Obolodiplosis robiniae Will Infect All Black Locust In Eurasia Under Climate Change

doi:10.21203/rs.3.rs-1556580/v1

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Research Article

Obolodiplosis robiniae Will Infect All Black Locust In Eurasia Under Climate Change

https://doi.org/10.21203/rs.3.rs-1556580/v1

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posted 19 Apr, 2022

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Obolodiplosis robiniae was discovered in Eurasia at the beginning of the 21st century and was then spread at an explosive rate. Here, we explore the current and future (in years 2050 and 2070) trends in the potential distribution of O. robiniae in Eurasia under diverse climate change scenarios based on a maximum entropy (MaxEnt) model. Our results showed that the current potential distribution area of O. robiniae is within the range of 21.58°-65.66°N in the Eurasian continent. The total current potential distribution (CPD) area of O. robiniae in Eurasia was 10,896,309.16 km², with suitable areas covering a substantial section of Europe. The Annual Mean Temperature (Bio1), Annual Precipitation (Bio12), and the Precipitation of the Driest Month (Bio14) are the most important bioclimatic variables determining the potential distribution of O. robiniae. The future area suitable for habitat of O. robiniae is characterized by a large-scale northward expansion trend with temperature elevation. The marginally suitable and highly suitable areas would thus increase, whereas the southern appropriate areas would shrink. Under the SSP585 scenario, in 2070, the suitable area of O. robiniae would be the largest, up to 14,696,253.77 km2, which is 34.87% more than the current suitable area. This information would facilitate the provision of early warning on the potential distribution areas of O. robiniae issued by the forestry quarantine departments of Asian and European countries and provide a scientific basis for the prevention and control of O. robiniae spread and outbreaks.

invasive pest

CMIP6

shared socio-economic pathways

MaxEnt

potential distribution

management measures

Current and future potential distribution of O. robiniae was modeled.

Temperature is the key determinant factor driving the distribution of O. robiniae.

O. robiniae is a beneficiary of climate warming.

Potential distribution will expand to the north and the south will shrink.

The trend in the potential distribution is consistent with that of the host.

Due to the globalization of trade and the increasing tourist traffic between continents, the yearly introduction and spread of new species have been increasing each year (Essl et al., 2020; Seebens et al., 2021). Invasive alien species (IAS) can cause significant negative ecosystem-level, economic, and human health effects in the area of their introduction (Diagne et al., 2021; Mack and Smith, 2011; Vanbergen et al., 2018). In fact, because of their impact on the environment, invasive species are predicted to among the biggest driving forces of global change (Vilà et al., 2007). In addition, the elevated temperature of the global climate is expected to increase the suitability for living of increasingly more new areas that have been previously unsuitable habitats of such species (Descombes et al., 2020; McCain and Garfinkel, 2021). Insects, in particular, are more harmful as invasive species due to their high reproductive rate and abundance, as well as their remarkable physiological tolerance to temperature extremes and ability to fly, giving them the leverage to spread faster and farther (Kenis and Branco, 2010). A previous investigation revealed that 940 of 1600 insects species were significantly affected by global warming, including its effects on the number of insect populations, the acceleration of insect development, the increase of alien invasive insect species range, the migration of insects to high altitude areas, the increase in the probability of insect outbreaks, and the reduced insect population diversity (Raza et al., 2015).

Locust gall midge, Obolodiplosis robiniae Haldeman (Diptera: Cecidomyiidae), is a Nearctic pest with similar body color, size and morphology to the adult Anopheles mosquito (Tóth et al., 2009). O. robiniae is a monophagous species, with specialized feeding on Robinia species, such as, R. pseudoacacia L, R. hisqida L, R. pseudoacacia Aurea. The gregariously feeding larvae cause the margins of the leaflets to thicken and to bend downwards, forming the characteristic leaf margin roll galls (Shao et al., 2010; Wermelinger and Skuhrava, 2007; Zang, 2015). This insect causes harm throughout the year, from the initial leaf development of the black locust (Robinia pseudoacacia) to the fall of its leaves in winter, hindering leaf photosynthetic processes and causing early leaf abscission. Consequently, this leads to a decline in the tree growth and productivity, thus affecting the economic, ecological efficiency, and ornamental value of the black locust. Moreover, these injuries facilitate the attack by secondary pests such as longhorn beetles and jewel beetles, which eventually causes the death of trees (Glavendekić et al., 2009; Yao et al., 2015).

In the 19th century, O. robiniae was first described as Cecidomyia robiniae in Pennsylvania (USA) (Haldeman, 1847). Its habitat was restricted to North America, and O. robiniae did not receive much attention until its discovery in Asia in 2002 (in Japan and Korea) and later in Europe (Italy) in 2003 (Duso et al., 2005; Kodoi et al., 2003; Uechi et al., 2005; Woo et al., 2003). In Europe, O. robiniae has been spreading faster than expected, with 26 European countries recently reporting infestations (Bálint et al., 2010). From 2003 to 2006, O. robiniae moved approximately 2000 kilometers eastward from Veneto in Italy to Donetsk, Ukraine (Berest and Titar, 2007). In 2007, it reportedly crossed the English Channel to Oxford, England (UK) in Western Europe (Skuhravá et al., 2007). A year later, in 2008, it was found in Sweden's Lund in Northern Europe, showing a tendency for O. robiniae spread eastward (Molnar et al., 2009). In China, O. robiniae was discovered in Qinhuangdao, Hebei Province in 2004 (Yang et al., 2006). After that, an explosive spread occurred throughout China, and the species was detected in Northeast Liaoning in 2005 (Wang et al., 2006); it also spread to Jilin, Beijing, and Shandong in 2006 (Mu et al., 2010; Yan et al., 2007; Zhang et al., 2008). Currently, it has been detected in 17 provinces (municipalities/ autonomous regions) of China, which are roughly distributed within the range of 26.59°-43.98°N and 103.80°-121.25°E, at an altitude of 8.05m-1561.33 m.

Zhang et al. used the CLIMEX model to predict and analyze the potential geographic distribution of O. robiniae in China. The quantitative analysis of the pest risk conducted by these researchers predicted that the risk value in China was 2.26, which represented a highly dangerous organism according to the International Plant Protection Convention (IPPC) of risk values (Zhang et al., 2009). Zhao et al. analyzed the current and future (2050s) changes in the areas suitable as O. robiniae habitat in China by using the maximum entropy model. They found that the future habitat is larger than the total habitat range under the current climatic conditions, and the main factor for this increase was the expansion of the highly and moderately suitable areas (Zhao and Shi, 2019). Due to the limited previous research and scarce data of its real spread, O. robiniae was then considered to be still in a state of diffusion. Here, we present our survey of the occurrence of O. robiniae in China, with more complete occurrence records and updated global climate data collected from v1.4 to v2.1 of the WorldClim database in 2020 (Fick and Hijmans, 2017; Hijmans et al., 2005). The most significant feature of the WorldClim v2.1 is that it contains historical climate data from 1970 to 2000. The prediction future climate data adopts the Coupled Model Intercomparison Project Phase 6 (CMIP6), which adopts four shared socio-economic pathways (SSPs) for climate change scenarios. SSPs can determine accurately the correlation between socio-economic development and climate scenarios; furthermore, the novel SSP370 program was recently created, which considerably facilitates the achieving of this purpose (Jiang and O’Neill, 2017; Kriegler et al., 2012; Moss et al., 2010). The CMIP6 model is better than CMIP5 in many aspects (Saha et al., 2021), such as improved prediction accuracy of the temperature variables by 5–15%. The following global cross-validation correlation values were determined: temperature and humidity ≥ 0.99, precipitation = 0.86, and wind speed = 0.76, The simulation results of CMIP6 were closer to the data of the actual observations (Fan et al., 2020; Nie et al., 2020), which provided an opportunity for the update and improvement of the prediction of the potential distribution range of O. robiniae.

Using the maximum entropy model and new climate data, combined with the results of our observations in China, in this study, we aimed to predict the current potential distribution (CPD) of O. robiniae in Eurasia and its future (years 2050s and 2070s) potential distribution (FPD) change trend. Furthermore, we determined the dominant climate factors influencing the distribution of O. robiniae. Our findings provide an important reference and guidance for the current and future control and quarantine of O. robiniae by forestry and customs quarantine authorities.

Species occurrence data and environmental variables

We identified the availability of 1008 occurrence records of O. robiniae in the Eurasia: (1) All occurrence records collected in China originated from our field survey; finally, 125 occurrence data of O. robiniae were recorded in 26 cities in 15 provinces (municipalities/ autonomous regions); (2) The data of the distribution points outside China were derived from the Global Biodiversity Information Facility (GBIF, https://www.gbif.org/) (648 records) and published in the literature statistics (236 records) (Fig. S1).

The climate data were downloaded from the WorldClim website (http://www.worldclim.org). The Global Climate Data Version 2.1 with a resolution of 2.5 minutes was employed. It included a total number of 19 bioclimatic variables (Table S1). The bioclimatic variables were derived from analyses of the annual trends and biologically significant parameters obtained from seasonal temperature and rainfall data values, which are essential for the species survival in a habitat. These climatic parameters were used ecological research to assess the impact of climatic conditions and their possible distribution (Ashoori et al., 2018; Fois et al., 2018).

To comprehensively evaluate the changes in the potential suitable areas of O. robiniae in the future periods, namely years 2041–2060 (2050s) and 2061–2080 (2070s), we used three different global climate models (GCMs): BCC-CSM2-MR, CNRM -CM6-1, and IPSL-CM6A-LR(Tang et al., 2022). We implemented the GCMs from the CMIP6 of the sixth assessment report (AR6) of the Intergovernmental Panel on Climate Change (IPCC). Three Shared Socio-economic Pathways (SSPs) were selected for each of the GCMs: SSP245 (Fricko et al., 2017), SSP370 (Fujimori et al., 2017), and SSP585 (Kriegler et al., 2017). Then, these three SSPs emission scenarios were considered to represent a low-forcing, medium-forcing, and high-forcing scenario of climate change with economic development.

Optimization of the model parameter

MaxEnt software is an ecological niche model based on environmental variable layers and species occurrence records. It integrates machine learning and the principle of maximum entropy to simulate the potential geographic distribution of species (Phillips et al., 2006). To reduce the sampling bias due to oversampled areas, we calibrated the CPD for each species by filtering the specimen records to the spatial resolution of the environmental layers used (2.5 arc-minutes), resulting in one record per cell (Martínez-López et al., 2021). By this approach, we obtained 659 points after filtering.

There is a certain correlation among the 19 bioclimatic variables, and too many variables increase the dimensionality of the ecological niche, thereby affecting the prediction performance and accuracy of the maximum entropy model (Sillero, 2011; Verbruggen et al., 2013). Next, we used the ArcMap version 10.3 (ESRI, Redlands, CA, USA) software to couple the 19 bioclimatic variables with 659 occurrence records to perform Pearson's correlation analysis (Fig. S2); we removed the climate layer with a low biological significance in the high-correlation variable group, and filtered out 10 environment layers (Table S1).

Further, we conducted our first exploratory analysis using MaxEnt version 3.4.4 (results not shown) and the “ENMTools” package in R, version 4.0.5 (https://www.r-project.org/), to adjust and optimize the feature combination (FC) of the MaxEnt and regularization multiplier (RM) β parameters. Hence, we effectively reduced the complexity of the model and improved the degree of fit between the predicted and actual results. The β multiplier settings of 0.1-5, and 0.5 gradually increased. The FC included linear (L), quadratic (Q), hinge (H), product (P), and threshold (T).We tested eight different FC combinations, including L, LQ, LQP, QHP, LQH, LQHP, QHPT, and LQHP (Martínez-López et al., 2021; Merow et al., 2013; Radosavljevic and Anderson, 2014), and obtained the corrected Akaike Information Criterion (AICc) of different parameter combinations. We then selected the minimum value of the AICc as the optimal setting and established the model (Fig. S3a) (Warren and Seifert, 2011).

To assess its predictive performance, the species occurrence records were utilized for model calibration by their division into a training set (75% of the total occurrence records) and a test set (25% of the total occurrence records). The relative probability calculated for each grid is used here as the relative habitat suitability of O. robiniae. To improve the accuracy of the prediction results and reduce the level of uncertainty, subsample validation was set up in the model, and 10-fold repetitions were performed to obtain average results. Then, the response curves and jackknife were created to measure the importance of the variables, removing climate variables with low contributions to obtain the final six climate variables (Table S1) (Negrete et al., 2020).

To minimize model overfitting, Principal-component analysis (PCA) of the climate variables was performed to estimate the heterogeneity of six bioclimatic variables using ArcMap software (ArcToolbox: SDM Tools). We aimed to ensure that the occurrence records were spatially independent, thereby reducing the over-fitting of the model to environmental biases. Next, we performed spatial filtering based on the value of the environmental heterogeneity, and finally obtained the occurrence records (Fig. S1) (Boria et al., 2014; Brown et al., 2017).

The performance of the Maxent model was evaluated by the Receiver operating characteristic (ROC) method and the area under the curve (AUC) was calculated as a measure of the prediction accuracy. The AUC values > 0.5 imply a better than random fit, with 0.9 < AUC < 1 representing high predictive ability.

Classification of CPD and FPD

A second construction of the model using the selected occurrence records and bioclimatic variables was used for the development of CPD maps and 18 FPD maps for the prediction of O. robiniae spread (Fig. S4 and S5). To balance the differences between GCMs and present a trend for a higher likelihood of FPD occurrence (Zhou et al., 2021), we averaged the results of these three GCMs for SSP126, SSP370, and SSP585, respectively, and finally obtained six CPD maps (years 2050 and 2070) for different SSPS scenarios of O. robiniae spread.

We used the lowest presence threshold (LPT) to define the suitable and non-suitable areas (Pearson et al., 2007). The potential area distribution was divided into four categories, including unsuitable (0-LPT), marginally suitable (LPT-0.4), moderately suitable (0.4–0.6), and highly suitable (0.6–1.0) areas. We used the ArcMap 10.3 software “ArcToolbox: Spatial Analyst Tools” to analyze the changes in the CPD and FPD areas and the centroid movement trend.

We constructed the current model using 248 occurrence records of 6 bioclimatic variables, FC for LQHP and RM of 0.5 (Fig. S3c), which showed very good performance (AUC = 0.952 ± 0.005) (Fig. S6b) and the LPT of 0.043.

The most important bioclimatic variables that determined the potential distribution of O. robiniae were the Annual Mean Temperature (Bio1), Annual Precipitation (Bio12), and the Precipitation of the Driest Month (Bio14). The total contribution of these three climatic factors was 86.6% (Table 1). The response curve (Fig. S7b-d) showed that the climatic suitability of O. robiniae had a unimodal relationship with BIO1 and BIO12, while the BIO14 had two peaks at 2.80mm and 46.93mm. For the BIO1, the range of the highly suitable for O. robiniae was 8.31°C -12.31°C, with the standard deviation was 1.17°C. For the BIO12, the range of the highly suitable was 632.99mm -1392.57mm, the standard deviation of the BIO14 was 18.5mm. The future values of these three layers were larger than the current values, with a wider range and an average increase of 9.7% (Table S2). According to Jackknife (Fig. S7a), a shorter green band indicates that the environmental variable has more information than other variables; in this case, the influence on the species distribution is greater. As can be seen in the figure, Bio1, Bio3, and Bio15 provided more information specific to the prediction of the distribution area of O. robiniae and were thus indispensable.

Table 1

MaxEnt results of the percentage contribution and permutation importance of Bioclimatic variables for the selected model developed for *O. robiniae.*
Code	Environmental variables	Percent contribution	Permutation importance	AUC
BIO1	Annual Mean Temperature	59.2	59.4	0.91
BIO12	Annual Precipitation	14.3	8.1	0.84
BIO14	Precipitation of Driest Month	13.1	0.9	0.84
BIO3	Isothermality	5.5	15.2	0.84
BIO15	Precipitation Seasonality	4.9	7.9	0.74
BIO6	Min Temperature of Coldest Month	3.0	8.5	0.89

The total CPD area of O. robiniae in Eurasia was 10,896,309.16 km² (Figs. 1 and 3), with suitable areas covering a substantial section of Europe. The moderately and highly suitable areas (orange and red) were predominant, reaching 38.91% of the total European land, including most of Western Europe (the central and southern parts of the United Kingdom, the north of Spain, France, Germany, etc.), the southwestern region of Central Europe (southwestern Poland, Hungary, etc.), the north of Southern Europe (the south of Romania, the north of Greece, Serbia, etc.), a small part of Northern Europe (Denmark and south of Sweden), and Eastern Europe, mainly in the plain area on the east side of the Black Sea. In Asia, Turkey and northern Iran in West Asia, and southern Kazakhstan and eastern Uzbekistan in Central Asia, were suitable areas, but with a relatively low degree of fitness. The highly and moderately suitable areas were distributed mainly in East Asia, the eastern part of Japan, the southwest of the Korean Peninsula, and in northeast China (Liaoning Province), north China (Beijing, Tianjin, Hebei, Shandong, etc.), and southwest China (Guizhou Province, Sichuan Province, etc.). The O. robiniae suitable area in West Asia was closely associated with that in Europe. To assist our research and minimize fragmentation of the suitable areas, our next study divides the potential distribution areas into two categories, namely, the suitable areas in Europe and Western Asia ( EWA ) are divided into one category, and the other is composed of East Asian countries.

The results of the MaxEnt model obtained under the future climate change scenarios SSP245, SSP375, SSP585 for 2050s and 2070s are presented in Fig. 2. It can be seen that, compared with CPD, in the same year of FPD, the total suitable area of O. robiniae becomes larger with the increase in the radiative force in the SSPs emission scenario. Similarly, in the same SSPs emission scenario, the suitable area in 2070 would be larger than that in 2050 (Fig. 3). The marginally suitable area occupied the main part, followed by the highly suitable area. Except for 2070-SSP370 and 2070-SSP585, the moderately suitable area was more than the highly suitable area. The largest FPD area was under the scenario of SSP585 in 2070. The total area was 34.87% larger than that of CPD, reaching 14,696,253.77 km², mainly due to the expansion of the marginally and moderately suitable areas, which increased by 43.15% and 35.91%, respectively. As can be seen in Fig. 2 in the future, the moderately and highly suitable areas for O. robiniae habitats would continue to spread northwards in Eurasia. In EWA, the west coast of Norway, Poland, the central and western parts of Ukraine, and the southern part of Belarus and Sweden would become the new worst-hit areas by O. robiniae spread. In East Asia, Japan and South Korea would gradually become marginally suitable areas as O. robiniae habitats. In China, the moderately and highly suitable areas would gradually decrease in the southwest, and the three northeastern provinces would gradually become the worst-hit areas. Although the CPD of O. robiniae generally tended to spread northwards, subtle differences existed between EWA and East Asia. In EWA, the expansion of the moderately and highly suitable areas was predominant, whereas in East Asia, the growth of the marginally suitable sites was dominant, and the moderately suitable areas were declining.

Figure 4 illustrates the trends of the expansion and contraction of CFD of O. robiniae, mainly showing large-scale expansion in the north (red) but small-scale reduction in the south (blue). The central and southern parts of Spain and most of the southern parts of China would gradually become non-suitable areas. However, the European Alps, the Taurus Mountains in West Asia, and the Hexi Corridor in China, which are currently unsuitable areas, would gradually increase the suitable areas of O. robiniae. Combined with the trend of centroid change (Fig. 5), it can be seen that the centroid of FPD in East Asia and EWA shifted to the northeast, whereas the centroid of East Asia was altered to the northeast of China (azimuth angle 20.03 ± 7.6°), and the centroid in Europe changed at a larger angle, mainly towards central Russia (azimuth angle 40.10 ± 4.74°). With the enhancement of the SSPs emission scenarios, the FPD centroid offset distance was also increasing. The farthest EWA SSP585 scenario in 2070 was 773.81 km from the current centroid. At that time, the O. robiniae suitable area would cross the Ural Mountains, reaching the West Siberian Plain.

The assessment and prediction of impact of invasive alien species on a global scale have attracted considerable research attention (Tingley et al., 2014; Zhu et al., 2020). O. robiniae, originating from the Nearctic region, has invaded almost simultaneously from the eastern and western parts of Eurasia at the beginning of the 21st century and then spread explosively mainly due to the perception that it did not pose a major risk to forest stands, frequent trade activities, and the widespread presence of its host R. pseudoacacia (Tóth et al., 2009; Tóth et al., 2011). However, our research discovered that human negligence was the major cause for its spread in almost every corner of the distribution of R. pseudoacacia in China. It is distributed not only in the coastal protective and timber forests, as well as other forest lands, but is also widely distributed in urban corners such as university campuses, wetland parks, and residential neighborhoods. O. robiniae is reproduced illegally in China. A compound leaf can contain a maximum of 54 galls, and a maximum of 18 larvae can feed gregariously within each gall, leading to damage rates reaching 90–100% in July and August (Bakay and J., 2010; Han et al., 2010; Wang et al., 2006). The infestation of O. robiniae, which perms the crown of black locusts into "curls", has a serious ecological and socio-economic impact. Furthermore, its distribution range continues to expand outwards, reaching the city of Lanzhou in 2017 (It had previously spread only to Tianshui in western China). Although O. robiniae is a newly introduced species, it is already a common insect, because of its unique galls and exclusive host features, which make its identification easy and accurate; it can be easily found by careful observation of black locust leaves (Петров, 2019). To prevent the further spread of O. robiniae, it is essential to identify the main climatic factors influencing the distribution of O. robiniae and to predict the potential distribution area. MaxEnt software has high reliability as a model for predicting the potential distribution area of species (Peterson et al., 2007).

Analysis of model results and CPD

We have completed the first study of the potential range of O. robiniae distribution in Eurasia using MaxEnt software, based on literature evidence and data obtained from GBIF and a comprehensive field survey conducted in China. Through relevant screening of the available occurrence records, optimization of bioclimatic variables, and adjustment of model parameters, the performance of the present MaxEnt model was confirmed to be good; the ROC curve and omission rates (Fig. S6) objectively validated these results.

In this study, the suitable and non-suitable areas were defined by the LPT, indicating that the CPD of O. robiniae was distributed between 21.58–48.05°N in East Asia and between 34.96–65.66°N in Europe. The results showed that the distribution of O. robiniae was strongly driven by three factors: Annual Mean Temperature (Bio1), Annual Precipitation (Bio12), and Precipitation of the Driest Month (Bio14). The most suitable climate for O. robiniae breeding is under the following values of the main factors: Bio1 = 9.42°C, Bio12 = 798.15 mm, and Bio14 = 46.94 mm (Fig. S7b-d). These results were in line the data obtained from our survey in China where O. robiniae was heavily infested, and in which we found that not only the degree of harm caused by O. robiniae in semi-humid, semi-arid, and warm areas was serious, but also the number of the larvae in a single gall was significantly larger. These areas were also areas with strong germination and tillering abilities of the host black locust, highly overlapping with the moderately and highly suitable areas of the CPD of O. robiniae. Because adults only lay eggs on newly sprouted leaves, these areas also provided facilities and chances for the prolific expansion of O. robiniae.

We used climate data collected from the latest WorldClim Version 2.1, but, compared with the current period (2021) released at the time of manuscript preparation, there was still a lack of 20-year data, and a remarkable trend in the climate warming is observed for the period from 2000 to present time(Fan et al., 2021; Wu et al., 2019), so the predictive result of the CPD of O. robiniae is rather conservative. In addition, the host black locust is widely planted in parks, roadsides, and other areas in many countries: sites that are significantly influenced by human management. For example, we found planted black locusts in residential quarters and parks in Turpan, Xinjiang, China. By human management, a microclimate suitable for its growth was created, which promoted the growth of these black locust trees. This unique artificial microclimate (Bakay and Kollár, 2014), combined with the biological characteristics of O. robiniae larvae, whose supercooling point is -12.19°C (data not published) and that overwinter as cocoons in the soil, would certainly facilitate their successful future establishment and spread in Turpan. The aforementioned two points inferred that the suitable area of O. robiniae in Eurasia was wider than the CPD range predicted.

Analysis of the trends of the FPD of O. robiniae

In 2050s and 2070s, along with global climate warming, the FPD of O. robiniae would continue to expand in the Eurasian continent, mainly to the north. The average suitable area in 2050 would increase by 14.72 ± 4.26% compared to the CPD area, and the area in 2070 would be expanded by 8.56 ± 7.81% compared with the area in 2050, dominated by an increase in the marginally and moderately suitable areas. These results show that O. robiniae is a beneficiary of climate warming. Although the southern regions of China and Spain would no longer be suitable for O. robiniae due to high temperature and humidity changes in the future, the reduced area is far less than the increased area to the north (Fig. 4), with the largest expansion in EWA, averaging 1,607,771.89 km², 3.23 times larger than the area of growth in East Asia. Similar results were obtained in the shifts movement of the centroids. The average moving distance of centroids in EWA in 2070 was predicted to be 554.98 km, which is 23.77% more than the offset distance of centroids in East Asia. Currently, O. robiniae has covered the black locust planting area on a large scale in the Eurasian continent, and its FPD expansion trend is highly coincident with the FPD expansion trend of black locust in Europe (Puchałka et al., 2021), which provides an opportunity for the explosive spread of O. robiniae into a large area in the future.

The impact of climate change on the distribution of species is becoming increasingly more significant. IPCC AR6 has performed a large number of scientific assessments and concluded that the recent global warming has been more widespread, faster, and more intense than that observed for thousands of years (CLIMATE(IPCC), 2020). Studies have shown that changes in the trend of FPD may appear earlier than previously expected. For example, black locust seems to have a high potential to adapt to changes in climatic conditions, and its potential distribution in Eastern Europe may increase 20 years earlier than previously predicted (Klisz et al., 2021). Although we have not yet found any infestation of O. robiniae in Heilongjiang Province, China (Changchun, Jilin Province, has the northernmost occurrence records in China.), during our surveys we established that the local semi-humid environment may be suitable for O. robiniae colonization, which also requires regular observations of the margins where O. robiniae has been recorded to occur. It is likely that in this year it has already spread 200 km outwards.

Final considerations and quarantine management measures

O. robiniae is a monophagous pest that solely attacks the black locust, which is also native to North America. Black locust is considered a problematic woody plant. It has long been controversy whether the black locust is a beneficial plant. As a result, whether O. robiniae is an invasive species is likewise debatable. Robinia pseudoacacia is regarded a contributor to forest stand and biodiversity degradation in several European countries, and it has a vast and aggressive root system (Rumlerová et al., 2016), and has even been blacklisted in some European countries, including Switzerland, Norway, the Czech Republic, Italy and Germany (Vítková et al., 2020). However, black locust is also useful for social development, as a supplementary fodder source for the animal industry, as a quality timber plant, and as a rehabilitation plant for reclaimed mining areas, etc. (Filcheva et al., 2000; Vítková et al., 2017). In Hungary, R. pseudoacacia occupies 24% of the country’s forest area and provides 25% of the annual wood production (Honfy et al., 2021; Tobisch and Kottek, 2013). In South Korea, R. pseudoacacia provides more than 70% of the honey production, accounting for a large proportion of farmers’ income (Kim et al., 2021). In China, R. pseudoacacia is a pioneer tree species used for afforestation in the arid areas of North China and Northwest China, which is of great significance for ensuring ecological security (Yin et al., 2014). There are also industrial and medical studies on green corrosion inhibitor and antioxidant, cytotoxic and antitumor activities of black locust fruit and flower extracts (Bratu et al., 2021; Pourzarghan and Fazeli-Nasab, 2021). Furthermore, society accepts black locust as an internal part of the landscape (Fischer et al., 2011). Therefore, black locust can more likely be considered to be a deliberately introduced alien species, which is now naturalized. However, O. robiniae is more like a "stowaway," the high-level infestation of black locust by O. robiniae has directly or indirectly caused serious ecological and economic impacts. It can be classified as an alien invasive species; China has listed it as a quarantine object (Mihajlović et al., 2008).

Although many species can spread on their own, biological invasion also has an anthropogenic factor, and long-distance dispersal is often caused by or related to human activities (Gilbert et al., 2005). For example, motorway networks are involved in the distribution of O. robiniae. The transportation of black locust with larvae is an important source of the long-distance transmission of O. robiniae, and the adults or the infected leaves may be disseminated by the wheels and other parts of motor vehicles (Pernek and Matošević, 2009). In our investigation, we found that the numbers of O. robiniae individuals in cities and villages were not significantly different (Bakay and Kollár, 2014), abundant pest occurrence was observed on isolated hills or small islands in the middle of lakes, for which the wind might have played a leading role due to the weak body of adults (Duso et al., 2011). This spread was also closely related to the exponential growth of the population during the growing season and the large-scale cultivation of black locust.

Currently, the natural enemies of O. robiniae include predatory insects such as lacewing, ladybeetle, and crickets(Tóth et al., 2011; Yu et al., 2009), as well as parasitic insects- Platygaster robiniae Buhl and Duso, Systasis obolodiplosis Eulophidae, Genus Systasis Walker species, etc. (Tóth et al., 2011; Yao et al., 2009), among which Platygaster robiniae occupies a dominant position in parasitic wasps. It has been detected in European and East Asian countries, where it is considered to be among the key factors that reduce the population density of O. robiniae (Bella, 2007; Buhl and Duso, 2008; Lu et al., 2010). However, the outbreak period of Platygaster robiniae lags behind that of O. robiniae, and its role in population reduction is exerted mainly from the 3rd O. robiniae generation and thereafter. Even when O. robiniae is parasitized, parasitic wasps would delay the development stage, staying in a prolonged egg stage or embryonic period until the host larva has almost fully grown, and would not prevent the leaves from curling and forming galls; thus, an ideal control effect cannot be achieved (Kim et al., 2011). We believe that, in addition to biological control, human intervention is necessary to prevent the spread of O. robiniae. Due to the protection to O. robiniae provided by the gall during the vegetation period and the high reproductive power of females, early prevention and control can be more effective as management strategies. Therefore, winter and spring are the key periods when prevention and control should be realized. After the leaf fall of black locust at the end of October, the fallen leaves should be timely cleaned, burned, and buried to prevent larvae overwintering. In spring, the leaf-expansion period of black locust is also a peak period of overwintering adult emergence. Sprays with systemic insecticides are also an effective approach against the spread of the pest. The main strategies for pest management are the control of the total occurrence of larvae, achieving a reduction in the population density and the occurrence base of pests, and obtaining one-time protection ensuring no harm throughout the year (Mu et al., 2010; Park et al., 2009).

Climate warming causes the spring phenology of plants in most parts of the world to be ahead of schedule, such as leaf bud opening, leaf spreading, and flowering, which further affects predator activities (Fitter and Fitter, 2002; Ma et al., 2021). O. robiniae is a beneficiary in this respect. It is an adaptive multivoltine insect whose numbers of generations change with the alterations in the temperature and host. In Europe, a number of 2–4 generations a year is common, whereas seven generations a year were observed in Lunan area of China. With climate warming, the abundance and destructive activities of O. robiniae will increase, which will reduce the growth rate of black locust in large areas (Bella, 2014; Zhao et al., 2011). Although it seems that O. robiniae has not reached the status of pests until now, this status may change over time. Hence, its future occurrence and possible economic importance should be carefully monitored. The rapid spread of O. robiniae is due to its fast reproduction and wide spread of its host. Similarly to the current coronavirus disease 2019 (COVID-19) pandemics, it has a greater potential impact on human life and natural environment. Its control or eradication after its invasion and spread have started are extremely difficult and costly(Vaes-Petignat and Nentwig, 2014). Therefore, it is strongly recommended that corresponding control measures have been promptly undertaken, based on the predicted FPD trend of O. robiniae distribution, to prevent its further spread.

This study was based on a field survey of O. robiniae in China, a thorough understanding of the biological characteristics of O. robiniae, and the development of various models through appropriate parameter screening, breaking the limitations of previous modeling based solely on literature or database occurrences. The results of the existing and projected future appropriate regions show that O. robiniae will benefit from global warming. Temperature is the primary predictor of O. robiniae distribution. A large-scale northward expansion tendency with temperature elevation characterizes the region suited for O. robiniae habitat. Our investigation found that human neglect was the primary source for O. robiniae spread in almost every corner of the distribution of R. pseudoacacia in China. It has a bigger potential impact on human life and the natural environment, similar to the current COVID-19 pandemics. Controlling or eradicating it after its invasion and spread has begun is exceedingly tough and costly. The existing and future possible distribution and change patterns of O. robiniae are more intuitively described by ecological niche models. This information would help the forestry quarantine departments of Asian and European nations provide early warnings about the probable distribution regions of O. robiniae, as well as offer a scientific basis for the prevention and control of O. robiniae spread and outbreaks.

Author contributions

JZ and JS conceived and designed research. JZ collected the data sets. JZ,TG and JD analyzed data. JZ wrote the manuscript. All authors read and approved the manuscript. JS made the corrections.

Acknowledgments

We appreciate Yanxia Yao of the Research Institute of Forest Ecology，Environment and Protection, Chinese Academy of Forestry for assisting us with field survey and sampling in China, as well as Yuqian Xiao for her direction and assistance with mapping. The editor and reviewers are deeply thanked for their helpful and valuable comments, which helped enhance this work. This study was supported by the National Key Research and Development Program of China (2021YFC2600405) and the General Program of National Natural Science Foundation of China (31770687).

Data Availability Statement

The Global Climate Data Version 2.1 dataset was acquired from https://www.worldclim.org/data/index.html.The data used in this study are available at https://zenodo.org/record/6326587#.YiGCwMiKvZs.

Conflicts of Interest

The authors declare no conflicts of interest.

Supplementary Data

Supplementary data to this article can be found online at version of this article.

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No competing interests reported.

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Obolodiplosis robiniae Will Infect All Black Locust In Eurasia Under Climate Change

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Abstract

Figures

Key Message

Introduction

Material And Methods

Species occurrence data and environmental variables

Optimization of the model parameter

Classification of CPD and FPD

Results

Discussion

Analysis of model results and CPD

Final considerations and quarantine management measures

Conclusions

Declarations

References

Competing Interests

Supplementary Files

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