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Climate warming disrupts mast seeding and its fitness benefits in European beech

Abstract

Many plants benefit from synchronous year-to-year variation in seed production, called masting. Masting benefits plants because it increases the efficiency of pollination and satiates predators, which reduces seed loss. Here, using a 39-year-long dataset, we show that climate warming over recent decades has increased seed production of European beech but decreased the year-to-year variability of seed production and the reproductive synchrony among individuals. Consequently, the benefit that the plants gained from masting has declined. While climate warming was associated with increased reproductive effort, we demonstrate that less effective pollination and greater losses of seeds to predators offset any benefits to the plants. This shows that an apparently simple benefit of climate warming unravels because of complex ecological interactions. Our results indicate that in masting systems, the main beneficiaries of climate-driven increases in seed production are seed predators, not plants.

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Fig. 1: Temporal trends in European beech (F. sylvatica) seed production in England: population- and individual-level variability, and within- and among-site synchrony of reproduction for 12 sites and 139 trees (1980–2018).
Fig. 2: Temporal contribution of the predictor variables.
Fig. 3: Weakening benefits to European beech from mast seeding.
Fig. 4: Temporal trends in European beech total and effective seed production.

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The data that support the findings of this study are available on request from the corresponding author.

References

  1. Seidl, R. et al. Forest disturbances under climate change. Nat. Clim. Change 7, 395–402 (2017).

    Google Scholar 

  2. Zohner, C. M., Mo, L. & Renner, S. S. Global warming reduces leaf-out and flowering synchrony among individuals. eLife 7, e40214 (2018).

    PubMed  PubMed Central  Google Scholar 

  3. Bastin, J.-F. et al. The global tree restoration potential. Science 365, 76–79 (2019).

    CAS  PubMed  Google Scholar 

  4. Luo, Y., McIntire, E. J. B., Boisvenue, C., Nikiema, P. P. & Chen, H. Y. H. Climatic change only stimulated growth for trees under weak competition in central boreal forests. J. Ecol. 108, 36–46 (2019).

  5. Angert, A. L. et al. Do species’ traits predict recent shifts at expanding range edges? Ecol. Lett. 14, 677–689 (2011).

    PubMed  Google Scholar 

  6. Koenig, W. D. et al. Is the relationship between mast-seeding and weather in oaks related to their life-history or phylogeny? Ecology 97, 2603–2615 (2016).

    PubMed  Google Scholar 

  7. McKone, M. J., Kelly, D. & Lee, W. G. Effect of climate change on mast-seeding species: frequency of mass flowering and escape from specialist insect seed predators. Glob. Change Biol. 4, 591–596 (1998).

    Google Scholar 

  8. Vacchiano, G. et al. Spatial patterns and broad-scale weather cues of beech mast seeding in Europe. New Phytol. 215, 595–608 (2017).

    PubMed  Google Scholar 

  9. Kelly, D. The evolutionary ecology of mast seeding. Trends Ecol. Evol. 9, 465–470 (1994).

    CAS  PubMed  Google Scholar 

  10. Fernández-Martínez, M., Vicca, S., Janssens, I. A., Espelta, J. M. & Peñuelas, J. The role of nutrients, productivity and climate in determining tree fruit production in European forests. New Phytol. 213, 669–679 (2017).

    PubMed  Google Scholar 

  11. Monks, A., Monks, J. M. & Tanentzap, A. J. Resource limitation underlying multiple masting models makes mast seeding sensitive to future climate change. New Phytol. 210, 419–430 (2016).

    PubMed  Google Scholar 

  12. Pearse, I. S., Koenig, W. D. & Kelly, D. Mechanisms of mast seeding: resources, weather, cues, and selection. New Phytol. 212, 546–562 (2016).

    CAS  PubMed  Google Scholar 

  13. Bogdziewicz, M., Crone, E. E., Steele, M. A. & Zwolak, R. Effects of nitrogen deposition on reproduction in a masting tree: benefits of higher seed production are trumped by negative biotic interactions. J. Ecol. 105, 310–320 (2017).

    CAS  Google Scholar 

  14. Kelly, D. et al. Of mast and mean: differential-temperature cue makes mast seeding insensitive to climate change. Ecol. Lett. 16, 90–98 (2013).

    PubMed  Google Scholar 

  15. Koenig, W. D., Knops, J. M., Carmen, W. J. & Pearse, I. S. What drives masting? The phenological synchrony hypothesis. Ecology 96, 184–192 (2015).

    PubMed  Google Scholar 

  16. Kelly, D., Hart, D. E. & Allen, R. B. Evaluating the wind pollination benefits of mast seeding. Ecology 82, 117–126 (2001).

    Google Scholar 

  17. Rees, M., Kelly, D. & Bjørnstad, O. N. Snow tussocks, chaos, and the evolution of mast seeding. Am. Nat. 160, 44–59 (2002).

    PubMed  Google Scholar 

  18. Tachiki, Y. & Iwasa, Y. Both seedling banks and specialist seed predators promote the evolution of synchronized and intermittent reproduction (masting) in trees. J. Ecol. 98, 1398–1408 (2010).

    Google Scholar 

  19. Norton, D. A. & Kelly, D. Mast seeding over 33 years by Dacrydium cupressinum Lamb. (rimu) (Podocarpaceae) in New Zealand: the importance of economies of scale. Funct. Ecol. 2, 399–408 (1988).

  20. Rapp, J. M., McIntire, E. J. & Crone, E. E. Sex allocation, pollen limitation and masting in whitebark pine. J. Ecol. 101, 1345–1352 (2013).

    Google Scholar 

  21. Moreira, X., Abdala-Roberts, L., Linhart, Y. B. & Mooney, K. A. Masting promotes individual- and population-level reproduction by increasing pollination efficiency. Ecology 95, 801–807 (2014).

    PubMed  Google Scholar 

  22. Linhart, Y. B., Moreira, X., Snyder, M. A. & Mooney, K. A. Variability in seed cone production and functional response of seed predators to seed cone availability: support for the predator satiation hypothesis. J. Ecol. 102, 576–583 (2014).

    Google Scholar 

  23. Kelly, D. et al. Predator satiation and extreme mast seeding in 11 species of Chionochloa (Poaceae). Oikos 90, 477–488 (2000).

    Google Scholar 

  24. Espelta, J. M., Cortés, P., Molowny-Horas, R., Sánchez-Humanes, B. & Retana, J. Masting mediated by summer drought reduces acorn predation in Mediterranean oak forests. Ecology 89, 805–817 (2008).

    PubMed  Google Scholar 

  25. Kelly, D. & Sork, V. L. Mast seeding in perennial plants: why, how, where? Annu. Rev. Ecol. Syst. 33, 427–447 (2002).

    Google Scholar 

  26. Bogdziewicz, M., Steele, M. A., Marino, S. & Crone, E. E. Correlated seed failure as an environmental veto to synchronize reproduction of masting plants. New Phytol. 219, 98–108 (2018).

    PubMed  Google Scholar 

  27. Pearse, I. S., LaMontagne, J. M. & Koenig, W. D. Inter-annual variation in seed production has increased over time (1900–2014). Proc. R. Soc. B 284, 20171666 (2017).

    PubMed  Google Scholar 

  28. Walther, G.-R. et al. Ecological responses to recent climate change. Nature 416, 389–395 (2002).

    CAS  Google Scholar 

  29. Chen, I.-C., Hill, J. K., Ohlemüller, R., Roy, D. B. & Thomas, C. D. Rapid range shifts of species associated with high levels of climate warming. Science 333, 1024–1026 (2011).

    CAS  Google Scholar 

  30. Koenig, W. D. et al. Dissecting components of population-level variation in seed production and the evolution of masting behavior. Oikos 102, 581–591 (2003).

    Google Scholar 

  31. Bogdziewicz, M. et al. Masting in wind-pollinated trees: system-specific roles of weather and pollination dynamics in driving seed production. Ecology 98, 2615–2625 (2017).

    PubMed  Google Scholar 

  32. Peñuelas, J. & Filella, I. Responses to a warming world. Science 294, 793–795 (2001).

    PubMed  Google Scholar 

  33. Richardson, S. J. et al. Climate and net carbon availability determine temporal patterns of seed production by Nothofagus. Ecology 86, 972–981 (2005).

    Google Scholar 

  34. Buechling, A., Martin, P. H., Canham, C. D., Shepperd, W. D. & Battaglia, M. A. Climate drivers of seed production in Picea engelmannii and response to warming temperatures in the southern Rocky Mountains. J. Ecol. 104, 1051–1062 (2016).

    CAS  Google Scholar 

  35. Satake, A. & Bjørnstad, O. N. Spatial dynamics of specialist seed predators on synchronized and intermittent seed production of host plants. Am. Nat. 163, 591–605 (2004).

    PubMed  Google Scholar 

  36. Bogdziewicz, M., Shealyn, M., Bonal, R., Zwolak, R. & Steele, M. A. Rapid aggregative and reproductive responses of weevils to masting of North American oaks counteract predator satiation. Ecology 99, 2575–2582 (2018).

    PubMed  Google Scholar 

  37. Verheyen, K. et al. Juniperus communis: victim of the combined action of climate warming and nitrogen deposition? Plant Biol. 11, 49–59 (2009).

    CAS  PubMed  Google Scholar 

  38. Zwolak, R., Bogdziewicz, M., Wróbel, A. & Crone, E. E. Advantages of masting in European beech: timing of granivore satiation and benefits of seed caching support the predator dispersal hypothesis. Oecologia 180, 749–758 (2016).

    PubMed  Google Scholar 

  39. Jensen, T. S. Seed–seed predator interactions of European beech, Fagus silvatica and forest rodents, Clethrionomys glareolus and Apodemus flavicollis. Oikos 44, 149–156 (1985).

    Google Scholar 

  40. Piovesan, G. & Adams, J. M. Masting behaviour in beech: linking reproduction and climatic variation. Can. J. Bot. 79, 1039–1047 (2001).

    Google Scholar 

  41. Satake, A. & Iwasa, Y. O. H. Pollen coupling of forest trees: forming synchronized and periodic reproduction out of chaos. J. Theor. Biol. 203, 63–84 (2000).

    CAS  PubMed  Google Scholar 

  42. Crone, E. E. & Rapp, J. M. Resource depletion, pollen coupling, and the ecology of mast seeding. Ann. NY Acad. Sci. 1322, 21–34 (2014).

    CAS  PubMed  Google Scholar 

  43. Satake, A. & Bjørnstad, O. N. A resource budget model to explain intraspecific variation in mast reproductive dynamics. Ecol. Res. 23, 3–10 (2008).

    Google Scholar 

  44. Sykes, M. T., Prentice, I. C. & Cramer, W. A bioclimatic model for the potential distributions of north European tree species under present and future climates. J. Biogeogr. 23, 203–233 (1996).

    Google Scholar 

  45. Vacchiano, G. et al. Reproducing reproduction: how to simulate mast seeding in forest models. Ecol. Modell. 376, 40–53 (2018).

    Google Scholar 

  46. Penuelas, J. & Boada A global change‐induced biome shift in the Montseny mountains (NE Spain). Glob. Change Biol. 9, 131–140 (2003).

    Google Scholar 

  47. Jump, A. S., Hunt, J. M. & Penuelas, J. Climate relationships of growth and establishment across the altitudinal range of Fagus sylvatica in the Montseny Mountains, northeast Spain. Ecoscience 14, 507–518 (2007).

    Google Scholar 

  48. Clement, J. et al. Relating increasing hantavirus incidences to the changing climate: the mast connection. Int. J. Health Geogr. 8, 1 (2009).

    PubMed  PubMed Central  Google Scholar 

  49. Bogdziewicz, M., Zwolak, R. & Crone, E. E. How do vertebrates respond to mast seeding? Oikos 125, 300–307 (2016).

    Google Scholar 

  50. Ostfeld, R. S. & Keesing, F. Pulsed resources and community dynamics of consumers in terrstrial ecosystems. Trends Ecol. Evol. 15, 232–237 (2000).

    CAS  PubMed  Google Scholar 

  51. Szymkowiak, J. & Thomson, R. L. Nest predator avoidance during habitat selection of a songbird varies with mast peaks and troughs. Behav. Ecol. Sociobiol. 73, 91 (2019).

    Google Scholar 

  52. Schmidt, K. A. & Ostfeld, R. S. Numerical and behavioral effects within a pulse-driven system: consequences for shared prey. Ecology 89, 635–646 (2008).

    PubMed  Google Scholar 

  53. Elliott, G. & Kemp, J. Large-scale pest control in New Zealand beech forests. Ecol. Manag. Restor. 17, 200–209 (2016).

    Google Scholar 

  54. Bogdziewicz, M. et al. From theory to experiments for testing the proximate mechanisms of mast seeding: an agenda for an experimental ecology. Ecol. Lett. 23, 210–220 (2020).

    PubMed  PubMed Central  Google Scholar 

  55. Nilsson, S. G. & Wastljung, U. Seed predation and cross-pollination in mast-seeding beech (Fagus sylvatica) patches. Ecology 68, 260–265 (1987).

    Google Scholar 

  56. Packham, J. R., Thomas, P. A., Lageard, J. G. A. & Hilton, G. M. The English beech masting survey 1980–2007: variation in the fruiting of the common beech (Fagus sylvatica L.) and its effects on woodland ecosystems. Arboric. J. 31, 189–214 (2008).

    Google Scholar 

  57. Dore, A. J. et al. The influence of model grid resolution on estimation of national scale nitrogen deposition and exceedance of critical loads. Biogeosciences 9, 1597–1609 (2012).

    CAS  Google Scholar 

  58. Tipping, E. et al. Long-term increases in soil carbon due to ecosystem fertilization by atmospheric nitrogen deposition demonstrated by regional-scale modelling and observations. Sci. Rep. 7, 1–11 (2017).

    CAS  Google Scholar 

  59. Cornes, R. C., van der Schrier, G., van den Besselaar, E. J. & Jones, P. D. An ensemble version of the E-OBS temperature and precipitation data sets. J. Geophys. Res. Atmos. 123, 9391–9409 (2018).

    Google Scholar 

  60. Fernández-Martínez, M. et al. Global trends in carbon sinks and their relationships with CO2 and temperature. Nat. Clim. Change 9, 73 (2019).

    Google Scholar 

  61. Fernández-Martínez, M. et al. Atmospheric deposition, CO2, and change in the land carbon sink. Sci. Rep. 7, 9632 (2017).

    PubMed  PubMed Central  Google Scholar 

  62. Hacket-Pain, A. J. et al. Climatically controlled reproduction drives interannual growth variability in a temperate tree species. Ecol. Lett. 21, 1833–1844 (2018).

    PubMed  PubMed Central  Google Scholar 

  63. Drobyshev, I. et al. Masting behaviour and dendrochronology of European beech (Fagus sylvatica L.) in southern Sweden. For. Ecol. Manag. 259, 2160–2171 (2010).

    Google Scholar 

  64. Burnham, K. P. & Anderson, D. R. Model Selection and Multimodel Inference: A Practical Information-Theoretic Approach (Springer, 2003).

  65. Brooks, M. E. et al. glmmTMB balances speed and flexibility among packages for zero-inflated generalized linear mixed modeling. R J. 9, 378–400 (2017).

    Google Scholar 

  66. Hartig, F. DHARMa: Residual diagnostics for hierarchical (multi-level/mixed) regression models. R package v.0.1.5 (CRAN, 2017).

  67. Tavares, H. windowscanr: Apply functions using sliding windows. R package version v.0.1 (RDRR, 2019).

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Acknowledgements

The study was partially funded by the UK Natural Environment Research Council grant no. NE/S007857/1. M.B. was supported by the Polish National Science Centre (grants Sonatina no. 2017/24/C/NZ8/00151 and Uwertura no. 2018/28/U/NZ8/00003). We thank M. Fernández-Martínez for statistical consultation and R. Chiverrell, A. Morse and L. McGarty for comments on the manuscript. The late J.R. Packham and G.M. Hilton are acknowledged for initiating the English Beech Masting Survey, as are friends, family and colleagues who have assisted in annual data collection. We acknowledge the E-OBS dataset from the EU-FP6 project UERRA (http://www.uerra.eu) and the data providers in the ECA&D project (https://www.ecad.eu). We thank U. Dragosits and S. Tomlinson (NERC Centre for Ecology & Hydrology) for providing nitrogen deposition data and advice.

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M.B. conceived the study and drafted the manuscript. M.B. led the analysis with input from A.H.P. and D.K. P.A.T., J.G.A.L. and A.H.-P. collected and managed the data. All authors interpreted the results, revised the text and provided critical feedback, and helped shape the final text.

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Correspondence to Michał Bogdziewicz.

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Peer review information Nature Plants thanks Eliane Schermer and the other, anonymous, reviewers for their contribution to the peer review of this work.

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Bogdziewicz, M., Kelly, D., Thomas, P.A. et al. Climate warming disrupts mast seeding and its fitness benefits in European beech. Nat. Plants 6, 88–94 (2020). https://doi.org/10.1038/s41477-020-0592-8

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