For the scanning of media and scientific sources, EFSA uses the IT platform of the Medical Information System (MEDISys)[1] developed by the EC Joint Research Centre (JRC). This is a fully automatic event-based surveillance system that was initially developed for public health surveillance (Linge et al., 2009) and later expanded to cover plant health threats. The system collects and automatically analyses articles which are grouped according to multilingual categories, source, and country. In spring 2022 the scanning process was covering 19,000 sources in 79 languages from 204 countries all over the world, with these figures set to increase further due to the regular update of new sources and categories. The system also provides the possibility of categorising the selection of automatically retrieved articles according to individual categories that correspond to specific keywords (Linge et al., 2012). The categories, which have been manually created, correspond to the scientific name and the multilingual common names for a given pest as keywords. By the beginning of spring 2022, the system included more than 2,130 pests grouped in terms of their status in the legislation: ANNEX II Part A of the Commission Implementing Regulation (EU) 2019/ 2072[2], ANNEX II Part B of the Commission Implementing Regulation (EU) 2019/ 2072, Other EU legal acts[3], European and Mediterranean Plant Protection Organisation (EPPO) Lists (A1[4], A2[5] and Alert List[6]) and pests non-listed in EU legal acts or in EPPO Lists. In addition to the categories corresponding to already known pests for EFSA, generic keywords (‘pest’, ‘plant disease’, ‘crop’, ‘yield losses’) have been added to enable the retrieval of articles regarding the discovery of new and emerging pests of plants, which are non-listed in the EU plant health regulation.
Based on these categories, hundreds of articles are retrieved daily by the system. A further selection of these automatically-retrieved-articles is manually performed. This selection is based on specific criteria, which differ depending on the status of the pest in the EU legislation (non-listed pests, pests included in the lists of the EPPO and quarantine pests) (EFSA et al., 2022). For the quarantine pests, scientific articles may refer to new diagnostic, surveillance, detection, identification and control methods, epidemiology, risk management, estimation and communication, potential distribution, impact of implemented measures, potential impact of pest invasion. Furthermore, media and scientific articles are selected when the topic is related to the eradication in an area where the pest is known to occur. For all the above-mentioned pests, media and scientific articles with the following topics are considered eligible: novel taxon with a description of its impact on the plant species concerned, first finding in areas known to be free from the pest, new finding in regions where the pest has already been known to occur and new host plant. Articles that were manually selected from MEDISys reported, for example, the first finding of Neofusicoccum mediterraneum in Italy (Brunetti et al., 2022), a new finding of Citrus concave gum-associated virus in the US (Diaz‐Lara et al., 2022) and Hordeum vulgare as a new host plant for Chinese wheat mosaic virus (Kondo et al., 2022). These are all non-listed pests by the EU plant health regulation. Articles satisfying at least one of the above-mentioned criteria are included in a monthly newsletter, published in the EFSA Journal (Wiley) and presented each month to the Plant Health section of the Plants, Animals, Food and Feed (PAFF) Committee. The overall aim of this newsletter serves as an alert report for the quarantine pests as well as the new and emerging plant health threats.
The selection of the articles and their inclusion in the Plant Health Newsletter constitutes only the very first step of the horizon scanning process, which aims to identify early signals of potential invasive pests. The next step is the screening of the identified pests in terms of their potential threat to the EU, which can be done using the PeMoScoring.
The pests eligible to the PeMoScoring, in the EU horizon scanning context, have to fulfil the following conditions: a) they can cause damages to plant species of economic relevance to the EU, b) they should be able to enter the EU territory by at least one commodity not banned for import into the EU or by natural spread from non-EU territories.
PeMoScoring is composed of 15 criteria including:
- data about the pest (host range, distribution, spread mechanisms including vectors transmission, type of damages),
- data about host plants (distribution and surface area covered by the hosts in the area under assessment),
- data about the European specific scenario (trade pathways prohibited by the EU legislation, suitability of European climate, availability of detection and control measures).
PeMoScoring is currently implemented in Microsoft Excel, therefore any Excel basic user should be able to reproduce its structure, following the exemplum provided in Appendix A (PeMoScoring multicriteria matrix). Additional guidance is provided by EFSA et al., 2022. Current efforts are oriented towards a more accessible platform for all interested users. The information needed to conduct the screening is obtained from publications; when decisive, experts’ judgement can be requested. Even if the method is conceived to allow screening pests under limited evidence availability, some novel taxa are so scarcely known to impede conducting even a partial PeMoScoring. In these circumstances, the species remains monitored on the horizon scanning tool until more evidence is obtained.
During the screening, the assessor replies to the questions/criteria organised in a multicriteria matrix, for each pest of interest. A rate is associated to each answer and all the rates combined define a final score called net Phi value, ranging from -1 to +1 and representing the minimum and maximum levels of expected risk, respectively. This value is submitted to a pairwise comparison with Phi values of other pests used as reference, therefore enabling to position the new scored pest within the reference ranking system. In this way, the assessor obtains a relative ranking for all pests scored. To decide whether a pest can be suggested for further action, it is necessary to define a threshold that distinguishes between “negative” (insufficient evidence of risk, therefore no action) and “positive” pests (sufficient evidence of risk, supporting the possibility of further action). This definition of the threshold is based on the scoring of a set of reference pests, commonly recognizing as threats for the EU. Density functions used to determine the threshold are provided by EFSA et al. (2022). This methodology allows to change the set of reference pests, and, therefore, revise the threshold, keeping PeMoScoring updated with time and needs. The threshold is a straightforward numerical information, that provides the assessor with a defined outcome: whether the pest scored positive (Phi higher or equal to the threshold) or negative (Phi lower than the threshold). PeMoScored pests are signalled in the monthly EFSA newsletter with an icon (⚠️).
Case studies selected
Insect pests represent the most numerous taxa introduced in novel geographic ranges (Seebens et al., 2017), with damage potential causing massive yet underestimated costs worldwide (Bradshaw et al., 2016). Insects are the most represented pest taxon in our personal experience as well, when running PeMoScoring exercises. Therefore, four insect species are presented, displaying the information used to PeMoScore these species: data about the pest, data about host plats, data about the scenario of the area of assessment.
Adelges tsugae (Annand) (Hemiptera: Adelgidae), Arboridia kakogawana (Matsumura) (Hemiptera: Cicadellidae), Phenacoccus solenopsis Tinsley (Hemiptera: Pseudococcidae), and Singhiella simplex (Singh) (Hemiptera: Aleyrodidae) are the four species selected. Arboridia kakogawana and Phenacoccus solenopsis have been raised to the attention of EU risk managers as possible plant health threats while Adelges tsugae and Singhiella simplex are kept monitored on MEDISys without immediate further action. The information needed to run PeMoScoring are of easy access online, i.e.: open sources, and should not require a high level of users’ specialisation to be collected and fed to the PeMo-criteria. These characteristics make PeMoScoring a fast-response and user-friendly tool.
Arboridia kakogawana, the Japanese grape leafhopper, is an insect of the Cicadellidae family. It was first described in Asia (Japan, Korea, China), then found in Russia and Ukraine (Gnezdilov et al., 2008). More recently the pest was spotted in Serbia, Bulgaria and Romania (Chireceanu et al., 2019; Tomov, 2020; Šćiban et al., 2021) inflicting symptoms in European vineyards (Gnezdilov et al., 2008; Chireceanu et al., 2019). The infested leaves show bleaching spots along the central vein of their upper side and, in the case of severe attacks, on their whole surface. When pest populations are numerous, the spots merge, forming large chlorotic zones with negative consequences on the physiological functioning of the leaves (Chireceanu et al., 2019). Grapes are not attacked by the pest (Biosecurity Australia, 2011).
Concerning the potential entry by trade, the main pathway, represented by grapevine plants (Vitis sp.) is closed by the current EU legislation, while Parthenocissus quinquefolia its other known host species, constitutes an open pathway and is also present in the EU territory as a non-cultivated species. A. kakogawana has already entered the EU, a territory of natural and historical vocation for wine production. According to the State of the Vitiviniculture World Market 2018 (http://www.oiv.int), Europe vineyards account for approximately 52.7% of the total vine cultivation area worldwide (Cardell et al., 2019). Some areas of the EU territory show climatic similarities with the ones in the known distribution of the pest, according to the Köppen–Geiger classification from the Institute for Veterinary Public Health of the University of Vienna, based on Kottek et al. (2006) rescaled after Rubel et al. (2017)[7]. This version of the Köppen–Geiger climate classification, is chosen to provide a quick comparison in the PeMoScoring analysis, since also adopted by the EFSA tool to support climate suitability analysis (EFSA and Maiorano, 2022). PeMoScoring users can decide whether adopting another climate classification, according to their needs. A. kakogawana adults can actively fly from one plant to the neighbouring one (Martynov et al., 2019), although precise information on its flight capability is missing. Transportation of infested plants contributes to the pest’s movement. Wood with bark has been also deemed as a possible carrier of A. kakogawana, given that the bark of broad-leaved trees is an overwintering shelter. Plant protection products are used for its control (Baranets, 2021), while biological control options based on parasitoids are under development (Hu and Triapitsyn, 2016; Triapitsyn et al., 2020).
The insect P. solenopsis, commonly known as the cotton mealybug, is presumably native to North America (Tinsley, 1898). It is a polyphagous species, attacking about 300 plant species mostly belonging to Anacardiaceae, Amaranthaceae, Asteraceae, Cucurbitaceae, Euphorbiaceae, Fabaceae, Lamiaceae, Liliaceae, Nyctaginaceae, Malvaceae and Solanaceae (Health et al., 2021). Many host plants, such as tomato, eggplant, sunflower (Beshr et al., 2016) and cotton (Suresh, 2010), are important crops for the EU agriculture (Eurostat, 2023).
P. solenopsis has a widespread distribution in non-EU territory; it has been found in tropical and subtropical regions in the Americas, Middle East, Asia and Africa (Fand and Suroshe, 2015). From these regions, human assisted spread to the EU territory is possible by the importation of plants for planting, fresh fruits, vegetables and cut flowers, infested with adult females, nymphal instars, and eggs (Arif et al., 2012). The European climatic conditions for the establishment of P. solenopsis are sub-optimal, although irrigation can be a factor facilitating its establishment in the Mediterranean (Wang et al., 2010). Indeed, the pest has already been under official control in Cyprus (EPPO Global Database, 2010). Furthermore, it was recently reported in Italy (Sannino et al., 2019), in Greece and France (EPPO Global Database, 2020). Its detection is possible during visual inspections, although it could remain unnoticed if present on the roots of herbaceous plants (Spodek et al., 2018). The morphology of the adult female can be used for identification at the species level (Ramamurthy, 2008). Although the pest is not able to spread over long distances by itself, its movement can be facilitated by the wind. Humans, animals and agricultural machinery can passively disperse the first (crawling) instar of the mealybug on local scales (Arif et al., 2012).
Reported symptoms on cotton, include dehydration, halt of plant growth and, if severe infestation occurs, even defoliation, loss of flower buds, flowers, and immature bolls (Hodgson et al., 2008). Yield losses between 30 to 60% have been reported in India and Pakistan on cotton (Fand and Suroshe, 2015). Plant death occurred after severe infestation on tomato (Ibrahim et al., 2015).
Control methods include mechanical, biological (Spodek et al., 2018) and chemical control (Health et al., 2021).
Adelges tsugae, the hemlock woolly adelgid, is an invasive aphid-like insect of the Adelgidae family (Paradis et al., 2007). This insect seems to be native to Asia, where it is currently present in China, India, Japan and Taiwan. It is widespread in North America and Canada. It feeds on plants of the Pinaceae family, mainly Tsuga sp. (hemlock) and Picea sp. (spruce) (Canadian Food Inspection Agency, 2021). Picea abies and P. sitchensis are economically important plants for the commercial forestry sector in the EU (Calin et al., 2015; Cameron, 2015; Neiva et al., 2018).
A consistent trade of Pinaceae wood in the EU territory exists, including wood imported from areas where the pest is present (EFSA et al., 2023). A.tsugae adults lay very small eggs, up to 300 together in a single clutch, recognizable from the woolly ovisac made of white waxy filaments (Canadian Food Inspection Agency, 2021). Given the actual distribution of the pest, the possibility that it could arrive in Europe through natural means is unlikely. However, larvae can be transported by birds over long distances (Canadian Food Inspection Agency, 2021). Tsuga spp. are cultivated in Europe, mainly in Northern countries (Euro+Med PlantBase, 2005). Some areas of the EU territory show climatic similarities with the ones in the known distribution of the pest, according to the Köppen–Geiger climate classification adopted and describe above. The pest can be spread if carried on plants for planting or by agricultural practices. Birds are thought to be one of the main carriers (Canadian Food Inspection Agency, 2021 Russo et al., 2016). Serious infestations caused by the hemlock woolly adelgid can provoke trees’ death, within 4-15 years (Canadian Food Inspection Agency, 2021). Physical, chemical and biological control measures are available (Jeffrey S. Ward, 2004; Mausel et al., 2010). Trials for natural control, mainly with predators, are under study (Crandall et al., 2020; Mayfield et al., 2015).
Singhiella simplex, the ficus whitefly, is an insect from Southeast Asia (Hodges, 2007; Malumphy and Guillem, 2021). It infests several species of Ficus spp., mainly grown and traded worldwide as ornamental plants (Laudani et al., 2019).
Singhiella simplex suck the sap on both sides of the leaves, causing yellowing, defoliation, honeydew secretion, sooty mold and branch dieback. These symptoms can eventually lead to stunting, wilting and even plant death (Mannion et al., 2008). The severity of the impact depends not only on the infestation level, but also on other factors such as temperature, irrigation, and fertilisation (Ahmed et al., 2022). Contrary to other Aleurodidae, S. simplex doesn’t produce white wax (Ahmed et al., 2022), neither specific symptoms, requiring the use of dichotomous keys for its identification, otherwise complex in the field (Hodges 2007).
S. simplex has been considered as an invasive pest since it invaded Africa, North and South America as well as the Middle East (EPPO Global Database, 2020). The international trade of Ficus trees, which is an open pathway for entry in the EU, has been deemed as the reason for its wide distribution (Laudani et al., 2019; Ahmed et al., 2022). In the EU, it has been reported in Cyprus (EPPO Global Database, 2014), France (EPPO Global Database, 2017), Italy (Laudani et al., 2019), in the Balearic Islands and Gibraltar (Malumphy and Guillem, 2021). The pest spreads at short distances: adults have a limited flying capacity, displacing from one leaf to another (Ahmed et al., 2022). Its limited flight capacity suggests that the pest is unlikely to reach other EU countries by natural means dispersal. Although, infested leaves transported by atmospheric agents, represent a mean of dispersal not to underestimate. Therefore, fallen or pruned leaves should be carefully removed from the fields (Mannion 2010). Control measures include scouting of host plants, chemical and biological control.
[1] https://medisys.newsbrief.eu/medisys/groupedition/en/PlantHealthAll.html
[2] Commission implementing Regulation (EU) 2019/2072 of 28 November 2019 establishing uniform conditions for the implementation of Regulation (EU) 2016/2031 of the European Parliament and the Council, as regards protective measures against pests of plants, and repealing Commission Regulation (EC) No 690/2008 and amending Commission Implementing Regulation (EU) 2018/2019. Official Journal of the European Union L 319, latest consolidated version.
[3] https://food.ec.europa.eu/plants/plant-health-and-biosecurity/legislation/control-measures_en
[4] EPPO A1 List: https://www.eppo.int/ACTIVITIES/plant_quarantine/A1_list
[5] EPPO A2 List: https://www.eppo.int/ACTIVITIES/plant_quarantine/A2_list
[6] EPPO Alert List: https://www.eppo.int/ACTIVITIES/plant_quarantine/alert_list
[7] https://koeppen-geiger.vu-wien.ac.at/present.htm