Extended leaf phenology and the autumn niche in deciduous forest invasions

Journal name:
Date published:
Published online

The phenology of growth in temperate deciduous forests, including the timing of leaf emergence and senescence, has strong control over ecosystem properties such as productivity1, 2 and nutrient cycling3, 4, and has an important role in the carbon economy of understory plants5, 6, 7. Extended leaf phenology, whereby understory species assimilate carbon in early spring before canopy closure or in late autumn after canopy fall, has been identified as a key feature of many forest species invasions5, 8, 9, 10, but it remains unclear whether there are systematic differences in the growth phenology of native and invasive forest species11 or whether invaders are more responsive to warming trends that have lengthened the duration of spring or autumn growth12. Here, in a 3-year monitoring study of 43 native and 30 non-native shrub and liana species common to deciduous forests in the eastern United States, I show that extended autumn leaf phenology is a common attribute of eastern US forest invasions, where non-native species are extending the autumn growing season by an average of 4weeks compared with natives. In contrast, there was no consistent evidence that non-natives as a group show earlier spring growth phenology, and non-natives were not better able to track interannual variation in spring temperatures. Seasonal leaf production and photosynthetic data suggest that most non-native species capture a significant proportion of their annual carbon assimilate after canopy leaf fall, a behaviour that was virtually absent in natives and consistent across five phylogenetic groups. Pronounced differences in how native and non-native understory species use pre- and post-canopy environments suggest eastern US invaders are driving a seasonal redistribution of forest productivity that may rival climate change in its impact on forest processes.

At a glance


  1. Seasonal patterns of leaf emergence and leaf fall for native and non-native species over three growing seasons.
    Figure 1: Seasonal patterns of leaf emergence and leaf fall for native and non-native species over three growing seasons.

    Boxplots show data range with boxed first and third quartiles, median as heavy line, and point outliers; numbers of species for each group are indicated. Leaf emergence was monitored at 2- to 5-day intervals using a classification of budbreak stages and dates at which 50% and 90% of total leaves had fallen were interpolated from biweekly monitoring. Values indicate median difference in days between natives (green) and non-natives (red). P values are from Mann–Whitney U-tests adjusted for multiple testing (*P<0.05, **P<0.01, ***P<0.001).

  2. Relative leaf Chl content for native and non-native species.
    Figure 2: Relative leaf Chl content for native and non-native species.

    Mean (±s.e.m.) content for native (green) and non-native (red) species are grouped by whether leaves were produced before (filled circles and lines) or after (open circles and dashed lines) canopy shading (grey region). Histograms show distributions of the date of 50% Chl loss, relative to peak Chl reading per leaf, for native (n = 354 leaves) and non-native species (n = 253) pooled across 2009 and 2010 growing seasons.

  3. Proportion of total annual C assimilated in spring and autumn for native and non-native species.
    Figure 3: Proportion of total annual C assimilated in spring and autumn for native and non-native species.

    Values of assimilation before (a, b) and after (c, d) shade cloth placement for native (green) and non-native (red) species were estimated by stochastic simulation of daily leaf area, light levels and photosynthetic capacity using empirical measurements (2008–2010). Values are means (±s.e.m.) of 1,000 permutations incorporating measured variation in individual and interannual leaf production and photosynthetic light curves. Inset figures (b, d) show mean (±s.e.m.) species values summarized by phylogenetic group, with sample sizes indicated. Black asterisks indicate statistical significance for overall native–non-native comparisons and Mann–Whitney U-tests within groups (*P<0.05, ***P<0.001). Coloured asterisks denote autumn C gain less than 0.5%. NS, not significant.


  1. Richardson, A. D. et al. Influence of spring and autumn phenological transitions on forest ecosystem productivity. Phil. Trans. R. Soc. B 365, 32273246 (2010)
  2. Polgar, C. A. & Primack, R. B. Leaf-out phenology of temperate woody plants: from trees to ecosystems. New Phytol. 191, 926941 (2011)
  3. Muller, R. N. & Bormann, F. H. Role of Erythronium americanum Ker. in energy flow and nutrient dynamics of a northern hardwood forest ecosystem. Science 193, 11261128 (1976)
  4. Ehrenfeld, J. G. Effects of exotic plant invasions on soil nutrient cycling processes. Ecosystems 6, 503523 (2003)
  5. Harrington, R. A., Brown, B. J. & Reich, P. B. Ecophysiology of exotic and native shrubs in southern Wisconsin. I. Relationship of leaf characteristics, resource availability, and phenology to seasonal patterns of carbon gain. Oecologia 80, 356367 (1989)
  6. Augsperger, C. K., Chesseman, J. M. & Salk, C. F. Light gains and physiological capacity of understorey woody plants during phenological avoidance of canopy shade. Funct. Ecol. 19, 537546 (2005)
  7. Rothstein, D. E. & Zak, D. R. Photosynthetic adaptation and acclimation to exploit seasonal periods of direct irradiance in three temperate, deciduous-forest herbs. Funct. Ecol. 15, 722731 (2001)
  8. Schierenbeck, K. A. & Marshall, J. D. Seasonal and diurnal patterns of photosynthetic gas exchange for Lonicera sempervirens and L. japonica (Caprifoliaceae). Am. J. Bot. 80, 12921299 (1993)
  9. Xu, C.-Y., Griffin, K. L. & Schuster, W. S. F. Leaf phenology and seasonal variation of photosynthesis of invasive Berberis thunbergii (Japanese barberry) and two co-occurring native understory shrubs in a northeastern United States deciduous forest. Oecologia 154, 1121 (2007)
  10. Myers, C. V. & Anderson, R. C. Seasonal variation in photosynthetic rates influences success of an invasive plant, garlic mustard (Alliaria petiolata). Am. Midl. Nat. 150, 231245 (2003)
  11. Wolkovitch, E. M. & Cleland, E. E. The phenology of plant invasions: a community ecology perspective. Front. Ecol. Environ 9, 287294 (2011)
  12. Willis, C. G., Ruhfel, B. R., Primack, R. B., Miller-Rushing, A. J. & Losos, J. B. Favorable climate change response explains non-native species’ success in Thoreau’s Woods. PLoS ONE 5, e8878 (2010)
  13. Gill, D. S., Amthor, J. S. & Bormann, F. H. Leaf phenology, photosynthesis, and the persistence of saplings and shrubs in a mature northern hardwood forest. Tree Physiol. 18, 281289 (1998)
  14. Augsperger, C. K. & Bartlett, E. A. Differences in leaf phenology between juvenile and adult trees in a temperate deciduous forest. Tree Physiol. 23, 517525 (2003)
  15. Webster, C. R., Jenkins, M. A. & Jose, S. Woody invaders and the challenges they pose to forest ecosystems in the Eastern United States. J. For. 104, 366374 (2006)
  16. Fridley, J. D. Of Asian forests and European fields: Eastern U.S. plant invasions in a global floristic context. PLoS ONE 3, e3630 (2008)
  17. May, J. D. & Killingbeck, K. T. Effects of preventing nutrient resorption on plant fitness and foliar nutrient dynamics. Ecology 73, 18681878 (1992)
  18. Saxe, H., Cannell, G. R., Johnsen, Ø., Ryan, M. G. & Vourlitis, G. Tree and forest functioning in response to global warming. New Phytol. 149, 369400 (2001)
  19. Mitchell, T. D. & Jones, P. D. An improved method of constructing a database of monthly climate observations and associated high-resolution grids. Int. J. Climatol. 25, 693712 (2005)
  20. Aber, J. D., Nadelhoffer, K. J., Steudler, P. & Melillo, J. M. Nitrogen saturation in northern forest ecosystems. Bioscience 39, 378387 (1989)
  21. Mack, R. N. Plant naturalizations and invasions in the Eastern United States: 1634–1860. Ann. Mo. Bot. Gard. 90, 7790 (2003)
  22. Frelich, L. E. et al. Earthworm invasion into previously earthworm-free temperate and boreal forests. Biol. Invasions 8, 12351245 (2006)
  23. Nuzzo, V. A., Maerz, J. C. & Blossey, B. Earthworm invasion as the driving force behind plant invasion and community change in Northeastern North American forests. Conserv. Biol. 23, 966974 (2009)
  24. Ehlers, J. & Gibbard, P. L. The extent and chronology of Cenozoic global glaciation. Quat. Int. 164, 620 (2007)
  25. Lechowicz, M. J. Why do temperate deciduous trees leaf out at different times? Adaptation and ecology of forest communities. Am. Nat. 124, 821842 (1984)
  26. Mack, R. N. Phylogenetic constraint, absent life forms, and preadapted alien plants: a prescription for biological invasions. Int. J. Plant Sci. 164, S185S196 (2003)
  27. Goulden, M. L., Munger, J. W., Fan, S.-M., Daube, B. C. & Wofsy, S. C. Exchange of carbon dioxide by a deciduous forest: response to interannual climate variability. Science 271, 15761578 (1996)
  28. Piao, S. et al. Net carbon dioxide losses of northern ecosystems in response to autumn warming. Nature 451, 4952 (2008)
  29. Liao, C. et al. Altered ecosystem carbon and nitrogen cycles by plant invasion: a meta-analysis. New Phytol. 177, 706714 (2008)
  30. Chapin, F. S. Nitrogen and phosphorus nutrition and nutrient cycling by evergreen and deciduous understory shrubs in an Alaskan black spruce forest. Can. J. For. Res. 13, 773781 (1983)
  31. Canham, C. D. et al. Light regimes beneath closed canopies and tree-fall gaps in temperate and tropical forests. Can. J. For. Res. 20, 620631 (1990)
  32. Morgan, D. C. & Smith, H. A. systematic relationship between phytochrome-controlled development and species habitat, for plants grown in simulated natural radiation. Planta 145, 253258 (1979)
  33. Hothorn, T. & Hornik, K. exactRankTests: exact distributions for rank and permutation tests. R package version 0.8-19. (2010)
  34. Hochberg, Y. A sharper Bonferroni procedure for multiple tests of significance. Biometrika 75, 800802 (1988)
  35. Richardson, A. D., Duigan, S. P. & Berlyn, G. P. An evaluation of noninvasive methods to estimate foliar chlorophyll content. New Phytol. 153, 185194 (2002)
  36. Pinheiro, J., Bates, D., DebRoy, S., Sarkar, D. & the R Development Core Team nlme: Linear and Nonlinear Mixed Effects Models. R package version 3.1-102. (2011)
  37. Hothorn, T., Bretz, F. & Westfall, P. Simultaneous inference in general parametric models. Biometrical J. 50, 346363 (2008)
  38. Lambers, H., Chapin, F. S. & Pons, T. L. Plant Physiological Ecology (Springer, 1998)
  39. Koenker, R. quantreg: Quantile Regression. R package version 4.44. (2009)
  40. Wood, S. N. Fast stable direct fitting and smoothness selection for generalized additive models. J. R. Stat. Soc. B 70, 495518 (2008)
  41. Hutchison, B. A. & Matt, D. R. The distribution of solar radiation within a deciduous forest. Ecol. Monogr. 47, 185207 (1977)

Download references

Author information


  1. Department of Biology, Syracuse University, 107 College Place, Syracuse, New York 13244, USA

    • Jason D. Fridley


J.D.F. designed the study, supervised data collection, performed the analyses and wrote the paper.

Competing financial interests

The author declares no competing financial interests.

Corresponding author

Correspondence to:

Author details

Supplementary information

PDF files

  1. Supplementary Information (428K)

    This file contains Supplementary Figures 1-3. Figure 1 includes spring heat accumulation over 2008-2010, Figure 2 a comparison of seasonal photosynthetic rate between native and non-native species, and Figure 3 the seasonal light distribution used in carbon gain models.

Excel files

  1. Supplementary Table 1 (111K)

    This file contains data and metadata.

Additional data