After the recent high-impact European outbreaks of Xylella fastidiosa (Xf), a xylem-limited plant pathogenic bacterium native to the Americas, this research aims to rank the risks of potential entry, establishment and spread of Xf in new countries across Europe, the Middle East and North Africa. A novel risk-ranking technique is developed, based on combining entry risk drivers (imported plants, direct flights and ferry connections) with risk factors related to establishment and spread (presence of potential insect vectors, vulnerable economic crops, alternative hosts and climate suitability) of this pathogen. This reveals that western European countries have the highest risk for entry, but that the Mediterranean basin runs the highest risk for establishment and spread of Xf. Lebanon in particular has the highest level of risk for Xf dispersal within its suitable territory. Countries without current outbreaks combining high risks of Xf arrival and establishment are mainly in the Mediterranean basin: Turkey is at the highest level of risk, followed by Greece, Morocco and Tunisia, which are ranked at the high level. The ranking model also confirms the vulnerability, in terms of invasion by Xf, of southern European countries (Italy, Portugal and Spain) in which the pathogen has already been reported. High summer temperatures in these southern countries are likely to be the significant determinant for the overall invasion process, while northern European countries have a high level risk for the arrival of the pathogen, but relatively low summer temperatures may limit establishment and spread of major outbreaks. In general, our study provides a useful approach for mapping and comparing risks of invasive non-native species and emerging pathogens between countries, which could be useful for regional horizon scanning and phytosanitary and biosecurity management.

alien species, biological invasion, entry, dispersal, plant bacterium, risk drivers

Global trade networks are implicated in increasing rates of global spread of plant diseases through transport of live plants and other plant-related products (Chapman et al. 2017). The plant pathogenic bacterium Xylella fastidiosa (hereafter Xf) is an important example of this process. Originating in the Americas, this plant pathogen has recently been detected for the first time in several European and Near Eastern countries: Italy in 2013 (Saponari et al. 2013), France in 2015 (Denancé et al. 2017), Switzerland in 2015 (European and Mediterranean Plant Protection Organization 2015), Spain in 2016 (Olmo et al. 2017), Germany in 2016, Portugal in 2019, and more recently, Israel in June 2019 (European and Mediterranean Plant Protection Organization 2016, 2019a, b). This dangerous non-native pathogen causes several devastating plant diseases that have huge socio-economic and ecological impacts, motivating risk assessment for the entry and spread of Xf into new countries (European Food Safety Authority 2019).

Following detection of Xf outbreaks in Europe, the EU and some Middle East and North African (MENA) countries have implemented several risk reduction options to combat this plant disease and prevent its entry and spread. Despite these actions, there remains a risk that Xf will continue to spread to new countries and regions through the movement of infected host plants (asymptomatic or unknown hosts) or via unintentional transport of insect vectors through equipment as a commodity contaminant or vehicle “hitchhiker”. This transport risk is likely to be highest in countries with well-developed transport links to current outbreak areas (Chapman et al. 2017). However, transport connectivity will only present a serious risk of damaging outbreaks if there is also a suitable climate and land use to support the establishment and spread (Early et al. 2018). Therefore, there is a need for an overall country-level risk ranking for Xf simultaneously across the EU and MENA region which would allow the selection of priority countries for more detailed country-specific pest risk analyses.

As such, we aimed to rank the likelihood of potential invasion by Xf of new countries in these regions, and to provide an overall risk rating by combining rankings for entry, establishment and spread in order to assess each country’s overall vulnerability to Xf invasion. Over the past 20 years, there have been several model frameworks and studies of alien species risk assessment at an individual-country scale. These include invasive alien species risk assessment in Great Britain (Mumford et al. 2010), risk assessment simultaneously prioritizing the control of invasive plant species and the conservation of rare plant species in the USA (Miller et al. 2010), risk assessment models for invasive species and uncertainty in rankings from multi-criteria analysis in Australia (Benke et al. 2010), a weed screening tool for the US (Koop et al. 2011), generic ecological impact assessments of alien species in Norway (Sandvik et al. 2013), risk screening tools for potentially invasive plants, animals and their pathogens in Belgium (D’hondt et al. 2015), and development of a plant risk evaluation tool to assess the invasive potential of ornamental plants (Conser et al. 2015). In contrast to these country-specific assessment, only a few studies assess risk across multiple countries, for example the EPPO prioritization process for invasive alien plants (Brunel et al. 2010), the new protocols for assessment of the environmental impact of pests in the EPPO decision support scheme for pest risk analysis (Kenis et al. 2012), guidance on environmental risk assessment of plant pests (European Food Safety Authority 2010), and the generic impact scoring system (Nentwig et al. 2016) in Europe. Moreover, a few protocols regarding alien taxa have been developed at the global level, such as the framework and guidelines for implementing the proposed IUCN (International Union for Conservation of Nature) environmental impact classification for alien taxa (Hawkins et al. 2015).

Concerning Xf, the few published studies that have performed risk assessment for this biological invader are limited to one country (Afechtal et al. 2018), one region (European Food Safety Authority, 2015, 2018, 2019; Godefroid et al. 2019;) or a subset of territories (Bosso et al. 2016) mainly based on climate suitability indicators. Thus, the novelty of the current research is to integrate multiple Xf risk drivers (i.e. plant trade, human movements, insect-vectors, host-plants, temperature suitability) and simultaneously ranks all countries in Europe and MENA region in a way that is useful for decision makers. In addition, these selected ranking variables (Table 1) are quantitative (except for vectors), objective (i.e. based on statistics and not on expert opinions), transparent, consistent, sufficiently specific, and available simultaneously to all the countries concerned. By quantifying these risk drivers with best available scientific evidence, the proposed approach is simple to apply and may be used as a conceptual framework in rating-based risk assessment of other pests to support policy for appropriate and efficient biosecurity management of Xf and other invading pests.

The risk indicators used in the ranking are shown in Figure 4. Factor analysis on these transformed indicators produced an adequate description of their multivariate pattern. Bartlett’s test of sphericity showed significant correlation among risk drivers (χ² = 305.2, df = 45, P < 0.001), while the Kaiser-Meyer-Olkin statistic had a value of 0.695, which is above the 0.5 threshold that is usually accepted for adequate explained variation.

Figure 4.

Maps of the risk indicators used for ranking potential for Xf entry (ENT) and establishment and spread (EST) as described in Table 1.

The loadings table (Table 2) shows high positive loadings for entry risk variables on the first factor, except for direct ferry lines (ENT₆), while none of the entry factors loaded strongly on the second factor. By contrast, establishment and spread risk drivers loaded strongly on the second factor, except forest cover, but not on the first. Given this structure, the first factor was interpreted as a latent variable associated with entry, and the second factor interpreted as a latent variable indicating risk of establishment and spread.

Entry risk

Figure 5 displays the ranking of Europe and MENA countries according to the entry risk drivers. Most western European countries have high values of most entry risk indicators (Fig. 4) and as such have the highest overall entry risk. Most MENA countries appear less exposed to entry risk factors, except for Tunisia, Morocco, Jordan, Kuwait, Saudi Arabia and the UAE, where the entry risk level is high.

Figure 5.

Rank categorization of Europe and MENA countries according to the six entry risk drivers of Xylella fastidiosa in relation to the importation of plants for planting, direct air flights and ferry traffic.

Establishment and spread risk

Figure 6 shows the ranking of Europe and MENA countries according to the four establishment and spread risk factors relating to insect vectors, host plants and climate suitability (see also Fig. 4). Among the establishment and spread risk indicators, suitable crops and summer temperatures were concentrated around the Mediterranean, leading to most Middle East and Mediterranean countries being classified at high to highest risk levels.

Figure 6.

Rank categorization of Europe and MENA countries according to the four establishments and spread risk drivers of Xylella fastidiosa in relation to vectors, vulnerable economical crops, alternative hosts and climate suitability.

In the MENA region, Lebanon is the only country at the highest level of risk, followed by Morocco, Tunisia, Egypt, Israel and State of Palestine which are classified at high risk level. Algeria, Jordan and Syria are ranked at the medium level risk, while the remaining MENA countries are at least risk rank for Xf establishment and spread. In Europe, Albania, Cyprus, Greece, Italy, Macedonia, Malta, Portugal, Serbia, Spain and Turkey are classified at highest risk level, while Iceland, Ireland and Norway are at least risk level.

Overall risk of exposure to invasion by Xf

When we combined the risk rankings for entry (Fig. 5) and establishment and spread (Fig. 6) using the matrix in Figure 2 the countries ranked as most vulnerable were Italy, Portugal, Spain and Turkey (Fig. 7). Additionally Greece, Morocco and Tunisia were ranked at a high risk level. Only three countries (Bahrain, Libya and Yemen) yield the least level of combined risk, although the risk was generally low in northern Europe and the non-Mediterranean Middle East.

Figure 7.

Overall rank categorization of Europe and MENA region according to exposure to invasion by Xf with respect to combined all entry, establishment and spread risk drivers and using the matrix of Early et al. (2016).

The threat of intentional or unintentional species movements leading to the entry and spread of invasive alien organisms is increased by international trade and travel (Tatem 2009; Early et al 2016; Chapman et al 2017). For Xf, recent outbreaks and interceptions of infected imported plants for planting in Europe show that Xf spreads to new countries via this pathway (European Food Safety Authority 2015). Most countries in Europe and the MENA region are increasingly connected with each other and with global sources of Xf in the Americas and Asia through the trade in imported plants and human travel. Given weaknesses in current phytosanitary regulations and airport inspection structures in parts of the region, especially in some MENA countries, it is possible that passengers could carry with them potentially infected planting material, or that transport infrastructure could accidentally carry Xf insect vectors. Consequently, there is a real risk that Xf may continue to overcome geographical barriers and infect new countries, potentially leading to major new disease outbreaks. Our assessment of the joint risks of Xf entry and establishment and spread therefore provides a useful approach for regional risk assessment by ranking the relative risk across 56 countries.

In particular our analysis identified a contrast between entry risk and the risk of establishment and spread. This was clearly seen in the factor analysis loadings, in which entry risk drivers loaded strongly on axis 1, while establishment and spread risk drivers loaded strongly on axis 2. Based on this, countries in western Europe and also Turkey tended to score highly for entry risk, principally because they import greater volumes of plants from infected countries in Europe and globally and had greater numbers of direct flight connections originating in infected regions. By contrast, risk of establishment and spread was ranked mostly based on the degree to which crops grown in a country are known to be susceptible to Xf and whether the summer temperature was apparently well suited to Xf colony growth. Presence of vectors was also weighted strongly in the factor analysis, but did not have a big influence on the results since nearly all countries had at least one potential vector species recorded as present (Fig. 4g). Countries with vulnerable crop types and summer mean land surface temperatures close to the optimum of 28 °C (Feil and Purcell 2001) were mainly located around the Mediterranean basin, where many countries were assessed to have low entry risk. The known world distribution of Xf is shown in the Suppl. material 5: Table S4.

Consequently, few countries were ranked very highly for both entry risk and establishment. Of those that were, three countries already have major Xf outbreaks, namely Italy, Spain and Portugal, whose outbreak was discovered after this study was conducted. Greece and Turkey were also ranked in the highest risk group but so far remain disease free. Güldür et al. (2005) reported the detection of Xf on seven almond trees uprooted in Turkey. However, following this detection, the Turkish National Plant Protection Organization declared that Xf did not occur in the country. Outside of the top-ranked countries, Morocco and Tunisia were ranked as high risk countries, on the basis that they scored fairly highly for both entry and establishment and spread. So far, Xf has not been detected in those countries. However, a pest risk analysis conducted for Morocco concluded that the overall likelihood of Xf spread in the country is very likely, providing support for our assessment (Afechtal et al. 2018). Interestingly, in our study France was ranked as medium overall risk, despite it having outbreaks on its south coast and on the Mediterranean island of Corsica. The primary reason for this is that France also includes more northerly regions with less suitable summer temperatures and less vulnerable crop types. Therefore, despite France clearly having areas at high risk of the disease, the national–scale resolution of the study reduced its overall risk ranking.

Our findings are broadly consistent with other risk assessment studies for Xf in Europe and MENA region. For example, data-driven species distribution modelling studies using a wider range of climate variables than we assessed generally confirm our simple mapping of temperature risk (Bosso et al. 2016; European Food Safety Authority 2019). For example, Godefroid et al. (2019) predicted the potential distribution of Xf subsp. fastidiosa in Spain, France, Italy, Croatia, Greece and Turkey, and the coastal regions of North Africa, which is consistent with our simple forward projections based only on an in vitro growth curve (see Suppl. material 1: Fig. S1). In addition there have been recent detections of Xf in some of the countries that we rated as high risk for establishment based on temperature and crop types. This includes Lebanon, in which Temsah et al. (2015) reported Xf on oleander, although Habib et al. (2016) disagreed with this finding. It also includes Israel, in which Xf is under containment after a recent detection on almonds in the Hulla Valley (European and Mediterranean Plant Protection Organization 2019b). By contrast, countries such as Germany, Switzerland and Netherlands were ranked as having low or medium risk for establishment and spread. In those countries Xf has been intercepted in trade or infected plants within protected indoor locations (consistent with their highest ranking for entry), but has not been able to spread to the wider environment (European Food Safety Authority 2019).

Regional risk assessment for high-impact invasive alien species such as Xf requires approaches that incorporate multiple risk drivers to simultaneously rank countries for multiple stages of invasion, such as the approach developed here. The world is increasingly connected by international plant trade and human travel, which are potential drivers of Xf entry into new areas where the presence of insect vectors, the abundance of host-plants as well as the climate suitability play an important role for its dispersal. As such our approach could be useful for both individual countries to understand their risk of Xf relative to other countries, and if applied across many different pests it could be useful to identify priority species. It is also useful for supra-national organizations interested in Plant Health (i.e. EPPO, EFSA, and EU) who can use country-level risk rankings to prioritize phytosanitary resources among countries. In this context, the strength of this study is that it creates a tool for mapping, ranking and combining multiple sources of invasion risk at country-level.

Overall, we identified the most vulnerable new countries to Xf invasion are mainly located in the Mediterranean basin, particularly Turkey, Greece, Morocco and Tunisia. As such, this research provides important information in terms of potential exposure by Xf, for policy makers or stakeholders in high risk countries where Xf has not yet been reported. We suggest that these countries and other ranked with relatively high risk should conduct detailed individual risk analysis, take preventive measures, and if necessary, improve their surveillance systems for early Xf detection in plants and insect-vectors, and raise awareness to prevent socio-economic and ecological impacts on their ecosystems. In addition, our approach could be adapted to assess the specific risks for other important invasive alien species, irrespective of their origin, potential area of invasion and whether or not they have already invaded parts of the risk assessment region. As such, it provides a useful addition to tools and methods more commonly applied in regional-scale risk assessment for invasive alien species.

Michel Frem thanks the UK Centre for Ecology and Hydrology, CIHEAM Bari (Italy) and UNIBA Aldo Moro Bari (Italy) for their hospitality, bibliography, data collection and treatment. Thanks also to Sarah Jane Christopher of UNIBA Aldo Moro Bari (Italy) for her careful revision of the Manuscript. This research was supported by CURE-Xf, an EU-funded project, coordinated by CIHEAM Bari (H2020-Marie Sklodowska-Curie Actions – Research and Innovation Staff Exchange. Reference number: 634353).