Dimensions of invasiveness: Links between local abundance,geographic range size,and habitat breadth in Europe’s alien and native floras

Understanding drivers of success for alien species can inform on potential future invasions. Recent conceptual advances highlight that species may achieve invasiveness via performance along at least three distinct dimensions: 1) local abundance, 2) geographic range size, and 3) habitat breadth in naturalized distributions. Associations among these dimensions and the factors that determine success in each have yet to be assessed at large geographic scales. Here, we combine data from over one million vegetation plots covering the extent of Europe and its habitat diversity with databases on species’ distributions, traits, and historical origins to provide a comprehensive assessment of invasiveness dimensions for the European alien seed plant flora. Invasiveness dimensions are linked in alien distributions, leading to a continuum from overall poor invaders to super invaders—abundant, widespread aliens that invade diverse habitats. This pattern echoes relationships among analogous dimensions measured for native European species. Success along invasiveness dimensions was associated with details of alien species’ introduction histories: earlier introduction dates were positively associated with all three dimensions, and consistent with theory-based expectations, species originating from other continents, particularly acquisitive growth strategists, were among the most successful invaders in Europe. Despite general correlations among invasiveness dimensions, we identified habitats and traits associated with atypical patterns of success in only one or two dimensions—for example, the role of disturbed habitats in facilitating widespread specialists. We conclude that considering invasiveness within a multidimensional framework can provide insights into invasion processes while also informing general understanding of the dynamics of species distributions.

Human socioeconomic activities are altering species’ global distributions, bridging natural dispersal barriers through the accidental and intentional relocation of organisms, and opening opportunities for them to expand into new regions beyond their historic native ranges (1). The outcome of any given introduction event, however, is dependent on ecological and stochastic processes, and many introduced alien species fail to establish and persist (2, 3). Even species that do achieve persistent, self-sustaining populations (i.e., become naturalized sensu ref. 4) show varying degrees of success (i.e., invasiveness) in newly occupied regions. This has been true for natural colonization events throughout Earth’s history e.g., on islands (5, 6) and during continental biotic interchanges (7–9)] and is certainly the case for the ongoing surge of human-mediated introductions (10–12). Disentangling the factors that lead to invasion success provides an opportunity not only for anticipating and mediating future anthropogenic invasions but also for better understanding the dynamics underlying natural range expansions (13).Quantifying a species’ success in invading the alien range is complex, a fact reflected in the diverse criteria applied by different authorities when deciding whether or not to classify naturalized species as invasive (14). Recent efforts have therefore recognized that invasiveness cannot be captured by a single metric but rather encompasses multiple aspects of ecological success and impact (15, 16). Some proposed metrics, such as spread rate and socioeconomic impacts, are difficult to quantify for large numbers of species (4, 17). However, Rabinowitz’s three-dimensional scheme for characterizing the rarity or commonness of species in their native distributions (18, 19) has been successfully co-opted as a valuable perspective for better understanding the success of alien species (16, 20, 21). Applied in the context of introduced species, this framework recognizes the potential for established aliens to vary along at least three demographic dimensions of invasiveness: 1) in local abundance within the naturalized range, 2) in geographic range size or extent of the naturalized range, and 3) in habitat breadth in the naturalized range (16). We subsequently distinguish these metrics as dimensions of invasiveness when measured in the naturalized distributions of alien species and dimensions of commonness when measured in species native distributions.Considering invasiveness within a multidimensional framework is particularly important if species vary independently among different dimensions (16, 21). Such a scenario opens the possibility for aliens to achieve invasion success in many different ways (Fig. 1). In other words, there could exist different forms of invasiveness, similar to the different forms of rarity or commonness originally proposed by Rabinowitz (19). On the other hand, theoretical concepts and empirical examples suggest correlations between Rabinowitz’s dimensions of commonness among species in their native distributions (6, 22, 23). For example, a positive relationship between local abundance and extent of geographic occurrence or range size has been documented at various scales for numerous taxa (24–26), including plants (24, 27–31), with niche breadth proposed as a linking mechanism (24, 26, 32). If the processes that generate these patterns in native distributions act similarly in species alien distributions, some of the forms of invasiveness outlined in Fig. 1 should be less likely to occur than others. More specifically, if the invasiveness dimensions are correlated, species should vary from excelling (abundant, widespread, generalists; form AWG in Fig. 1) to performing poorly (scarce, restricted, specialists; form 0 in Fig. 1) in all three invasiveness dimensions (33). On the other hand, these macroecological patterns are not without exception, and a recent assessment found little support for correlations among commonness dimensions in Europe’s native flora (34). Alien distributions may further differ because aliens vary in their residence time, and particularly recently introduced species may be in disequilibrium and still increasing along one or more of the invasiveness dimensions (21, 35–37). In line with these alternatives, a continuum from overall poor invaders to species succeeding in all three dimensions has been documented for the regional alien flora of French grassland communities (20), while associations among dimensions were found to be low for the herbaceous alien flora of Southeast Australia (16). The correspondence among different invasiveness dimensions at broader geographic scales has yet to be assessed.Open in a separate windowFig. 1.Conceptual diagram outlining the eight different forms of invasiveness depending on success in zero, one, two, or three dimensions of invasiveness (based on refs. 16, 18, and 20). Forms of invasiveness within the cyan polygon are associated with high naturalized abundance, within the magenta polygon with widespread naturalized geographic extent, and within the yellow polygon with high naturalized habitat breadth. The overlap between magenta and cyan is blue, between cyan and yellow is green, between magenta and yellow is red, and between all three is black. The forms of invasiveness are comparable to analogous forms of commonness used to describe species in their native distributions, and we refer to the same abbreviations in both cases.Functional traits play a role in mediating invasion processes, but efforts to identify characteristics of successful invaders have generally resulted in few or inconsistent associations (38, 39). However, distinguishing between different components of invasiveness may provide additional clarity if each is influenced by different traits or if the same trait has contrasting effects on different dimensions (15, 16, 21, 40, 41). For example, many plant traits are associated with general trade-offs between rapid growth (i.e., acquisitive growth strategies) versus stress tolerance and survival (i.e., conservative growth strategies) (42–44), and one can hypothesize scenarios where these divergent strategies are associated with success in different dimensions of invasiveness (40, 41). Another example are specialized adaptations for long-distance dispersal that may promote rapid range expansion, both in extent and into new habitats, but likely do not provide any advantages that would influence local abundances (45, 46). For habitat specialists, their specific habitat associations may additionally be important for determining whether or not they become widespread (31).A number of hypotheses for invasion success additionally emphasizes the importance of unique ecological dynamics that emerge when species are decoupled from constraints experienced in their native environments (47). For example, because species are able to occupy unfilled niches where introduced i.e., Darwin’s naturalization hypothesis (48, 49)] or because they leave behind important herbivores, competitors, or pathogens that limit populations in the native distribution i.e., enemy release (50, 51)]. These mechanisms may be less likely when species expand into areas near the native range, for example, during natural range expansions or intracontinental introductions, as the alien individuals are more likely to encounter conditions similar to those that limited their native distribution compared to species introduced from further abroad (e.g., those with extracontinental origins) (52–54).Here, we combine vegetation plot data covering Europe (55) with databases of alien and native distributions (56, 57), plant traits (58, 59), and historical dates of introduction (60) to provide a comprehensive assessment of multidimensional invasion success for the European alien seed plant flora. First, we test for correlations among local abundance, geographic extent, and habitat breadth of alien species in their naturalized distributions and classify species into one of the eight forms of invasiveness (Fig. 1). We ask whether some forms of invasiveness rarely occur and specifically whether species tend to fit along a continuum ranging from generally poor invaders to super invaders—species excelling in all three dimensions. In addition, we compare relationships among dimensions of invasiveness to those among dimensions of commonness measured for Europe’s native flora, assessing similarities and differences in patterns of distribution between contexts. Next, we explore likely drivers of each invasiveness dimension, testing whether the year of first alien occurrence in Europe, functional traits related to ecological strategies, specialized adaptations for long-distance dispersal, habitat associations, and region of origin explain different forms of invasion success.