Reproductive characteristics as drivers of alien plant naturalization and invasion

Abstract

Due to human activity and global movements, many plant species have been introduced to non-native regions where they experience novel abiotic and biotic conditions. Some of these alien species manage to establish reproducing naturalized populations, and some naturalized alien species subsequently become invasive. Invasion by alien plant species can negatively affect native communities and ecosystems, but what gives the alien species an advantage under novel conditions is still not clear. Therefore, identifying the drivers of invasions has become a major goal in invasion ecology. Reproduction is crucial in plant invasions, because propagule supply is required for founding new populations, population maintenance and spread in non-native regions. Baker’s Law, referring to the superior advantage of species capable of uniparental reproduction in establishing after long distance dispersal, has received major interest in explaining plant invasions. However, previous findings regarding Baker’s Law are contradicting. Moreover, there has been an increasing interest in understanding the integration of alien plant species into native plant-pollinator networks but few studies have looked at the pollination ecology of successful (naturalized and invasive) and unsuccessful (non-naturalized and non-invasive) alien plant species. Previous findings are also biased towards specific taxonomic groups and geographical areas. More generalized approaches are required to advance our knowledge of the role of reproductive characteristics in alien plant naturalization and invasion. Our quantitative breeding-system database of 1752 species from 116 regions around the globe, combined with data on species’ native range size and global naturalization success, is a powerful tool for testing Baker’s Law in alien plant naturalization. Consistent with Baker’s Law, our results show that selfing ability (self-compatibility and autofertility) is positively related to naturalization success. The effects are both direct and indirect, as selfing ability has a positive effect on native range size, which in turn has a positive effect on naturalization. We demonstrate that selfing ability contributes to naturalization, which strongly suggests that a lack of mates and pollinators is an important barrier to the establishment of alien plant species. To test whether alien plant naturalization is related to the ability to attract resident pollinators in non-native regions, we did a comparative study on flower visitation of 185 native, 37 naturalized alien and 224 non-naturalized alien plant species in the Botanical Garden of Bern, Switzerland. Botanical gardens offer unique opportunities for hosting comparative studies because species from a broad taxonomic range and from a wide geographic area are growing under comparable conditions. Our phylogenetically-informed analysis showed that non-naturalized alien species received fewer flower visits than both naturalized alien and native species. Native, naturalized alien and non-naturalized alien species were visited by similar flower visitor communities. Furthermore, among the naturalized alien species, those with a broader distribution in Switzerland received a more diverse set of flower visitors. We provide the first evidence that the capacity to attract flower visitors in non-native regions is different for naturalized and non-naturalized alien plants, which strongly suggests that naturalization is related to flower visitation. To test whether pollen limitation and low autofertility are important constraints to invasion, we performed a common garden breeding-system experiment. Using pollination treatments (pollen supplementation, open pollination, and pollinator exclusion), we assessed the degrees of pollen limitation and autofertility of 24 native and alien (both invasive and non-invasive, but naturalized) plant species (eight confamilial or congeneric triplets). The three plant groups had low degrees of pollen limitation and were almost all autofertile to some degree. The groups did not differ in their degrees of pollen limitation or autofertility. Because invasive alien species did not suffer lower pollen limitation and did not have higher autofertility than non-invasive aliens, our results suggest that pollen limitation and low autofertility may not play a major role in the spread of alien plants, once they have become naturalized. Taken together, our findings strongly suggest that reproductive characteristics contribute to alien plant naturalization. Thus, a lack of mates and pollinators may be an important barrier to establishment in new non-native regions. A breeding system that favors uniparental reproduction and the ability to attract suitable pollinators may help alien plants successfully found and maintain reproducing populations in non-native ranges. However, once the alien plant species becomes naturalized, reproductive characteristics may no longer play an important role. Other factors may be more important during invasion, when the alien plant species spread in the non-native ranges.