Abstract

Differences in phenological responses to climate change among species can desynchronise ecological interactions and thereby threaten ecosystem function. To assess these threats, we must quantify the relative impact of climate change on species at different trophic levels. Here, we apply a Climate Sensitivity Profile approach to 10,003 terrestrial and aquatic phenological data sets, spatially matched to temperature and precipitation data, to quantify variation in climate sensitivity. The direction, magnitude and timing of climate sensitivity varied markedly among organisms within taxonomic and trophic groups. Despite this variability, we detected systematic variation in the direction and magnitude of phenological climate sensitivity. Secondary consumers showed consistently lower climate sensitivity than other groups. We used mid-century climate change projections to estimate that the timing of phenological events could change more for primary consumers than for species in other trophic levels (6.2 versus 2.5–2.9 days earlier on average), with substantial taxonomic variation (1.1–14.8 days earlier on average).

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References

  1. 1.

    IPCC. Climate Change 2014: Impacts, Adaptation, and Vulnerability. Part A: Global and Sectoral Aspects. Contribution of Working Group II to the Fifth Assessment Report of the Intergovernmental Panel on Climate Change 1132 (Cambridge Univ. Press, 2014)

  2. 2.

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

  3. 3.

    et al. Fingerprints of global warming on wild animals and plants. Nature 421, 57–60 (2003)

  4. 4.

    , , , & Climate change and unequal phenological changes across four trophic levels: constraints or adaptations? J. Anim. Ecol. 78, 73–83 (2009)

  5. 5.

    , & Shifts in caterpillar biomass phenology due to climate change and its impact on the breeding biology of an insectivorous bird. Oecologia 147, 164–172 (2006).

  6. 6.

    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)

  7. 7.

    & A freshwater predator hit twice by the effects of warming across trophic levels. Nat. Commun. 6, 5992 (2015)

  8. 8.

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

  9. 9.

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

  10. 10.

    et al. Ecology. Tracking progress toward the 2010 biodiversity target and beyond. Science 325, 1503–1504 (2009)

  11. 11.

    et al. Global biodiversity: indicators of recent declines. Science 328, 1164–1168 (2010)

  12. 12.

    , , , & Towards an integrated framework for assessing the vulnerability of species to climate change. PLoS Biol. 6, e325 (2008)

  13. 13.

    & Climate change reduces reproductive success of an Arctic herbivore through trophic mismatch. Philos. Trans. R. Soc. B Biol. Sci. 363, 2367–2373 (2008)

  14. 14.

    , & Long-term change in the phenology of spring phytoplankton: species-specific responses to nutrient enrichment and climatic change. J. Ecol. 96, 523–535 (2008)

  15. 15.

    , & Heterogeneous intra-annual climatic changes drive different phenological responses at two trophic levels. Clim. Res. 36, 181–190 (2008)

  16. 16.

    , , & Warmer springs lead to mistimed reproduction in great tits (Parus major). Proc. R. Soc. Lond. B 265, 1867–1870 (1998)

  17. 17.

    & Identifying the critical climatic time window that affects trait expression. Am. Nat. 177, 698–707 (2011)

  18. 18.

    , , , & When phenology matters: age–size truncation alters population response to trophic mismatch. Proc. R. Soc. Lond. B 281, 20140938 (2014)

  19. 19.

    , , & Eight decades of phenological change for a freshwater cladoceran: what are the consequences of our definition of seasonal timing? Freshw. Biol. 57, 345–359 (2012)

  20. 20.

    , , & Differences in spawning date between populations of common frog reveal local adaptation. Proc. Natl Acad. Sci. USA 107, 8292–8297 (2010); correction 109, 5134 (2012)

  21. 21.

    , , & A 250-year index of first flowering dates and its response to temperature changes. Proc. R. Soc. Lond. B 277, 2451–2457 (2010)

  22. 22.

    et al. Spring phytoplankton phenology — are patterns and drivers of change consistent among lakes in the same climatological region? Freshw. Biol. 57, 331–344 (2012)

  23. 23.

    , , , & Constraints on plastic responses to climate variation in red deer. Biol. Lett. 1, 457–460 (2005)

  24. 24.

    & Aphids as Crop Pests. 717 (CABI, 2007)

  25. 25.

    , & Divergent responses to spring and winter warming drive community level flowering trends. Proc. Natl Acad. Sci. USA 109, 9000–9005 (2012)

  26. 26.

    , , , & Population growth in a wild bird is buffered against phenological mismatch. Science 340, 488–491 (2013)

  27. 27.

    et al. Links between plant species’ spatial and temporal responses to a warming climate. Proc. R. Soc. Lond. B 281, 20133017 (2014)

  28. 28.

    , , & The effects of phenological mismatches on demography. Philos. Trans. R. Soc. B 365, 3177–3186 (2010)

  29. 29.

    & A perspective on match/mismatch of phenology in community contexts. Oikos 121, 489–495 (2012)

  30. 30.

    et al. Creating a safe operating space for iconic ecosystems. Science 347, 1317–1319 (2015)

  31. 31.

    & The generation of monthly gridded data sets for a range of climatic variables over the UK. Int. J. Climatol. 25, 1041–1054 (2005)

  32. 32.

    , & Assessment of long-term changes in habitat availability for Arctic charr (Salvelinus alpinus) in a temperate lake using oxygen profiles and hydroacoustic surveys. Freshw. Biol. 53, 393–402 (2008)

  33. 33.

    Numerical changes and population regulation in young migratory trout Salmo trutta in a Lake District stream, 1966–83. J. Anim. Ecol. 53, 327–350 (1984)

  34. 34.

    , & A nonlinear regression model for weekly stream temperatures. Wat. Resour. Res. 34, 2685–2692 (1998)

  35. 35.

    et al. Global analyses of sea surface temperature, sea ice, and night marine air temperature since the late nineteenth century. J. Geophys. Res. 108, 4407 (2003)

  36. 36.

    , , & The Continuous Plankton Recorder: concepts and history, from Plankton Indicator to undulating recorders. Prog. Oceanogr. 58, 117–173 (2003)

  37. 37.

    et al. Detecting nonlinear response of spring phenology to climate change by Bayesian analysis. Glob. Change Biol. 19, 1518–1525 (2013)

  38. 38.

    R Development Core Team. R: A Language and Environment for Statistical Computing (2011)

  39. 39.

    Stable and efficient multiple smoothing parameter estimation for generalized additive models. J. Am. Stat. Assoc. 99, 673–686 (2004)

  40. 40.

    , & lme4: Linear Mixed-Effects Models using S4 Classes (2011)

Download references

Acknowledgements

This work was funded by Natural Environment Research Council (NERC) grant NE/J02080X/1. We thank O. Mountford for assigning species traits for plants, H. Feuchtmayr for extracting plankton data for analysis and N. Dodd for air and water temperature data from the Tarland Burn. We also thank P. Verrier, the staff and many volunteers and contributors, including Science and Advice for Scottish Agriculture, to the Rothamsted Insect Survey (RIS) over the last half century. The RIS is a National Capability strategically funded by BBSRC. The consortium represented by the authorship list hold long-term data that represent a considerable investment in scientific endeavour. Whilst we are committed to sharing these data for scientific research, users are requested to collaborate before publication of these data to ensure accurate biological interpretation.

Author information

Affiliations

  1. Centre for Ecology & Hydrology, Lancaster Environment Centre, Library Avenue, Bailrigg, Lancaster, Lancashire LA1 4AP, UK

    • Stephen J. Thackeray
    • , Peter A. Henrys
    • , Ian D. Jones
    • , Eleanor B. Mackay
    •  & Ian J. Winfield
  2. Met Office, FitzRoy Road, Exeter, Devon EX1 3PB, UK

    • Deborah Hemming
  3. Rothamsted Research, West Common, Harpenden, Hertfordshire AL5 2JQ, UK

    • James R. Bell
    •  & Richard Harrington
  4. Centre for Ecology & Hydrology, Maclean Building, Benson Lane, Crowmarsh Gifford, Wallingford, Oxfordshire OX10 8BB, UK

    • Marc S. Botham
  5. Centre for Ecology & Hydrology, Bush Estate, Penicuik, Midlothian EH26 0QB, UK

    • Sarah Burthe
    • , Laurence Carvalho
    •  & Sarah Wanless
  6. The Sir Alister Hardy Foundation for Ocean Science, The Laboratory, Citadel Hill, Plymouth, Devon PL1 2PB, UK

    • Pierre Helaouet
    • , David G. Johns
    •  & Martin Edwards
  7. British Trust for Ornithology, The Nunnery, Thetford, Norfolk IP24 2PU, UK

    • David I. Leech
    • , Dario Massimino
    •  & James W. Pearce-Higgins
  8. The Woodland Trust, Kempton Way, Grantham, Lincolnshire NG31 6LL, UK

    • Sian Atkinson
  9. Futtie Park, Banchory, Aberdeen AB31 4RX, UK

    • Philip J. Bacon
  10. Butterfly Conservation, Manor Yard, East Lulworth, Wareham, Dorset BH20 5QP, UK

    • Tom M. Brereton
  11. Department of Zoology, University of Cambridge, Downing Street, Cambridge CB2 3EJ, UK

    • Tim H. Clutton-Brock
  12. Sea Mammal Research Unit, Scottish Oceans Institute, East Sands, University of St Andrews, St Andrews, Fife KY16 8LB, UK

    • Callan Duck
  13. The Freshwater Biological Association, The Ferry Landing, Far Sawrey, Ambleside, Cumbria LA22 0LP, UK

    • J. Malcolm Elliott
  14. University of Lincoln, Riseholme Hall, Riseholme Park, Lincoln, Lincolnshire LN2 2LG, UK

    • Stephen J. G. Hall
  15. Aarhus Institute of Advanced Studies, Department of Bioscience and Arctic Research Centre, Aarhus University, Høegh-Guldbergs Gade 6B, DK-8000 Aarhus C, Denmark

    • Toke T. Høye
  16. Institute of Evolutionary Biology, School of Biological Sciences, University of Edinburgh, Edinburgh EH9 3FL, UK

    • Loeske E. B. Kruuk
    •  & Josephine M. Pemberton
  17. Research School of Biology, The Australian National University, ACT 2612 Australia

    • Loeske E. B. Kruuk
  18. Faculty of Engineering and Computing, Coventry University, Priory Street, Coventry CV1 5FB, UK

    • Tim H. Sparks
  19. Institute of Zoology, Poznan´ University of Life Sciences, Wojska Polskiego 71C, 60-625 Poznan´, Poland

    • Tim H. Sparks
  20. University of Aberdeen, Lighthouse Field Station, George Street, Cromarty, Ross-shire IV11 8YJ, UK

    • Paul M. Thompson
  21. People’s Trust for Endangered Species, 15 Cloisters House, 8 Battersea Park Road, London SW8 4BG, UK

    • Ian White

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Contributions

S.J.T. and S.W. conceived and coordinated the study and led writing of the manuscript. P.A.H. developed the analysis routine and wrote statistical code to be applied to all data sets. D.H. extracted all climatic and sea surface temperature data. I.D.J. and E.B.M. calculated water temperatures for lakes and streams, respectively. S.J.T., J.R.B., M.S.B., S.B., P.H., T.T.H., D.G.J., D.I.L., E.B.M. and D.M. led analysis of specific data sets using code from P.A.H. S.A., P.J.B., T.M.B., L.C., T.H.C.-B., C.D., M.E., J.M.E., S.J.G.H., R.H., J.W.P.-H., L.E.B.K., J.M.P., T.H.S., P.M.T., I.W. and I.J.W. derived phenological data for analysis, advised on interpretation, and assisted in assigning species traits. All co-authors commented on the manuscript.

Competing interests

The authors declare no competing financial interests.

Corresponding author

Correspondence to Stephen J. Thackeray.

Reviewer Information Nature thanks D. Inouye, M. Visser and the other anonymous reviewer(s) for their contribution to the peer review of this work.

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    Supplementary Information

    This file contains a Supplementary Discussion, a schematic overview of the analytical approach and Supplementary Tables 1-2.

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https://doi.org/10.1038/nature18608

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