Abstract
Climate warming has caused the seasonal timing of many components of ecological food chains to advance. In the context of trophic interactions, the match–mismatch hypothesis postulates that differential shifts can lead to phenological asynchrony with negative impacts for consumers. However, at present there has been no consistent analysis of the links between temperature change, phenological asynchrony and individual-to-population-level impacts across taxa, trophic levels and biomes at a global scale. Here, we propose five criteria that all need to be met to demonstrate that temperature-mediated trophic asynchrony poses a growing risk to consumers. We conduct a literature review of 109 papers studying 129 taxa, and find that all five criteria are assessed for only two taxa, with the majority of taxa only having one or two criteria assessed. Crucially, nearly every study was conducted in Europe or North America, and most studies were on terrestrial secondary consumers. We thus lack a robust evidence base from which to draw general conclusions about the risk that climate-mediated trophic asynchrony may pose to populations worldwide.
This is a preview of subscription content, access via your institution
Relevant articles
Open Access articles citing this article.
-
Ten best practices for effective phenological research
International Journal of Biometeorology Open Access 29 July 2023
-
Experimental warming causes mismatches in alpine plant-microbe-fauna phenology
Nature Communications Open Access 15 April 2023
-
Summer temperature—but not growing season length—influences radial growth of Salix arctica in coastal Arctic tundra
Polar Biology Open Access 22 July 2022
Access options
Access Nature and 54 other Nature Portfolio journals
Get Nature+, our best-value online-access subscription
$29.99 / 30 days
cancel any time
Subscribe to this journal
Receive 12 digital issues and online access to articles
$119.00 per year
only $9.92 per issue
Rent or buy this article
Prices vary by article type
from$1.95
to$39.95
Prices may be subject to local taxes which are calculated during checkout




Data availability
All data files related to this review are available at the Open Science Framework: https://osf.io/c8xzd/.
Code availability
All R code to generate the results in this paper can be combined with the data files, and are available at the Open Science Framework: https://osf.io/c8xzd/.
References
Walther, G.-R. et al. Ecological responses to recent climate change. Nature 416, 389–395 (2002).
Parmesan, C. & Yohe, G. A globally coherent fingerprint of climate change impacts across natural systems. Nature 421, 37–42 (2003).
Walther, G.-R. Community and ecosystem responses to recent climate change. Phil. Trans. R. Soc. B 365, 2019–2024 (2010).
Daufresne, M., Lengfellner, K. & Sommer, U. Global warming benefits the small in aquatic ecosystems. Proc. Natl Acad. Sci. USA 106, 12788–12793 (2009).
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).
Parmesan, C. Ecological and evolutionary responses to recent climate change. Annu. Rev. Ecol. Evol. Syst. 37, 637–669 (2006).
Thackeray, S. J. et al. Phenological sensitivity to climate across taxa and trophic levels. Nature 535, 241–245 (2016).
Cohen, J. M., Lajeunesse, M. J. & Rohr, J. R. A global synthesis of animal phenological responses to climate change. Nat. Clim. Change 8, 224–228 (2018).
Cushing, D. D. H. D. Plankton production and year-class strength in fish populations: an update of the match/mismatch hypothesis. Adv. Mar. Biol. 26, 249–293 (1990).
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).
Durant, J., Hjermann, D., Ottersen, G. & Stenseth, N. C. Climate and the match or mismatch between predator requirements and resource availability. Clim. Res. 33, 271–283 (2007).
Renner, S. S. & Zohner, C. M. Climate change and phenological mismatch in trophic interactions among plants, insects, and vertebrates. Annu. Rev. Ecol. Evol. Syst. 49, 165–182 (2018).
Visser, M. E. & Gienapp, P. Evolutionary and demographic consequences of phenological mismatches. Nat. Ecol. Evol. 3, 879–885 (2019).
IPCC Climate Change 2014: Impacts, Adaptation, and Vulnerability. Part A: Global and Sectoral Aspects (eds, Field, C. B. et al.) (Cambridge Univ. Press, 2014).
Johansson, J., Kristensen, N. P., Nilsson, J. Å. & Jonzén, N. The eco-evolutionary consequences of interspecific phenological asynchrony - a theoretical perspective. Oikos 124, 102–112 (2015).
Deacy, W. W. et al. Phenological synchronization disrupts trophic interactions between Kodiak brown bears and salmon. Proc. Natl Acad. Sci. USA 114, 10432–10437 (2017).
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).
Kharouba, H. M. et al. Global shifts in the phenological synchrony of species interactions over recent decades. Proc. Natl Acad. Sci. USA 115, 5211–5216 (2018).
Willson, M. F. & Womble, J. N. Vertebrate exploitation of pulsed marine prey: a review and the example of spawning herring. Rev. Fish Biol. Fish. 16, 183–200 (2006).
Dunn, P. O., Winkler, D. W., Whittingham, L. A., Hannon, S. J. & Robertson, R. J. A test of the mismatch hypothesis: how is timing of reproduction related to food abundance in an aerial insectivore? Ecology 92, 450–61 (2011).
Reneerkens, J. et al. Effects of food abundance and early clutch predation on reproductive timing in a high Arctic shorebird exposed to advancements in arthropod abundance. Ecol. Evol. 6, 7375–7386 (2016).
Samplonius, J. M., Kappers, E. F., Brands, S. & Both, C. Phenological mismatch and ontogenetic diet shifts interactively affect offspring condition in a passerine. J. Anim. Ecol. 85, 1255–1264 (2016).
Mallord, J. W. et al. Diet flexibility in a declining long-distance migrant may allow it to escape the consequences of phenological mismatch with its caterpillar food supply. Ibis 159, 76–90 (2017).
Youngflesh, C. et al. Circumpolar analysis of the Adélie Penguin reveals the importance of environmental variability in phenological mismatch. Ecology 98, 940–951 (2017).
Varpe, Ø. & Fiksen, Ø. Seasonal plankton-fish interactions: light regime, prey phenology, and herring foraging. Ecology 91, 311–318 (2010).
Kharouba, H. M. & Wolkovich, E. M. Disconnects between ecological theory and data in phenological mismatch research. Nat. Clim. Change 10, 406–415 (2020).
Visser, M. E., te Marvelde, L. & Lof, M. E. Adaptive phenological mismatches of birds and their food in a warming world. J. Ornithol. 153, 75–84 (2012).
Singer, M. C. & Parmesan, C. Phenological asynchrony between herbivorous insects and their hosts: Signal of climate change or pre-existing adaptive strategy? Phil. Trans. R. Soc. B 365, 3161–3176 (2010).
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).
Reed, T. E., Jenouvrier, S. & Visser, M. E. Phenological mismatch strongly affects individual fitness but not population demography in a woodland passerine. J. Anim. Ecol. 82, 131–144 (2013).
Reed, T. E., Grøtan, V., Jenouvrier, S., Sæther, B.-E. & Visser, M. E. Population growth in a wild bird is buffered against phenological mismatch. Science 340, 488–491 (2013).
van Asch, M., Salis, L., Holleman, L. J. M., van Lith, B. & Visser, M. E. Evolutionary response of the egg hatching date of a herbivorous insect under climate change. Nat. Clim. Change 3, 244–248 (2013).
Gienapp, P., Reed, T. E. & Visser, M. E. Why climate change will invariably alter selection pressures on phenology. Proc. R. Soc. B 281, 20141611 (2014).
Ramakers, J. J. C., Gienapp, P. & Visser, M. E. Phenological mismatch drives selection on elevation, but not on slope, of breeding time plasticity in a wild songbird. Evolution 73, 175–187 (2019).
Winder, M. & Schindler, D. E. Climate change uncouples trophic interactions in an aquatic ecosystem. Ecology 85, 2100–2106 (2004).
Both, C., Bouwhuis, S., Lessells, C. & Visser, M. E. Climate change and population declines in a long-distance migratory bird. Nature 441, 81–83 (2006).
Miller-Rushing, A. J., Høye, T. T., Inouye, D. W. & Post, E. The effects of phenological mismatches on demography. Phil. Trans. R. Soc. B 365, 3177–3186 (2010).
Plard, F. et al. Mismatch between birth date and vegetation phenology slows the demography of roe deer. PLoS Biol. 12, e1001828 (2014).
Edwards, M. & Richardson, A. J. Impact of climate change on marine pelagic phenology and trophic mismatch. Nature 430, 881–884 (2004).
Poloczanska, E. S. et al. Global imprint of climate change on marine life. Nat. Clim. Change 3, 919–925 (2013).
Keogan, K. et al. Global phenological insensitivity to shifting ocean temperatures among seabirds. Nat. Clim. Change 8, 313–317 (2018).
Visser, M. E. & Holleman, L. J. Warmer springs disrupt the synchrony of oak and winter moth phenology. Proc. R. Soc. B 268, 289–294 (2001).
Kingsolver, J. G., Diamond, S. E., Siepielski, A. M. & Carlson, S. M. Synthetic analyses of phenotypic selection in natural populations: lessons, limitations and future directions. Evol. Ecol. 26, 1101–1118 (2012).
Radchuk, V. et al. Adaptive responses of animals to climate change are most likely insufficient. Nat. Commun. 10, 3109 (2019).
Vedder, O., Bouwhuis, S. & Sheldon, B. C. Quantitative assessment of the importance of phenotypic plasticity in adaptation to climate change in wild bird populations. PLoS Biol. 11, e1001605 (2013).
Both, C. et al. Avian population consequences of climate change are most severe for long-distance migrants in seasonal habitats. Proc. R. Soc. B 277, 1259–1266 (2010).
Franks, S. E. et al. The sensitivity of breeding songbirds to changes in seasonal timing is linked to population change but cannot be directly attributed to the effects of trophic asynchrony on productivity. Glob. Change Biol. 24, 957–971 (2018).
Visser, M. E., Holleman, L. J. M. & Gienapp, P. 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).
Atkinson, A. et al. Questioning the role of phenology shifts and trophic mismatching in a planktonic food web. Prog. Oceanogr. 137, 498–512 (2015).
Ross, M. V., Alisauskas, R. T., Douglas, D. C. & Kellett, D. K. Decadal declines in avian herbivore reproduction: density-dependent nutrition and phenological mismatch in the Arctic. Ecology 98, 1869–1883 (2017).
Chambers, L. E. et al. Phenological changes in the Southern Hemisphere. PLoS ONE 8, e77514 (2013).
Hurlbert, A. H. & Liang, Z. Spatiotemporal variation in avian migration phenology: citizen science reveals effects of climate change. PLoS ONE 7, e31662 (2012).
Newson, S. E. et al. Long-term change in spring and autumn migration phenology of common migrant breeding birds in Britain: results from large-scale citizen science bird recording schemes. Ibis 158, 481–495 (2016).
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).
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).
Richardson, A. J. & Poloczanska, E. S. Under-resourced, under threat. Science 320, 1294–1295 (2008).
Mackas, D. L., Pepin, P. & Verheye, H. Interannual variability of marine zooplankton and their environments: within- and between-region comparisons. Prog. Oceanogr. 97–100, 1–14 (2012).
O’Brien, T. D., Lorenzoni, L., Isensee, K. & Valdés, L. What are Marine Ecological Time Series telling us about the Ocean? A Status Report IOC Technical Series No. 129 (IOC-UNESCO, 2017).
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).
Stepanian, P. M. et al. Declines in an abundant aquatic insect, the burrowing mayfly, across major North American waterways. Proc. Natl Acad. Sci. USA 117, 2987–2992 (2020).
Schmidt, K. et al. Increasing picocyanobacteria success in shelf waters contributes to long-term food web degradation. Glob. Change Biol. 26, 5574–5587 (2020).
Sauve, D., Divoky, G. & Friesen, V. L. Phenotypic plasticity or evolutionary change? An examination of the phenological response of an arctic seabird to climate change. Funct. Ecol. 33, 2180–2190 (2019).
Bradshaw, C. J. A., Mollet, H. F. & Meekan, M. G. Inferring population trends for the world’s largest fish from mark-recapture estimates of survival. J. Anim. Ecol. 76, 480–489 (2007).
Bell, J. R. et al. Long-term phenological trends, species accumulation rates, aphid traits and climate: five decades of change in migrating aphids. J. Anim. Ecol. 84, 21–34 (2015).
Macgregor, C. J., Williams, J. H., Bell, J. R. & Thomas, C. D. Moth biomass increases and decreases over 50 years in Britain. Nat. Ecol. Evol. 3, 1645–1649 (2019).
Tanentzap, A. J. et al. Terrestrial support of lake food webs: synthesis reveals controls over cross-ecosystem resource use. Sci. Adv. 3, e1601765 (2017).
Estiarte, M. & Peñuelas, J. Alteration of the phenology of leaf senescence and fall in winter deciduous species by climate change: effects on nutrient proficiency. Glob. Change Biol. 21, 1005–1017 (2015).
Beaugrand, G. & Kirby, R. R. How do marine pelagic species respond to climate change? Theories and observations. Ann. Rev. Mar. Sci. 10, 169–197 (2018).
Thackeray, S. J., Jones, I. D. & Maberly, S. C. Long-term change in the phenology of spring phytoplankton: species-specific responses to nutrient enrichment and climatic change. J. Ecol. 96, 523–535 (2008).
Ji, R., Jin, M. & Varpe, Ø. Sea ice phenology and timing of primary production pulses in the Arctic Ocean. Glob. Change Biol. 19, 734–741 (2013).
Durant, J. M. et al. Timing and abundance as key mechanisms affecting trophic interactions in variable environments. Ecol. Lett. 8, 952–958 (2005).
Ramakers, J. J. C., Gienapp, P. & Visser, M. E. Comparing two measures of phenological synchrony in a predator–prey interaction: simpler works better. J. Anim. Ecol. 89, 745–756 (2020).
Walters, A. W., De Los Ángeles González Sagrario, M. & Schindler, D. E. Species- and community-level responses combine to drive phenology of lake phytoplankton. Ecology 94, 2188–2194 (2013).
Shutt, J. D., Burgess, M. D. & Phillimore, A. B. A spatial perspective on the phenological distribution of the spring woodland caterpillar peak. Am. Nat. 194, E109–E121 (2019).
Pochardt, M. et al. Environmental DNA facilitates accurate, inexpensive, and multiyear population estimates of millions of anadromous fish. Mol. Ecol. Resour. 20, 457–467 (2020).
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).
Pearce-Higgins, J. W. & Green, R. E. Birds and Climate Change: Impacts and Conservation Responses (Cambridge Univ. Press, 2014).
Samplonius, J. M. et al. Phenological sensitivity to climate change is higher in resident than in migrant bird populations among European cavity breeders. Glob. Change Biol. 24, 3780–3790 (2018).
Burgess, M. D. et al. Tritrophic phenological match-mismatch in space and time. Nat. Ecol. Evol. 2, 970–975 (2018).
Visser, M. E. et al. Effects of spring temperatures on the strength of selection on timing of reproduction in a long-distance migratory bird. PLoS Biol. 13, e1002120 (2015).
Cholewa, M. & Wesołowski, 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).
Simmonds, E. G., Cole, E. F., Sheldon, B. C. & Coulson, T. Phenological asynchrony: a ticking time-bomb for seemingly stable populations? Ecol. Lett. https://doi.org/10.1111/ele.13603 (2020).
Simmonds, E. G., Cole, E. F., Sheldon, B. C. & Coulson, T. Testing the effect of quantitative genetic inheritance in structured models on projections of population dynamics. Oikos 129, 559–571 (2020).
Prevéy, J. et al. Greater temperature sensitivity of plant phenology at colder sites: implications for convergence across northern latitudes. Glob. Change Biol. 23, 2660–2671 (2017).
Assmann, J. J. et al. Local snow melt and temperature—but not regional sea ice—explain variation in spring phenology in coastal Arctic tundra. Glob. Change Biol. 25, 2258–2274 (2019).
Bjorkman, A. D., Elmendorf, S. C., Beamish, A. L., Vellend, M. & Henry, G. H. R. Contrasting effects of warming and increased snowfall on Arctic tundra plant phenology over the past two decades. Glob. Change Biol. 21, 4651–4661 (2015).
Lameris, T. K. et al. Arctic geese tune migration to a warming climate but still suffer from a phenological mismatch. Curr. Biol. 28, 2467–2473 (2018).
Doiron, M., Gauthier, G. & Lévesque, E. Trophic mismatch and its effects on the growth of young in an Arctic herbivore. Glob. Change Biol. 21, 4364–4376 (2015).
Iler, A. M. et al. Maintenance of temporal synchrony between syrphid flies and floral resources despite differential phenological responses to climate. Glob. Change Biol. 19, 2348–2359 (2013).
Ovaskainen, O. et al. Chronicles of nature calendar, a long-term and large-scale multitaxon database on phenology. Sci. Data 7, 47 (2020).
Brohan, P. et al. Marine observations of old weather. Bull. Am. Meteorol. Soc. 90, 219–230 (2009).
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).
Wang, S. et al. Limitations and challenges of MODIS-derived phenological metrics across different landscapes in pan-Arctic regions. Remote Sens. 10, 1784 (2018).
Helman, D. Land surface phenology: what do we really ‘see’ from space? Sci. Total Environ. 618, 665–673 (2018).
van de Pol, M. et al. Identifying the best climatic predictors in ecology and evolution. Methods Ecol. Evol. 7, 1246–1257 (2016).
Bailey, L. D. & Van De Pol, M. Climwin: an R toolbox for climate window analysis. PLoS ONE 11, e0167980 (2016).
Teller, B. J., Adler, P. B., Edwards, C. B., Hooker, G. & Ellner, S. P. Linking demography with drivers: climate and competition. Methods Ecol. Evol. 7, 171–183 (2016).
Simmonds, E. G., Cole, E. F. & Sheldon, B. C. Cue identification in phenology: a case study of the predictive performance of current statistical tools. J. Anim. Ecol. 88, 1428–1440 (2019).
Iler, A. M., Inouye, D. W., Schmidt, N. M. & Høye, T. T. Detrending phenological time series improves climate-phenology analyses and reveals evidence of plasticity. Ecology 98, 647–655 (2017).
Both, C. et al. Large-scale geographical variation confirms that climate change causes birds to lay earlier. Proc. R. Soc. B 271, 1657–1662 (2004).
Visser, M. E. et al. Variable responses to large-scale climate change in European Parus populations. Proc. R. Soc. B 270, 367–372 (2003).
Verhulst, S. & Nilsson, J.-Å. The timing of birds’ breeding seasons: a review of experiments that manipulated timing of breeding. Phil. Trans. R. Soc. B 363, 399–410 (2008).
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).
Gienapp, P. et al. Predicting demographically sustainable rates of adaptation: can great tit breeding time keep pace with climate change? Phil. Trans. R. Soc. B 368, 20120289 (2013).
Acknowledgements
We thank A. Husby, T. Reed, M. Visser, I. Myers-Smith and M. Singer for constructive criticism on an earlier version of this manuscript.
Author information
Authors and Affiliations
Contributions
All authors contributed to conceiving ideas and editing the manuscript. J.M.S., A.B.P., A.A., C.H., K.K., S.J.T., J.J.A., M.D.B., J.J., K.H.M., J.W.P.-H., E.G.S., Ø.V. and J.C.W. extracted data for the analyses. J.M.S., A.B.P., A.A., C.H., K.K. and S.J.T. contributed to writing the manuscript. J.M.S. and A.B.P. expanded on the initial ideas to determine the structure and content of the manuscript and wrote most of it. J.M.S. conducted the analyses.
Corresponding author
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.
Extended data
Extended Data Fig. 1 Records returned from literature search.
Total publications by year and sum of times cited for the studies captured by our search terms.
Extended Data Fig. 2 PRISMA flowchart for records included and excluded.
Flow chart of the number of papers screened, and those included and excluded using three filters. This process resulted in 109 relevant papers, which provided information on 132 taxa.
Extended Data Fig. 3 Criteria per study.
Overview of all the study-by-taxon combinations identified (200 in 109 papers), showing which (and how many) criteria were studied in individual papers.
Supplementary information
Supplementary Information
Supplementary Methods and Table 1.
Supplementary Data 1
Contains three tabs with spreadsheets that are read by the R script and used for the analyses.
Supplementary Data 2
R script to reproduce the analyses for this article.
Rights and permissions
About this article
Cite this article
Samplonius, J.M., Atkinson, A., Hassall, C. et al. Strengthening the evidence base for temperature-mediated phenological asynchrony and its impacts. Nat Ecol Evol 5, 155–164 (2021). https://doi.org/10.1038/s41559-020-01357-0
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1038/s41559-020-01357-0
This article is cited by
-
Experimental warming causes mismatches in alpine plant-microbe-fauna phenology
Nature Communications (2023)
-
Ten best practices for effective phenological research
International Journal of Biometeorology (2023)
-
Summer temperature—but not growing season length—influences radial growth of Salix arctica in coastal Arctic tundra
Polar Biology (2022)
-
Bird populations most exposed to climate change are less sensitive to climatic variation
Nature Communications (2022)
-
Migratory strategy drives species-level variation in bird sensitivity to vegetation green-up
Nature Ecology & Evolution (2021)