Contrasting patterns from two invasion fronts suggest a niche shift of an invasive predator of native bees

Introduction

The niche concept is broadly used to characterize requirements and impacts of species (Chase & Leibold, 2003), and to predict ecological and evolutionary responses to environmental change (Lavergne et al., 2010). If the niche characteristics of a species in its native range are known to a large extent (they can never be completely inferred from occurrence data studies), it is possible to anticipate with greater precision the potential geographic course of its spread, should the species be introduced in a new area and become an invader (Peterson, 2003). Niches are defined by the species’ physiological tolerances (the fundamental niche which represents the conditions under which a species can live indefinitely), as well as by biotic interactions and dispersal barriers, which constrain the fundamental niche to the realized niche, i.e., the conditions under which a species actually lives (Tingley et al., 2014).

Non-native species, when introduced to new geographic areas, may establish in environmental conditions different from their native range because of the lack of natural enemies (i.e., occupying a larger realized niche) or local adaptation (i.e., changing their fundamental niche), or both. Therefore, the analysis of the changes in the niche depicted by an invasive species between its native and introduced ranges may be useful in understanding range expansion and invasion potential (González-Moreno et al., 2014; Kumar et al., 2015). Non-analogue climates represent a severe problem when calculating these niche change metrics, because no insight on the biology of the species in these non-analogue climates can be inferred from a comparison between ranges (Guisan et al., 2014). The colonization of parts of environmental space not present in the native range cannot be unambiguously considered as resulting from evolution (i.e., changes in fundamental niche) in the non-native range. To address this issue, Guisan et al. (2014) proposed a framework for niche comparison between native and invasive ranges with three basic components (Fig. 1): (i) niche unfilling, representing environmental conditions similar to the niche of the native population not (yet) occupied in the invasive range (quantifying niche unfilling areas in the invaded range is critically important because it suggests the likelihood of further spread: González-Moreno et al., 2014); (ii) niche stability, representing overlapping environmental conditions used by the species in both the native and invasive ranges; (iii) niche expansion, representing environmental conditions used by the species in the invasive range that although available in the native range are not exploited by the native population, due to physical barriers or biotic interactions, like competition, predators.

Inspecting marginality is also important to draw inferences about a species invasion ability. Marginality can be defined as the distance between the mean habitat conditions used by the species and the mean environmental conditions over the entire area (Hernández Fariñas et al., 2015). Populations with marginal niches occur in less common environmental conditions in a given area, contrasting with those with non-marginal niches (Hernández Fariñas et al., 2015), which are closer to the centre of the niche hyperspace; see Fig. S1). This means that species with a marginal niche in a given region usually have low tolerance to one or more of the commonest local features, and this can reduce their invasion ability. Hence, by inspecting the marginality of an invasive population we are also adding new information about its potential ability to continue the invasion process.

Ecological niche modelling is often used to anticipate the potential geographic extent of an invasive process. In particular, ensemble forecast predictions (Araújo & New, 2007) have been frequently used in invasive ecology, as they represent a consensus approach that offers more robust predictions for the potential and realized distribution of species than techniques that rely on a single algorithm. Reciprocal distribution modelling (RDM) emerged as a powerful tool by considering both the invasive and native ranges in distribution models (Medley, 2010); otherwise, the potential range of a species may be seriously underestimated (Václavík & Meentemeyer, 2012). Niche conservation is indicated if both the native model accurately predicts non-native distributions, and non-native models accurately predict the native distribution (Medley, 2010). Alternatively, a niche shift is suspected whenever reciprocal models poorly predict one another, although that situation can also be caused by a narrower niche in the invasive range. Indeed, this RDM approach has previously revealed niche shifts for the spotted knapweed and fire ant invasions in the United States (Broennimann et al., 2007; Fitzpatrick et al., 2007). In a recent work by Hill, Gallardo & Terblanche (2017), the authors suggest that distribution models should not be used in isolation to predict insect invasions or invaded range extents, but instead need to be coupled at least with some analysis of changes in environmental/climatic space.

Many invasive insects are not in equilibrium in their invasive ranges, and have the potential to further expansion (Hill, Gallardo & Terblanche, 2017). As invasive insects can respond quickly to novel environments (including biotic interactions) through either phenotypic plasticity, changes in adaptive traits or some combination of both (Urbanski et al., 2012; Gibert et al., 2016), niche shifts may be relatively common within this group. Frequently a single species invades several regions, and this provides an opportunity to study and model its invasion ability, particularly to assess potential niche shifts. One of the most recent examples of a successful invasion in Europe is the yellow-legged hornet, Vespa velutina Lepeletier, 1836. Native to south-east Asia, V. velutina is a predator of honeybees and other beneficial insects (Monceau, Bonnard & Thiéry, 2014; Rome et al., 2021; Verdasca et al., 2021a), being considered a serious threat to honey production, pollination services and consequently food security (Monceau, Bonnard & Thiéry, 2014; Requier et al., 2019; Verdasca et al., 2021b). The mere presence of V. velutina near beehives induces stress to honeybees (Leza et al., 2019) and decreases their foraging activity, thus reducing pollen and nectar collection, with impacts on winter survival of the colony (Requier et al., 2019). Further, as V. velutina can attack a broad variety of wild pollinators, it could also pose additional negative effects on crop production as well as on biodiversity (Monceau, Bonnard & Thiéry, 2014). Since the accidental introduction in France, in 2004 (in a temperate bioclimatic region: Sayre et al., 2020) of a single female fertilized by several males (Arca et al., 2015), V. velutina has spread to other European countries, being considered an invasive alien species of concern in the European Union (European Commission, 2016). In 2011, a new invasion by V. velutina was found in the North of Portugal (Fig. 2–P2) in the region of Viana do Castelo (Grosso-Silva & Maia, 2012), near a paper mill, where the species probably arrived in a load of timber from France (Marco Portocarrero, pers. comm., 2018), in a transitional region between a temperate hyper oceanic climate to the north and a Mediterranean climate to the south; the latter conditions with no apparent parallel with any bioclimatic region of the native range (Sayre et al., 2020). The new invasive population has been expanding south into central Portugal (Verdasca et al., 2021c), and to the north and east into Galicia (Spain), where it arrived at the end of 2012 (Rodríguez-Flores et al., 2019).

Genetic analyses of individuals from different countries of the invaded area (France, Spain, Portugal, Italy, and UK) confirm a low genetic variability of V. velutina in Europe and that they all derived from the spreading (natural or human mediated) of the invasive population initially established in France (Fig. 2–P1) (Budge et al., 2017; Granato et al., 2019; Quaresma et al., 2022). Founding of P2 from P1 was accompanied by a reduction in the species genetic diversity (Quaresma et al., 2022), but this did not hamper the successful spread of V. velutina in Portugal (Carvalho et al., 2020; Verdasca et al., 2021c).

Recently, Barbet-Massin et al. (2018) suggested that the climatic niche of V. velutina in France expanded during the past few years, raising the hypothesis of a change in the niche dynamics during the invasion process. However, their model was not able to predict some of the already invaded areas in Portugal and Germany. Here, we expand on this previous work to assess niche shifts in a newly invaded region, the NW of Iberian Peninsula, and compare them to the realized niche seen in the older invasive population in France, incorporating the impacts of time since invasion on niche metrics. Specifically, we compared the realized niche of these two genetically related populations of V. velutina in Europe and coupled niche dynamic analysis and RDM with an ensemble forecast to address three main questions: (i) Has V. velutina shifted its niche during the invasion process? (ii) Is V. velutina occupying the most common environmental conditions of the invasive range? (iii) Is there potential for further expansion? Answering these questions is crucial to understand niche flexibility and its potential for evolution in different regions of the invaded range, to identify areas at risk, and to inform management plans.

Material and Methods

Environmental data

We considered an initial dataset of 22 environmental variables (climatic, topographic and land use: ‘see Table S1 for details’) which potentially affect the ecophysiology of Vespa velutina (Villemant et al., 2011; Bessa et al., 2016). We calculated the distance to each land cover type since distance variables are acknowledged to achieve a better performance for species associations to landscape features (Rainho & Palmeirim, 2011). As nests are made in trees, but also in the ground, on walls, on slopes with vegetation, we decided to test for a number of topographic components (slope included). All the layers were clipped to the same extent and upscaled to a 5 km pixel resolution, to match known V. velutina homing ability (Poidatz et al., 2018). Climatic data of the available environmental space and of the occupied niche in both native and invasive ranges were compiled to compare its range of variation (’see S4’). All calculations regarding the preparation of variables for analysis were carried out in ArcGIS 10.4.1 software (ESRI 2016). To avoid high collinearity, variables that were highly correlated (r ≥ 0.70: Dormann et al., 2013), examined on both ranges, see Tables S2 and S3) were excluded from subsequent analysis, keeping the ones with higher acknowledged biological importance. With the remaining twelve variables (Table 1), a multivariate environmental similarity surface (MESS) calculated in MaxEnt, spatially identified which areas in the invasive range possess similar environmental characteristics to the native range (see Fig. S2). The native range was delimited to contain only the regions where the species is acknowledged to live (we took care to not include areas with extreme climates that have no parallel in Europe, like the cold regions of Himalayas or the tropical regions of Malaysia). V. velutina is still expanding in the invasive range, thus to estimate its potential distribution we used three different non-parametric presence-only algorithms (please see below) using the ‘biomod2’ package (Thuiller, Georges & Engler, 2014) in R (R Core Team, 2019).

Table 1:

Variables used in the modelling of the realized niche of Vespa velutina (for details of resolution and source of each variable, see Table S1).

Type	Variables
Climatic	BIO1 = Annual Mean Temperature
	BIO7 = Temperature Annual Range (BIO5-BIO6)
	BIO10 = Mean Temperature of Warmest Quarter
	BIO11 = Mean Temperature of Coldest Quarter
	BIO17 = Precipitation of Driest Quarter
	BIO19 = Precipitation of Coldest Quarter
Topography	slp = Slope
	northn = Northeness
	eastn = Eastness
Land cover	durb = Distance to urban areas
	dfor = Distance to forest
	dwat = Distance to water

DOI: 10.7717/peerj.13269/table-1

Results

Is there potential for further expansion?

Before modelling procedures, we checked for the existence of analogous conditions between native and invasive ranges. The MESS analysis showed that almost 100% (>99.99%) of the invasive range did not have one or more environmental variables outside the range present in the training data (Fig. S2), enabling the predictions for these areas. Regarding the predictive models for the invasive range, AUC values were high (all over 0.93) for the different algorithms, although for the native model the AUC values ranged between 0.73 and 0.91 (Fig. S5). The model with highest fit was obtained using RF (higher AUC values than GBM and Maxent). Comparing model sensitivity to small changes in occurrence points and using the model developed for the invasive range, the predicted area for the species in Europe was relatively similar for the different algorithms but with larger within-model variance for Maxent and RF (see Fig. S6A). For the projection of native occurrences into Europe, the sensitivity to small changes in the presence data varied more between algorithms, being Maxent the more susceptible regarding model variance (see Fig. S6B).

When only the P1 or P2 invasive ranges were considered for the modelling procedure, the full extent of areas already invaded were not detected (Figs. 4B, 4C). However, the native range model overlapped and covered most occurrences in the invasive range (Figs. 4A and 4D). As the native model identified 99% of the high-risk areas, we considered these as the regions that are not (yet) occupied despite having similar environmental conditions to those used by the species in the native range. In contrast, the predicted presence of the species in Asia using the model developed for Europe did not accurately predict its native distribution.

An agreement between native and invasive models occurred for only 15% of the potential distribution in the invaded range. The remaining areas of concordance between both models that are still unoccupied by the hornet are in the south of Italy, Corsica, Croatia and Montenegro. About 65% of the area where the species is predicted to occur in Europe was considered at high-risk of being invaded, as it represents similar environmental conditions to those found on V. velutina’s native range, though this area remains uninvaded (Fig. 4D). Concerning the presence records, all were located on high-risk areas. At this continental scale, the climatic variables related with precipitation and temperature contributed the most to explain the distribution of V. velutina (Fig. S7). More specifically, the species is thriving in Europe in regions where the winters are mild and rainy, and the summers are neither too hot nor too dry.

Discussion

Our results suggest that a shift in the niche of V. velutina occurred in Europe, probably in the NW of Iberian Peninsula, and that it is essential to consider both native and invasive records in modelling procedures to accurately predict the species invasive potential. Our study also revealed that the colonization process by V. velutina is still ongoing with a high potential for geographical expansion, as a large extent of Europe with analogue environmental conditions to those of the native niche is still unoccupied. The fact that the area we predicted to be suitable for V. velutina is larger than in previous studies, makes this the first study to accurately predict all the currently invaded area in Europe (even the very recent records in Hamburg, Germany, and the southwestern occurrences in the Iberian Peninsula): this was due to the innovative approach here conducted - coupling reciprocal distribution models with niche analysis; and using of all V. velutina occurrences in the native range, irrespective of the different colormorphs (except for the clear divergent forms of Indonesia and Malaysia), allied with the use of the largest dataset so far to model this invasive. Further, we also evidenced that this species is using the most frequently available conditions in Europe, hence is less prone to possible stochastic events that could hamper its progress.

Describing species’ niches and understand whether these can change rapidly (niche shifts) or not (niche conservatism) between different geographic areas or time periods is important to anticipate invasions in the context of ongoing global change (Guisan et al., 2014). A genuine shift in the fundamental niche would reflect evolutionary adaptation of a species to novel environmental conditions, whereas occupying new portions of the same fundamental niche does not change the environmental potential of the species (Qiao, Escobar & Peterson, 2017). Regardless of the clearly different environmental conditions occupied by the two European invasive populations chosen for this work, V. velutina is well established in both regions.

Despite some variability across taxa, a recent review with over 400 species showed limited niche expansion between native and introduced ranges, supporting the niche conservatism hypothesis (Liu et al., 2020). However, in our study, niche expansion contributes respectively to 34% (P1) and 92% (P2) of the global population niche, meaning that this species can successfully occupy different environmental conditions from those occupied in the native range. Differences between environmental conditions in the native range and the P2 invaded range (suggesting niche shift) were particularly clear (only 3% of niche overlap). However, as the analyses of niche dynamics are necessarily restricted to the environmental space with analogue conditions between native and invaded ranges (region Fig. 1H), we cannot fully assess the use of novel conditions (i.e., that are not available in the native range) in the invaded range. Still, we can state that, within the same available conditions, our estimate of the realized niche of the species in the Iberian Peninsula is different from its equivalent realized niche in its native range, and that the ability to occupy obviously different realized niches may help explain the species invasiveness.

As recently introduced species do not have enough time to spread to regions far from the introduction site, their occupied climatic space in the introduced range would always be expected to be much smaller than older introductions, and the unoccupied climatic space would gradually decrease in the process of colonization (Petitpierre et al., 2012; Strubbe et al., 2013). Indeed, in France, the invasion began under environmental conditions of expansion and stability, and then the species has been progressively colonizing the unfilled environmental space. Interestingly, in a very short time (less than ten years) it is possible to measure significant changes in niche unfilling metric of this P1 population. However, it is also possible that other invasive populations (like P2) use totally different environmental conditions from those of the native niche right from the very beginning of the expansion process. This supports the high invasive potential of the species. For both populations, V. velutina experienced measurable changes in environmental niche occupancy but as would be expected, both invasive niches tend to be more similar to the native niche than would be expected by chance, and niche similarity could not be rejected.

Similar to previous studies (Villemant et al., 2011; Bessa et al., 2016; Fournier et al., 2017; Barbet-Massin et al., 2018), we identified climatic variables as the ones that most contributed to the current distribution of V. velutina. Regardless of the adequacy of particular environmental conditions for a species, if they are uncommon on a given area the species can still be limited in its potential to further expand. In our case, by addressing species marginality, we showed that V. velutina is using the most common environmental conditions available in Europe. This suggests that the species has all the necessary conditions to continue its expansion process. The increasing high values of the metric Maximum Niche Stability for P1, even when marginal conditions were removed from the analyses, means that the occupied conditions of this population overlap with the core of the species’ realized niche in its native range. In contrast, from the very beginning, the population of the Iberian Peninsula thrives on conditions that are not exploited in the native range.

Niche theory tackles a variety of issues, including evolutionary processes, competition and predation dynamics (Hirzel & Lay, 2008). Hence, the apparent niche shift of the P2 population must be interpreted with caution. Although the European environmental envelope of the species greatly overlaps with the native one, there are some conditions of the realized niche in the invasive range that are not explored in the native. Therefore, the shift may have resulted from several factors: alleviation of biotic constraints and geographic barriers, adaptation to novel conditions, or under sampling of the species in its native range. Invasive species frequently experience release from biotic interactions and dispersal barriers in their invasion process (Colautti et al., 2004). Biotic constraints in the native range that are not present in the invasive one (e.g., presence of efficient predators, parasitoids and pathogens, or competition with other hornets for food resources or nesting sites) will contribute to the expansion of V. velutina to conditions not explored in the native range. Indeed, while the invasive V. velutina might compete with Vespa crabro, for food resources (Cini et al., 2018), reproductive females of V. velutina, have a higher pathogen resistance than their native counterpart, which might represent a key factor for the ecological success and spread of this invader (Cappa et al., 2021). Further, if the native dataset is not representative of the full Asian distribution, the entire native environmental envelope might not have been fully captured. This indication of a niche shift may also be simply stochastic (once it depends on the available environmental conditions of the invaded range), or due to a partial filling of the potential native niche in the invaded range, not representing a “true” niche change (Strubbe et al., 2013). The most likely scenario is a realized niche shift in P2 population; however, without experimental evidence it is impossible to elucidate the mechanisms driving the observed shift. It is also possible that the species is rapidly evolving and adapting to the novel conditions in the Iberian Peninsula. Indeed, a recent review by Sherpa & Després (2021) of insect invasion studies showed several examples of post-introduction adaptation and niche shift in invasive insect populations, despite their recent single-source introduction events (see also the work by Sherpa and collaborators (2019) focused on the Asian tiger mosquito Aedes albopictus). Although a low level of genetic diversity was detected in the European populations of V. velutina (Arca et al., 2015; Granato et al., 2019; Quaresma et al., 2022), this is not necessarily related with inbreeding depression and, in some cases, may lead to local adaptations (Valladares et al., 2014). Further studies on the morphology, ecophysiology, genetic variability, admixture, adaptation, and plasticity of the European populations will elucidate on their degree of local differentiation.

We detected suitable conditions for V. velutina in Europe in areas much larger than those estimated by prior prediction exercises (Ibáñez Justicia & Loomans, 2011; Villemant et al., 2011; Fournier et al., 2017; Barbet-Massin et al., 2018; Barbet-Massin, Salles & Courchamp, 2020; Kim et al., 2021). This is particularly relevant for central and eastern Europe where our models have identified, for the first time, suitable conditions for V. velutina. This was expected, as this species is still expanding. As we used a higher amount of available environmental information compared to previous studies, our predictions of expansion potential of V. velutina are expected to better reflect the environmental space used by the species (Raes, 2012; Carretero & Sillero, 2016). We are aware that the fact we have used the realized native niche (we do not have information on the full fundamental native niche) does not guarantee that all the suitable areas for the species were identified. In fact, most of the already invaded area in Portugal and the new record of V. velutina in Hamburg (Husemann et al., 2020) occurred in regions that recent studies identified as unsuitable for the hornet (Fournier et al., 2017; Barbet-Massin et al., 2018; Barbet-Massin, Salles & Courchamp, 2020). The fact that our model has predicted for the first time all the current invaded area in Europe, supports the validity of the risk map provided in this work. Barbet-Massin and collaborators (2018) argue that, to predict the hornet short-term potential of expansion, it is better to run species distribution models without accounting for native data. However, such an approach may not capture the entire environmental envelope where the species is able to thrive. In fact, by using only native occurrences, we predicted a large unoccupied extent with suitable conditions for the species in Europe. Another explanation for the narrower expansion area predicted by Barbet-Massin et al. (2018) is that their study is mostly based on the data from France (corresponding to P1) which used environmental conditions that are relatively similar to those found on the core of the species’ native niche. Our study clearly demonstrates that using only part of invasive records has limited predictive power. On the other hand, as the hornet is still expanding and the realized niche is not stable, the invasive model failed to predict most of native occurrences. This may also be an indication that the niche in Europe is currently changing.

The genetic paradox of invasions suggests that the success of invasive species may result from rapid neutral and even adaptative evolutionary changes that do not require high genetic variability (reviewed by Schrieber & Lachmuth, 2016. During an invasion the gene pool of the new population is likely much smaller than in the source population (Arca et al., 2015). However, Garnas et al. (2016) showed that founder effects rarely limit fitness in invasive insects and may in fact be beneficial by purging harmful alleles or increasing additive genetic variance. Indeed, the European invasive process originated from a single founder female in France, and was followed by a second colonization process in the north-western Iberian Peninsula, where a second founder effect occurred (Quaresma et al., 2022). The establishment of P1 and P2 populations and their ongoing expansion, evidence that a related genetic constitution enables the successful invasion of two climatically distinct regions. The different environmental conditions in the Atlantic coastal zone of Iberian Peninsula did not seem to have hampered the invasion process (Verdasca et al., 2021c). Given that suitable climatic conditions exist and due to the high dispersal ability of this species, the primary front has being expanding throughout the north Atlantic coast in Spain all the way to Galicia, where it recently met the secondary front from Portugal (Quaresma et al., 2022). A substantial gain in the genetic diversity of the Iberian populations ensued, most probably through the incorporation of first-generation migrants both from P1 and P2 populations (Quaresma et al., 2022). This gene-flow can alleviate the negative effects of bottlenecks and bring new allelic combinations and may be contributing to increase population fitness and boost the invasion ability of the species. Therefore, potential genetic adaptation underlying niche shift cannot be completely excluded in the Iberian populations of V. velutina.

Apparently, V. velutina has a high ability to cope with the challenges presented by the novel European abiotic and biotic features, but the lack of competitors or the enemy release hypothesis (Keane & Crawley, 2002) can also justify its success. Little is known about the composition of natural enemies’ communities (e.g., predators, parasites) and their potential importance on the regulation of V. velutina populations. However, in the Asian tropics and subtropics this hornet faces competition with six other hornet species while in Europe it only competes with Vespa crabro (Choi, Martin & Lee, 2012). Despite the great overlap in trophic preferences between V. velutina and V. crabro (Cini et al., 2018), a recent study in a mountainous region in Italy showed that native Vespidae are probably avoiding or minimizing the competition pressure due to their ability to take refuge at high altitudes (>600 m) or to their later life cycle when compared to V. velutina (Carisio et al., 2020). Identifying such biotic constrains in the native region could be important to predict (and potentially avoid) new invasions, providing essential information for the development of control strategies.

To develop cost-effective strategies on managing invasions, more attention should be paid to surveying and controlling the spread of invasive species into climatic conditions that are occupied in their native range but (not yet) colonized in their introduced ranges (Guisan et al., 2014). Our results suggest that the invasion process of both invasive populations is likely to continue towards other European countries and that the centre, east and centre-north of Europe are at a high risk of invasion. Otherwise, our models jointly with the expansion sequence so far, and with the temperature and precipitation characteristics of the current colonized areas seem to confirm that V. velutina distribution is constrained by climatic factors, namely a need for high precipitation and a relatively narrow range of annual temperatures (Balmori, 2015; Verdasca et al., 2021c). Hence, the expansion of this invasive may be hampered in areas of the Iberian Peninsula subject to a marked thermo-Mediterranean climate (Bessa et al., 2016; Verdasca et al., 2021c). According to Villemant et al. (2011), other suitable regions for V. velutina, located in north and south America and in Australia, may also be vulnerable to invasion if another accidental introduction occurs in these continents. The fact that few (9%) records of the invasive population are in high-risk areas (that were only predicted by one of the models—native or invasive) is not surprising, since the invasion started recently. In 2017 very few occurrences were detected in British Isles (not dealt in this work), but in the end of 2019 new nests were detected, highlighting the need for attention to the potential of V. velutina to rapidly colonise the British mainland, if control strategies are not timely applied (Keeling et al., 2017). As V. velutina gynes can fly over long distances (Monceau et al., 2015; Robinet, Suppo & Darrouzet, 2017) and as jump-dispersal mediated by humans also occurs (Robinet, Darrouzet & Suppo, 2019; Verdasca et al., 2021c), the non-invaded high-risk regions of south of Italy, Corsica, Croatia and Montenegro, should be vigilant. This is relevant, because in a previous work, we evidenced that in regions where the climatic conditions are suitable for V. velutina, motorways play an important role in accelerating the natural invasion dynamics of this invasive (Verdasca et al., 2021c). Independently of the colonization mechanisms, countries more at risk of being invaded should elaborate action plans focusing on biosecurity policies (particularly targeted to the interception of wooden products’ transportation and man-made goods associated with garden trade, due to the potential of these commodities to shelter hibernating queens) and addressing the expected impacts on native biodiversity, crop pollination, beekeeping activities and public health.

Conclusions

Our approach of combining reciprocal distribution models with analyses of niche dynamics strengthens our predictions on the potential of V. velutina to continue its invasion process. With RDM we identified which areas are most sensitive to invasion and with niche analysis we confirmed (i) its ability to colonize different environmental envelopes from its native realized niche (evidence of a putative niche shift, especially in NW of Iberian Peninsula) and (ii) that the species is using the most common available conditions in Europe (hence less prone to stochastic events that can limit its expansion process). This approach is useful to forecast the future of the V. velutina expansion in western and central Europe and might be used with success for many other invasives.

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