Introduction history is frequently mentioned as one of the major determinants of the current invasiveness status of alien plants (Williamson 1996; Lockwood et al. 2005; Pyšek & Jarošik 2005; Colautti 2005). However, few studies included reasonably accurate data on both the time since introduction (i.e. in contrast to the time since first record in the wild, which is frequently used) and propagule pressure (Mulvaney 2001; Křivánek et al. 2006; Dehnen-Schmutz et al. 2007a,b) to test this. In our study, time since introduction and, particularly, planting frequency (i.e. propagule pressure) determined the current degree of naturalization of North American woody plants in Europe. Similar results were found for 289 ornamental woody species in south-eastern Australia (Mulvaney 2001), and for 28 alien tree species planted for forestry purposes in the Czech Republic (Křivánek et al. 2006). Although these results do not unambiguously prove it, they at least strongly suggest that the introduction history determines the current invasiveness status of alien species rather than that species with high invasion potential happen to have been earlier or more widely planted than species without invasion potential. This implies that studies comparing invasiveness of species should account for introduction history.
In our study system planting frequency explained more of the variation in naturalization success than time since introduction. A potential reason for the relatively small effect of time since introduction could be that our data set included only species that had been introduced to Europe before 1915. Although the species might not have spread to their full potential yet, it is likely that time since introduction would have been more important as determinant of current naturalization success if our data set had also included more recently introduced species. In line with this, time since introduction did not significantly determine naturalization success in the subset of species used to test the effects of species characteristics, and in which late-introduced species were even less represented than in the complete data set (see Methods).
Six of the 26 species characteristics we studied had a significant effect on naturalization success, although they only explained a relatively small percentage (16.3% vs. 61.4% for introduction history and taxonomy) of the variation in naturalization success. Nevertheless, their significance implies that if we were to simultaneously introduce two or more species of the same family at equal frequencies, their characteristics would at least in part determine their naturalization success.
Tree species had a lower naturalization success in Europe than non-tree species (i.e. vines, shrubs and subshrubs). A similar result was found for 165 woody species introduced into New England (Herron et al. 2007). A potential explanation for the low naturalization success of trees could be that they are less frequently used as ornamentals than non-trees. Another potential explanation could be that trees usually have longer juvenile periods than non-trees, and as a consequence require more time before they can reproduce and spread. This is consistent with the findings of Rejmánek & Richardson (1996) that invasive Pinus species have shorter juvenile periods than non-invasive ones.
Most interestingly, the positive effect of planting frequency on naturalization success was much smaller for trees than for non-trees. This could be because some of the tree species that are not planted frequently in gardens, but have naturalized, are used in forestry (Křivánek et al. 2006). It could also be that many of the naturalized tree species were introduced to the UK, which has a strong horticultural tradition, but was not covered by our source for planting frequency (Bartels et al. 1982). Another explanation could be that gardens usually contain fewer individuals of each tree species than of non-trees. Despite their larger potential seed output, trees might thus rarely reproduce due to mate limitation. The presence of trees and non-trees in the same number of gardens may therefore not reflect the same propagule pressure.
Evergreen species had a higher naturalization success in Europe than deciduous species. This pattern could reflect the successful naturalization of many coniferous species (Richardson & Rejmánek 2004), and the successful establishment of evergreen broad-leaved woody plants in the Mediterranean parts of Europe. Also at higher latitudes, shrub layers have become increasingly dominated by alien evergreen broad-leaved species – possibly as a consequence of climate change (Walther et al. 2002). In contrast, for North America the evergreen woody species are less likely to become invasive (Reichard & Hamilton 1997; Herron et al. 2007). Although the biological reason for these different patterns remains obscure, they indicate that the importance of leaf retention for invasiveness of woody species is continent-specific.
Environmental tolerance of species is probably a strong determinant of naturalization success (Baker 1974; Richards et al. 2006). In line with this, the woody species occurring over a wide precipitation gradient in North America had a higher naturalization success in Europe than the species that occur over a narrow precipitation gradient in North America. Although many other species characteristics in our data set are directly related to environmental tolerance, none had a significant effect on naturalization success. Nevertheless, the positive effect of precipitation tolerance supports the hypothesis that environmental tolerance increases invasiveness (Baker 1974; Richards et al. 2006).
Size of the native range may indirectly reflect environmental tolerance of the species (Scott & Panetta 1993; Goodwin et al. 1999; Prinzing et al. 2002). However, wide-spread species may also have a higher chance of being encountered by horticulturalists and being selected for introduction elsewhere than species with a small native range (Pyšek et al. 2004). Van Kleunen et al. (2007) showed that the probability of southern African Iridaceae to be introduced elsewhere for horticultural purposes was positively associated with native range size, but that subsequent naturalization of these species was not associated with size of the native range. This suggests that size of the native range mainly reflects the chance of being introduced elsewhere. In our study, however, because we directly corrected for planting frequency in our analysis, the remaining variation in naturalization success explained by size of the native range most likely reflects some component of environmental tolerance that was not covered by the other species characteristics in our data set (e.g. tolerance to herbivores and pathogens).
One of the potential characteristics of invasive species is rapid growth (Baker 1974). Our study did, however, not reveal a significant association between growth rate and naturalization success of North American woody species in Europe. This could be because the estimates of growth rate were semi-quantitative (slow, moderate and fast). Nevertheless, two previous studies that used the same data source for growth rate as we did found that invasiveness of woody species is positively associated with growth rate (Frappier & Eckert 2003; Herron et al. 2007). Of the few studies that used experimentally determined relative growth rates of alien woody species, Bellingham et al. (2004) found no significant association between growth rate of seedlings and invasiveness, but Grotkopp et al. (2002) and Grotkopp & Rejmánek (2007) found a significant association. So, although invasiveness of woody species is frequently associated with rapid growth, this did not appear to be the case for North American woody species in Europe. Clearly, experimentally determined estimates of growth rate are needed to test whether this also holds when more accurate data are used.
Competitiveness of plants is likely to increase with size (Pianka 1970), and therefore it has often been suggested that plant size may promote naturalization of a species (Crawley 1987; Blossey & Nötzold 1995). This is consistent with our finding that naturalization was positively associated with plant height, although this positive association was only present among the tree species in our data set. On the other hand, the invasiveness of alien woody species in New England is not significantly associated with mature plant height (Herron et al. 2007). Overall, it seems that the association between invasiveness and plant height depends on the growth form of the species and the target region, but in the studies that found an association it was always a positive one.
Dispersal characteristics are likely to be important determinants of spread of alien species (Baker 1974). As expected, seed spread rate was positively associated with naturalization success in Europe. However, again this positive association was present among the tree species in our data set but not among the non-tree species. Similarly, Herron et al. (2007) found that wind dispersal was positively associated with invasiveness of trees in New England but was not associated with invasiveness of non-trees. Together these results suggest that seed dispersal characteristics are determinants of invasiveness of trees but not of invasiveness of other woody species.
A major aim in invasion biology is the identification of species characteristics that determine invasiveness. Although the number of studies comparing species with different degrees of invasiveness is increasing, their overall number is still low (Pysek & Richardson 2007), and very few studies have included introduced species that failed to establish (e.g. Dehnen-Schmutz et al. 2007a,b; van Kleunen et al. 2007) or corrected for both time since introduction and propagule pressure. Our study showed that the current naturalization success of North American woody species in Europe is mainly determined by their introduction history, particularly planting frequency. This implies that many of the species that have been introduced recently or at low frequency might not have reached their full invasion potential yet, and therefore should not be ignored by conservation authorities.
Although a large proportion of the variation in naturalization success was explained by introduction history, species characteristics related to environmental tolerance, plant size, dispersal and growth form also contributed significantly to naturalization success of North American woody species in Europe. This implies that these traits are good candidates to be used in screening procedures for predicting potential naturalization success of woody species considered for introduction. It also shows, however, that even species that do not possess the optimal suite of characteristics might eventually establish when planted frequently.
For several characteristics the available data were very crude, and for other potentially important traits no data were available. Therefore, the explanatory power of species characteristics might further increase when more accurate data and data on larger numbers of species characteristics become available. Many of these characteristics, such as breeding system, phenotypic plasticity and competitive ability, will have to be assessed experimentally (van Kleunen & Johnson 2007; van Kleunen & Richardson 2007; van Kleunen et al. 2008).
Another important finding of our study is that the strength of the association between species characteristics strongly depends on the growth form of the species. This shows that the importance of some species characteristics cannot be generalized for all growth forms, and that it is crucial to test for interactions between growth form and other characteristics, when searching for determinants of invasiveness.