Skip to main content

Thank you for visiting nature.com. 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.

  • Article
  • Published:

The urban imprint on plant phenology

Nature Ecology & Evolution volume 3, pages 1668–1674 (2019)Cite this article

Subjects

Abstract

The modification of the surface radiation and energy balance in urban areas causes the temperatures in these areas to exceed those of the surrounding countryside. It has thus been suggested that urban environments may serve as field laboratories for studying the effects of a warming climate on biota in a space-for-time substitution. Here we investigated changes in the timing of plant phenology and temperature across study sites that differed in the degree of urbanization using publicly available pan-European datasets for the period 1981–2010. We found a significant advancement in the phenological phases of leaf development, flowering and fruiting with higher degrees of urbanization, whereas a significant delay was observed for phenological phases of leaf senescence. In addition to these phenological changes, an increase in air temperature with higher degrees of urbanization was observed. This increase was largest during the periods of leaf development, flowering and fruiting and smallest during the period of leaf senescence. On the basis of these results, we show that the apparent temperature sensitivity of phenological phases to urban warming is either significantly dampened (leaf development, flowering and fruiting) or reversed (leaf senescence) compared with the temperature sensitivity inferred from temporal changes in phenology and temperature. We conclude that gradients in urbanization represent a poor analogue for the temporal changes in plant phenology, apparently owing to confounding factors associated with urbanization.

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

Access options

Buy this article

  • Purchase on Springer Link
  • Instant access to full article PDF
Buy now

Prices may be subject to local taxes which are calculated during checkout

Fig. 1: Coefficients of the MLR analysis describe unique changes in plant phenology with changes in UF.
Fig. 2: Coefficients of the MLR regression analysis describe unique changes in air temperature with changes in UF.
Fig. 3: Apparent temperature sensitivities of aggregated phenological phases.
Fig. 4: Coefficients of the MLR analysis describe unique changes in plant phenology over time.

Similar content being viewed by others

Data availability

The phenological data used in this study are available from www.pep725.eu and the air temperature data from www.ecad.eu. The data underlying the CORINE land cover, the imperviousness degree and the European settlement map are available from the Copernicus Land Monitoring Service (https://land.copernicus.eu/pan-european).

Code availability

The MATLAB (MathWorks) scripts used to analyse data are available at https://doi.org/10.5281/zenodo.3422079.

References

  1. Cleland, E. E., Chuine, I., Menzel, A., Mooney, H. A. & Schwartz, M. D. Shifting plant phenology in response to global change. Trends Ecol. Evol. 22, 357–365 (2007).

    Article  Google Scholar 

  2. Zhou, B., Rybski, D. & Kropp, J. P. On the statistics of urban heat island intensity. Geophys. Res. Lett. 40, 5486–5491 (2013).

    Article  Google Scholar 

  3. Stewart, I. D. & Oke, T. R. Local climate zones for urban temperature. Stud. Bull. Am. Meteorol. Soc. 93, 1879–1900 (2012).

    Article  Google Scholar 

  4. Jochner, S. & Menzel, A. Urban phenological studies—past, present, future. Environ. Pollut. 203, 250–261 (2015).

    Article  CAS  Google Scholar 

  5. Neil, K. & Wu, J. Effects of urbanization on plant flowering phenology: a review. Urban Ecosyst. 9, 243–257 (2006).

    Article  Google Scholar 

  6. Menzel, A. et al. European phenological response to climate change matches the warming pattern. Glob. Change Biol. 12, 1969–1976 (2006).

    Article  Google Scholar 

  7. Harrison, T., Winfree, R. & Evans, K. Urban drivers of plant–pollinator interactions. Funct. Ecol. 29, 879–888 (2015).

    Article  Google Scholar 

  8. Zhao, S., Liu, S. & Zhou, D. Prevalent vegetation growth enhancement in urban environment. Proc. Natl Acad. Sci. USA 113, 6313–6318 (2016).

    Article  CAS  Google Scholar 

  9. Wang, S. et al. Urban–rural gradients reveal joint control of elevated CO2 and temperature on extended photosynthetic seasons. Nat. Ecol. Evol. 3, 1076–1085 (2019).

    Article  Google Scholar 

  10. Herrmann, D. L., Schifman, L. A. & Shuster, W. D. Widespread loss of intermediate soil horizons in urban landscapes. Proc. Natl Acad. Sci. USA 115, 6751–6755 (2018).

    Article  Google Scholar 

  11. Zipper, S. C., Schatz, J., Kucharik, C. J. & Loheide, S. P. Urban heat island-induced increases in evapotranspirative demand. Geophys. Res. Lett. 44, 873–881 (2017).

    Article  Google Scholar 

  12. Mitchell, L. E. et al. Long-term urban carbon dioxide observations reveal spatial and temporal dynamics related to urban characteristics and growth. Proc. Natl Acad. Sci. USA 115, 2912–2917 (2018).

    Article  CAS  Google Scholar 

  13. Grange, S. K., Lewis, A. C., Moller, S. J. & Carslaw, D. C. Lower vehicular primary emissions of NO2 in Europe than assumed in policy projections. Nat. Geosci. 10, 914–918 (2017).

    Article  CAS  Google Scholar 

  14. Tsai, D. H., Wang, J. L., Wang, C. H. & Chan, C. C. A study of ground-level ozone pollution, ozone precursors and subtropical meteorological conditions in central Taiwan. J. Environ. Monit. 10, 109–118 (2008).

    Article  CAS  Google Scholar 

  15. Jochner, S. et al. The effects of short- and long-term air pollutants on plant phenology and leaf characteristics. Environ. Pollut. 206, 382–389 (2015).

    Article  CAS  Google Scholar 

  16. Honour, S. L., Bell, J. N., Ashenden, T. W., Cape, J. N. & Power, S. A. Responses of herbaceous plants to urban air pollution: effects on growth, phenology and leaf surface characteristics. Environ. Pollut. 157, 1279–1286 (2009).

    Article  CAS  Google Scholar 

  17. Sanz, J. et al. Plant phenology, growth and nutritive quality of Briza maxima: responses induced by enhanced ozone atmospheric levels and nitrogen enrichment. Environ. Pollut. 159, 423–430 (2011).

    Article  CAS  Google Scholar 

  18. Škvareninová, J. et al. Effects of light pollution on tree phenology in the urban environment. Morav. Geogr. Rep. 25, 282–290 (2017).

    Google Scholar 

  19. Massetti, L. Assessing the impact of street lighting on Platanus x acerifolia phenology. Urban For. Urban Green. 34, 71–77 (2018).

    Article  Google Scholar 

  20. Gorton, A. J., Moeller, D. A. & Tiffin, P. Little plant, big city: a test of adaptation to urban environments in common ragweed (Ambrosia artemisiifolia). Proc. R. Soc. B 285, 20180968 (2018).

    Article  Google Scholar 

  21. Stewart, I. D. A systematic review and scientific critique of methodology in modern urban heat island literature. Int. J. Climatol. 31, 200–217 (2011).

    Article  Google Scholar 

  22. Comber, A. & Brunsdon, C. A spatial analysis of plant phenophase changes and the impact of increases in urban land use. Int. J. Climatol. 35, 972–980 (2015).

    Article  Google Scholar 

  23. Jochner, S. C., Sparks, T. H., Estrella, N. & Menzel, A. The influence of altitude and urbanisation on trends and mean dates in phenology (1980–2009). Int J. Biometeorol. 56, 387–394 (2012).

    Article  Google Scholar 

  24. Roetzer, T., Wittenzeller, M., Haeckel, H. & Nekovar, J. Phenology in central Europe – differences and trends of spring phenophases in urban and rural areas. Int J. Biometeorol. 44, 60–66 (2000).

    Article  CAS  Google Scholar 

  25. Templ, B. et al. Pan European Phenological database (PEP725): a single point of access for European data. Int J. Biometeorol. 62, 1109–1113 (2018).

    Article  Google Scholar 

  26. Klein Tank, A. M. G. et al. Daily dataset of 20th-century surface air temperature and precipitation series for the European Climate Assessment. Int. J. Climatol. 22, 1441–1453 (2002).

    Article  Google Scholar 

  27. Chrysanthou, A., van der Schrier, G., van den Besselaar, E. J. M., Klein Tank, A. M. G. & Brandsma, T. The effects of urbanization on the rise of the European temperature since 1960. Geophys. Res. Lett. 41, 7716–7722 (2014).

    Article  Google Scholar 

  28. Keenan, T. F., Richardson, A. D. & Hufkens, K. On quantifying the apparent temperature sensitivity of plant phenology. New Phytol. https://doi.org/10.1111/nph.16114 (2019).

  29. van Hove, L. W. A. et al. Temporal and spatial variability of urban heat island and thermal comfort within the Rotterdam agglomeration. Build. Environ. 83, 91–103 (2015).

    Article  Google Scholar 

  30. Peterson, T. C. & Owen, T. W. Urban heat island assessment: metadata are important. J. Clim. 18, 2637–2646 (2005).

    Article  Google Scholar 

  31. Zhou, Y. et al. A global map of urban extent from nightlights. Environ. Res. Lett. 10, 054011 (2015).

    Article  Google Scholar 

  32. Meier, U. in Phenology: An Integrative Environmental Science (ed. Schwartz, M. D.) 269–283 (Kluwer Academic, 2003).

  33. Fu, Y. H. et al. Declining global warming effects on the phenology of spring leaf unfolding. Nature 526, 104–107 (2015).

    Article  CAS  Google Scholar 

Download references

Acknowledgements

Phenological data were provided by the members of the PEP725 project. We acknowledge the air temperature data providers of the ECA&D project. This work was partially supported through a grant by the Austrian National Science Fund (FWF, grant number FP27176-B16).

Author information

Authors and Affiliations

  1. Department of Ecology, University of Innsbruck, Innsbruck, Austria

    Georg Wohlfahrt & Albin Hammerle

  2. Faculty of Science and Technology, Free University of Bolzano, Bolzano, Italy

    Enrico Tomelleri

Authors
  1. Georg Wohlfahrt
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Enrico Tomelleri
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Albin Hammerle
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

G.W. conceived the study, analysed the data and wrote the manuscript together with E.T. and A.H.

Corresponding author

Correspondence to Georg Wohlfahrt.

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 Figs. 1–12 including figure legends.

Reporting Summary

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Wohlfahrt, G., Tomelleri, E. & Hammerle, A. The urban imprint on plant phenology. Nat Ecol Evol 3, 1668–1674 (2019). https://doi.org/10.1038/s41559-019-1017-9

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1038/s41559-019-1017-9

This article is cited by

Search

Advanced search

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