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Article

Invasive Pest and Invasive Host: Where Might Spotted-Wing Drosophila (Drosophila suzukii) and American Black Cherry (Prunus serotina) Cross Paths in Europe?

by
Yefu Zhou
1,†,
Chunhong Wu
1,†,
Peixiao Nie
1,
Jianmeng Feng
1,2,* and
Xiaokang Hu
1,2
1
College of Agriculture and Biological Science, Co-Innovation Center for Cangshan Mountain and Erhai Lake Integrated Protection and Green Development of Yunnan Province, Dali University, Dali 671003, China
2
Yunnan Key Laboratory of Biodiversity of Gaoligong Mountain, Yunnan Academy of Forestry and Grassland, Kunming 650201, China
*
Author to whom correspondence should be addressed.
†
These authors contributed equally to this work.
Forests 2024, 15(1), 206; https://doi.org/10.3390/f15010206
Submission received: 16 December 2023 / Revised: 2 January 2024 / Accepted: 12 January 2024 / Published: 19 January 2024
(This article belongs to the Section Forest Health)
Browse Figures
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Abstract

:
Both spotted-wing drosophila (SWD, Drosophila suzukii) and American black cherry (ABC, Prunus serotina) are invasive species with major deleterious effects on forest ecosystems in Europe. ABC, a host of SWD, can sustain large populations of SWD, and SWD in turn can constrain the regeneration of its host. Here, we examined the range shifts of SWD, ABC, and their range overlap under future scenarios using range shift models. In the current–future scenarios, both SWD and ABC were predicted to undergo potential range expansions in Europe, suggesting that their invasion risks might increase in the future. Climate change might be the major driver of range shifts of both the pest and host, followed by land-use and host availability changes; therefore, mitigating future climate change might be key for controlling their future invasions in Europe. The relative contribution of climate and host availability to shaping the potential ranges of invasive species might not only vary with their feeding habitats (polyphagy/oligophagy) but also with the relative abundance of hosts among available host reservoirs. Range overlap under current and future scenarios was mainly observed in the UK, Germany, France, Switzerland, Italy, and Eastern Europe; this area is of high and low priority for the control of SWD and ABC, respectively.

1. Introduction

Spotted-wing drosophila (Drosophila suzukii) is native to Southeast Asia and was introduced to Europe approximately a decade ago [1,2]. It has a broad host range, including thin-skinned berries (e.g., blueberries, caneberries, and strawberries) and stone fruits (e.g., cherries, peaches, and plums) [3], and its preferred hosts appear to be raspberries and strawberries [3,4]. The minimum, optimal, and maximum temperatures for its development are approximately 13.4, 21.0, and 29.4 °C, respectively [5]. It is considered one of Europe’s most invasive alien pests [6,7,8]. Populations of this pest have become established in many European countries because of its ability to proliferate rapidly [8,9]. Females of this pest lay eggs in ripening fruits, which results in the massive decay of fruit and major economic losses [10,11]. For example, this pest has been estimated to be responsible for the loss of ca. 13% of the revenue of the berry industry in Trento Province, Italy [12]. Thus, there is an urgent need to devise effective strategies for the control of populations of this pest and to prevent its further spread in Europe [7].
American black cherry (Prunus serotina), a native woody plant of North America and a host of spotted-wing drosophila, was introduced to Europe approximately 300 years ago [13]. It prefers a cool and moist habitat, the optimal average annual precipitation ranges from 970 to 1120 mm, and the optimal annual potential evapotranspiration ranges from 430 to 710 mm [14]. Seedlings can survive shaded conditions and grow rapidly when light conditions improve [15,16]. Populations of this species were rapidly established in many European forests [15,16,17]. In Europe, the success of this invasive plant stems from its high propagule pressure, rapid biomass production, high rates of fecundity, and adaptability to shaded conditions [18,19]; these characteristics also contribute to its ability to competitively exclude native plants in Europe [20,21]. This invasive alien plant thus poses a major threat to native biodiversity in Europe. American black cherry also has substantial effects on forest ecosystems by altering nutrient cycles and soil conditions [22,23]. Its ability to rapidly colonize and invade, coupled with its effects on local biodiversity and forest ecosystems, make American black cherry one of the most invasive plants in Europe [24]. Thus, there is a need to implement measures to control invasions of American black cherry in Europe.
Determining the potential ranges of these two species could provide useful information for identifying their invasion hotspots. Several case studies have determined their potential ranges in Europe [25,26,27,28]. For example, dos Santos et al. (2017) predicted that extreme northern Spain and Portugal [29], France, Austria, Greece, Italy, Switzerland, Albania, and southern Germany comprised invasion hotspots for spotted-winged drosophila; these findings were largely consistent with those of Nair et al. (2023) [30]. American black cherry’s potential range in Europe has also received much attention [31,32,33]. For example, Segura et al. (2018) predicted that American black cherry might invade the western portion of the European continent [34]. These case studies have enriched our knowledge of their invasions in Europe. Although many previous studies have focused on characterizing spatial patterns of the two invasive species, few studies have examined their range shifts under current–future scenarios. For example, few studies have determined the expanded ranges and unfilled ranges of these invasive species under current and future scenarios (i.e., potential ranges only under future and current scenarios, respectively). Therefore, additional studies of their range shifts in Europe under current–future scenarios are needed.
Climatic conditions have major effects on the development, reproduction, phenology, and behavior of spotted-wing drosophila [2,35,36,37]. Climatic conditions might play a major role in determining the potential range of spotted-wing drosophila. For example, Gutierrez et al. (2016) identified the potential range of spotted-wing drosophila in Europe and found that winter temperature played a key role in determining its potential range [25]. Recently, Nair and Peterson (2023) predicted the potential range of this pest in 17 European countries, including Ukraine, and found that precipitation in the driest month and precipitation in the driest quarter were the most important variables [30]. Climatic variables have also been shown to play a major role in the potential range of American black cherry in Europe. For example, Segura et al. (2018) found that temperature-related variables made the largest contribution in shaping the potential range of this invasive plant in Europe [34].
Land use may affect the potential range of invasive species, in addition to climate, most likely because changes in land use can affect access to suitable habitats [38,39]. For example, Liu et al. (2000) found that land-use changes had a substantial effect on the global potential range of the fall armyworm, which is a highly invasive species [40]. Although the relative effects of land use and climate variables on the potential range of invasive species might vary with the spatial scale (e.g., the relative role of climate predictors might be greater at large scales than at small scales), their relative effects have been the subject of debate [40,41,42]. However, few studies have evaluated the relative importance of land use as a driver of the distribution of our target species, as well as its importance relative to climatic variables.
Host availability might also affect the potential ranges of invasive species, especially those of herbivorous pests, because host availability ultimately determines resource availability [43,44]. For example, Castro-Sosa et al. (2017) showed that the potential range of spotted-wing drosophila in Mexico was strongly affected by non-crop host availability [45]. However, few studies have evaluated the role of host availability on the potential distribution of spotted-wing drosophila in Europe. Additionally, more research is needed to determine the relative roles of climate and host availability on the potential ranges of invasive pests. For example, Robinet et al. (2006) found that host availability had a greater effect on the potential range of the pine processionary moth in France than climatic factors [46]. In contrast, Battisti et al. (2005) observed that climatic factors had a greater effect on the potential range of this species than host availability in Italy [47].
American black cherry is an invasive plant in Europe and also a host for spotted-wing drosophila. Poyet et al. (2014) found that American black cherry is a suitable reservoir for spotted-wing drosophila [48]. Additionally, Turcotte et al. (2018) argued that the predilection of spotted-wing drosophila for American black cherry might enhance their abundance [49]. Therefore, the potential range of American black cherry might be future source regions for the invasion of spotted-wing drosophila. This suggests that the area of range overlap between spotted-wing drosophila and American black cherry might be hotspots for controlling the invasion of spotted-wing drosophila. By contrast, spotted-wing drosophila might have a major negative effect on the dispersal, fruit production, seed viability, and regeneration of American black cherry. This suggests that the area of range overlap between spotted-wing drosophila and American black cherry might be of low priority for controlling the invasion of American black cherry. Nevertheless, few studies have evaluated these possibilities.
Here, we hypothesize that the relative importance of future land-use and climate changes in driving range shifts of spotted-wing drosophila and American black cherry in Europe differs; we also hypothesize that the availability of American black cherry might have a strong effect on the range shifts of spotted-wing drosophila. Therefore, our major aim is to develop range shift models to explore the range shifts of spotted-wing drosophila and American black cherry in Europe; their range overlap under future scenarios, and the relative roles of climate, land use, and host availability in driving range shifts. The results of this study provide novel insights that could aid the development of strategies to control invasions of these two species in Europe.

2. Materials and Methods

2.1. Occurrence Records

We obtained occurrence data for our target species from the Global Biodiversity Information Facility (http://www.gbif.org, accessed on 1 October 2023); we obtained 2977 and 199,225 occurrence records for spotted-wing drosophila and American black cherry, respectively. We eliminated duplicated occurrences (i.e., occurrences with the same geographical coordinates) and those with geographic coordinate uncertainty > 5 km. To minimize the effect of sample bias on our models, we used the SDM toolbox, a package for species distribution modeling, to spatially thin the occurrences with a radius of 5 km [50]. Next, we developed an occurrence dataset that included 228 spotted-wing drosophila records and 3832 American black cherry records (Figure 1, Table S1).

2.2. Predictors in the Species Distribution Models (SDMs)

The potential range of American black cherry in Europe was predicted using SDMs; three categories of 30 predictors were used in the SDMs: topography (3), land use (8), and climate (19). Four categories of the 31 predictors—host availability (1), topography (3), land use (8), and climate (19)—were used to develop SDMs for calibrating the potential range of spotted-wing drosophila. The habitat suitability for American black cherry was used to indicate host availability, and it was calibrated using the Biomod2 platform [51]. Topographical predictor data were obtained from the Worldclim database [52], including digital elevation models (DEMs) at a five-arc-minute spatial resolution. We obtained spatial layers of slope and aspect at the same spatial resolution from the DEM. Eight land-use variables with a 0.25 arc-degree spatial resolution were obtained from the Land-use Harmonization dataset (http://luh.umd.edu, accessed on 5 October 2023), and they included the proportion of primary forested land, the proportion of primary non-forested land, the proportion of potential and secondary forested land, the proportion of potential and secondary non-forested land, the proportion of managed pasture, the proportion of rangeland, the proportion of urban land, and the proportion of cropland. To make the spatial resolution of land-use variables and climatic variables consistent, we resampled the land-use variables to a five-arc-minute spatial resolution.
We downloaded datasets of monthly rainfall and temperature data from 1990 to 2020 from the Climate Research Division (https://crudata.uea.ac.uk/, accessed on 1 October 2023), and the Biovarcs R package was utilized to calibrate 19 climate predictors with a spatial resolution of 5 arc-minutes [52]. Each climate predictor corresponded to a bioclimatic variable in the Worldclim database [52]. Nineteen future climate predictors in 2100 with a 5 arc-minute spatial resolution were obtained from the Worldclim database [52], and the two future scenarios included SSP126 and SSP585, which represented optimistic and pessimistic scenarios, respectively. Additionally, future climate variables were calibrated using FIO-ESM-2-0, which is one of the most robust general circulation models for climate change [53]. Therefore, three scenarios were used in our study: current, SSP126, and SSP585 scenarios.
To mitigate the effect of collinearity on our SDMs, we first created preliminary SDMs to assess the importance value (IV) of each predictor (Table S2). Next, an absolute correlation coefficient threshold of 0.7 in the Pearson correlation analysis was used to identify strong collinearity between pairs of predictors (Table S3). If strong collinearity was detected, we removed the predictor with the lower IV. We then employed the remaining predictors to develop our formal SDMs to project the potential ranges of our target species as well as habitat suitability for American black cherry.

2.3. Model Construction

We used the Biomod2 platform [51] to calibrate the habitat suitability maps for American black cherry. We input all retained variables into the SDM platform, and we used nine algorithms for this process: Classification Tree Analysis, Flexible Discriminant Analysis, Generalized Linear Model, Random Forest for Classification and Regression, Generalized Boosting Model, Multiple Adaptive Regression Splines, Surface Range Envelope, Artificial Neural Network, and Maximum Entropy Modeling [51]. To obtain pseudo-absences (PAs), we used a random selection procedure with three repetitions [51]. If the number of American black cherry occurrences was less than 1000, 1000 PAs were retrieved; otherwise, the number of PAs retrieved was equal to the number of American black cherry occurrences [54]. We then calibrated the habitat suitability for American black cherry (Figure S1), which, as a candidate predictor, was input into the SDMs to calibrate the potential range of spotted-wing drosophila. The potential range of American black cherry was calibrated using the maximum sensitivity–specificity sum (MSS) approach [55]. The reliability of our SDMs was evaluated using five-fold cross-validation. To develop SDMs, 70% of the records were randomly selected; the remaining 30% were used to evaluate the reliability of the SDMs [51,56]. We removed calibrated SDMs with an AUC less than 0.8 and true skill statistic (TSS) less than 0.6; in our ensembled SDMs, the prediction of each model was assigned a weight based on its TSS [50]. A similar technique was used to estimate the potential range of spotted-wing drosophila.

2.4. Range Shifts of the Two Species

Following Cao and Feng (2023), we used range stabilized (RS), range unfilled (RU), and range expanded (RE) to characterize range shifts of each species under future scenarios [57]. RU indicates the potential range that a species is only expected to occupy under current scenarios. RS indicates the range that a species could potentially occupy under both current and future scenarios. Finally, RE is the potential range that a species is expected to occupy under future scenarios.
We used the range ratio index (RRI) to characterize shifts in the range sizes of species under future scenarios [50], which was calibrated as follows:
R R I = R F R C ,
where RF is the potential range under future scenarios and is the sum of RS and RE. RC is the potential range under the current scenario and is the sum of RS and RU.
We used the range similarity index (IRS) to calibrate shifts in the range centroids of species under current–future scenarios, which were calibrated as follows:
I R S = 2 R S R C + R F ,

3. Results

3.1. Model Reliability

High values were obtained for AUC and TSS, indicating that the reliability of all the assembled SDMs was high. The SDMs for the potential range of spotted-wing drosophila had TSS and AUC scores of 0.837 and 0.969, respectively, and the TSS and AUC scores of the models for the potential range of American black cherry were 0.804 and 0.964, respectively.

3.2. Relative Importance of Predictors

Mean temperature of the coldest season (0.534), the proportion of urban land (0.180), and max temperature of the warmest month (0.094) had the highest importance values in our formal SDMs for the potential range of spotted-wing drosophila, and the proportion of primary non-forested land (0.006), the proportion of range land (0.006), and aspect (0.005) were the predictors with the lowest significance (Table 1). Our SDMs also showed that minimum temperature of the coldest month (0.441), mean temperature of the warmest season (0.108), and proportion of primary forested land (0.052) were the main predictors of the potential range of American black cherry, and the proportion of potentially secondary forested land (0.006), mean diurnal range (0.004), and aspect (0.003) were the predictors with the lowest significance (Table 1). In sum, winter temperature had a major effect on the range shifts of our target species.

3.3. Range Shifts of Spotted-Wing Drosophila

The MSS thresholds for determining the potential range of spotted-wing drosophila under current conditions, SSP126, and SSP585 were 0.40, 0.50, and 0.39, respectively. The current potential range, which covered an area of approximately 1.07 million km2, was primarily detected in the following regions: the UK, Ireland, Germany, France, Denmark, Switzerland, Italy, Austria, Croatia, Portugal, and Spain (Figure 2a). The potential range under SSP126 revealed range expansions in these aforementioned regions and covered approximately 1.33 million km2, including large areas in Norway and Sweden (Figure 2b). The potential range under SSP585 was similar to that under SSP126, with the exception of a larger area in Norway and Sweden, and covered 1.36 million km2 (Figure 2c). In sum, the potential range of this pest covered a larger area under SSP126 and SSP585 than under the current scenario.
Under the current-SSP126 scenario, the range expansion area (0.31 million km2) of this pest was mainly scattered in Eastern Europe, Italy, France, Germany, Switzerland, Austria, and the UK (Figure 2d). Its stable range under this scenario mainly covered the British Isles, France, Germany, Italy, Switzerland, Denmark, and Portugal (total of 1.01 million km2). Under the current-SSP126 scenario, this pest’s unfilled range was primarily 0.059 million km2 and covered Ireland, France, and Portugal (Figure 2d). The range expansion area of this pest under the current-SSP585 scenario covered 0.46 million km2, including the potential range under the current-SSP126 scenario, as well as areas in Iceland, Ireland, the UK, Slovakia, West Russia, and high-latitude regions (i.e., Norway, Sweden, and Finland). The stable range of this pest under this scenario covered 0.90 million km2, which included Ireland, the UK, Germany, France, Denmark, Switzerland, Austria, Italy, Poland, Spain, and Portugal. The unfilled range of this pest covered 0.18 million km2 under the same scenario, including Ireland, Italy, and North France (Figure 2e). The range ratio index under the current-SSP126 scenario was slightly lower than that under the current-SSP585 scenario (1.23 vs. 1.27). The range similarity index was higher under the current-SSP126 scenario than under the current-SSP585 scenario (0.85 vs. 0.74). Furthermore, the expanded range under the current-SSP585 scenario was ca. 1.5 times that under the current-SSP126 scenario. In sum, substantial range expansions were projected under current–future scenarios, especially under the current-SSP585 scenario and in high-latitude regions, and no substantial shifts in the position of the range of the pest were detected.

3.4. Range Shifts of American Black Cherry

The MSS thresholds for determining the potential range of American black cherry under current conditions, SSP126, and SSP585 were 0.49. 0.47, and 0.32, respectively. Under the current scenario, the main area of the predicted range of American black cherry was 1.45 million km2 and included the UK, France, Germany, Denmark, Switzerland, Czech Republic, Poland, and Hungary (Figure 3a). The potential range of this species under SSP126 was mostly detected in Ireland, the UK, Germany, France, Denmark, Poland, Czech Republic, Lithuania, Finland, and Sweden, and covered an area of 1.83 million km2 (Figure 3b). The potential range under the SSP585 scenario was 2.19 million km2 across Ireland, the UK, France, Germany, Czech Republic, Austria, Italy, Poland, Lithuania, and high-latitude regions in Norway, Sweden, Finland, and West Russia (Figure 3c). In sum, the area of the potential range of American black cherry in higher latitude regions and West Russia was largest under the SSP585 scenario.
The stable range of American black cherry under the current-SSP126 scenario (1.32 million km2) was mainly detected in the UK, Germany, France, Denmark, Czech Republic, and Poland (Figure 3d). The expanded range of American black cherry was primarily observed in Ireland, Sweden, Finland, Latvia, Lithuania, Belarus, and Ukraine and covered 0.51 million km2, and the unfilled range was primarily observed in France and Hungary and covered 0.13 million km2 (Figure 3d). Under this scenario, the expanded range of American black cherry covered 0.51 million km2, including Ireland, Sweden, Finland, Latvia, Lithuania, Belarus, and Ukraine, and the unfilled range covered 0.13 million km2, including France and Hungary (Figure 3d). The same patterns were observed under the current-SSP126 scenario; the stabilized range of American black cherry under the current-SSP585 scenario covered 1.20 million km2 (Figure 3e). The expanded range of American black cherry covered 0.99 million km2 under the current-SSP585 scenario, including Ireland, the UK, Italy, Switzerland, Austria, Norway, Sweden, and West Russia. The unfilled range of American black cherry under this scenario covered 0.25 million km2, including France, Hungary, and the Czech Republic (Figure 3e). Under the current-SSP126 and current-SSP585 scenarios, the corresponding range ratio indices were 1.26 and 1.51, respectively, and the range similarity indices were 0.80 and 0.66, respectively. Additionally, the expanded range under the current-SSP585 scenario was ca. two times higher than that under the current-SSP126 scenario. In sum, substantial range expansions of American black cherry in high-latitude regions were observed under current–future scenarios, especially under the current-SSP585 scenario; however, no substantial shifts in range position were detected.

3.5. Potential Range Overlap between the Pest and Its Host

Under the current scenario, range overlap between spotted-wing drosophila and American black cherry covered 0.67 million km2, including Germany, France, the UK, Switzerland, Italy, and scattered regions in Eastern Europe (Figure 4a). Their area of range overlap, which covered 0.90 million km2 under SSP126, was mainly observed in Ireland, the UK, Switzerland, Germany, France, Italy, Slovakia, Norway, Sweden, and scattered regions in Eastern Europe (Figure 4b). The area of range overlap under SSP585 covered 1.00 million km2, which included the potential range under the SSP126 scenario as well as West Russia, Italy, Norway, Sweden, Finland, and Eastern Europe (Figure 4c). In sum, we predicted a substantial expansion in the range overlap between spotted-wing drosophila and American black cherry under current–future scenarios, especially under the SSP585 scenario.

4. Discussion

Climate change is expected to alter the potential ranges of invasive species through its effects on the temporal and spatial distribution of suitable habitat [58,59]. However, the effects of future climate change on the potential ranges of invasive species have been the subject of debate [59,60,61,62,63]. Observations of range expansions and contractions have been made in previous studies [60,61,62,63]. In most cases, future climate change is expected to promote the range expansions of invasive species [61,62]. Future climate change might weaken the filtering effect of freezing (i.e., decreased mortality due to the freezing of body fluids) [64]. Additionally, winter temperature has been observed to be one of the key factors affecting the life history of our target species [37,65,66,67,68]. For example, the phenotype of this pest insect can be altered by exposure to low temperatures in winter [69]. These results are consistent with our finding that winter temperature plays a critically important role in determining the range shifts of spotted-wing drosophila and American black cherry. In other words, warmer winters might facilitate invasions of spotted-wing drosophila and American black cherry in Europe, including their expansion into high-latitude regions such as Norway, Sweden, and Finland.
The potential ranges of our target species were predicted to expand in Europe, and this finding was supported by the results of dos Santos et al. (2017) [29] and Segura et al. (2018) [34]. This suggests that more effort is needed to control their invasions in Europe. Additionally, their future range expansions were mainly projected in high-latitude regions, especially for spotted-wing drosophila. Therefore, we expected that high-latitude regions might be hotspots of their future invasions; thus, these regions merit increased attention. Among all the predictors examined, future climate change played a critically important role in determining the extent of their future range expansions. This suggests that mitigating future climate change is important for controlling future invasions of spotted-wing drosophila and American black cherry in Europe.
The relative effects of climate and land-use change on the potential ranges of invasive species might vary with spatial scale; at large scales, the relative strength of climatic factors might be stronger than land-use factors [40]. This might stem from the fact that land use is closely associated with small-scale habitat traits such as soil depth, soil moisture content, and microclimate for most invasive alien species; however, range shifts at large spatial scales often require that invasive species adapt to novel climate conditions [40,70]. Our finding that land-use factors had weaker effects on the potential ranges of spotted-wing drosophila and American black cherry than climate factors in Europe is consistent with this hypothesis; few studies have evaluated the effects of land use on the potential ranges of these invasive species. However, a global-scale study on globally invasive fall armyworms showed that land use had a stronger effect on its potential range than climate, as land use is thought to be closely associated with food availability for fall armyworms [43]. Therefore, the relative importance of climate and land use on the potential ranges of invasive alien species does not vary with spatial scale in a uniform manner; generally, diverse mechanisms might underlie variation in the relative importance of climate and land use in shaping the potential ranges.
The potential ranges of invasive alien species might also be affected by host availability, especially for herbivorous pests. For example, the potential range of the pine processionary moth is strongly associated with the distributions of its host trees in France [46]. However, the relative roles of climate conditions and host availability have been observed to be closely related to the feeding habits (oligophagy/polyphagy) of pests, with host availability playing a greater role in shaping the potential ranges of oligophagous pests than polyphagous pests [71,72]. Our findings revealed that the habitat suitability/availability of American black cherry had a weaker effect on the potential range of spotted-wing drosophila than climatic predictors. This might stem from the fact that spotted-wing drosophila is a highly polyphagous pest and can use a wide range of hosts in Europe [73]; thus, the availability of American black cherry does not have a major effect on the overall food supply for spotted-wing drosophila, which explains why it was not the primary determinant of its potential range. However, the results of a previous study suggest that non-crop host availability had the largest effect on the potential range of spotted-wing drosophila in Mexico [45]. This difference might be explained by the fact that American black cherry represents a very small portion of the host spectrum for spotted-wing drosophila in Europe, whereas non-crop hosts might represent a high proportion of the hosts available to spotted-wing drosophila in Mexico. Thus, the relative effects of host availability on the potential ranges of invasive alien species likely depend on both the feeding habits (polyphagy/oligophagy) of the pest as well as the relative abundance of the host among all available hosts; additional studies are needed to clarify this possibility.
Spotted-wing drosophila is thought to have major negative effects on the dispersal, fruit production, seed viability, and regeneration of American black cherry [49]. This suggests that the invasiveness of American black cherry or its effects on forest ecosystems could be substantially reduced by spotted-wing drosophila. Additionally, under current and future scenarios, we observed range overlap between spotted-wing drosophila and American black cherry in the UK, Germany, France, Switzerland, Italy, and Eastern Europe. These observations suggest that these areas of range overlap should not be considered hotspots requiring attention in strategies for controlling invasions of American black cherry because of the effects of spotted-wing drosophila.
Although spotted-wing drosophila could have a substantially negative effect on American black cherry, such as on its growth, reproduction, and regeneration, the feeding of spotted-wing drosophila on American black cherry can lead to spotted-wing drosophila infestations [48]. The occurrence of American black cherry might promote the formation of invasion hotspots of spotted-wing drosophila; thus, areas with American black cherry might serve as source regions for the invasion of spotted-wing drosophila in Europe. Therefore, the observed areas of range overlap in the UK, Germany, France, Switzerland, Italy, and Eastern Europe might be hotspots for controlling invasions of spotted-wing drosophila. Populations of this pest might be particularly large in these regions, and the implementation of countermeasures against spotted-wing drosophila invasions in the area of range overlap might be highly effective; additional studies will be needed to evaluate the efficacy of this strategy.

5. Conclusions

Under current–future scenarios, the potential ranges of both the pest and host were projected to expand in Europe, suggesting that their invasion risk will increase in the future. Climate change was the major driver of range shifts of both the pest and its host, followed by land-use and host availability changes; this suggests that mitigating climate change will be key for controlling future invasions of these species. The relative importance of climate and host availability in determining the potential ranges of these invasive species might not only depend on the feeding habits (polyphagy/oligophagy) of the pest but also on the proportion of the host relative to all available hosts. Therefore, the role of host availability as a driver of changes in the potential ranges of spotted-wing drosophila might have been underestimated because only one of its several hosts was studied. Range overlap under current and future scenarios was mainly observed in the UK, Germany, France, Switzerland, Italy, and Eastern Europe, and these might be source regions or hotspots for future invasions of spotted-wing drosophila in Europe and, thus, low-priority areas for the invasion of American black cherry.

Supplementary Materials

The following supporting information can be downloaded at: https://www.mdpi.com/article/10.3390/f15010206/s1, Table S1: Datasets of the occurrence records. Table S2: Predictors’ importance values in preliminary SDMs. Table S3: Correlation analyses in each pair of the predictors. Figure S1: Habitat suitability maps of American black cherry.

Author Contributions

Conceptualization, J.F., X.H. and Y.Z.; methodology, Y.Z., C.W. and J.F.; software, Y.Z., C.W. and P.N.; validation, Y.Z., C.W. and P.N.; formal analysis, Y.Z., P.N. and C.W.; investigation, Y.Z., C.W. and P.N.; resources, Y.Z.; data curation, J.F., Y.Z. and C.W.; writing—original draft preparation, Y.Z. and J.F.; writing—review and editing, Y.Z., C.W. and J.F.; visualization, Y.Z., C.W. and P.N.; supervision, J.F. and X.H.; project administration, J.F. and X.H.; funding acquisition, X.H. All authors have read and agreed to the published version of the manuscript.

Funding

This study has been funded by the National Natural Science Foundation of China (Grant ID: 41963007), Foundation of Yunnan Province Science and Technology Department (Grant No: 202305AM070003).

Data Availability Statement

The data that support the findings of this study are available from the corresponding author upon reasonable request.

Acknowledgments

We are grateful to Yanjie Zhang for his valuable comments on the study. We would also like to thank Tianmeng Liu for his valuable suggestions on the statistical analyses.

Conflicts of Interest

The authors declare that they have no known conflicts of interest that could have influenced the work reported in this paper.

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Figure 1. Occurrence records of the target species in Europe. (a) Spotted-wing drosophila records (total of 228); (b) American black cherry records (total of 3832).
Figure 1. Occurrence records of the target species in Europe. (a) Spotted-wing drosophila records (total of 228); (b) American black cherry records (total of 3832).
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Figure 2. Range dynamics of spotted-wing drosophila. (a–c) The potential range of spotted-wing drosophila under current conditions, SSP126, and SSP585, covering 1.07, 1.33, and 1.36 million km2, respectively, with orange indicating the potential range of spotted-wing drosophila. (d,e) Range dynamics of spotted-wing drosophila under the current-SSP126 and current-SSP585 scenarios, with red, blue, and yellow indicating stabilized, expanded, and unfilled ranges, respectively.
Figure 2. Range dynamics of spotted-wing drosophila. (a–c) The potential range of spotted-wing drosophila under current conditions, SSP126, and SSP585, covering 1.07, 1.33, and 1.36 million km2, respectively, with orange indicating the potential range of spotted-wing drosophila. (d,e) Range dynamics of spotted-wing drosophila under the current-SSP126 and current-SSP585 scenarios, with red, blue, and yellow indicating stabilized, expanded, and unfilled ranges, respectively.
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Figure 3. Range dynamics of American black cherry. (a–c) The potential range of American black cherry under current, SSP126, and SSP585, covering 1.45, 1.83, and 2.19 million km2, respectively, with orange indicating the potential range of American black cherry. (d,e) Range dynamics of American black cherry under the current-SSP126 and current-SSP585 scenarios, respectively, with red, blue, and yellow indicating stabilized, expanded, and unfilled ranges, respectively.
Figure 3. Range dynamics of American black cherry. (a–c) The potential range of American black cherry under current, SSP126, and SSP585, covering 1.45, 1.83, and 2.19 million km2, respectively, with orange indicating the potential range of American black cherry. (d,e) Range dynamics of American black cherry under the current-SSP126 and current-SSP585 scenarios, respectively, with red, blue, and yellow indicating stabilized, expanded, and unfilled ranges, respectively.
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Figure 4. Overlap in the potential ranges of spotted-wing drosophila and American black cherry. (a–c) Potential range overlap under current conditions, SSP126, and SSP585, covering 0.67, 0.90, and 1.00 million km2, respectively.
Figure 4. Overlap in the potential ranges of spotted-wing drosophila and American black cherry. (a–c) Potential range overlap under current conditions, SSP126, and SSP585, covering 0.67, 0.90, and 1.00 million km2, respectively.
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Table 1. Importance values of the predictors in the formal SDMs.
Table 1. Importance values of the predictors in the formal SDMs.
Spotted-Wing DrosophilaAmerican Black Cherry
CategoryPredictorsImportance ValuesCategoryPredictorsImportance Values
Climate predictorsMTCQ0.534Climate predictorsMTCM0.441
Land-use predictorsURBAN0.179Climate predictorsMTWS0.108
Climate predictorsMTWM0.094Land-use predictorsPRIMFL0.052
Climate predictorsTAR0.092Land-use predictorsURBAN0.031
Host availabilityHAVA0.036Climate predictorsPWS0.030
Climate predictorsPDM0.035Land-use predictorsSECDNL0.024
Climate predictorsISO0.031Land-use predictorsPRIMN0.019
Climate predictorsPWS0.027Land-use predictorsPASTER0.018
Climate predictorsPS0.023Topographical predictorsSLOP0.015
Climate predictorsPCQ0.022Topographical predictorsELEV0.013
Land-use predictorsSECDF0.019Land-use predictorsCROPL0.012
Land-use predictorsPRIMFL0.017Climate predictorsMTWETS0.011
Land-use predictorsCROPL0.015Climate predictorsPS0.007
Climate predictorsMTWETS0.008Land-use predictorsRANG0.007
Land-use predictorsPASTR0.007Climate predictorsPDS0.007
Topographical predictorsELEV0.007Land-use predictorsSECDFL0.006
Land-use predictorsSECDNL0.006Climate predictorsMDR0.004
Land-use predictorsPRIMN0.006Topographical predictorsASP0.003
Land-use predictorsRANG0.006
Topographical predictorsASP0.005
Note: HAVA: availability of American black cherry; MDR: mean diurnal range (°C); ISO: isothermality; MTWM: maximum temperature of the warmest month; MTCM: minimum temperature of the coldest month; TAR: temperature annual range; MTWETS: mean temperature of the wettest season (°C); MTWS: mean temperature of the warmest season (°C); MTCQ: mean temperature of the coldest quarter; PDM: precipitation of the driest month; PS: precipitation seasonality (mm); PDS: precipitation of the driest season (mm); PWS: precipitation of warmest season (mm); PCQ: precipitation of coldest quarter ASP: aspect (°); Slop: slope (°); ELEV: elevation; URBAN: urban land; CROPL: cropland; PRIMFL: forested primary land; PASTR: managed pasture; PRIMN: non-forested primary land; RANG: rangeland; SECDFL: potentially forested secondary land; SECDNL: potentially non-forested secondary land.
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Zhou, Y.; Wu, C.; Nie, P.; Feng, J.; Hu, X. Invasive Pest and Invasive Host: Where Might Spotted-Wing Drosophila (Drosophila suzukii) and American Black Cherry (Prunus serotina) Cross Paths in Europe? Forests 2024, 15, 206. https://doi.org/10.3390/f15010206

AMA Style

Zhou Y, Wu C, Nie P, Feng J, Hu X. Invasive Pest and Invasive Host: Where Might Spotted-Wing Drosophila (Drosophila suzukii) and American Black Cherry (Prunus serotina) Cross Paths in Europe? Forests. 2024; 15(1):206. https://doi.org/10.3390/f15010206

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Zhou, Yefu, Chunhong Wu, Peixiao Nie, Jianmeng Feng, and Xiaokang Hu. 2024. "Invasive Pest and Invasive Host: Where Might Spotted-Wing Drosophila (Drosophila suzukii) and American Black Cherry (Prunus serotina) Cross Paths in Europe?" Forests 15, no. 1: 206. https://doi.org/10.3390/f15010206

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