A lack of mates and pollinators as a barrier to naturalization
My findings that self-compatibility and autofertility have a positive effect on global naturalization strongly suggest that a lack of mates and pollinators may constrain establishment of alien plants that lack those reproductive traits. A study by van Kleunen and Johnson (2007a)
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on 361 plant species suggested that mate limitation, rather than pollinator limitation, is the main barrier for establishment in non-native regions. Mate limitation can cause Allee effects in small populations (Berec, Angulo & Courchamp 2007), but previous studies on Allee effects due to reduced mate availability in non-native regions had different outcomes. In a field experiment in North America, fruit set and seed set were reduced in small populations of the self-incompatible invasive Raphanus sativus (Elam et al. 2007). Other studies found that self-fertilization in invasive plants is not related to population size (van Kleunen, Fischer & Johnson 2007; Rodger, van Kleunen & Johnson 2013). Studies looking at Allee effects in alien plants have so far focused on species that had already naturalized and were spreading in the non-native range, i.e.
during the invasion stage. Future studies should explicitly test whether mate limitation hampers naturalization, i.e. founding and maintenance of populations in new non-native regions.
As naturalized species were better than non-naturalized ones in attracting pollinators in my botanical-garden study, not only mate limitation but also pollinator limitation may constrain establishment in non-native regions. Burns et al. (2011) also suggested that enhanced pollination drives greater invasiveness. Previous studies looking at pollinator and pollen limitation of alien plant species focused on invasion. Small populations of the invasive Solanum rostratum suffered more pollen limitation than large populations in their invaded range in China (Zhang & Lou 2015). In contrast, three invasive milkweed species in Australia were less pollen limited in small populations, compared to large populations, due to lower competition for pollinator services (Ward, Johnson & Zalucki 2013). The invasive thistle Cirsium vulgare attracted more visitors than did its five native counterparts, and it also did not depend on pollinators for seed set
(Powell, Krakos & Knight 2011). Because founder populations are likely to be small at the early stage of establishment, i.e. naturalization, alien plants might not be able to attract sufficient pollinators and therefore might be pollen limited (Ågren 1996; Knight 2003; Ward & Johnson 2005). In chapter II of this thesis, I provide the first evidence that flower visitation is higher in naturalized compared to non-naturalized alien plant species (Razanajatovo et al. 2015).
Nevertheless, because flower visitation might not always result in effective pollination, the causal relationship between flower visitation and naturalization success remains to be tested.
In my botanical-garden study, naturalized species tended to receive a more generalized set of flower visitors compared to non-naturalized ones. So, pollinator generalization might favor
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establishment in non-native regions. In line with this, it has been suggested that pollinator generalization facilitates invasion (Baker 1965; Richardson et al. 2000b). Three invasive milkweed species in Australia were generalized with regard to pollinators, and the composition of pollinator species of these plants were highly variable among populations (Ward 2012). The invasive Cirsium vulgare was also visited by many different insect species (Powell, Krakos &
Knight 2011). In contrast, a study on 118 European species that became invasive outside Eurasia found, for self-compatible species, a trend that invasion success is related to pollinator
specialization (Chrobock et al. 2013b). A few plant species with specialized pollinators also became invasive in non-native regions where their suitable pollinators naturally occur or were also introduced (e.g. Morales & Aizen 2006; Rodger, van Kleunen & Johnson 2010; Kaiser-Bunbury et al. 2011). Therefore, the role pollinator generalization and specialization plays in alien plant invasion might depend on the availability of pollinators. Nevertheless, previous studies on pollinator generalization of alien plants focused on invasion. My findings suggest that the ability to attract suitable pollinators operates earlier on in the process, i.e. it might facilitate naturalization, when alien plants found and maintain populations in non-native ranges.
Little role of reproductive characteristics during the invasion stage
As the degrees of autofertility and pollen limitation did not differ between invasive and non-invasive naturalized alien plant species in my common-garden experiment, these
reproductive characteristics might play little role once a species has naturalized. This is in line with the idea that reproductive characteristics are likely more important during alien plant naturalization, and less during subsequent spread (Richardson & Pyšek 2012). Invasive and non-invasive naturalized alien plant species in my common-garden experiment did not differ in their degrees of pollen limitation and autofertility, but might differ in their dispersal ability. High reproductive output, for example, may be related to greater invasiveness (Baker 1965;
Moravcova et al. 2010; van Kleunen, Weber & Fischer 2010; Powell, Krakos & Knight 2011;
Burns et al. 2013; also suggested in chapter III of this thesis). High reproductive output may also increase propagule pressure (Colautti, Grigorovich & MacIsaac 2007), which in turn can reduce Allee effects (Lockwood, Cassey & Blackburn 2005). Dispersal traits favoring dispersibility can also increase invasiveness (e.g. Moravcová et al. 2015). In conclusion, compared to pollen
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limitation and autofertility, other factors related to dispersal and spread might be more important during invasion.
A stage-focused approach in invasion ecology
The stage-focused approach used in this thesis allows to identify which characteristics are important at which invasion stage, or during a transition from one stage to the following (van Kleunen et al. 2010; van Kleunen, Dawson & Maurel 2015). By comparing flower visitation between naturalized alien species and alien species that did not manage to establish reproducing populations in the wild, I found a difference that might play a key role in the transition from introduction to naturalization (chapter II). My comparison of pollen limitation and autofertility between invasive and non-invasive naturalized alien plant species revealed no difference, which suggests that these reproductive characteristics might not be important in the transition from naturalization to invasion (chapter III). The comparisons among native, successful and unsuccessful alien species reveal which characteristics the successful alien species have in common with the natives, which might also play a role in their success. Naturalized alien plant species in my botanical-garden study received at least as many flower visits as the natives (Fig.
II.1a), supporting the idea that naturalization may be related to flower visitation. Invasive and non-invasive alien species in my common-garden study had similar degrees of pollen limitation and autofertility as native species, suggesting that these characteristics might have played a role earlier on in the invasion process. The studies presented in this thesis support the idea that different factors may determine naturalization and invasion, and that it is highly relevant to choose the appropriate comparators (van Kleunen et al. 2010; Richardson & Pyšek 2012; van Kleunen, Dawson & Maurel 2015). Future studies testing the species’ characteristics associated with each stage in the invasion process should ideally compare four categories of alien species:
non-naturalized alien, non-invasive naturalized alien, invasive naturalized alien and native species.
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