Global phenological insensitivity to shifting ocean temperatures among seabirds

  • Nature Climate Changevolume 8pages313318 (2018)
  • doi:10.1038/s41558-018-0115-z
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Reproductive timing in many taxa plays a key role in determining breeding productivity1, and is often sensitive to climatic conditions2. Current climate change may alter the timing of breeding at different rates across trophic levels, potentially resulting in temporal mismatch between the resource requirements of predators and their prey3. This is of particular concern for higher-trophic-level organisms, whose longer generation times confer a lower rate of evolutionary rescue than primary producers or consumers4. However, the disconnection between studies of ecological change in marine systems makes it difficult to detect general changes in the timing of reproduction5. Here, we use a comprehensive meta-analysis of 209 phenological time series from 145 breeding populations to show that, on average, seabird populations worldwide have not adjusted their breeding seasons over time (−0.020 days yr−1) or in response to sea surface temperature (SST) (−0.272 days °C−1) between 1952 and 2015. However, marked between-year variation in timing observed in resident species and some Pelecaniformes and Suliformes (cormorants, gannets and boobies) may imply that timing, in some cases, is affected by unmeasured environmental conditions. This limited temperature-mediated plasticity of reproductive timing in seabirds potentially makes these top predators highly vulnerable to future mismatch with lower-trophic-level resources2.

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  1. 1.

    Visser, M. E. & Both, C. Shifts in phenology due to global climate change: the need for a yardstick. Proc. R. Soc. B 272, 2561–2569 (2005).

  2. 2.

    Thackeray, S. J. et al. Phenological sensitivity to climate across taxa and trophic levels. Nature 535, 241–245 (2016).

  3. 3.

    Thackeray, S. J. et al. Trophic level asynchrony in rates of phenological change for marine, freshwater and terrestrial environments. Glob. Change Biol. 16, 3304–3313 (2010).

  4. 4.

    Visser, M. E., Both, C. & Lambrechts, M. M. Global climate change leads to mistimed avian reproduction. Adv. Ecol. Res. 35, 89–110 (2004).

  5. 5.

    Richardson, A. J. & Poloczanska, E. S. Under-resourced, under threat. Science 320, 1294–1295 (2008).

  6. 6.

    Walther, G. et al. Ecological responses to recent climate change. Nature 416, 389–395 (2002).

  7. 7.

    Miller-Rushing, A. J., Høye, T. T., Inouye, D. W. & Post, E. The effects of phenological mismatches on demography. Phil. Trans. R. Soc. Lond. B 365, 3177–3186 (2010).

  8. 8.

    Purvis, A., Gittleman, J. L., Cowlishaw, G. & Mace, G. M. Predicting extinction risk in declining species. Proc. R. Soc. Lond. B 267, 1947–1952 (2000).

  9. 9.

    Poloczanska, E. S. et al. Global imprint of climate change on marine life. Nat. Clim. Change 3, 919–925 (2013).

  10. 10.

    Chambers, L. E. et al. Phenological changes in the Southern hemisphere. PLoS ONE 8, e75514 (2013).

  11. 11.

    Poloczanska, E. S. et al. Responses of marine organisms to climate change across oceans. Front. Mar. Sci. 3, 1–21 (2016).

  12. 12.

    Sydeman, W. J., Poloczanska, E. S., Reed, T. E. & Thompson, S. A. Climate change and marine vertebrates. Science 350, 772–777 (2015).

  13. 13.

    Sydeman, W. J., Thompson, S. A. & Kitaysky, A. Seabirds and climate change: roadmap for the future. Mar. Ecol. Prog. Ser. 454, 107–117 (2012).

  14. 14.

    Parmesan, C. & Yohe, G. A globally coherent fingerprint of climate change impacts across natural systems. Nature 421, 37–42 (2003).

  15. 15.

    Dunn, P. O. & Møller, A. P. Changes in breeding phenology and population size of birds. J. Anim. Ecol. 83, 729–739 (2014).

  16. 16.

    Hadfield, J. D. & Nakagawa, S. General quantitative genetic methods for comparative biology: phylogenies, taxonomies and multi-trait models for continuous and categorical characters. J. Evol. Biol. 23, 494–508 (2010).

  17. 17.

    Youngflesh, C. et al Circumpolar analysis of the Adelie penguin reveals the importance of environmental variability in phenological mismatch. Ecology 98, 940–951 (2017).

  18. 18.

    Croxall, J. P. et al. Seabird conservation status, threats and priority actions: a global assessment. Bird Conserv. Int. 22, 1–34 (2012).

  19. 19.

    Schreiber, E. A. & Burger, J. Biology of Marine Birds (CRC, Boca Raton, 2002).

  20. 20.

    Chambers, L. E., Dann, P., Cannell, B. & Woehler, E. J. Climate as a driver of phenological change in southern seabirds. Int. J. Biometeorol. 58, 603–612 (2014).

  21. 21.

    Cheung, W. W. L., Watson, R. & Pauly, D. Signature of ocean warming in global fisheries catch. Nature 497, 365–368 (2013).

  22. 22.

    Ainley, D. & Boekelheide, R. Seabirds of the Farallon Islands: Ecology Dynamics and Structure of an Upwelling-system Community (Stanford University Press, Palo Alto, 1990).

  23. 23.

    Mesquita, M. D. S. et al. There is more to climate than the North Atlantic Oscillation: a new perspective from climate dynamics to explain the variability in population growth rates of a long-lived seabird. Front. Ecol. Evol. 3, 1–14 (2015).

  24. 24.

    Nakagawa, S. & Santos, E. S. A. Methodological issues and advances in biological meta-analysis. Evol. Ecol. 26, 1253–1274 (2012).

  25. 25.

    Wanless, S., Harris, M. P., Lewis, S., Frederiksen, M. & Murray, S. Later breeding in northern gannets in the eastern Atlantic. Mar. Ecol. Prog. Ser. 370, 263–269 (2008).

  26. 26.

    Burr, Z. M. et al. Later at higher latitudes: large-scale variability in seabird breeding timing and synchronicity. Ecosphere 7, 1–12 (2016).

  27. 27.

    Bradshaw, W. E. & Holzapfel, C. M. Light, time, and the physiology of biotic response to rapid climate change in animals. Annu. Rev. Physiol. 72, 147–166 (2010).

  28. 28.

    Moussus, J.-P., Clavel, J., Jiguet, F. & Julliard, R. Which are the phenologically flexible species? A case study with common passerine birds. Oikos 120, 991–998 (2011).

  29. 29.

    Gwinner, E. Circannual clocks in avian reproduction and migration. Ibis 138, 47–63 (1996).

  30. 30.

    Dawson, A. Control of the annual cycle in birds: endocrine constraints and plasticity in response to ecological variability. Phil. Trans. R. Soc. B 363, 1621–1633 (2008).

  31. 31.

    Daunt, F. et al. Longitudinal bio-logging reveals interplay between extrinsic and intrinsic carry-over effects in a long-lived vertebrate. Ecology 95, 2077–2083 (2014).

  32. 32.

    McLean, N. Lawson, C. R., Leech, D. I. & van de Pol, M. Predicting when climate-driven phenotypic change affects population dynamics. Ecol. Lett. 19, 595–608 (2016).

  33. 33.

    Durant, J. M., Hjermann, D. O., Ottersen, G. & Stenseth, N. C. Climate and the match or mismatch between predator requirements and resource availability. Clim. Res. 33, 271–283 (2007).

  34. 34.

    Burthe, S. et al. Phenological trends and trophic mismatch across multiple levels of a North Sea pelagic food web. Mar. Ecol. Prog. Ser. 454, 119–133 (2012).

  35. 35.

    Reed, T. E., Grotan, V., Jenouvrier, S., Saether, B.-E. & Visser, M. E. Population growth in a wild bird is buffered against phenological mismatch. Science 53, 1689–1699 (2013).

  36. 36.

    Howells, R. J. et al. From days to decades: short- and long-term variation in environmental conditions affect diet composition of a marine top-predator. Mar. Ecol. Prog. Ser. 583, 227–242 (2017).

  37. 37.

    Stevenson, I. R. & Bryant, D. M. Climate change and constraints on breeding. Nature 406, 366–367 (2000).

  38. 38.

    Furness, R. W. & Tasker, M. L. Seabird-fishery interactions: quantifying the sensitivity of seabirds to reductions in sandeel abundance, and identification of key areas for sensitive seabirds in the North Sea. Mar. Ecol. Prog. Ser. 202, 253–264 (2000).

  39. 39.

    Chavez, F. P. & Messié, M. A comparison of Eastern Boundary upwelling ecosystems. Prog. Oceanogr. 83, 80–96 (2009).

  40. 40.

    Reed, T. E. et al. Timing is everything: flexible phenology and shifting selection in a colonial seabird. J. Anim. Ecol. 78, 376–387 (2009).

  41. 41.

    IPCC: Summary for Policmakers. In Climate Change 2013: The Physical Science Basis (eds Stocker, T. F. et al.) 1–30 (Cambridge Univ. Press, 2013).

  42. 42.

    Reynolds, R. W., Rayner, N. A., Smith, T. M., Stokes, D. C. & Wang, W. An improved in situ and satellite SST analysis for climate. J. Clim. 15, 1609–1625 (2002).

  43. 43.

    Trujillo, A. & Thurman, H. Essentials of Oceanography 11th edn (Pearson Prentice Hall, Upper Saddle River, 2014).

  44. 44.

    Longhurst, A. Ecological Geography of the Sea (Academic, San Diego, 2006).

  45. 45.

    Stenseth, N. C. et al. Studying climate effects on ecology through the use of climate indices: the North Atlantic Oscillation, El Niño Southern Oscillation and beyond. Proc. R. Soc. B 270, 2087–2096 (2003).

  46. 46.

    Passuni, G. et al. Seasonality in marine ecosystems: Peruvian seabirds, anchovy and oceanographic conditions. Ecology 97, 182–193 (2015).

  47. 47.

    Sabarros, P. S., Durant, J. M., Grémillet, D., Crawford, R. J. M. & Stenseth, N. C. Differential responses of three sympatric seabirds to spatio-temporal variability in shared resources. Mar. Ecol. Prog. Ser. 468, 291–301 (2012).

  48. 48.

    Cabot, D. & Nisbet, I. Terns (HarperCollins, London, 2013).

  49. 49.

    Reiss, M. J. The Scaling of Average Daily Metabolic Rate and Energy Intake. The Allometry of Growth and Reproduction (Cambridge Univ. Press, Cambridge, 1989).

  50. 50.

    Romero-Romero, S., Molina-Ramírez, A., Höfer, J. & Acuña, J. L. Body size-based trophic structure of a deep marine ecosystem. Ecology 97, 171–181 (2016).

  51. 51.

    Jetz, W., Thomas, G. H., Joy, J. B., Hartmann, K. & Mooers, A. O. The global diversity of birds in space and time. Nature 491, 444–448 (2012).

  52. 52.

    Hackett, S. J. et al. A phylogenomic study of birds reveals their evolutionary history. Science 320, 1763–1768 (2008).

  53. 53.

    Hadfield, J. D. MCMC methods for multi-response generalized linear mixed models: The MCMCglmm R package. J. Stat. Softw. 33, 1–22 (2010).

  54. 54.

    Housworth, E. A., Martins, E. P. & Lynch, M. The phylogenetic mixed model. Am. Nat. 163, 84–96 (2004).

  55. 55.

    Nakagawa, S. et al. Meta-analysis of variation: ecological and evolutionary applications and beyond. Methods Ecol. Evol. 6, 143–152 (2015).

  56. 56.

    Pinheiro, J. & Bates, D. Mixed-Effects Models in S and S-PLUS (Springer, New York, 2000).

  57. 57.

    Box, G. E. P. & Jenkins, G. Time Series Analysis, Forecasting and Control (ACM, New York, 1990).

  58. 58.

    Brierley, A. S. & Kingsford, M. J. Impacts of climate change on marine organisms and ecosystems. Curr. Biol. 19, R602–R614 (2009).

  59. 59.

    Pagel, M. & Lutzoni, F. Accounting for phylogenetic uncertainty in comparative studies of evolution and adaptation. Biol. Evol. Stat. Phys. 148–162 (2002).

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The work presented here could not have been carried out without the long-term data collection by field workers at all sites. The authors thank the staff of the Alaska Maritime National Wildlife Refuge; Department of Fisheries; DPaW; Environment Canada; Natural Resources Canada; New Bedford Harbor Trustee Council; Oamaru Blue Penguin Colony; Phillip Island Nature Parks; Government of Greenland (Ministry of Domestic Affairs, Nature and Environment) in Nuuk; Island Conservation Society for permission to work on Aride Island, Seychelles; Aage V Jensen Charity Foundation; The Norwegian Environment Agency (and its predecessors), the SEAPOP programme (www.seapop.no) and its key institutions: The Norwegian Institute for Nature Research, The Norwegian Polar Institute and Tromsø University Museum; South African National Antarctic Programme; US Fish and Wildlife Service; Government of Tristan da Cunha; the British Antarctic Survey. Specific thanks go to B. Sydeman, S. Surman, M. McCrae, B. Fogg, M. Davidson, P. Boschetti, T. Catry, P. Pedro, L. Demongin, M. Eens, P. Quillfeldt, B. Sabard, J. Moreau, E. Buchel, V. Gilg, V. Heuacker, A. Harding, F. Amélineau, J. Nezan, K. Kerry, J. Clarke, A. Kato, T. Deguchi, M. Ito, P. Dann, L. Renwick, P. Wasiak, A. Gómez-Laich, P. Giudicci, L. Gallo, S. Harris, D. Houston, P. Menkhorst, F. I. Norman, C. M. Burke, N. Laite, P. Mallam, P. M. Regular, H. Renner, N. Rojek, M. Romano, L. Slater, T. Birkhead, J. Hadfield and A. Gaston. K.K. was supported by a Principal’s Career Development Scholarship from the University of Edinburgh. A.B.P. was funded by a NERC fellowship (Ne/I020598/1). S.L. was funded by a NERC fellowship (NE/E012906/1) and by NERC National Capability. F.D. and S.W. were funded by CEH and JNCC. N.D. and M.P. were supported with post-doctoral fellowship grants by the Research Fund – Flanders FWO (1265414N and 12Q6915N to N.D.) and (1.2.619.10.N.00 and to M.P.). F.Q. was funded by the National Research Council of Argentina (CONICET): PIP 5387/05, PIP 11420100100186 and PIP 11220130100268, Ministerio de Ciencia, Tecnología e Innovación Productiva Argentina: PICT 04-20343, PICT 13-1229 and Wildlife Conservation Society research grant (ARG_5AR03). P.C. and J.P.G. were funded by FCT – Portugal through UID/MAR/04292/2013 granted to MARE and the Falkland Islands Government. W.A.M. and A.H. were supported by NSERC (Discovery Grant (W.A.M.) and PDF (A.H.)), Environment Canada and Memorial University of Newfoundland. A.W.D. is funded by NSERC, Environment Canada and the New Brunswick Wildlife Council, by agreement with the Canadian Wildlife Service (Atlantic Region). R.A.P., M.J.D. and A.G.W. work as part of British Antarctic Survey Polar Science for Planet Earth Programme (Ecosystems component), funded by the Natural Environment Research Council. T.M.P. was funded by BirdLife Australia, Deakin University, Department of Conservation and Natural Resources, and Holsworth Wildlife Research Fund. The Banter See common tern study was performed under a licence of the city of Wilhelmshaven and supported by the Deutsche Forschungsgemeinschaft (BE 916/3 to 9). Data from Béchervaise Island were collected following protocols approved by the Australian Antarctic Animal Ethics Committee and supported through the Australian Antarctic programme through Australian Antarctic Science projects 2205, 2722 and 4087. The field work in Norway and Svalbard was an integrated part of the SEAPOP programme, with financial support from the Norwegian Environment Agency, Ministry of Climate and Environment, Ministry of Petroleum and Energy and the Norwegian Oil and Gas Association. The French Polar Institute funded the field work at Hochstetter (IPEV; program ‘1036 Interactions’) and Ukaleqarteq (program ‘388’). D.G.A., G.B., K.M.D., P.J.K. and A.L. were supported by US National Science Foundation grants OPP 9526865, 9814882, 0125608, 0944411 and 0440643 with logistical support from the US Antarctic Program. P.O.L. and P.R.W. were supported by New Zealand’s Ministry of Business, Innovation and Employment Grants C09X0510 and C01X1001, with logistical support from the NZ Antarctic Programme.

Author information

Author notes

  1. These authors contributed equally: Albert B. Phillimore and Sue Lewis.


  1. Institute of Evolutionary Biology, University of Edinburgh, Ashworth Laboratories, Edinburgh, UK

    • Katharine Keogan
    • , Craig A. Walling
    • , Albert B. Phillimore
    •  & Sue Lewis
  2. Centre for Ecology & Hydrology, Bush Estate, Penicuik, UK

    • Francis Daunt
    • , Sarah Wanless
    • , Mike Harris
    • , Mark Newell
    •  & Sue Lewis
  3. British Antarctic Survey, Natural Environment Research Council, High Cross, Cambridge, UK

    • Richard A. Phillips
    • , Michael J. Dunn
    •  & Andrew G. Wood
  4. Oamaru Blue Penguin Colony, Oamaru, New Zealand

    • Philippa Agnew
  5. HT Harvey and Associates, Los Gatos, CA, USA

    • David G. Ainley
  6. Norwegian Institute for Nature Research (NINA), Trondheim, Norway

    • Tycho Anker-Nilssen
    • , Signe Christensen-Dalsgaard
    • , Sveinn A. Hanssen
    • , Magdalene Langset
    • , Svein-Håkon Lorentsen
    •  & Børge Moe
  7. Point Blue Conservation Science, Petaluma, CA, USA

    • Grant Ballard
    • , Russell W. Bradley
    • , Jaime Jahncke
    •  & Pete Warzybok
  8. Department of Natural Sciences, Tromsø University Museum, Tromsø, Norway

    • Robert T. Barrett
  9. Landcare Research , Nelson, New Zealand

    • Kerry J. Barton
  10. Department of Biology, Norwegian University of Science and Technology, Trondheim, Norway

    • Claus Bech
  11. Institute of Avian Research, Wilhelmshaven, Germany

    • Peter Becker
    •  & Sandra Bouwhuis
  12. Institute of Marine Research, Department of Aquatic Resources, Swedish University of Agricultural Sciences, Uppsala, Sweden

    • Per-Arvid Berglund
  13. Groupe de Recherche en Ecologie Arctique, Francheville, France

    • Loïc Bollache
    • , Olivier Gilg
    • , Johannes Lang
    •  & Benoit Sittler
  14. Laboratoire Chrono-environnement, Université de Bourgogne France Comté, Besançon, France

    • Loïc Bollache
  15. RSPB Centre for Conservation Science, Royal Society for the Protection of Birds, The Lodge, Sandy, UK

    • Alexander L. Bond
    •  & Richard Cuthbert
  16. Department of Biology, Memorial University of Newfoundland, St John’s, Newfoundland and Labrador, Canada

    • Alexander L. Bond
  17. The University Centre in Svalbard, Longyearbyen, Norway

    • Zofia M. Burr
  18. Department of Coastal Systems, Royal Netherlands Institute for Sea Research Den Burg, Texel & Utrecht University, Utrecht, Netherlands

    • Kees Camphuysen
  19. MARE – Marine and Environmental Sciences Centre, ISPA – Instituto Universitário, Lisbon, Portugal

    • Paulo Catry
  20. Phillip Island Nature Parks, Cowes, Victoria, Australia

    • Andre Chiaradia
  21. School of Biological Sciences, Monash University, Melbourne, Victoria, Australia

    • Andre Chiaradia
  22. Department of Biology, Behavioural Ecology and Ecophysiology Group, University of Antwerp, , Antwerp (Wilrijk), Belgium

    • Nina Dehnhard
    •  & Maud Poisbleau
  23. Norwegian Polar Institute (FRAM), High North Research Centre for Climate and the Environment, Tromsø, Norway

    • Sébastien Descamps
    • , Kjell Einar Erikstad
    •  & Tone Kirstin Reiertsen
  24. University of New Brunswick, Fredericton, New Brunswick, Canada

    • Tony Diamond
  25. Friends of Cooper Island, Seattle, WA, USA

    • George Divoky
  26. Instituto de Ecología, Universidad Nacional Autónoma de México , Mexico City, Mexico

    • Hugh Drummond
    •  & Cristina Rodríguez
  27. US Geological Survey, Oregon Cooperative Fish and Wildlife Research Unit Department of Fisheries and Wildlife , Corvallis, OR, USA

    • Katie M. Dugger
  28. Australian Antarctic Division, Kingston, Tasmania, Australia

    • Louise Emmerson
    •  & Colin Southwell
  29. Centre for Conservation Biology, Department of Biology, Norwegian University of Science and Technology, Trondheim, Norway

    • Kjell Einar Erikstad
  30. Littoral Environnement et Sociétés (LIENSs), UMR 7266, CNRS – Université de La Rochelle, La Rochelle, France

    • Jérôme Fort
  31. Polar Oceans Research Group, Sheridan, MT, USA

    • William Fraser
  32. Population Ecology Group, IMEDEA (CSIC-UIB), Esporles, Spain

    • Meritxell Genovart
    • , José Manuel Igual
    • , Daniel Oro
    •  & Ana Sanz-Aguilar
  33. Laboratoire Biogéosciences, UMR 6282, CNRS – Université de Bourgogne Franche Comté, Dijon, France

    • Olivier Gilg
  34. Departament de Biologia Animal, Universitat de Barcelona, Barcelona, Spain

    • Jacob González-Solís
    •  & Raül Ramos
  35. CESAM, Departamento de Biologia Animal, Faculdade de Ciências, Universidade de Lisboa, Campo Grande, Lisbon, Portugal

    • José Pedro Granadeiro
  36. Centre d’Ecologie Fonctionnelle et Evolutive, UMR 5175, CNRS – Université de Montpellier – Université Paul-Valéry Montpellier – EPHE, Montpellier, France

    • David Grémillet
    •  & Amélie Lescroël
  37. FitzPatrick Institute, DST-NRF Centre of Excellence at the University of Cape Town, Rondebosch, South Africa

    • David Grémillet
  38. Department of Bioscience, Aarhus University, Aarhus, Denmark

    • Jannik Hansen
  39. Wildlife Research Division, Science and Technology Branch, Environment and Climate Change Canada, Mount Pearl, Newfoundland and Labrador, Canada

    • April Hedd
  40. Antarctic Ecosystem Research Division, National Marine Fisheries Service, National Oceanic and Atmospheric Administration, La Jolla, CA, USA

    • Jefferson Hinke
  41. Department of Biology, Memorial University, St John’s, Newfoundland and Labrador, Canada

    • Ian Jones
  42. Oregon Cooperative Fish and Wildlife Research Unit, Department of Fisheries and Wildlife , Corvallis, OR, USA

    • Peter J. Kappes
  43. Clinic for Birds, Reptiles, Amphibians and Fish, Justus-Liebig-University Giessen, Giessen, Germany

    • Johannes Lang
  44. Landcare Research, Lincoln, New Zealand

    • Phil O’B. Lyver
  45. Biology, Acadia University, Wolfville, Nova Scotia, Canada

    • Mark Mallory
  46. Department of Psychology, Biology and Ocean Sciences, Memorial University of Newfoundland, St John’s, Newfoundland and Labrador, Canada

    • William A. Montevecchi
  47. MARE – Marine and Environmental Sciences Centre, Department of Life Sciences, University of Coimbra, Coimbra, Portugal

    • David Monticelli
    •  & Jaime A. Ramos
  48. Massachusetts Division of Fisheries and Wildlife, Westborough, MA, USA

    • Carolyn Mostello
  49. Halfmoon Biosciences, Ocean Beach, Western Australia, Australia

    • Lisa Nicholson
    •  & Christopher Surman
  50. I. C. T. Nisbet & Company, North Falmouth, MA, USA

    • Ian Nisbet
  51. Stockholm Resilience Centre, Stockholm University, Stockholm, Sweden

    • Olof Olsson
  52. Laskeek Bay Conservation Society, Queen Charlotte, British Columbia, Canada

    • Vivian Pattison
  53. Deakin Centre for Integrative Ecology, School of Life and Environmental Sciences, Deakin University, Burwood, Victoria, Australia

    • Tanya Pyk
  54. Instituto de Biología de Organismos Marinos (IBIOMAR-CONICET), Puerto Madryn, Chubut, Argentina

    • Flavio Quintana
  55. Percy FitzPatrick Institute of African Ornithology, DST/NRF Centre of Excellence, University of Cape Town, Rondebosch, South Africa

    • Peter Ryan
  56. Arctic Research Centre, Department of Bioscience, Aarhus University, Aarhus, Denmark

    • Niels M. Schmidt
  57. National Audubon Society Seabird Restoration Program, Bremen, ME, USA

    • Paula Shannon
  58. Chair Nature Protection and Landscape Ecology, University of Freiburg, Freiburg, Germany

    • Benoit Sittler
  59. Instituto de Investigaciones Marinas y Costeras (IIMyC), Universidad Nacional de Mar del Plata-CONICET, Mar del Plata, Buenos Aires, Argentina

    • Walter S. Svagelj
  60. 5959 Shoreline Highway, Bolinas, CA, USA

    • Wayne Trivelpiece
  61. Graduate School of Fisheries Sciences, Hokkaido University, Hakodate, Japan

    • Yutaka Watanuki
  62. CEBC, Centre National de la Recherche Scientifique (CNRS), Villiers-en-Bois, France

    • Henri Weimerskirch
  63. Landcare Research, Tamaki Campus, Auckland, New Zealand

    • Peter R. Wilson


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K.K., S.L., A.B.P., S.W., F.D. and R.P. conceived the study and wrote the manuscript. K.K. coordinated the study, compiled the data set and wrote the first draft of the manuscript. K.K. conducted the statistical analyses under the guidance of A.B.P. and with advice from S.L. and C.A.W. All others provided data and comments on later drafts of the manuscript.

Competing interests

The authors declare no competing interests.

Corresponding authors

Correspondence to Katharine Keogan or Albert B. Phillimore or Sue Lewis.

Supplementary information

  1. Supplementary Information

    Supplementary Tables 1–9, Supplementary Figure 1, Supplementary Methods, Supplementary References, PRISMA checklist

  2. Supplementary Data 1

    This file includes population-level estimates of interannual mean breeding phenology (and standard error); between-year standard deviation (and its sampling variance); the slope estimates (and standard error) for the change in phenology over time and in relation to sea surface temperature. It also includes the life history and biogeographical data for each population that we use in the meta-analyses