Skip to main content

Thank you for visiting You are using a browser version with limited support for CSS. To obtain the best experience, we recommend you use a more up to date browser (or turn off compatibility mode in Internet Explorer). In the meantime, to ensure continued support, we are displaying the site without styles and JavaScript.

Tritrophic phenological match–mismatch in space and time


Increasing temperatures associated with climate change may generate phenological mismatches that disrupt previously synchronous trophic interactions. Most work on mismatch has focused on temporal trends, whereas spatial variation in the degree of trophic synchrony has largely been neglected, even though the degree to which mismatch varies in space has implications for meso-scale population dynamics and evolution. Here we quantify latitudinal trends in phenological mismatch, using phenological data on an oak–caterpillar–bird system from across the UK. Increasing latitude delays phenology of all species, but more so for oak, resulting in a shorter interval between leaf emergence and peak caterpillar biomass at northern locations. Asynchrony found between peak caterpillar biomass and peak nestling demand of blue tits, great tits and pied flycatchers increases in earlier (warm) springs. There is no evidence of spatial variation in the timing of peak nestling demand relative to peak caterpillar biomass for any species. Phenological mismatch alone is thus unlikely to explain spatial variation in population trends. Given projections of continued spring warming, we predict that temperate forest birds will become increasingly mismatched with peak caterpillar timing. Latitudinal invariance in the direction of mismatch may act as a double-edged sword that presents no opportunities for spatial buffering from the effects of mismatch on population size, but generates spatially consistent directional selection on timing, which could facilitate rapid evolutionary change.

This is a preview of subscription content, access via your institution

Relevant articles

Open Access articles citing this article.

Access options

Buy article

Get time limited or full article access on ReadCube.


All prices are NET prices.

Fig. 1: Number of years of data for each 50 km grid cell used for each trophic level and bird species.
Fig. 2: Latitudinal effects on phenology, and the relationship between oak first leaf dates and peak frass.
Fig. 3: Relationships between latitude and mismatch, and the timing of peak frass and first egg date in three avian species.


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

    Article  CAS  Google Scholar 

  2. Cushing, D. Plankton production and year-class strength in fish populations: an update of the match/mismatch hypothesis. Adv. Mar. Biol. 26, 249–293 (1990).

    Article  Google Scholar 

  3. Durant, J. M., Hjermann, D. Ø., 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 

  4. Edwards, M. & Richardson, A. J. Impact of climate change on marine pelagic phenology and trophic mismatch. Nature 430, 881–884 (2004).

    Article  CAS  Google Scholar 

  5. Donnelly, A., Caffarra, A. & O’Neill, B. F. A review of climate-driven mismatches between interdependent phenophases in terrestrial and aquatic ecosystems. Int. J. Biometeorol. 55, 805–817 (2011).

    Article  Google Scholar 

  6. Phillimore, A. B., Stålhandske, S., Smithers, R. J. & Bernard, R. Dissecting the contributions of plasticity and local adaptation to the phenology of a butterfly and its host plants. Am. Nat. 180, 655–670 (2012).

    Article  Google Scholar 

  7. Phillimore, A. B., Leech, D. I., Pearce-Higgins, J. W. & Hadfield, J. D. Passerines may be sufficiently plastic to track temperature-mediated shifts in optimum lay date. Glob. Change Biol. 22, 3259–3272 (2016).

    Article  Google Scholar 

  8. Bourne, E. C. et al. Between migration load and evolutionary rescue: dispersal, adaptation and the response of spatially structured populations to environmental change. Proc. R. Soc. Lond. B 281, 20132795 (2014).

    Article  Google Scholar 

  9. 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 

  10. Both, C., Asch, M., Bijlsma, R. G., van den Burg, A. B. & Visser, M. E. Climate change and unequal phenological changes across four trophic levels: constraints or adaptations? J. Anim. Ecol. 78, 73–83 (2009).

    Article  Google Scholar 

  11. Vatka, E., Orell, M. & Rytkönen, S. Warming climate advances breeding and improves synchrony of food demand and food availability in a boreal passerine. Glob. Change Biol. 17, 3002–3009 (2011).

    Article  Google Scholar 

  12. Visser, M. E., van Noordwijk, A. J., Tinbergen, J. M. & Lessells, C. M. Warmer springs lead to mistimed reproduction in great tits (Parus major). Proc. R. Soc. B 265, 1867–1870 (1998).

  13. Smith, K. W. et al. Large-scale variation in the temporal patterns of the frass fall of defoliating caterpillars in oak woodlands in Britain: implications for nesting woodland birds. Bird Study 58, 506–511 (2011).

    Article  Google Scholar 

  14. Tansey, C. J., Hadfield, J. D. & Phillimore, A. B. Estimating the ability of plants to plastically track temperature-mediated shifts in the spring phenological optimum. Glob. Change Biol. 23, 3321–3334 (2017).

    Article  Google Scholar 

  15. Both, C., Van Asch, M., Bijlsma, R. G., van den Burg, A. B. & Visser, M. E. Climate change and unequal phenological changes across four trophic levels: constraints or adaptations? J. Anim. Ecol. 78, 73–83 (2009).

    Article  Google Scholar 

  16. Buse, A., Dury, S., Woodburn, R., Perrins, C. & Good, J. Effects of elevated temperature on multi‐species interactions: the case of Pedunculate Oak, Winter Moth and Tits. Funct. Ecol. 13, 74–82 (1999).

    Article  Google Scholar 

  17. Lundberg, A. & Alatalo, R. V. The Pied Flycatcher (T & A D Poyser, London, 1992).

  18. Perrins, C. M. Tits and their caterpillar food supply. Ibis 133, 49–54 (1991).

    Article  Google Scholar 

  19. Charmantier, A. et al. Adaptive phenotypic plasticity in response to climate change in a wild bird population. Science 320, 800–803 (2008).

    Article  CAS  Google Scholar 

  20. Cresswell, W. & McCleery, R. How great tits maintain synchronization of their hatch date with food supply in response to long-term variability in temperature. J. Anim. Ecol. 72, 356–366 (2003).

    Article  Google Scholar 

  21. Eeva, T. & Lehikoinen, E. Polluted environment and cold weather induce laying gaps in great tit and pied flycatcher. Oecologia 162, 533–539 (2010).

    Article  Google Scholar 

  22. Sanz, J. J. Effect of food availability on incubation period in the pied flycatcher (Ficedula hypoleuca). Auk 113, 249–253 (1996).

    Article  Google Scholar 

  23. Tomás, G. Hatching date vs laying date: what should we look at to study avian optimal timing of reproduction? J. Avian Biol. 46, 107–112 (2015).

    Article  Google Scholar 

  24. Morrison, C. A., Robinson, R. A., Butler, S. J., Clark, J. A. & Gill, J. A. Demographic drivers of decline and recovery in an Afro-Palaearctic migratory bird population. Proc. R. Soc. B 283, 20161387 (2016).

  25. Both, C., G Bijlsma, R. & E Visser, M. Climatic effects on timing of spring migration and breeding in a long-distance migrant, the pied flycatcher Ficedula hypoleuca. J. Avian Biol. 36, 368–373 (2005).

    Article  Google Scholar 

  26. Ouwehand, J. et al. Light-level geolocators reveal migratory connectivity in European populations of pied flycatchers Ficedula hypoleuca. J. Avian Biol. 47, 69–83 (2016).

    Article  Google Scholar 

  27. Ouwehand, J. & Both, C. African departure rather than migration speed determines variation in spring arrival in pied flycatchers. J. Anim. Ecol. 86, 88–97 (2017).

    Article  Google Scholar 

  28. Both, C. & te Marvelde, L. Climate change and timing of avian breeding and migration throughout Europe. Clim. Res. 35, 93–105 (2007).

    Article  Google Scholar 

  29. Ockendon, N., Leech, D. & Pearce-Higgins, J. W. Climatic effects on breeding grounds are more important drivers of breeding phenology in migrant birds than carry-over effects from wintering grounds. Biol. Lett. 9, 20130669 (2013).

    Article  Google Scholar 

  30. Cholewa, M. & Wesolowski, T. Nestling food of European hole-nesting passerines: do we know enough to test the adaptive hypotheses on breeding seasons? Acta Ornithol. 46, 105–116 (2011).

    Article  Google Scholar 

  31. Hinks, A. E. et al. Scale-dependent phenological synchrony between songbirds and their caterpillar food source. Am. Nat. 186, 84–97 (2015).

    Article  Google Scholar 

  32. Burger, C. et al. Climate change, breeding date and nestling diet: how temperature differentially affects seasonal changes in pied flycatcher diet depending on habitat variation. J. Anim. Ecol. 81, 926–936 (2012).

    Article  Google Scholar 

  33. Both, C., Bouwhuis, S., Lessells, C. M. & Visser, M. E. Climate change and population declines in a long-distance migratory bird. Nature 44, 81–83 (2006).

    Article  Google Scholar 

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

    Article  Google Scholar 

  35. Morrison, C. A., Robinson, R. A., Clark, J. A. & Gill, J. A. Spatial and temporal variation in population trends in a long-distance migratory bird. Divers. Distrib. 16, 620–627 (2010).

    Article  Google Scholar 

  36. Morrison, C. A., Robinson, R. A., Clark, J. A., Risely, K. & Gill, J. A. Recent population declines in Afro-Palaearctic migratory birds: the influence of breeding and non-breeding seasons. Divers. Distrib. 19, 1051–1058 (2013).

    Article  Google Scholar 

  37. Crick, H. Q., Baillie, S. R. & Leech, D. I. The UK Nest Record Scheme: its value for science and conservation. Bird. Study 50, 254–270 (2003).

    Article  Google Scholar 

  38. R Development Core Team R: A Language and Environment for Statistical Computing (R Foundation for Statistical Computing, 2015).

  39. 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 

  40. Phillimore, A. B., Hadfield, J. D., Jones, O. R. & Smithers, R. J. Differences in spawning date between populations of common frog reveal local adaptation. Proc. Natl Acad. Sci. USA 107, 8292–8297 (2010).

    Article  CAS  Google Scholar 

  41. Hadfield, J. D., Heap, E. A., Bayer, F., Mittell, E. A. & Crouch, N. M. A. Intraclutch differences in egg characteristics mitigate the consequences of age-related hierarchies in a wild passerine. Evolution 67, 2688–2700 (2013).

    Article  Google Scholar 

  42. Brooks, S. P. & Gelman, A. General methods for monitoring convergence of iterative simulations. J. Comput. Graph. Stat. 7, 434–455 (1998).

    Google Scholar 

  43. Warton, D. I., Wright, I. J., Falster, D. S. & Westoby, M. Bivariate line‐fitting methods for allometry. Biol. Rev. 81, 259–291 (2006).

    Article  Google Scholar 

  44. Evans, K. L., Leech, D. I., Crick, H. Q. P., Greenwood, J. J. D. & Gaston, K. J. Latitudinal and seasonal patterns in clutch size of some single-brooded British birds. Bird. Study 56, 75–85 (2009).

    Article  Google Scholar 

  45. Naef-Daenzer, B. & Keller, L. F. The foraging performance of great and blue tits (Parus major and P. caeruleus) in relation to caterpillar development, and its consequences for nestling growth and fledging weight. J. Anim. Ecol. 68, 708–718 (1999).

    Article  Google Scholar 

  46. Royama, T. Factors governing feeding rate, food requirement and brood size of nestling great tits Parus major. Ibis 108, 313–347 (1966).

    Article  Google Scholar 

Download references


We thank the many contributors of the UK Phenology Network and BTO Nest Record Scheme, as well as J. Hadfield for statistical advice and J. Shutt for helpful discussion. The UK Phenology Network is coordinated by the Woodland Trust. The Nest Record Scheme is a partnership jointly funded by the BTO, the Joint Nature Conservation Committee and the fieldworkers themselves. A.B.P. was funded by a Natural Environment Research Council Advanced Fellowship (Ne/I020598/1).

Author information

Authors and Affiliations



M.D.B., A.B.P. and K.W.S. conceived the study. M.D.B. led and coordinated the study. A.B.P. analysed the data. M.D.B. and A.B.P. wrote the manuscript with significant contributions from K.L.E. M.D.B., K.W.S., C.J.B., K.B., J.R.C., K.L.E., C.R.dF., R.G.N., B.C.S., J.A.S., R.C.W. and S.G.W. collected the frass data. K.L. provided the oak leafing data. D.L. and J.W.P.-H. provided the bird data. All authors commented on and edited the manuscript.

Corresponding author

Correspondence to Malcolm D. Burgess.

Ethics declarations

Competing interests

The authors declare no competing interests.

Additional information

Publisher’s note: Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Supplementary information

Supplementary Information

Supplementary Methods, Supplementary Tables 1–5, Supplementary Figures 1–2, Supplementary References

Reporting Summary

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Burgess, M.D., Smith, K.W., Evans, K.L. et al. Tritrophic phenological match–mismatch in space and time. Nat Ecol Evol 2, 970–975 (2018).

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI:

This article is cited by


Quick links

Nature Briefing

Sign up for the Nature Briefing newsletter — what matters in science, free to your inbox daily.

Get the most important science stories of the day, free in your inbox. Sign up for Nature Briefing