Global phenological insensitivity to shifting ocean temperatures among seabirds


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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Fig. 1: SST trends and map of study sites included in the analyses.
Fig. 2: Mean and between-year variance in phenology separated by hemisphere.
Fig. 3: Funnel plots of phenological trends in relation to year and SST.


  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).

    Article  Google Scholar 

  2. 2.

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

    CAS  Article  Google Scholar 

  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).

    Article  Google Scholar 

  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).

    Article  Google Scholar 

  5. 5.

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

    CAS  Article  Google Scholar 

  6. 6.

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

    CAS  Article  Google Scholar 

  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).

    Article  Google Scholar 

  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).

    CAS  Article  Google Scholar 

  9. 9.

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

    Article  Google Scholar 

  10. 10.

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

    CAS  Article  Google Scholar 

  11. 11.

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

    Article  Google Scholar 

  12. 12.

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

    CAS  Article  Google Scholar 

  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).

    Article  Google Scholar 

  14. 14.

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

    CAS  Article  Google Scholar 

  15. 15.

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

    Article  Google Scholar 

  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).

    CAS  Article  Google Scholar 

  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).

    Article  Google Scholar 

  18. 18.

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

    Article  Google Scholar 

  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).

    Article  Google Scholar 

  21. 21.

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

    CAS  Article  Google Scholar 

  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).

    Article  Google Scholar 

  24. 24.

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

    Article  Google Scholar 

  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).

    Article  Google Scholar 

  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).

    Article  Google Scholar 

  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).

    CAS  Article  Google Scholar 

  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).

    Article  Google Scholar 

  29. 29.

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

    Article  Google Scholar 

  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).

    Article  Google Scholar 

  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).

    CAS  Article  Google Scholar 

  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).

    Article  Google Scholar 

  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).

    Article  Google Scholar 

  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).

    Article  Google Scholar 

  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).

    Google Scholar 

  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).

    Article  Google Scholar 

  37. 37.

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

    CAS  Article  Google Scholar 

  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).

    Article  Google Scholar 

  39. 39.

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

    Article  Google Scholar 

  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).

    Article  Google Scholar 

  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).

    Article  Google Scholar 

  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).

    Article  Google Scholar 

  46. 46.

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

    Article  Google Scholar 

  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).

    Article  Google Scholar 

  48. 48.

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

    Google Scholar 

  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).

    Article  Google Scholar 

  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).

    CAS  Article  Google Scholar 

  52. 52.

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

    CAS  Article  Google Scholar 

  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).

    Article  Google Scholar 

  54. 54.

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

    Article  Google Scholar 

  55. 55.

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

    Article  Google Scholar 

  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).

    CAS  Article  Google Scholar 

  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 ( 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.

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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.

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

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Supplementary Information

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

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

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Keogan, K., Daunt, F., Wanless, S. et al. Global phenological insensitivity to shifting ocean temperatures among seabirds. Nature Clim Change 8, 313–318 (2018).

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