jakubas K, Lavergne S, Renaud J, Jakubas D, Descamps S. A two-fold increase in migration distance does not have breeding consequences in a long-distance migratory seabird with high flight costs. Mar Ecol Prog Ser. 2021;676:117–126. doi: 10.3354/meps13535. DOI

Pedersen L, Onrubia A, Vardanis Y, Barboutis C, Waasdorp S, van Helvert M, et al. Remarkably similar migration patterns between different red-backed shrike populations suggest that migration rather than breeding area phenology determines the annual cycle. J Avian Biol. 2020;51:jav.02475. doi: 10.1111/jav.02475. DOI

Webster MS, Marra PP, Haig SM, Bensch S, Holmes RT. Links between worlds: unraveling migratory connectivity. Trends Ecol Evol. 2002;17:76–83. doi: 10.1016/S0169-5347(01)02380-1. DOI

Åkesson S, Ilieva M, Karagicheva J, Rakhimberdiev E, Tomotani B, Helm B. Timing avian long-distance migration: from internal clock mechanisms to global flights. Philos Trans R Soc B: Biol Sci. 2017;372:20160252. doi: 10.1098/rstb.2016.0252. PubMed DOI PMC

Furness RW. The Skuas. London: T. & A.D. Poyser; 1987.

Olsen KM, Larsson H. Skuas and jaegers. A guide to the skuas and jaegers of the world. East Sussex: Pica Press; 1997.

Briedis M, Hahn S, Adamík P. Cold spell en route delays spring arrival and decreases apparent survival in a long-distance migratory songbird. BMC Ecol. 2017;17:11. doi: 10.1186/s12898-017-0121-4. PubMed DOI PMC

Davies TE, Carneiro APB, Tarzia M, Wakefield E, Hennicke JC, Frederiksen M, et al. Multispecies tracking reveals a major seabird hotspot in the North Atlantic. Conserv Lett. 2021;14:e12824. doi: 10.1111/conl.12824. DOI

O’Hanlon NJ, van Bemmelen RSA, Snell KRS, Conway GJ, Thaxter CB, Aiton H, et al. Atlantic populations of a declining oceanic seabird have complex migrations and weak migratory connectivity to staging areas. Mar Ecol Prog Ser. 2024;730:113–129. doi: 10.3354/meps14533. DOI

Sittler B, Aebischer A, Gilg O. Post-breeding migration of four Long-tailed Skuas (Stercorarius longicaudus) from North and East Greenland to West Africa. J Ornithol. 2011;152:375–381. doi: 10.1007/s10336-010-0597-6. DOI

Verhoeven MA, Loonstra AHJ, McBride AD, Macias P, Kaspersma W, Hooijmeijer JCEW, et al. Geolocators lead to better measures of timing and renesting in black-tailed godwits and reveal the bias of traditional observational methods. J Avian Biol. 2020;51:jav.02259. doi: 10.1111/jav.02259. DOI

Cohen EB, Hostetler JA, Hallworth MT, Rushing CS, Sillett TS, Marra PP. Quantifying the strength of migratory connectivity. Methods Ecol Evol. 2018;9:513–524. doi: 10.1111/2041-210X.12916. DOI

McFarlane Tranquilla LA, Montevecchi WA, Fifield DA, Hedd A, Gaston AJ, Robertson GJ, et al. Individual winter movement strategies in two species of murre (Uria spp) in the Northwest Atlantic. PLoS ONE. 2014;9:e90583. doi: 10.1371/journal.pone.0090583. PubMed DOI PMC

Gelman A, Hill J, Yajima M. Why we (usually) don’t have to worry about multiple comparisons. J Res Educ Effect. 2012;5:189–211.

Kruschke JK. Doing Bayesian data analysis: A tutorial with R, JAGS, and Stan. 2014.

Nakagawa S, Schielzeth H. Repeatability for Gaussian and non-Gaussian data: a practical guide for biologists. Biol Rev. 2010;85:935–956. doi: 10.1111/j.1469-185X.2010.00141.x. PubMed DOI

Bürkner P-C. Brms: an R package for Bayesian multilevel models using Stan. J Stat Softw. 2017;80:1–28. doi: 10.18637/jss.v080.i01. DOI

Team SD. Stan Modeling Language Users Guide and Reference Manual. 2021.

Dias MP, Granadeiro JP, Phillips RA, Alonso H, Catry P. Breaking the routine: Individual Cory’s shearwaters shift winter destinations between hemispheres and across ocean basins. Proc Biol Sci/R Soc. 2011;278:1786–1793. PubMed PMC

Phillips RA, Catry P, Silk JRD, Bearhop S, McGill R, Afanasyev V, et al. Movements, winter distribution and activity patterns of Falkland and brown skuas: insights from loggers and isotopes. Mar Ecol Prog Ser. 2007;345:281–291. doi: 10.3354/meps06991. DOI

Delord K, Cherel Y, Barbraud C, Chastel O, Weimerskirch H. High variability in migration and wintering strategies of brown skuas (Catharacta antarctica lonnbergi) in the Indian Ocean. Polar Biol. 2017;41:59–70. doi: 10.1007/s00300-017-2169-1. DOI

Weimerskirch H, Tarroux A, Chastel O, Delord K, Cherel Y, Descamps S. Population-specific wintering distributions of adult south polar skuas over three oceans. Mar Ecol Prog Ser. 2015;538:229–237. doi: 10.3354/meps11465. DOI

van Bemmelen R, Moe B, Hanssen S, Schmidt N, Hansen J, Lang J, et al. Flexibility in otherwise consistent non-breeding movements of a long-distance migratory seabird, the long-tailed skua. Mar Ecol Prog Ser. 2017;578:197–211. doi: 10.3354/meps12010. DOI

Neufeld LR, Muthukumarana S, Fischer JD, Ray JD, Siegrist J, Fraser KC. Breeding latitude is associated with the timing of nesting and migration around the annual calendar among Purple Martin (Progne subis) populations. J Ornithol. 2021;162:1009–1024. doi: 10.1007/s10336-021-01894-w. DOI

Wong JB, Lisovski S, Alisauskas RT, English WB, Harrison A-L, Kallett DK, et al. Variation in migration behaviors used by Arctic Terns (Sterna paradisaea) breeding across a wide latitudinal gradient. Polar Biol. 2022;45:909–922. doi: 10.1007/s00300-022-03043-2. DOI

Furness BL. The feeding behaviour of Arctic Skuas Stercorarius parasiticus wintering off South Africa. Ibis. 1983;125:245–251. doi: 10.1111/j.1474-919X.1983.tb03107.x. DOI

Stenhouse IJ, Egevang C, Phillips RA. Trans-equatorial migration, staging sites and wintering area of Sabine’s Gulls Larus sabini in the Atlantic Ocean. Ibis. 2012;154:42–51. doi: 10.1111/j.1474-919X.2011.01180.x. DOI

Hromádková T, Pavel V, Flousek J, Briedis M. Seasonally specific responses to wind patterns and ocean productivity facilitate the longest animal migration on Earth. Mar Ecol Prog Ser. 2020;638:1–12. doi: 10.3354/meps13274. DOI

Bonnet-Lebrun A-S, Dias MP, Phillips RA, Granadeiro JP, de Brooke ML, Chastel O, et al. Seabird migration strategies: flight budgets, diel activity patterns, and lunar influence. Front Mar Sci. 2021;8:683071. doi: 10.3389/fmars.2021.683071. DOI

Belopol’skii LO. Ecology of sea colony birds of the Barents Sea. Jerusalem: Israel Programme for Scientific Translations; 1961.

Hobson KA, Sirois J, Gloutney ML. Tracing nutrient allocation to reproduction with stable isotopes: a preliminary investigation using colonial waterbirds of Great Slave Lake. Auk. 2000;117:760–774. doi: 10.1093/auk/117.3.760. DOI

Pennycuick CJ. Modelling the flying bird. London: Academic Press; 2008.

Bergmann C. Ober die Verhaltnisse der Warmeokonomie der Thiere zu ihrer Grosse. Gott Stud. 1847;3:595–708.

Briedis M, Krist M, Král M, Voigt CC, Adamík P. Linking events throughout the annual cycle in a migratory bird non-breeding period buffers accumulation of carry-over effects. Behav Ecol Sociobiol. 2018;72:93. doi: 10.1007/s00265-018-2509-3. DOI

Carneiro C, Gunnarsson TG, Alves JA. Annual schedule adjustment by a long-distance migratory bird. Am Nat. 2023;201:353–362. doi: 10.1086/722566. PubMed DOI

Stutchbury BJM, Gow EA, Done T, MacPherson M, Fox JW, Afanasyev V. Effects of post-breeding moult and energetic condition on timing of songbird migration into the tropics. Proc R Soc B: Biol Sci. 2011;278:131–137. doi: 10.1098/rspb.2010.1220. PubMed DOI PMC

van Wijk RE, Schaub M, Bauer S. Dependencies in the timing of activities weaken over the annual cycle in a long-distance migratory bird. Behav Ecol Sociobiol. 2017;71:1–8.

Fayet AL, Freeman R, Shoji A, Kirk HL, Padget O, Perrins CM, et al. Carry-over effects on the annual cycle of a migratory seabird: an experimental study. J Anim Ecol. 2016;85:1516–1527. doi: 10.1111/1365-2656.12580. PubMed DOI PMC

van Bemmelen RSA, Clarke RH, Pyle P, Camphuysen CJ. Timing and duration of primary molt in Northern Hemisphere skuas and jaegers. Auk. 2018;135:1043–1054. doi: 10.1642/AUK-17-232.1. DOI

Åkesson S, Helm B. Endogenous programs and flexibility in bird migration. Front Ecol Evol. 2020;8:78. doi: 10.3389/fevo.2020.00078. DOI

Burnside RJ, Salliss D, Collar NJ, Dolman PM. Birds use individually consistent temperature cues to time their migration departure. Proc Natl Acad Sci. 2021;118:e2026378118. doi: 10.1073/pnas.2026378118. PubMed DOI PMC

Sergio F, Tanferna A, De Stephanis R, Jiménez LL, Blas J, Tavecchia G, et al. Individual improvements and selective mortality shape lifelong migratory performance. Nature. 2014;515:410–413. doi: 10.1038/nature13696. PubMed DOI

Battley PF, Conklin JR, Parody-Merino ÁM, Langlands PA, Southey I, Burns T, et al. Interacting roles of breeding geography and early-life settlement in godwit migration timing. Front Ecol Evol. 2020;8:52. doi: 10.3389/fevo.2020.00052. DOI

Edwards M, Hélaouët P, Goberville E, Lindley A, Tarling GA, Burrows MT, et al. North Atlantic warming over six decades drives decreases in krill abundance with no associated range shift. Commun Biol. 2021;4:644. doi: 10.1038/s42003-021-02159-1. PubMed DOI PMC

Kokko H. Competition for early arrival in migratory birds. J Anim Ecol. 1999;68:940–950. doi: 10.1046/j.1365-2656.1999.00343.x. DOI

Bearhop S, Fiedler W, Furness RW, Votier SC, Waldron S, Newton J, et al. Assortative mating as a mechanism for rapid evolution of a migratory divide. Science. 2005;310:502–504. doi: 10.1126/science.1115661. PubMed DOI

Bregnballe T, Frederiksen M, Gregersen J. Effects of distance to wintering area on arrival date and breeding performance in Great Cormorants. Ardea. 2006;94:619–630.

Grist H, Daunt F, Wanless S, Burthe SJ, Newell MA, Harris MP, et al. Reproductive performance of resident and migrant males, females and pairs in a partially migratory bird. J Anim Ecol. 2017;86:1010–1021. doi: 10.1111/1365-2656.12691. PubMed DOI PMC

Lok T, Veldhoen L, Overdijk O, Tinbergen JM, Piersma T. An age-dependent fitness cost of migration? Old trans-Saharan migrating spoonbills breed later than those staying in Europe, and late breeders have lower recruitment. J Anim Ecol. 2017;86:998–1009. doi: 10.1111/1365-2656.12706. PubMed DOI

Nightingale J, Gill JA, Gunnarsson TG, Rocha AD, Howison RA, Hooijmeijer JCEW, et al. Does early spring arrival lead to early nesting in a migratory shorebird? Insights from remote tracking. Ibis. 2023.

Perkins A, Ratcliffe N, Suddaby D, Ribbands B, Smith C, Ellis P, et al. Combined bottom-up and top-down pressures drive catastrophic population declines of Arctic skuas in Scotland. J Anim Ecol. 2018;87:1497–1748. doi: 10.1111/1365-2656.12890. PubMed DOI

van Bemmelen RSA, Schekkerman H, Hin V, Pot M, Janssen K, Ganter B, et al. Heavy decline of the largest European Arctic Skua Stercorarius parasiticus colony: interacting effects of food shortage and predation. Bird Study. 2021;68:13.

Santos I. Survival and breeding success of the declining Arctic Skua population of the Faroe Islands. University of Copenhagen, Denmark. MSc Thesis. 2018.

Mäntylä E, Mäntylä K, Nuotio J, Nuotio K, Sillanpää M. Longevity record of arctic skua (Stercorarius Parasiticus). Ecol Evol. 2020;ece3.6875. PubMed PMC

Santos IAM dos, Snell KRS, Bemmelen RS van, Moe B, Thorup K. Wintering, rather than breeding, oceanic conditions contribute to declining survival in a long-distance migratory seabird. bioRxiv; 2023. p. 2023.11.10.566398.

Fair JM, Jones J. Guidelines to the use of wild birds in research. Ornithol Counc; 2010.