Many invasive plants are threatening the already highly vulnerable habitats of coastal dunes in Europe. Setting priority target species to control is mandatory for an effective planning of invasion management strategies at European level. This can be possible after identifying the species that currently have greater invasion success, in consideration of their ecological traits and origin. We quantified the three main components of invasion success for the extra-European alien plants found on European coastal dunes: local abundance, regional distribution and niche breadth, and related them to their life forms and origins. We found that life form was a better predictor of invasion success. In particular, geophytes and therophytes were the species with the greatest invasion success. Quite surprisingly, alien plants from Africa appeared as the group with slightly higher mean invasion success although this result was no statistically significant. We also highlighted the species deserving special attention. Among these, Xanthium orientale, Erigeron canadensis and Oenothera gr. biennis showed the widest levels of niche breadth and regional distribution, and had overall the greatest invasion success, but other species also had high levels in one of the three components of invasion success.

alien plants, coastal vegetation, ecological success, generalist species, local abundance, niche breadth, regional distribution, sand dunes

The repeated introduction of alien species is a major component of ongoing global changes and a major threat to global biodiversity (Walther et al. 2009). After their direct or indirect introduction by humans (Rodríguez-Labajos et al. 2009; Pyšek et al. 2010; Tordoni et al. 2020), many plant species become naturalised, overcoming local abiotic and reproductive barriers to establish self-sustained populations. A subset of these spread across considerable distances and become invasive (Richardson et al. 2000), with impacts on wildlife, plant biodiversity, and ecosystem functioning (Vilà et al. 2011; Del Vecchio et al. 2015; Blackburn et al. 2019). Coastal dunes are among the most affected habitats (Heywood 1995; Chytrý et al. 2009), especially in Europe, due to the rapid increase in human settlements and activities (Campos et al. 2004; Carboni et al. 2010; Viciani et al. 2020; Lazzaro et al. 2020). As a consequence, their highly specialised flora is currently under serious threat (Prisco et al. 2020).

As effective invasion management strategies cannot possibly consider the large number of invasive plants currently present on European coastal dunes, a more realistic approach would be to focus management efforts on those aliens which have greater invasion success. The ecological success of introduced species depends on their biological traits, on the pressure of introduced propagules and on local ecosystem invasibility (Lonsdale 1999; Lloret et al. 2005; Catford et al. 2009). It can be quantified with different approaches. For example, Cadotte et al. (2006) used a general value of plant abundance, Selosse et al. (2004) used the measure of biomass, while Dyderski and Jagodziński (2018) considered also plant density. Rabinowitz (1981) introduced a framework (not specific for alien plants) which separates three components of success: local abundance, regional distribution and niche breadth (narrow niche breadth is proper of a specialist species, wide niche breadth of generalists). However, these components are not always correlated and could be highly variable, making it sometimes difficult to unequivocally identify the most successful aliens. In this sense, other authors proposed to consider these three components together in order to quantify the invasion success (Carboni et al. 2016; Cao Pinna et al. 2020).

Different studies have highlighted the importance of life forms and geographical species origin as factors related to invasion success (van Kleunen et al. 2015; Giulio et al. 2020; Cao Pinna et al. 2020). Life forms (Raunkiaer 1934) are among the most simple but informative ecological traits (Acosta et al. 2006), defining species ecological strategies in an extremely synthetic way. Some plant ecological strategies, associated with specific life forms, can convey an advantage for the ability of introduced species to establish in a coastal ecosystem. If invasion success is related to particular adaptations to the host habitats, we could expect that the most successful alien species would share the life forms that are most common among the native species of European coastal dunes, which tend to be annual species and biennial or perennial herbs (Acosta et al. 2006, Kuiters et al. 2009). However, other authors hypothesized that forms not widely represented among native species, such as woody plants in dune grasslands (Torca et al. 2019), could have the advantage to occupy empty niches (Elton 1958; MacDougall et al. 2009). Indeed, for plant invaders, being different is often equated with being successful (MacArthur and Wilson 1967; Daehler 2001; D’Antonio and Hobbie 2005).

Similarly, considering the geographic origin of successful invasive plants may allow to tune prevention strategies to avoid further introductions. Geographic origin of invasive species depends on different factors (Hayes and Barry 2008). According to the intermediate distance hypothesis (Seebens et al. 2017), we could expect higher invasion success by plant species from regions that are at intermediate distances from the invaded region. Indeed, over short distances, the proportion of potential alien species is low, because the native ranges of many species extend into the target region, where they are thus native. At large distances, the proportion of potential alien species increases, but the probability to be transported by humans and survive transportation decreases. Based on the climatic similarity hypothesis instead, the species coming from regions with similar climatic conditions are preadapted to successful invasions, for example those exchanged between North America and Europe, both located in temperate climates. At the same time, climatic similarity between regions favours the exchange of people and goods (Tatem and Hay 2007), which also favours biological introductions (Wilson et al. 2009; Seebens et al. 2015). An alternative hypothesis is that the regions richer in biodiversity, such as those at the tropics and in the southern hemisphere, have more chance to donate more species (van Kleunen et al. 2015), and hence more probability that a higher number of species have greater invasion success.

In a previous study, Giulio et al. (2020) provided a comprehensive assessment of alien plant invasions in the coastal dunes across Europe, highlighting that coastal dunes should be in the focus of European invasion management strategies. However, we still need to understand which factors are more important in the shaping of invasion pathways. On these bases, in this study we analysed the invasion success of alien species on the coastal dune habitats of Europe. To this aim we used data from the European Vegetation Archive (EVA) to quantify the invasion success based on Rabwinowits’ approach which is based on three components of alien success: local abundance, regional distribution and niche breadth. Moreover, we were interested in investigating the invasion success in relation to life forms and geographical origins.

The Kruskal-Wallis test highlighted that life forms had a statistically significant effect on local abundance, on regional distribution, and on the general invasion success, but not on niche breadth (Table 1). Geophytes had higher local abundance compared to phanerophytes (Fig. 3A) and therophytes, and also higher regional distribution with respect to phanerophytes. According to the synthetic index of ecological success, geophytes and therophytes showed the highest mean invasion success, but comparisons with the other groups were not statistically significant (Fig. 4A). Species from Africa showed the highest mean invasion success, although species origins did not have any statistically significant effects (Fig. 4B).

The species which showed the greatest invasion success was Xanthium orientale, followed by Erigeron canadensis and Oenothera gr. biennis (Appendix II). All these three species had very wide niche breadth and regional distribution, but low local abundance. The species with the widest niche breadth was Gomphocarpus fruticosus. Other species with wide niche breath were Amorpha fruticosa, Ambrosia artemisiifolia and Helianthus annuus, while other species with wide regional distribution were Carpobrotus spp. and Xanthium strumarium. Carpobrotus also had intermediate levels of local abundance and niche breadth, and Xanthium strumarium wide niche breadth. The other species with high invasion success had wide niche breadth, intermediate levels of regional distribution, and in some cases also intermediate levels of local abundance, such as Senecio inaequidens, Oenothera drummondii and Oenothera glazioviana. The species with greatest local abundance were Lepidium densiflorum, Amsinckia menziesii, Populus trichocarpa, Pseudognaphalium undulatum and Solanum tuberosum, but these occurred in no more than one plot across the study area. Arctotheca calendula had both very high local abundance and wide niche breadth, while Paspalum vaginatum high local abundance and an intermediate level of regional distribution. Also Lupinus arboreus and Epilobium brunnescens had high local abundance, but low levels of the other components. Ambrosia psilostachya had instead intermediate levels in all the three components.

Figure 3. 

Violin plots of the three components of ecological success related to (a) life forms and (b) species’ origins. Values were rescaled between 0 and 1 (by subtracting the minimum and dividing by the range) for comparability. Bold segment shows the mean and fine segments the quantiles. Asterisks highlight the groups with significantly higher values than other groups according to pairwise Wilcoxon test with Bonferroni correction (Local abundance of G > P, p-value = 0.026; G > T, p-value = 0.041; Regional distribution of G > P, p-value = 0.024). Oceanian origin and chamaephyte group were not represented in these graphs because they included a small number of species (respectively only one and three species). G = geophytes, H = hemicryptophytes, P = phanerophytes, T = therophytes.

Figure 4. 

Synthetic index of invasion success, related to (a) life forms and (b) species’ origins. Values are the normalized first component's scores. Bold segment shows the mean and the other segments the quantiles. Oceanian origin and Chamaephyte group were not represented in these graphs because they included a small number of species (respectively only one and three species). G = geophytes, H = hemicryptophytes, P = phanerophytes, T = therophytes.

In this study we quantified for the first time the main components of invasion success for alien plants from outside of Europe found on European coastal dunes. We observed that geophytes and therophytes were the species with the greatest invasion success, and African alien species were the group with slightly higher mean success. However, many of the alien plants with the highest invasion success were also of North American origin.

Life form confirmed to be a highly informative ecological trait in the coastal environment (Acosta et al. 2006), predicting two components of invasion success, local abundance and regional distribution, and the general index of invasion success. Annual therophytes confirmed to be among the species with most invasion success, reflecting a global invasion pattern (RBG Kew 2016). Their short life cycles and large amount of propagules give annual species more chance to adapt to the highly dynamic and disturbed coastal dune environment, compared to other life forms (Del Vecchio et al. 2015). Geophytes, although less represented among native coastal dune species than hemicryptophytes and therophytes (Acosta et al. 2006; Torca et al. 2019), also showed high values of invasion success, especially due to high local abundance levels. In fact, geophytes are already known as important weeds worldwide (Sala et al. 2007), first of all because widely introduced as garden ornamentals (Raymond 1996), and also because they are able to accumulate extensive underground reserves which enable them to crowd out native species.

Alien plants from Africa did include more species with high local abundance and consequently this was the group with slightly higher mean invasion success. However, we should note that the relationship between geographic origins and the invasion success of alien plants was not statistically significant. This result confirmed those of Cao Pinna et al. (2020), focused on the Mediterranean part of Europe and remarks that invasion success is not predictable by the species origin at continental scale. A possible explanation could be that species origin is more related to propagule pressure, depending especially on distance and human trade (van Kleunen et al. 2015; Seebens et al. 2015, 2017; Moser et al. 2018), than our three components of invasion success.

The plants with the highest invasion success level (Xanthium orientale, Erigeron canadensis and Oenothera gr. biennis) are all ruderal therophytes or hemicryptophytes from North America. Their invasion has been related to human disturbance (Stanisci et al. 2014). Among the species with wide niche breadth, Amorpha fruticosa can be considered as a major threat for the local native coastal biodiversity, altering the soil nitrogen cycle and microbial composition, and consequently related to plant species loss and to shifts in the local species composition (Boscutti et al. 2020). We also found dangerous alien invaders among species with wide regional distributions, such as Carpobrotus spp., another “transformer” (Richardson et al. 2000), which specifically alter the levels of pH in the soil and suffocates the local plants of lower cover (Campoy et al. 2018). Senecio inaequidens and Ambrosia artemisifolia, showing wide niche breadth and intermediate regional distribution, are instead characterized by high genetic diversity in the invaded ranges (Genton et al. 2005; Monty and Mahy 2009, 2010; Lachmuth et al. 2010). Among them, Senecio inaequidens is known to induce changes in the floristic composition of dune vegetation (Heger and Böhmer 2006). Among the species with high local abundance, we mentioned Arctotheca calendula (therophyte from Africa), and Paspalum vaginatum (geophyte probably originating from Africa; Chen et al. 2005). A. calendula is exclusive to dunes, has a successful dispersal mechanism, and is able to rapidly invade on anthropogenically disturbed coasts, especially in the Iberian Peninsula (Campos et al. 2004). Paspalum vaginatum is also already known as one of the most dangerous alien species on European coasts, associated to more brackish environments (Filigheddu et al. 2001), often forming dense and tall grasslands, sometimes monospecific or associated with other alien plants (Campos et al. 2004; CABI 2005–2020). Ambrosia psilostachya, geophyte from North America, showing intermediate levels of all the three components, colonizes habitats with high levels of human impact (Montagnani et al. 2017), including degraded dunes. Its clonal populations can cover large areas rapidly in France, where it seems to be increasing (Fried et al. 2015).

Overall, the present work provides useful information for keeping track of the alien species which have most invasion success on coastal dunes which is a key issue in European invasion management strategies. Our list of successful alien species could be particularly valuable to plan prioritising management targets, from regional to local scales. Management planning should target first the most successful invaders and monitor emerging invasions (Nel et al. 2004). Furthermore, reported differences in local abundance, regional distribution and niche breadth should also be taken into account as they could imply different types of management strategies depending on the target aliens.

Acosta ATR was supported by the Grant of Excellence Departments, MIUR Italy (article 1, subsection 314–337, law 232/2016), Carboni M by a Rita Levi Montalcini Grant, MIUR Italy, Giulio S and Cao Pinna L by PhD fellowship of Roma Tre University, and Marzialetti F by PhD fellowship of University of Molise.

We acknowledge the custodians and deputy custodians of the EVA project, who provided data to make this work possible (Corrado Marcenò, Maike Isermann, John Rodwell, Jan Pergl, Petr Pyšek, Juan Antonio Campos, Javier Loidi, Mercedes Herreira, John A. M. Janssen, Joop H. J. Schaminée, Zygmunt Kącki). We also acknowledge the Grant of Excellence Departments, MIUR-Italy (ARTICOLO 1, COMMI 314 – 337 LEGGE 232/2016).