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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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 1.5.020.11.N.00 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.
The authors declare no competing interests.
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Supplementary Tables 1–9, Supplementary Figure 1, Supplementary Methods, Supplementary References, PRISMA checklist
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). https://doi.org/10.1038/s41558-018-0115-z
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