Evolutionary and demographic consequences of phenological mismatches

Article metrics

Abstract

Climate change has often led to unequal shifts in the seasonal timing (phenology) of interacting species, such as consumers and their resource, leading to phenological ‘mismatches’. Mismatches occur when the time at which a consumer species’s demands for a resource are high does not match with the period when this resource is abundant. Here, we review the evolutionary and population-level consequences of such mismatches and how these depend on other ecological factors, such as additional drivers of selection and density-dependent recruitment. This review puts the research on phenological mismatches into a conceptual framework, applies this framework beyond consumer–resource interactions and illustrates this framework using examples drawn from the vast body of literature on mismatches. Finally, we point out priority questions for research on this key impact of climate change.

Access options

Rent or Buy article

Get time limited or full article access on ReadCube.

from$8.99

All prices are NET prices.

Fig. 1: Definitions of mismatch and mistiming.
Fig. 2: Optimal mismatches are caused by multiple fitness components of phenology.
Fig. 3: Relationships between mismatch and reproductive success at the individual and population level.

References

  1. 1.

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

  2. 2.

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

  3. 3.

    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).

  4. 4.

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

  5. 5.

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

  6. 6.

    Hjort, J. Fluctuations in the Great Fisheries of Northern Europe Viewed in the Light of Biological Research (ICES, 1914).

  7. 7.

    Cushing, D. H. Regularity of spawning season of some fishes. ICES J. Mar. Sci. 33, 81–92 (1969).

  8. 8.

    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. Biol. Sci. 265, 1867–1870 (1998).

  9. 9.

    Stenseth, N. C. & Mysterud, A. Climate, changing phenology, and other life history traits: nonlinearity and match-mismatch to the environment. Proc. Natl Acad. Sci. USA 99, 13379–13381 (2002).

  10. 10.

    Harrington, R., Woiwod, I. & Sparks, T. Climate change and trophic interactions. Trends Ecol. Evol. 14, 146–150 (1999).

  11. 11.

    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).

  12. 12.

    Miller-Rushing, A. J., Høye, T. T., Inouye, D. W. & Post, E. The effects of phenological mismatches on demography. Philos. Trans. R. Soc. Lond. B Biol. Sci. 365, 3177–3186 (2010).

  13. 13.

    Lindén, A. Adaptive and nonadaptive changes in phenological synchrony. Proc. Natl Acad. Sci. USA 115, 5057–5059 (2018).

  14. 14.

    Singer, M. C. & Parmesan, C. Phenological asynchrony between herbivorous insects and their hosts: signal of climate change or pre-existing adaptive strategy? Philos. Trans. R. Soc. Lond. B Biol. Sci. 365, 3161–3176 (2010).

  15. 15.

    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).

  16. 16.

    Visser, M. E. & Holleman, L. J. M. Warmer springs disrupt the synchrony of oak and winter moth phenology. Proc. Biol. Sci. 268, 289–294 (2001).

  17. 17.

    Hegland, S. J., Nielsen, A., Lázaro, A., Bjerknes, A.-L. & Totland, Ø. How does climate warming affect plant-pollinator interactions? Ecol. Lett. 12, 184–195 (2009).

  18. 18.

    Paull, S. H. & Johnson, P. T. J. Experimental warming drives a seasonal shift in the timing of host-parasite dynamics with consequences for disease risk. Ecol. Lett. 17, 445–453 (2014).

  19. 19.

    Stenseth, N. C. et al. Testing for effects of climate change on competitive relationships and coexistence between two bird species. Proc. Biol. Sci. 282, 20141958 (2015).

  20. 20.

    Bradshaw, A. D. Evolutionary significance of phenotypic plasticity in plants. Adv. Genet. 13, 115–155 (1965).

  21. 21.

    Pigliucci, M. Evolution of phenotypic plasticity: where are we going now? Trends Ecol. Evol. 20, 481–486 (2005).

  22. 22.

    McNamara, J. M., Barta, Z., Klaassen, M. & Bauer, S. Cues and the optimal timing of activities under environmental changes. Ecol. Lett. 14, 1183–1190 (2011).

  23. 23.

    Gwinner, E. Circannual Rhythms (Springer-Verlag, 1986).

  24. 24.

    Zann, R. A., Morton, S. R., Jones, K. R. & Burley, N. T. The timing of breeding by Zebra finches in relation to rainfall in Central Australia. Emu 95, 208–222 (1995).

  25. 25.

    Korn, H. & Taitt, M. J. Initiation of early breeding in a population of Microtus townsendii (Rodentia) with the secondary plant compound 6-MBOA. Oecologia 71, 593–596 (1987).

  26. 26.

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

  27. 27.

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

  28. 28.

    Ovaskainen, O. et al. Community-level phenological response to climate change. Proc. Natl Acad. Sci. USA 110, 13434–13439 (2013).

  29. 29.

    Vose, R. S., Easterling, D. R. & Gleason, B. Maximum and minimum temperature trends for the globe: an update through 2004. Geophys. Res. Lett. 32, L23822 (2005).

  30. 30.

    Gienapp, P., Reed, T. E. & Visser, M. E. Why climate change will invariably alter selection pressures on phenology. Proc. Biol. Sci. 281, 20141611 (2014).

  31. 31.

    Visser, M. E., Both, C. & Lambrechts, M. M. Global climate change leads to mistimed avian reproduction. Adv. Ecol. Res. 35, 89–110 (2004).

  32. 32.

    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).

  33. 33.

    Arlt, D. & Pärt, T. Marked reduction in demographic rates and reduced fitness advantage for early breeding is not linked to reduced thermal matching of breeding time. Ecol. Evol. 7, 10782–10796 (2017).

  34. 34.

    Bowers, E. K. et al. Spring temperatures influence selection on breeding date and the potential for phenological mismatch in a migratory bird. Ecology 97, 2880–2891 (2016).

  35. 35.

    Wesolowski, T. & Rowinski, P. Do blue tits Cyanistes caeruleus synchronize reproduction with caterpillar peaks in a primeval forest? Bird Study 61, 231–245 (2014).

  36. 36.

    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).

  37. 37.

    Marrot, P., Charmantier, A., Blondel, J. & Garant, D. Current spring warming as a driver of selection on reproductive timing in a wild passerine. J. Anim. Ecol. 87, 754–764 (2018).

  38. 38.

    Visser, M. E., Te Marvelde, L. & Lof, M. Adaptive phenological mismatches of birds and their food in a warming world. J. Ornithol. 153, S75–S84 (2012).

  39. 39.

    Brown, C. R. & Brown, M. B. Weather-mediated natural selection on arrival time in cliff swallows (Petrochelidon pyrrhonota). Behav. Ecol. Sociobiol. 47, 339–345 (2000).

  40. 40.

    Lof, M. E., Reed, T. E., McNamara, J. M. & Visser, M. E. Timing in a fluctuating environment: environmental variability and asymmetric fitness curves can lead to adaptively mismatched avian reproduction. Proc. Biol. Sci. 279, 3161–3169 (2012).

  41. 41.

    Ruel, J. J. & Ayres, M. P. Jensen’s inequality predicts effects of environmental variation. Trends Ecol. Evol. 14, 361–366 (1999).

  42. 42.

    Martin, T. L. & Huey, R. B. Why “suboptimal” is optimal: Jensen’s inequality and ectotherm thermal preferences. Am. Nat. 171, E102–E118 (2008).

  43. 43.

    Jonzén, N., Hedenström, A. & Lundberg, P. Climate change and the optimal arrival of migratory birds. Proc. Biol. Sci. 274, 269–274 (2007).

  44. 44.

    Johansson, J. & Jonzén, N. Effects of territory competition and climate change on timing of arrival to breeding grounds: a game-theory approach. Am. Nat. 179, 463–474 (2012).

  45. 45.

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

  46. 46.

    te Marvelde, L., Webber, S. L., Meijer, H. A. J. & Visser, M. E. Energy expenditure during egg laying is equal for early and late breeding free-living female great tits. Oecologia 168, 631–638 (2012).

  47. 47.

    Johansson, J., Kristensen, N. P., Nilsson, J. A. & Jonzen, N. The eco-evolutionary consequences of interspecific phenological asynchrony — a theoretical perspective. Oikos 124, 102–112 (2015).

  48. 48.

    Gienapp, P., Teplitsky, C., Alho, J. S., Mills, J. A. & Merilä, J. Climate change and evolution: disentangling environmental and genetic responses. Mol. Ecol. 17, 167–178 (2008).

  49. 49.

    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. Chang. 3, 244–248 (2013).

  50. 50.

    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).

  51. 51.

    Møller, A. P., Rubolini, D. & Lehikoinen, E. Populations of migratory bird species that did not show a phenological response to climate change are declining. Proc. Natl Acad. Sci. USA 105, 16195–16200 (2008).

  52. 52.

    Saino, N. et al. Climate warming, ecological mismatch at arrival and population decline in migratory birds. Proc. Biol. Sci. 278, 835–842 (2011).

  53. 53.

    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).

  54. 54.

    Saino, N. et al. Climate change effects on migration phenology may mismatch brood parasitic cuckoos and their hosts. Biol. Lett. 5, 539–541 (2009).

  55. 55.

    Plard, F. et al. Mismatch between birth date and vegetation phenology slows the demography of roe deer. PLoS Biol. 12, e1001828 (2014).

  56. 56.

    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).

  57. 57.

    Post, E. & Forchhammer, M. C. Climate change reduces reproductive success of an Arctic herbivore through trophic mismatch. Philos. Trans. R. Soc. Lond. B Biol. Sci. 363, 2369–2375 (2008).

  58. 58.

    Kristiansen, T., Drinkwater, K. F., Lough, R. G. & Sundby, S. Recruitment variability in North Atlantic cod and match–mismatch dynamics. PLoS One 6, e17456 (2011).

  59. 59.

    Regular, P.M. et al. Why timing is everything: energetic costs and reproductive consequences of resource mismatch for a chick-rearing seabird. Ecosphere 5, (2014).

  60. 60.

    Day, E. & Kokko, H. Relaxed selection when you least expect it: why declining bird populations might fail to respond to phenological mismatches. Oikos 124, 62–68 (2015).

  61. 61.

    Pelletier, F., Garant, D. & Hendry, A. P. Eco-evolutionary dynamics. Philos. Trans. R. Soc. Lond. B Biol. Sci. 364, 1483–1489 (2009).

  62. 62.

    Gienapp, P. et al. Genomic quantitative genetics to study evolution in the wild. Trends Ecol. Evol. 32, 897–908 (2017).

  63. 63.

    Rudman, S. M. et al. What genomic data can reveal about eco-evolutionary dynamics. Nat. Ecol. Evol. 2, 9–15 (2018).

  64. 64.

    Verhulst, S. & Nilsson, J. A. The timing of birds’ breeding seasons: a review of experiments that manipulated timing of breeding. Philos. Trans. R. Soc. Lond. B Biol. Sci. 363, 399–410 (2007).

  65. 65.

    Rafferty, N. E. & Ives, A. R. Effects of experimental shifts in flowering phenology on plant-pollinator interactions. Ecol. Lett. 14, 69–74 (2011).

  66. 66.

    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).

  67. 67.

    Beebee, T. J. C. Amphibian breeding and climate. Nature 374, 219–220 (1995).

  68. 68.

    Lehikoinen, A. Advanced autumn migration of sparrowhawk has increased the predation risk of long-distance migrants in Finland. PLoS One 6, e20001 (2011).

  69. 69.

    Bestion, E., García-Carreras, B., Schaum, C. E., Pawar, S. & Yvon-Durocher, G. Metabolic traits predict the effects of warming on phytoplankton competition. Ecol. Lett. 21, 655–664 (2018).

  70. 70.

    Robbirt, K. M., Roberts, D. L., Hutchings, M. J. & Davy, A. J. Potential disruption of pollination in a sexually deceptive orchid by climatic change. Curr. Biol. 24, 2845–2849 (2014).

  71. 71.

    Martinez-Bakker, M. & Helm, B. The influence of biological rhythms on host-parasite interactions. Trends Ecol. Evol. 30, 314–326 (2015).

  72. 72.

    Gehman, A. M., Hall, R. J. & Byers, J. E. Host and parasite thermal ecology jointly determine the effect of climate warming on epidemic dynamics. Proc. Natl Acad. Sci. USA 115, 744–749 (2018).

  73. 73.

    Santangeli, A. et al. Stronger response of farmland birds than farmers to climate change leads to the emergence of an ecological trap. Biol. Conserv. 217, 166–172 (2018).

  74. 74.

    Kelsey, K. C. et al. Phenological mismatch in coastal western Alaska may increase summer season greenhouse gas uptake. Environ. Res. Lett. 13, 044032 (2018).

  75. 75.

    CaraDonna, P. J., Iler, A. M. & Inouye, D. W. Shifts in flowering phenology reshape a subalpine plant community. Proc. Natl Acad. Sci. USA 111, 4916–4921 (2014).

  76. 76.

    Stevenson, T. J. et al. Disrupted seasonal biology impacts health, food security and ecosystems. Proc. Biol. Sci. 282, 20151453 (2015).

  77. 77.

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

  78. 78.

    Revilla, T. A., Encinas-Viso, F. & Loreau, M. (A bit) Earlier or later is always better: phenological shifts in consumer–resource interactions. Theor. Ecol. 7, 149–162 (2014).

  79. 79.

    Memmott, J., Craze, P. G., Waser, N. M. & Price, M. V. Global warming and the disruption of plant–pollinator interactions. Ecol. Lett. 10, 710–717 (2007).

  80. 80.

    Burkle, L. A., Marlin, J. C. & Knight, T. M. Plant–pollinator interactions over 120 years: loss of species, co-occurrence, and function. Science 339, 1611–1615 (2013).

  81. 81.

    Encinas-Viso, F., Revilla, T. A. & Etienne, R. S. Phenology drives mutualistic network structure and diversity. Ecol. Lett. 15, 198–208 (2012).

  82. 82.

    Revilla, T. A., Encinas-Viso, F. & Loreau, M. Robustness of mutualistic networks under phenological change and habitat destruction. Oikos 124, 22–32 (2015).

  83. 83.

    IPCC. Climate Change 2014: Synthesis Report (eds Core Writing Team, Pachauri, R. K. & Meyer, L. A.) (IPCC, 2014).

  84. 84.

    Tomotani, B. M. et al. Climate change leads to differential shifts in the timing of annual cycle stages in a migratory bird. Glob. Change Biol. 24, 823–835 (2018).

  85. 85.

    Dawson, A. The effect of latitude on photoperiodic control of gonadal maturation, regression and molt in birds. Gen. Comp. Endocrinol. 190, 129–133 (2013).

  86. 86.

    Carey, C. The impacts of climate change on the annual cycles of birds. Philos. Trans. R. Soc. Lond. B Biol. Sci. 364, 3321–3330 (2009).

  87. 87.

    Crozier, L. G. et al. Potential responses to climate change in organisms with complex life histories: evolution and plasticity in Pacific salmon. Evol. Appl. 1, 252–270 (2008).

  88. 88.

    Kristensen, N. P., Johansson, J., Ripa, J. & Jonzen, N. Phenology of two interdependent traits in migratory birds in response to climate change. Proc. Biol. Sci. 282, 20150288 (2015).

  89. 89.

    Both, C. & Visser, M. E. Adjustment to climate change is constrained by arrival date in a long-distance migrant bird. Nature 411, 296–298 (2001).

  90. 90.

    Moyes, K. et al. Advancing breeding phenology in response to environmental change in a wild red deer population. Glob. Change Biol. 17, 2455–2469 (2011).

Download references

Acknowledgements

We are grateful to B. Tomotani, J. Ramakers, I. Verhagen, W. Mooij, B. Helm and T. Reed for their comments on an earlier version of this paper, as well as J. Johansson for constructive review comments. This study was supported by an ERC Advanced Grant (339092 – E-Response to M.E.V.).

Author information

M.E.V. and P.G. contributed to the conception of and wrote the manuscript. P.G. generated the figures.

Correspondence to Marcel E. Visser or Phillip Gienapp.

Additional information

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

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Visser, M.E., Gienapp, P. Evolutionary and demographic consequences of phenological mismatches. Nat Ecol Evol 3, 879–885 (2019) doi:10.1038/s41559-019-0880-8

Download citation

Further reading