Extended leaf phenology: a secret of successful invaders?



Smith (2013), in this issue, reviews the consequences of extended leaf phenology of invasive plant species in native deciduous forests. How important is early leaf emergence and/or late leaf senescence for the success of non-native species? What are the direct and indirect impacts on invaded communities and ecosystems? We are just at the very early stage in answering such questions.

There are many factors influencing the invasion success of some introduced plant species, and there are many ways in which successful invaders may influence invaded communities and ecosystems (Ehrenfeld 2010; Van Kleunen et al. 2010; Rejmánek et al. 2013). For some time, extended leaf phenology (earlier leaf emergence and/or later leaf senescence and abscission) has been considered one of the attributes that may promote invasions and impacts of non-native plants (e.g. Harrington et al. 1989; Gérard & Guy 1998; Xu et al. 2007; Fridley 2012, 2013; Wang et al. 2012). For example, the leaf development of invasive Amur honeysuckle (Lonicera maackii) starts 2–3 weeks earlier than that of the native competitors growing in the same habitats in central Kentucky (McEwans et al. 2009). On the other hand, in the eastern United States, non-native woody species (e.g. Lonicera japonica, Frangula alnus, Berberis vulgaris) are extending the autumn growing season by an average of 4 weeks compared with natives (Fridley 2012). So far, most attention has been paid to increased invader growth and competitive advantages resulting from increased access to light and other resources due to longer periods of activity each year. However, as any ecologist would be immediately ready to admit, there must be many more direct and indirect ecological consequences of extended leaf duration in established non-native species (Fig. 1).

Figure 1.

Sapling of Hovenia dulcis Thunb. (Rhamnaceae) in the Parque Estadual Fritz Plaumann, Santa Catarina, Brazil. This deciduous invasive tree from East Asia exhibits an extended spring leaf phenology, i.e. earlier leaf emergence than native deciduous trees. (Photo by M. Rejmánek.)

In this issue of the Journal of Vegetation Science, Lauren M. Smith (2013) attempts to make a systematic review of all potential ecological impacts of extended leaf activity in introduced plant species. Smith distinguished seven categories of potential consequences of invasive plant taxa with extended leaf phenology: (1) enhancement of resource competition via shading and nutrient pre-emption; (2) increased production of allelochemicals; (3) alteration of indirect effects mediated by large herbivores; (4) temporal enemy escape; (5) alteration of indirect competition mediated by small mammal predators of seed and seedlings; (6) indirect impacts on birds, reptiles and amphibians; and (7) alteration of pollinator-mediated interactions. Some examples used in individual categories are from systems that do not include non-native species with extended leaf phenology, but the argumentation for the listed direct and indirect impacts of invaders with such phenology is powerful, and Smith's call for experiments is, of course, fully justified. This review will certainly stimulate a range of future studies.

Inevitably, some additional questions come to mind while reading Smith's review. First, the ultimate goal should be to understand the impact of extended leaf phenology on the fitness of non-native species. That, however, would have to take into account fertility and survival in individual age stages. It is well known that some successful invasive plant species have extended flowering and fruiting phenology (Rejmánek & Reichard 2001; Pyšek & Richardson 2007; Küster et al. 2010). Such ‘spreading of the risk’ most likely contributes to invaders’ fitness. Therefore, an important question is whether extended flowering and/or fruiting phenology is positively correlated with extended leaf phenology. On the other hand, if extended leaf phenology of seedlings is not associated with freezing tolerance, then increased mortality and, therefore, decreased fitness may be the result.

Second, as Fridley (2012) pointed out, the extended autumnal activity of invasive deciduous woody plants may lead to significant shifts in nutrient cycling, particularly if nitrogen and phosphorus resorption are reduced in non-natives as a result of delayed leaf senescence. In such situations, patterns of decomposition and nutrient availability may be significantly altered. Third, a widespread trend of a 20–40 day delay of the phenological end of the season has been observed across the eastern USA in the last 20 yrs (Dragoni & Rahman 2012). Does this mean that native species may catch up with some invaders, or will invaders with extended leaf phenology in the autumn always have the advantage? Finally, it is important to consider extended photosynthetic phenology in invasive species with photosynthetically active green stems. Many invasive legumes (e.g. Cytisus spp., Genista spp., Spartium junceum) are probably so successful in semi-arid environments because they shed leaves in the middle of summer, thereby reducing transpiration while maintaining positive carbon balance for the rest of the season (Bossard & Rejmánek 1992). Obviously, all kinds of extended phenology of non-native species represent an exciting topic for future research and new syntheses.