Extended leaf phenology and the autumn niche in deciduous forest invasions

Journal name:
Nature
Volume:
485,
Pages:
359–362
Date published:
DOI:
doi:10.1038/nature11056
Received
Accepted
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

Figures

  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.

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Author information

Affiliations

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

    • Jason D. Fridley

Contributions

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.

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Supplementary information

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  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.

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  1. Supplementary Table 1 (111K)

    This file contains data and metadata.

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